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Continuous monoculture of Xanthoceras sorbifolia Bunge leads to continuous cropping challenges due to fungal pathogen accumulation and reduced beneficial bacteria abundance

  • # Authors contributed equally: Gongshuai Wang, Lei Wang

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  • Received: 09 August 2024
    Revised: 29 October 2024
    Accepted: 30 October 2024
    Published online: 25 December 2024
    Fruit Research  4 Article number: e040 (2024)  |  Cite this article
  • Xanthoceras sorbifolium Bunge, a unique oil crop native to northern China, has a long history of cultivation. In this study, X. sorbifolium Bunge was continuously planted in Zibo and Weifang, Shandong Province, to explore the factors that cause a decline in X. sorbifolium Bunge yield and fruit quality after long-term continuous planting. The results showed that the continuous cropping of X. sorbifolium Bunge led to a significant decrease in the biomass of the plant's seedlings, markedly reduced the root activity, and reduced the soil nutrient content. A significant change in the soil microbial community structure was observed after years of X. sorbifolia Bunge monoculture. At the genus level, the relative abundance of soil pathogenic fungi, such as Neocosmospora, Aspergillus, and Penicillium, significantly increased after continuous cropping, with the relative abundance of Neocosmospora increasing significantly in the three study sites. The abundance of common soil bacterial genera, such as Mortierella, Bacillus, and Streptomyces, is significantly lower under continuous cropping than in regular soil. The number of soil-specific bacteria was also reduced. The results showed that the accumulation of fungal pathogens, particularly Neocosmospora, may be the main challenge in the continuous cropping of X. sorbifolium Bunge, as it reduces the abundance of beneficial bacteria, primarily Bacillus, Streptomyces, and Mortierella.
  • Sweet cherries (Prunus avium L.) are a major focus of agriculture in the Okanagan region of British Columbia (BC), Canada. A large portion of the cherries grown in BC are exported and undergo up to four weeks of storage during transportation before delivery and consumption[1]. In 2022, sweet cherries accounted for 11.6% of the revenue of exported fruit from Canada and have an export value of nearly CAD$130 million[2]. As such, sweet cherry is an important fruit with high commercial importance for Canada. Although the application of cold storage is a necessary postharvest tool to maintain fruit quality up to consumption, there are preharvest factors that impact quality after longer-term storage. The work of Serrano et al.[3] noted that the maturity stage at harvest determined the fruit quality of sweet cherries after storage. For this reason, producers use several parameters to establish the optimum time for harvesting. Producers have long used colour as a marker for maturity, yet the concept of fruit dry matter (DM) at harvest affecting post-storage quality has advanced[46]. In fact, Toivonen et al.[6] developed a predictive model for 'Lapins' sweet cherry DM content using a visible/near-infrared spectrometer and noted its potential application to other cultivars to provide a rapid and non-destructive means of determining DM linked to cherry fruit quality. If sweet cherries are harvested at the wrong time or stored improperly during transit the quality of the cherries at their final destination does not compare to that at the time of harvest. Therefore, it is of the utmost importance to harvest cherries at their optimal time to ensure quality retention. Cherry fruits have minimal reserve carbohydrates so respiration relies primarily upon organic acids[7]. Additionally, cherries have a high susceptibility to physical damage making them highly perishable, so it is imperative to store them properly to maintain their flavour profile and overall quality[811]. Lower respiration rates help to maintain higher titratable acidity (TA) levels, thereby retaining flavour quality[11,12]. Decreased respiration rates are achieved through low-temperature storage and shipping.

    Previous research linking cherry fruit maturity to flavour quality indicated early-harvested cherries with low soluble solids (SS) levels showed low consumer acceptance due to perceived low sweetness, while late-harvested cherries showed low consumer acceptance due to poor texture[13,14]. This information underscores the challenge growers face when determining picking date. Additionally, once cherries are harvested, quality changes occur which include changes in the balance of SS to TA levels. Previous work has shown that SS levels remain relatively constant while malic acid levels (the predominant acid in sweet cherries) decreased by 20% when stored for 4 d at 20 °C[8,14]. Further, SS, TA, and the SS/TA ratio are key parameters in defining flavour quality[15] and consumer acceptance[14] as SS and TA have been reported to be measures of the cherry fruit attributes of sweetness, and sourness, respectively. Additionally, the SS/TA ratio is regarded as an overall taste attribute determining sweet cherry acceptability[14,16,17].

    Depending on cultivar and growing location, SS values for sweet cherries have been reported to range from 12.3 to 23.7 °Brix[14]. Rootstock and storage conditions have also been reported to affect SS, TA, and SS/TA values[18]. Depending on rootstock, for 'Regina' sweet cherries, harvest SS values ranged from 14.8 to 16.6 °Brix and TA values ranged from 5.7 to 7.4 g·L−1, while SS values after storage ranged from 14.6 to 18.2 °Brix and TA values ranged from 4.4 to 6.0 g·L−1. The harvest SS/TA ratio ranged from 2.0 to 2.91 and the SS/TA ratio after storage ranged from 2.47 to 3.77 depending on rootstock. Based on sensory studies using various cherry cultivars and breeding selections to gauge flavour quality and consumer acceptance, the optimal SS/TA ratio was reported to be between 1.5 and 2.0, with SS values ranging between 17 and 19 °Brix[19].

    Unfortunately, members of British Columbia's sweet cherry industry have noted that while their cherries arrive at their export locations with good condition in terms of appearance (i.e. firm, shiny, with green stems), issues have been reported concerning flavour. Poor flavour has been associated with lower levels of TA and lower oxygen in the storage atmosphere. Our previous work noted that BC cherry growers tend to pick their cherries at lighter colours in an attempt to harvest the crop as soon as possible to avoid any weather or pest issues and achieve the highest yield possible[1]. Staccato (SC) is a late maturing economically important cultivar with little research data available. It has been reported that SC cherries have a respiration rate that is negatively correlated with colour when collected between a 2 to 6 colour level as determined with CTFIL (Centre Technique Interprofessionnel des Fruit et Legumes, Paris, France) colour chips[1], which have been typically used as a marker of maturity. For SC cultivars, data showed the lowest respiration levels with cherries harvested at CTFIL colour standards 4-5, and may potentially have better flavour quality retention due to these lower respiration rates[1]. The aim of the work was to: 1) examine indicators of maturity/readiness for harvest (colour, SS, DM, TA, and the ratio of soluble solids to titratable acidity (SS/TA)); and 2) determine whether colour at harvest or other parameters (SS, TA, SS/TA, and DM) better predict flavour quality retention after storage.

    Sweetheart (SH), Staccato (SC), and Sentennial (SL) sweet cherries were sourced from research plots located at the Summerland Research and Development Center (SuRDC, Summerland, BC, Canada) in the Okanagan Valley region of British Columbia over three growing seasons (2018, 2019, and 2021). In the 2018 growing season, two cherry cultivars (SH and SC were collected, in the 2019 growing season, in response to BC Cherry Association interest, three cherry cultivars (SH, SC, and SL) were collected. Due to COVID, data was not collected during the 2020 growing season. In the 2021 growing season, full data (SS, TA, DM, and respiration rate) was only collected on the SC cherry cultivar, while DM and respiration values at harvest were also collected for SH and SL cultivars.

    To collect fruit at different maturity levels, cherry fruits were collected at three different color levels using the CTFIL (Centre Technique Interprofessionnel des Fruit et Legumes, Paris, France) colour standard series at three harvest dates for each cultivar which corresponded to the 3-4, 4-5, and 5-6 colour levels.

    To collect environmental data, two trees were chosen in each orchard block and Onset HOBO (Bourne, MA, USA) temperature and humidity loggers were mounted in these trees as described by Ross et al.[1] and captured data at 10 min intervals. The temperature and humidity data were used to calculate average temperature (AT), average high temperature (AHT), average low temperature (ALT), and average relative humidity (ARH) for 28 d preceding the cherry harvest date.

    Cherries were generally harvested before 11:00 h on each harvest day. Harvested cherries were transported back to the lab for sorting, sampling, and storage. Upon arrival, cherries were placed into a walk-in cooler at 0.5 °C to mimic rapid hydro-cooling capabilities that the industry uses. In the afternoon of each harvest day, cherries were removed from the cooler and sorted following British Columbia Tree Fruits Company protocol: (i) size was greater than 25.4 mm (< 10.5 row size); (ii) stemless cherries were removed; and (iii) cherries with defects such as blemishes, splits, pitting, disease (rot, fungi), hail damage and insect damage were removed. Again, the colour of the cherries was assessed using the CTFIL colour standard series. Based on the harvest period, cherries were separated into different colour levels: 3-4, 4-5, and 5-6. For each colour category, quality assessments (DM, SS, TA, SS/TA ratio, firmness, size, stem pull force, stem shrivel, stem browning, pitting, and pebbling) were performed before and after storage.

    Maintaining the quality of sweet cherries undergoing long distance ocean container shipment (up to 28 d/4 weeks) is important for securing a successful export market for Canadian sweet cherries and for ensuring that current market demand is met[1]. For cherries to be marketable after storage, they must pass several quality attributes. Attributes of firmness, size, stem pull force, stem shrivel, stem browning, pitting, and pebbling were assessed using previously described methods[1,20] to assess fruit quality at harvest and after storage for 28 d at 0.5 °C, ideal refrigerated storage temperature, for all cherry cultivars, and also storage for 28 d at 3 °C, non-ideal refrigerated storage temperature, for SC cherries. The values of these parameters are provided in Supplementary Tables S1S6. As the focus of this work was to examine how maturity level at harvest influenced the flavour quality of SC, SH, and SL sweet cherry cultivars, SS, DM, TA, and respiration rate values were the focus for discussion. Respiration analysis was performed using methods described by Ross et al. on freshly harvested cherries[1]. Rates of CO2 production were expressed as mg CO2 kg−1·h−1.

    DM of the cherries was determined using a Felix F750 handheld spectrometer (Felix Instruments, Inc., Camas, WA, USA) loaded with a valid model developed at the Summerland Research and Development Centre for cherries[6]. DM was measured on 25 fruits that were randomly selected from each sample replicate (i.e. 50 cherries). For SS and TA analyses, the methods of Ross et al.[1,20] were used to test 25 fruits that were randomly selected from each sample replicate (i.e. 50 cherries). Briefly, de-stemmed cherries were transferred into a 15.2 cm × 22.9 cm polyethylene Ziplock bag. The bag was left partially open, and the cherries were pressed by hand to obtain juice. The juice was strained and collected into 60 mL polypropylene screw cap containers. The resulting filtrate was tested for SS (°Brix), and TA (g·L−1 malic acid). For SS determination, the refractive indices of the solutions were observed in °Brix temperature-corrected mode on a digital refractometer (Mettler-Toledo, Refracto 30PX, 13/02, LXC13237, Japan). An automated titrator (Metrohm 848 Tritrino Plus; Mississauga, ON, Canada) was used to measure the TA of 10 mL of the juice with 65 mL distilled water to an endpoint of 8.1 with 0.1 mol·L−1 NaOH.

    At each colour level (3-4, 4-5, or 5-6) 10 kg of cherry samples were cooled to either 0.5 or 3 °C (for SC in 2021) and then packed into cardboard boxes with a polyethylene liner, an absorbent pad, and an iButton (Thermodata, Whitewater, WI, USA), which measured temperatures experienced by the cherries in the cardboard boxes during storage. After 28 d, the same quality assessment tests were performed to see if values varied throughout storage time at each temperature.

    Statistical analysis was conducted using SAS Institute Inc. software version 9.3 (SAS Institute, Cary, NC, USA). Data were subjected to a four-way analysis of variance (ANOVA) using the SAS PROC GLM procedure. The four factors tested were colour level (3-4, 4-5, and 5-6), cultivar (SH, SC, and SL), growing year (2018, 2019, and 2021), and time (harvest or storage (0.5 °C)). The significance of the main effects and interaction of the four factors was determined using Type III sum of squares via the ANOVA test. Additionally, ANOVA using the SAS PROC GLM procedure was performed on data collected for SC cultivar in the 2021 growing year to assess the influence on storage temperature (0.5 and 3 °C) on quality parameters. Statistical significance was determined by least significant difference (LSD) Fisher's test at 5% significance level. Principal Component Analysis (PCA) was performed using SAS version 9.3 PROC PRINCOMP (SAS Institute Inc., Cary, NC, USA) on data collected from the three cultivars over the tested growing years at three colour levels (i.e., up to nine samples per cultivar) and 10 variables for each investigation. Variables included: AT, AHT, ALT, ARH, colour at harvest (ColourH), SS at harvest (SSH), SS after 28 d of storage at 0.5 °C (SS05), TA at harvest (TAH), TA after 28 d of storage at 0.5 °C (TA05), and DM of cherry fruit at harvest (DMH). Microsoft Excel was used to generate PCA plots from the data provided by SAS. Only data available for every growing year were included in the PCA. Correlation coefficients were determined using Pearson's correlation coefficient statistical function in Excel (version 2306, Microsoft, Redmond, WA, USA). Histograms and frequency data were generated using the statistical function in Excel (version 2306, Microsoft, Redmond, WA, USA). Dry matter bin sizes of 1.5% increments were used to present and analyze the histogram and frequency data.

    Tables 14 present data on flavour attributes via values of soluble solids (SS), titratable acidity (TA), SS/TA ratio, and dry matter (DM) as affected by cultivar, growing year, storage and colour level at harvest and after storage, respectively. The most influential parameters in sweet cherry flavour have been found to be SS, TA, and the SS/TA ratio[15]. Additionally, SS and TA values have been found to be related to DM values in kiwis[2124], apples[25], and cherries[6,26]. DM is a measure of solids which includes both soluble sugars and acids along with insoluble structural carbohydrates and starch. Crisosto et al.[4] proposed using DM as an additional quality parameter as DM was determined not to change during cold storage[22]. Toivonen et al.[6] have performed research linking dry matter measurements with sweet cherry quality. As cold storage is also used to maintain cherry quality, assessing DM at harvest and upon storage was of relevance, and a key aspect of this work was to examine how DM values relate to sweet cherry respiration rates and cherry quality parameters.

    Table 1.  Soluble solids values as affected by cultivar, growing year, storage, and colour level at harvest.
    Cultivar Colour level Soluble solids (SS, °Brix)
    2018 2019 2021
    Harvest Storage (0.5 °C) Harvest Storage (0.5 °C) Harvest Storage (0.5 °C) [3 °C]
    Sweetheart 3-4 18.1aA1 17.7aA1 18.1aA1 18.2aA1
    4-5 20.0bA1 19.8bA1 19.4bA1 18.8bA1
    5-6 21.9cA1* 21.1cA1* 19.9bA1* 19.6cA1*
    Staccato 3-4 17.2aA2 17.2aA1 17.1aA2 17.2aA1 18.8aA* 18.9aA*
    18.4a
    4-5 17.8aA2 17.9aA2 18.3bA23 18.1bA1 19.9bA* 18.6aB
    18.9ab
    5-6 20.2bA2 17.9aB2* 20.2cA1 20.3cA13 20.1bA 19.5aA
    19.7b
    Sentennial 3-4 18.1aA1 18.1aA1
    4-5 18.9bA13 18.5aA1
    5-6 20.8cA2 20.6bA23
    Main effects Significance F-value Degrees of freedom
    Cultivar p < 0.0001 36.90 2
    Colour level p < 0.0001 125.76 2
    Year p < 0.0001 9.26 2
    Time (harvest or storage at 0.5 °C) p = 0.0002 13.68 1
    Colour differences: within common time and cultivar, values followed by different lower case letters indicate significant differences (p ≤ 0.05); Cultivar differences: within common colour level and time, values followed by different numbers indicate significant differences (p ≤ 0.05); Growing year differences: within common time, colour level and cultivar, values followed by * indicate significant differences (p ≤ 0.05); Storage differences (Harvest versus 0.5 °C storage): within common cultivar, colour level and growing year, values followed by different uppercase letter indicate significant differences (p ≤ 0.05); Temperature differences: within Staccato cultivar at 28 d storage and at common colour level, bolded values indicate significant differences (p ≤ 0.05) between storage temperatures (0.5 °C vs 3 °C). (N.B. no bolded values appear in this table).
     | Show Table
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    Table 2.  Titratable acidity values as affected by cultivar, growing year, storage and colour level at harvest.
    Cultivar Colour level Titratable acidity (TA, g·L−1 malic acid)
    2018 2019 2021
    Harvest Storage (0.5 °C) Harvest Storage (0.5 °C) Harvest Storage (0.5 °C) [3 °C]
    Sweetheart 3-4 8.99aA1* 7.11aB1* 7.31aA1* 6.31aB1*
    4-5 9.55bA1* 7.57bB1* 7.14aA1* 6.13aB1*
    5-6 10.56cA1* 8.57cB1* 7.56aA1* 6.50aB1*
    Staccato 3-4 8.53aA2* 6.65aB2* 6.96aA1* 5.51aB2* 12.0aA* 10.5aB*
    9.7a
    4-5 8.87abA2* 7.04bB2* 7.30aA1* 6.21bB1* 12.8aA* 10.2aB*
    9.3a
    5-6 8.91bA2* 6.91abB2 7.18aA1* 6.46bB1 10.6bA* 9.5b*
    8.5b
    Sentennial 3-4 9.21acA2 7.60aB3
    4-5 9.33aA2 7.89aB2
    5-6 8.79bcA2 7.66aB2
    Main effects Significance F-value Degrees of freedom
    Cultivar p < 0.0001 193.58 2
    Colour level p = 0.0023 5.49 2
    Year p < 0.0001 1,007.20 2
    Time (harvest or storage at 0.5 °C) p < 0.0001 474.18 1
    Colour differences: within common time and cultivar, values followed by different lower case letters indicate significant differences (p ≤ 0.05); Cultivar differences: within common colour level and time, values followed by different numbers indicate significant differences (p ≤ 0.05); Growing year differences: within common time, colour level and cultivar, values followed by * indicate significant differences (p ≤ 0.05); Storage differences (Harvest versus 0.5 °C storage): within common cultivar, colour level and growing year, values followed by different uppercase letter indicate significant differences (p ≤ 0.05); Temperature differences: within Staccato cultivar at 28 d storage and at common colour level, bolded values indicate significant differences (p ≤ 0.05) between storage temperatures (0.5 °C vs 3 °C).
     | Show Table
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    Table 3.  Soluble solids to titratable acidity ratio values as affected by cultivar, growing year, storage and colour level at harvest.
    Cultivar Colour level Soluble solids to titratable acidity ratio (SS/TA)
    2018 2019 2021
    Harvest Storage (0.5 °C) Harvest Storage (0.5 °C) Harvest Storage (0.5 °C) [3 °C]
    Sweetheart 3-4 2.02a1A* 2.49a1B* 2.49a1A* 2.78a1B*
    4-5 2.09a1A* 2.61a1B* 2.71b1A* 3.06b1B*
    5-6 2.07a1A* 2.46a1B* 2.63b1A* 3.02b1B*
    Staccato 3-4 2.01a1A* 2.58a1B* 2.46a1A* 3.11a2B* 1.57aA* 1.79aB*
    1.89a
    4-5 2.0a1A* 2.54a1B* 2.51a2A* 2.91b1B* 1.55aA* 1.83aB*
    2.04a
    5-6 2.27b2A* 2.58a1B* 2.81b1A* 3.14a1B* 1.89bA* 2.06bB*
    2.32b
    Sentennial 3-4 1.97a2A 2.38a3B
    4-5 2.02a3A 2.34a2B
    5-6 2.37b2A 2.69b2B
    Main effects Significance F-value Degrees of freedom
    Cultivar p < 0.0001 94.79 2
    Colour level p < 0.0001 22.04 2
    Year p < 0.0001 361.13 2
    Time (harvest or storage at 0.5 °C) p < 0.0001 134.15 1
    Colour differences: within common time and cultivar, values followed by different lower case letters indicate significant differences (p ≤ 0.05); Cultivar differences: within common colour level and time, values followed by different numbers indicate significant differences (p ≤ 0.05); Growing year differences: within common time, colour level and cultivar, values followed by * indicate significant differences (p ≤ 0.05); Storage differences (Harvest versus 0.5 °C storage): within common cultivar, colour level and growing year, values followed by different uppercase letter indicate significant differences (p ≤ 0.05); Temperature differences: within Staccato cultivar at 28 d storage and at common colour level, bolded values indicate significant differences (p ≤ 0.05) between storage temperatures (0.5 °C vs 3 °C).
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    Table 4.  Dry matter values as affected by cultivar, growing year, storage and colour level at harvest.
    Cultivar Colour level Dry matter (DM, %)
    2018 2019 2021
    Harvest Storage (0.5 °C) Harvest Storage (0.5 °C) Harvest Storage (0.5 °C) [3 °C]
    Sweetheart 3-4 20.9aA1* 20.6aA1* 18.6aA1* 18.6aA1* 22.1aA1*
    4-5 21.9bA1 22.0bA1* 19.9bA1* 19.8acA1* 22.5bA1
    5-6 25.2cA1* 23.5cB1* 21.1cA1* 20.6bcA1* 23.6cA1*
    Staccato 3-4 20.2aA1* 19.5aA2* 18.4aA2* 18.1aA23* 21.0aA2* 20.6aA*
    19.8a
    4-5 20.4aA2* 20.8bA2* 19.1aA1* 18.8aA2* 22.0bA2* 21.6bA*
    21.9b
    5-6 22.4bA2 22.3cA2 22.9bA2* 21.6bA23 23.0cA2 22.2bA
    22.4b
    Sentennial 3-4 18.2aA2 18.4aA13 20.5aA2*
    4-5 19.3bA1 18.8bA2 22.6bA12*
    5-6 22.9cA2 20.9bA13 23.5cA12
    Main effects Significance F-value Degrees of freedom
    Cultivar p < 0.0001 11.36 2
    Colour level p < 0.0001 130.99 2
    Year p < 0.0001 56.64 2
    Time (harvest or storage at 0.5 °C) Not significant, p = 0.0922 2.97 1
    Colour differences: within common time and cultivar, values followed by different lower case letters indicate significant differences (p ≤ 0.05); Cultivar differences: within common colour level and time, values followed by different numbers indicate significant differences (p ≤ 0.05); Growing year differences: within common time, colour level and cultivar, values followed by * indicate significant differences (p ≤ 0.05); Storage differences (Harvest versus 0.5 °C storage): within common cultivar, colour level and growing year, values followed by different uppercase letter indicate significant differences (p ≤ 0.05); Temperature differences: within Staccato cultivar at 28 d storage and at common colour level, bolded values indicate significant differences (p ≤ 0.05) between storage temperatures (0.5 °C vs 3 °C). (N.B. no bolded values appear in this table).
     | Show Table
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    Data in Table 1 shows the SS levels at each colour level for each sweet cherry cultivar. Overall, SH cherries at harvest had ranges of 18.1%−21.9% over the 2018 and 2019 growing seasons. SC cherries at harvest had levels between 17.1%−20.2% over the three growing years (2018, 2019, and 2021), while SL cherries at harvest had levels of 18.1%−20.8% in 2019. Statistical analysis showed that the main effects of Cultivar (p < 0.0001; F-value = 36.90; degrees of freedom (df) = 2), Colour (p < 0.0001; F-value = 125.76, df = 2), Time (p = 0.0007; F-value = 13.68; df = 1), and Year (p < 0.0001; F-value = 9.26; df = 2) were all significant. Additionally, the interactions of Cultivar * Year (p < 0.0001, F-value = 26.37; df = 1), Colour * Year (p < 0.0069; F-value = 4.19; df = 4), Cultivar * Colour * Year (p < 0.0003; F-value = 10.28; df = 2) and Colour * Time * Year (p < 0.0131; F-value = 3.67; df = 4) were all significant.

    With respect to growing year differences, in 2018, SS levels in SH were greater than those of SC at all colour levels. In 2019, again at the 3-4 colour level SC, cherries exhibited lower SS levels than SH and SL cherries. At the 4-5 colour level, SH cherries again showed higher SS levels compared to SC cherries. At the 5-6 colour level, SL cherries showed higher SS levels compared to SC and SH, while SC and SH cherries showed comparable SS levels at the 5-6 colour level. The SS values of SC cherries at 3-4 and 4-5 colour levels from the 2021 growing year were higher than values observed at the same colour levels in 2018 and 2019 growing year samples. There was no difference observed in SS levels of SC cherries at the 5-6 colour level between growing years. The data shows that colour level, cultivar, and growing year all affected SS levels.

    Within cultivars, for SH in the 2018 growing season, as colour level increased, SS level increased. An increase in SS as colour at harvest increased for SH cultivar was reported by Puniran et al.[27]. In the 2019 growing year for SH cherries and in the 2021 growing year for SC cherries, SS levels plateaued at the 4-5 colour level. For SC (2018 and 2019 growing year) and SL cherries (2019 growing year) as colour level increased, SS level increased. Ross et al.[1] reported this same trend for SC cultivar on data collected from 2015, 2016, and 2017 growing years. This data demonstrates the influence of growing conditions on SS levels.

    In general the SS levels at each colour level for each sweet cherry cultivar did not change over the 28 d storage at 0.5 °C. It should be noted that SC cherries from the 2018 growing year at the 5-6 colour level and SC cherries from the 2021 growing year at the 4-5 colour level did show a significant (p ≤ 0.05) decrease in soluble solids after 28 d of storage at 0.5 °C. SS values for 2018 SC cherries at the 5-6 colour level harvest was 20.2 °Brix, while SS values after 28 day storage at 0.5 °C was 17.9 °Brix. SS values for 2021 SC cherries at the 4-5 colour level harvest was 19.9 °Brix, while SS values after 28 d of storage at 0.5 °C was 18.6 °Brix. In 2021 the effect of storage temperature (0.5 °C vs 3 °C) was investigated. SS levels in the SC cherries at the different colour levels were not affected by the different storage temperatures. This result was consistent with other findings[1,8,14], which suggested that under typical low temperature storage conditions and proper shipping conditions, the change in flavour profiles were likely not due to major changes in SS levels. It is important to note that Alique et al.[8] found that while SS values were consistent, the levels of glucose and fructose decreased by 13% and 10%, respectively, after 4 d under ambient conditions. It may be worth investigating if under a lower temperature environment, the levels of key monosaccharides would remain constant or change.

    This moves the focus of flavour retention to TA values. Table 2 shows the TA levels at each colour level for each sweet cherry cultivar. Statistical analysis showed that the main effects of Cultivar (p < 0.0001; F-value = 193.58; df = 2), Colour (p = 0.0023; F-value = 5.49, df = 2), Time (p < 0.0001; F-value = 474.18; df = 1), and Year (p < 0.0001; F-value = 1007.20; df = 2) were all significant. The interactions of Cultivar * Colour (p < 0.001; F-value = 5.81; df = 4); Cultivar * Year (p < 0.0001; F-value = 19.9; df = 1); Colour * Time (p = 0.0431; F-value = 3.44; df = 2); Colour * Year (p < 0.0001; F-value = 18.01; df = 4); Time * Year (p < 0.0001; F-value = 17.21; df = 2); Cultivar * Colour * Year (p = 0.0009; F-value = 8.63; df = 2); Colour * Time * Year (p = 0.0127; F-value = 3.70; df = 4) were all significant.

    SH cherries at harvest had TA value ranges of 8.99−10.56 g·L−1 in 2018, and 7.31−7.56 g·L−1 in 2019. In 2018, the highest TA value was at the 5-6 colour level for SH cherries, while for the 2019 SH cherries there was no difference between colour levels for the TA values. After storage SH cherries at the various colour levels showed TA levels of 7.11−8.57 g·L−1 and 6.31−6.50 g·L−1 for 2018 and 2019, respectively. Again the stored 2018 SH cherries at the 5-6 colour level showed the highest TA values, while the TA values for the stored 2019 SH cherries were not affected by colour level. SC cherries at harvest showed TA value ranges of 8.53−8.91 g·L−1 in 2018, 6.96−7.18 g·L−1 in 2019, and 10.6−12.8 g·L−1 in 2021. After storage SC cherries had lower TA values at all colour levels for all growing years. In 2018, 2019, and 2021, TA values for SC cherries after storage ranged from 6.65–7.04 g·L−1, 5.51−6.46 g·L−1 and 8.5−10.5 g·L−1, respectively. In 2021, for the SC cherries, the higher storage temperature (3 °C) resulted in a greater loss of TA values for all colour levels compared to the lower temperature of 0.5 °C. SL cherries at harvest had TA levels of 8.79−9.33 g·L−1 in 2019 and after storage at 0.5 C, TA values ranged from 7.60−7.89 g·L−1, with the highest value of TA at the 4-5 colour level. Therefore for all cultivars over all growing years, TA values decreased upon storage, which was expected. The data from Table 2 shows the magnitude of the decrease in TA values after storage varied by growing year. Additionally, trends for differences of TA magnitude change with respect to cultivar and colour level were not obvious. The magnitude of the decrease in TA values between harvest and storage was higher for the SC cherries stored at 3 °C compared to those stored at 0.5 °C.

    Comparing the effect of colour level on TA level within cultivar for SH cherries, TA values increased as colour level at harvest increased in 2018, but the trend did not continue in 2019, possibly due to different growing conditions such as orchard temperature and relative humidity values, which will be further discussed. For SC cherries, TA values peaked at the 4-5 colour level for 2018 and 2021 growing years, but were not significantly different between colour levels in 2019 (p ≤ 0.05). In the 2019 growing year, SL cherries also had the highest TA values at the 4-5 colour level. Comparing the effect of cultivar on TA level within comparable colour level, 2018 harvest SH cherries showed higher TA values than SC cherries. In the 2018 growing year, upon storage and at comparable colour level, SH cherries again showed higher TA values than SC cherries. In the 2019 harvest, SC cherries exhibited the same TA values as SH cherries, while SL cherries had higher TA values than SC and SH. In the 2019 growing year SL cherries harvested at the 3-4 colour level showed greater TA values after storage compared to SH and SC cherries; SC cherries had the lowest TA values at this colour level. When harvested at the 4-5 and 5-6 colour levels, SL cherries had higher TA values upon storage compared to SH and SC cherries.

    The data suggests that different cultivars tend to peak TA values, which may be affected by growing conditions/growing year and maturity level/colour level. This is further supported by the work of Miloševic & Miloševic[28] that indicated TA levels of sour cherries are affected by level of ripeness. Puniran et al.[27] also indicted that finding where peak TA values occur at harvest can help negate the decrease in values that occurs during storage and therefore promote flavour quality retention.

    In 2021 the effect of storage temperature (0.5 °C vs 3 °C) was investigated as 0.5 °C represents ideal storage temperature while 3 °C represents a storage temperature where quality deterioration would be promoted, and may be a more realistic temperature experienced during overseas/export shipping (personal communication, Dr. Peter Toivonen, May, 2021). TA levels in the SC cherries harvested at the different colour levels were affected by the different storage temperature as seen in Table 2. At common colour level, SC cherries from the 2021 growing season stored at 3 °C showed lower TA values than samples stored at 0.5 °C. The SC cherries at the 5-6 colour level stored at 3 °C showed the lowest TA values upon storage. As higher TA values are associated with flavour quality[11,12], the SC cherries harvested at the 5-6 colour level and stored at 3 °C would show poorer flavour quality.

    Table 3 shows the SS/TA ratio values as affected by cultivar, growing year, storage and colour level at harvest. Statistical analysis showed that the main effects of Cultivar (p = 0.0001; F-value = 94.79; df = 2), Colour (p < 0.0001; F-value = 22.04; df = 2), Time (p < 0.0001; F-value = 134.15; df = 1), and Year (p < 0.0001; F-value = 361.13; df = 2) were all significant. The interactions of Cultivar * Colour (p = 0.0009; F-value = 5.91; df = 4) and Time * Year (p = 0.0059; F-value = 5.95; df = 2) were significant. The SS/TA ratio values over all cultivars, colour levels and growing years ranged from 1.55 to 2.81 at harvest and 1.79 to 3.14 after storage at 0.5 °C for 28 d. SC cherries in the 2021 growing year were tested to determine the effect of storage temperature (0.5 or 3 °C) on flavour quality. The SS/TA ratio for the 2021 SC cherries stored at 0.5 °C for 28 d ranged from 1.79 to 2.06 while the SS/TA ratio for the 2021 SC cherries stored at 3 °C for 28 d ranged from 1.89 to 2.32. SS/TA ratios for the 3 °C stored cherries at the 4-5 and 5-6 colour levels were significantly higher (p ≤ 0.05) compared to corresponding SS/TA ratios for the 0.5 °C stored cherries at the 4-5 and 5-6 colour levels. Higher SS/TA ratio are due to lower TA values (data in Table 3) and impact flavour quality and therefore lower storage temperatures are preferable, which was expected.

    Comparing between growing years, for SH and SC cherries, the SS/TA ratio at harvest was higher in the 2019 growing year compared to the 2018 growing year. SC cherries from the 2021 growing year showed the lowest at harvest SS/TA ratio. Within cultivar, the SH cherries from the 2018 growing year showed no difference in harvest SS/TA ratio at the different colour levels. SH cherries from the 2019 growing year showed higher harvest SS/TA ratios at the 4-5 and 5-6 colour levels compared to the 3-4 colour level. The SC cherries at all growing years showed highest harvest SS/TA ratio levels at the 5-6 colour level and comparable harvest SS/TA ratio levels at the 3-4 and 4-5 colour levels. SL cherries also showed the highest harvest SS/TA ratio at the 5-6 colour level and comparable harvest SS/TA ratios at the 3-4 and 4-5 colour levels.

    Comparing cultivars at common colour level, in 2018 growing year SC cherries at the 5-6 colour level showed a higher harvest SS/TA ratio compared to SH cherries at the corresponding colour level. In the 2019 growing year SH and SC cherries showed higher harvest SS/TA ratios at the 3-4 colour level compared to SL cherries. At the 4-5 colour level, SH cherries showed the highest harvest SS/TA ratio value and SL cherries showed the lowest harvest SS/TA ratio value. At the 5-6 colour level, SH and SC cherries showed comparable SS/TA ratios while SL cherries showed the lowest SS/TA ratio.

    Overall, this data indicates that ensuring cherry flavour quality is complex as SS/TA ratio varied by growing year, colour level and cultivar. Comparing SS/TA ratio data for all cultivars over all growing years did not show an observable trend between colour level and SS/TA ratio. As such, colour is not a reliable indicator of flavor quality.

    Table 4 shows the DM values as affected by cultivar, growing year, storage and colour level at harvest. Statistical analysis showed that the main effects of Cultivar (p = 0.0001; F-value = 11.36; df = 2), Colour (p < 0.0001; F-value = 130.99; df = 2), and Year (p < 0.0001; F-value = 56.64; df = 2) were all significant. Notably, the main effect of Time (harvest vs stored) was not significant (p = 0.0922). The interactions of Cultivar * Year (p = 0.001; F-value = 6.45; df = 3); Colour * Year (p = 0.0004; F-value = 6.38; df = 4); Cultivar * Colour * Year (p = 0.0018; F-value = 4.64; df = 5) were all significant. Although SS and TA values were not obtained for all three cultivars in 2021, DM values at harvest were obtained for all three cultivars in 2021. Data in Table 4 show, in general, DM levels did not change over 28-d storage, which was expected. Additionally, data in Table 4 shows that in most cases, at common cultivar and colour level, DM values measured in 2021 were greater than DM values measured in 2018 and 2019 for all cultivars (SH, SC, and SL).

    Within each cultivar, over all growing years, the harvest DM values were significantly different (p < 0.05) at each colour level, except for SC cherries in the 2018 and 2019 growing years. 2018 and 2019 DM values were not significantly different from colour level 3-4 to colour level 4-5. At the 5-6 colour level, over all growing years, SH cherries showed higher DM values compared to dry matter values observed for SC cherries (p < 0.05). At the 3-4 colour level, over all growing seasons, the DM values for SL and SC cherries were not significantly different (p < 0.05). At the 4-5 colour level, over all growing seasons, the DM values for SL were not significantly different than the DM values exhibited by SH and SC cherries (p < 0.05). In 2021 the effect of storage temperature (0.5 °C vs 3 °C) was investigated. DM levels in the SC cherries at the different colour levels were not affected by the different storage temperature. Overall, DM levels ranged from 18.1 to 25.2 depending on cultivar, colour level, growing year, and storage.

    Figure 1ac shows the distribution of the three cherry cultivars relative to DM value ranges over all three growing years via histograms. Cherries at the same colour level did not all have the same DM; this was observed both within and between cultivars (Fig. 1ac). DM data, compiled over all available growing years, for each cultivar in the 3-4, 4-5, and 5-6 colour levels had considerable overlap. However, it is noted there is consistent shift to a higher DM at the 5-6 colour level.

    Figure 1.  Histogram representing distribution of dry matter data for: (a) Sweetheart (SH) cherries over the 2018, 2019, and 2021 growing years; (b) Staccato (SC) cherries over the 2018, 2019, and 2021 growing years; and (c) Sentennial (SL) cherries over the 2019 and 2021 growing years. For all parts, the 3-4 colour level is solid black, the 4-5 level is black stripes, and the 5-6 level is solid grey. On the horizontal axis different dry matter value (DM) ranges are shown via bins and on the vertical axis the frequency or proportion (%) of cherries within the DM bins/ranges are shown. Data was generated from two replicates of samples of 25 cherries (i.e. 50 cherries) from all available growing years.

    Over all growing years, DM values for SH cherries ranged from 14%−27%, 14%−28.5%, and 16.5%−33%, at the 3-4, 4-5, and 5-6 colour levels, respectively (Fig. 1a). SH cherries at the 3-4 and 4-5 colour levels showed the highest proportion (26% and 26%, respectively) of cherries resided in the 22.5 and 22.5% DM bins indicating the highest percentage of SH cherries in these colour levels exhibited a DM of 21% to 22.5%, while the highest proportion (21%) of cherries at the 5-6 colour level resided in the 24% DM bin indicating the highest percentage of SH cherries at this colour level exhibited a DM of 22.5% to 24% (Fig. 1a).

    For SC cherries over all growing years, DM values ranged from 14%−25.5%, 14%−30%, and 16.5%−30%, at the 3-4, 4-5, and 5-6 colour levels, respectively (Fig. 1b). SC cherries at the 3-4 colour level showed the highest proportion of cherries (27%) resided in the 19.5% DM bin which indicated the highest percentage of SC cherries at this colour level exhibited a DM of 18 to 19.5%. SC cherries at the 4-5 colour level showed the highest proportion of cherries (25%) resided in the in the 21% DM bin which indicated the highest percentage of SC cherries at this colour level exhibited a DM of 19.5% to 21 %. At the 5-6 colour level, the highest proportion (35%) of SC cherries resided in the 22.5% DM bin which indicated the highest percentage of SC cherries exhibited a DM of 21%−22.5% (Fig. 1b).

    Over the 2019 and 2021 growing years, SL cherries DM values ranged from 15%−25.5%, 15%−28.5%, and 16.5%−33% at the 3-4, 4-5 and 5-6 colour levels, respectively (Fig. 1c). SL cherries at the 3-4 colour level showed the highest proportion of cherries (36%) resided in the 21% DM bin which indicated the highest percentage of SL cherries at this colour level exhibited a DM of 19.5% to 21%. SL cherries at the 4-5 colour level showed the highest proportion of cherries (28%) resided in the in the 21% DM bin which indicated the highest percentage of SL cherries at this colour level exhibited a DM of 19.5% to 21 %. At the 5-6 colour level, the highest proportion (26%) of SC cherries resided in the 22.5% DM bin which indicated the highest percentage of SL cherries exhibited a DM of 21%−22.5% (Fig. 1c).

    In all, the data in Tables 14 and Fig. 1 indicate that colour is not a reliable indicator of maturity or flavor quality. Cherries of the same colour may differ in DM, SS, TA, and SS/TA ratio due to cultivar and growing conditions. The implication of these results are discussed in subsequent sections.

    Temperature, relative humidity and harvest date for the 2018, 2019, and 2021 growing years are detailed in Table 5. Environmental variations between years impacted colour development, which resulted in yearly variations in our harvest dates as cherry picks were based on cherry colour levels: 2018, July 16 to August 9; 2019, July 18 to August 6; and 2021, July 5 to July 27, nearly two weeks earlier than in previous years (Table 5). In terms of environmental data, the average temperature (AT), average high temperature (AHT), and average low temperature (ALT) values measured in 2021 were greater than the values determined in 2018 and 2019, while the average relative humidity (ARH) values determined in 2021 were lower than the values measured in 2018 and 2019 (Table 5). Depending on growing year and harvest date, average temperature values ranged from 17.17 to 24.28 °C, average high temperature values ranged from 28.59 to 50.68 °C, average low temperatures ranged from 7.17 to 10.68 °C, and average relative humidity values ranged from 40.68% to 66.16% (Table 5).

    Table 5.  Temperature and relative humidity environmental data for 2018, 2019, and 2021 growing years.
    Growing year Colour level Harvest date Average
    temperature
    (AT) (°C)
    Average relative humidity (ARH) Average low temperature (ALT) (°C) Average high temperature (AHT) (°C)
    2018 Sweetheart 3-4 July 16 18.96 61.5% 7.17 32.14
    4-5 July 23 18.85 59.8% 7.17 32.13
    5-6 July 30 20.45 56.85% 7.49 32.05
    Staccato 3-4 July 30 19.74 59.17% 7.42 32.04
    4-5 August 9 21.14 54.46% 7.42 32.77
    5-6 August 9 21.14 54.49% 7.42 32.77
    2018 overall average 20.05 57.71% 7.35 32.32
    2019 Sweetheart 3-4 July 18 17.86 66.04% 7.22 28.79
    4-5 July 24 18.39 66.1% 7.22 28.59
    5-6 July 24 18.39 66.1% 7.22 28.59
    Staccato 3-4 July 22 18.03 66.16% 7.22 28.59
    4-5 July 29 19.19 62.92% 8.67 29.39
    5-6 July 31 19.19 62.92% 8.67 29.39
    Sentennial 3-4 July 22 18.03 66.16% 7.22 28.59
    4-5 July 29 18.99 63.77% 8.67 29.39
    5-6 August 6 19.79 59.94% 8.67 29.39
    2019 overall average 18.87 63.65% 8.19 28.96
    2021 Sweetheart 3-4 July 5 24.01 40.68% 8.51 50.68
    4-5 July 12 24.28 40.68% 10.68 49.23
    5-6 July 20 24.10 40.68% 9.66 47.47
    Staccato 3-4 July 13 24.01 40.68% 8.51 50.68
    4-5 July 21 24.28 40.68% 10.68 49.23
    5-6 July 27 24.10 40.68% 9.66 47.47
    Sentennial 3-4 July 12 24.01 40.68% 8.51 50.68
    4-5 July 19 24.28 40.68% 10.68 49.23
    5-6 July 26 24.10 40.68% 9.66 47.47
    2021 overall average 24.12 40.68% 9.62 49.13
     | Show Table
    DownLoad: CSV

    Principal component analysis (PCA) was performed on all cultivars over all growing seasons to best resolve cultivar specific relationships between variables affecting flavour quality parameters: colour, DM, SS and TA (Fig. 2).

    Figure 2.  Principal component analysis (PCA) plot for: Sweetheart (SH) cherries with data from 2018 and 2019 growing years at the 3-4, 4-5, and 5-6 colours levels (SH34-2018, SH45-2018, SH56-2018, SH34-2019, SH45-2019, and SH56-2019; Staccato (SC) cherries with data from 2018, 2019 and 2021 growing years at the 3-4, 4-5, and 5-6 colour levels (SC34-2018, SC45-2018, SC56-2018, SC34-2019, SC45-2019, SC56-2019, SC34-2021, SC45-2021, and SC56-2021); and Sentennial (SL) cherries with data from 2019 growing year (SL34-2019, SL45-2019, and SL56-2019). PC1 and PC2 accounted for 84.75% variation. The variables include: average temperature (AT), average high temperature (AHT), average low temperature (ALT), average relative humidity (ARH), colour at harvest (ColourH), SS at harvest (SSH), SS after 28 d of storage at 0.5 °C (SS05), titratable acidity at harvest (TAH), titratable acidity after 28 d of storage at 0.5 °C (TA05) and dry matter of cherry fruit at harvest (DMH). Orchard growing factors, flavour quality attributes (loading factors), along with sweet cherry cultivars from each growing season (component scores) were presented as lines with arrows, lines with circles, and squares, respectively. Variables close to each other with small angles between them are strongly positively correlated; variables at right angles are likely not correlated; variables at large angles (close to 180°) are strongly negatively correlated.

    Figure 2 shows that principal components 1 and 2 described most of the variation (84.75%) in the model. SS at harvest (SSH) and SS at 28-d storage at 0.5 °C (SS05) along with DM at harvest (DMH) were positively correlated with colour at harvest (ColourH). TA at harvest (TAH) and TA at 28-d storage at 0.5 °C (TA05) were positively correlated with average high temperature (ATH). AHT, average low temperature (ALT) and average temperature (AT). DMH was more strongly correlated with TAH and TA05 compared to ColourH. TAH and TA05 were positively correlated, yet negatively correlated with average relative humidity (ARH). The 2021 SC samples at the 3-4, 4-5, and 5-6 colour levels (SC34-2021, SC45-2021, and SC56-2021) were clustered with TAH, TA05, ALT, AHT, and AT variables and located in a quadrant opposite of ARH. In late June 2021 a heatwave of unprecedented magnitude impacted the Pacific Northwest region of Canada and the United States; the Canadian national temperature record was broken with a new record temperature of 49.6 °C[29]. Also, the relative humidity levels during this period were also extremely low[30]. As the location of this study was impacted by this heatwave, the data shown in Table 6 shows higher temperatures and lower relative humidity values for the 2021 growing year. The TA values measured in the 2021 growing year were nearly two times the levels measured in the 2018 and 2019 growing years (Table 2). This shows an impact of growing conditions on flavor quality; both the negative correlation between ARH and TA and positive correlations of AT, AHT, and ALT with TA are notable. However, it is noted that correlation does not mean causation. The SH and SC cultivars from the 2018 growing year at the 5-6 colour level were clustered together, and were located in the same quadrant as ColourH, SSH, SS05, and DMH variables (Fig. 2). This indicates these samples were characterized by high values of SSH, SS05, and DMH. All cultivars at the 3-4 colour level from the 2018 (SH and SC), and 2019 (SH, SC, and SL) growing years along with all cultivars at the 4-5 colour level from the 2019 (SH, SC, and SL) growing year were clustered in quadrants opposite of the SSH, SS05, DMH, ColourH, TAH, and TA05 variables while near the ARH variable. The clustering of the samples indicates similarity and lower levels of SSH, SS05, DMH, TAH, and TA05.

    Table 6.  Average colour level and respiration rate of sweet cherries at harvest.
    Growing year Colour
    level
    Average colour measured at harvest
    [average dry matter at harvest]
    Dry matter bin (%), highest
    proportions of cherries
    Respiration rate (mg CO2 kg−1·h−1)
    assessed at 0.5, 5 or 10 °C
    0.5 °C 5 °C 10 °C
    2018 Sweetheart 3-4 3.74a1 [20.9%] 21, 38% 2.87a1 * 5.99a1* 9.75a1*
    4-5 4.66b1 [21.9%] 22.5, 38% 3.57b1* 5.53b1* 9.06a1*
    5-6 5.54c1 [25.2%] 25.5, 26% 3.50b1* 5.18b1* 9.58a1*
    Staccato 3-4 3.58a1 [20.2%] 19.5, 44% 4.43a2* 7.08a2* 9.90a1*
    4-5 4.62b1 [20.4%] 21, 36% 4.58a2* 8.05b2* 11.22b2*
    5-6 5.64c1 [22.4%] 22.5, 50% 4.12b2* 6.43c2* 9.78a1*
    2019 Sweetheart 3-4 3.76a1 [18.6%] 18, 26%; 19.5, 26% Nd 6.04 13.7
    4-5 4.42b1 [19.9%] 21, 32% Nd Nd 8.3
    5-6 5.42c1 [21.1%] 22.5, 28% Nd 6.95 13.5
    Staccato 3-4 3.46a1 [18.4%] 19.5, 32% Nd 5.8 12.47
    4-5 4.40b12 [19.1%] 19.5, 40% Nd 6.14 Nd
    5-6 5.40c1 [22.9%] 22.5, 26% Nd Nd Nd
    Sentennial 3-4 3.62a1 [18.2%] 18, 28% Nd 6.5 12.80
    4-5 4.22b2 [19.3%] 21, 40% Nd 3.76 Nd
    5-6 5.20c2 [22.9%] 22.5, 24% Nd Nd Nd
    2021 Sweetheart 3-4 Nd [22.1%] 22.5, 40% 3.18a1* 5.86a1* 8.8a1*
    4-5 Nd [22.5%] 22.5, 28% 2.78a1* 5.08b1* 8.1a1*
    5-6 Nd [23.6%] 24, 30% 2.65a1* 4.32c1* 9.19a1*
    Staccato 3-4 3.50a1 [21.0%] 19.5, 28% 2.72a1 4.65ab2 10.94a2*
    4-5 4.80b1 [22.0%] 21, 24%; 22.5, 20% 3.27a1* 4.38a2* 8.22b1*
    5-6 5.60c1 [23.0%] 24, 30% 3.05a1* 5.07b2* 9.57ab1*
    Sentennial 3-4 Nd [20.5%] 21, 48% 2.71a1* 4.77a2* 7.84a1*
    4-5 Nd [22.6%] 22.5, 28%; 24, 24% 2.78a1* 4.81a12* 8.28ab1*
    5-6 Nd [23.5%] 22.5, 28%; 24, 24% 4.23b2 4.47a12 9.88b1*
    Within common cultivar and growing year, values followed by different letters indicate significant differences (p ≤ 0.05)-shows colour differences; Within common colour level and growing year, values followed by different numbers indicate significant differences (p ≤ 0.05)-shows cultivar differences; Within common cultivar, growing year and colour level, values followed by * indicate significant differences (p ≤ 0.05)-shows respiration rate differences at the different temperatures. Due to incomplete data, statistical analysis was not performed on 2019 data. Nd = Actual colour was not calculated for Sweetheart and Sentennial cherries in 2021 although cherries were collected 3-4, 4-5, 5-6 colour levels as in previous years and can be considered to have colour levels of approximately 3.5, 4.5, and 5.5, respectively.
     | Show Table
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    High respiration rates have long been associated with rapid fruit quality deterioration[11]. Lower respiration rates help to maintain higher TA levels, thereby retaining flavour quality[11,12]. This work aimed to provide information on assessing whether rapid and non-invasive dry matter measurements can serve as a surrogate for respiration rate measurements and/or TA measurements to predict fruit quality as this information is essential for developing recommendations to optimize cherry quality retention upon long distance transport. Although it is well known that quality deteriorates more quickly in fruit with higher respiration rates, the respiration rate data for the SH, SC, and SL cherries was collected and analyzed with respect to the different colour levels and corresponding DM values to investigate a link between respiration rate and DM value. Examining the data with this perspective is very novel and additionally very little information on respiration rates is available for SC and SL sweet cherries cultivars in the literature.

    Table 6 shows the respiration rates for a) SH and b) SC cherries at different colour levels for the 2018 growing year and how they were affected by respiration rate assessment temperature (0.5, 5, and 10 °C). Table 6 also shows the respiration rates for a) SH, b) SC, and c) SL cherries at different colour levels for the 2021 growing year and how they are affected by respiration rate assessment temperature. Please note respiration data is incomplete for the 2019 growing year because of data constraints due to equipment difficulties and therefore no statistical analysis was performed on the available 2019 respiration data. As little information exists in the literature for SC and SL cherries, we have included the incomplete respiration data. Table 6 also shows average color data and average DM data for the cherries collected at the different colour levels. Additionally, Table 6 shows data on the DM (%) bins containing the highest proportion of cherries for each cultivar in each growing year at each colour level (histograms for each cultivar for individual growing year not shown).

    Table 6 shows the average colour measured for the cherries harvested at the 3-4, 4-5, and 5-6 colour levels all varied slightly depending on growing year and cultivar. In both the 2018 and 2019 growing years there was no difference in color levels between SH and SC at harvest. In the 2019 growing year, the SL cherries showed lower average colour values at the 4-5 and 5-6 colour levels compared to the average colour levels of SH and SC cherries at the same level. Nevertheless, results indicated the cherries were harvested and sorted to the desired colour levels. In 2021, average colour was not calculated for SH and SL cherries, although cherries were collected at the 3-4, 4-5, and 5-6 colour levels, as in previous years, and can be considered to have been within range. The average colour level was calculated for SC cherries in 2021, as SC cultivar received comprehensive study over all growing years (2018, 2019 and 2021). The calculated colour level values for SC cherries in the 2021 growing year at the 3-4, 4-5, and 5-6 colour levels were 3.5, 4.8, and 5.6, respectively.

    Table 6 shows the lower the respiration rate assessment temperature, the lower the respiration rate, which was expected as cherries are recommended to be stored at 0.5 °C to ensure quality retention due to this fact[1]. In 2018, SH respiration rate values were consistently lower than SC cherries at 0.5 and 5 °C. However, at 10 °C the respiration rate values become comparable between cultivars (Table 6). Comparing between colour level, SH at colour level 3-4 showed the lowest respiration rate at 0.5 °C but had the highest respiration rate when assessed at 5 °C (Table 6). While SC 5-6 cherries at the 5 °C respiration rate assessment temperature showed a significantly lower respiration rate compared to respiration rates measured for SC 3-4 and SC 4-5 cherries at 5 °C (Table 6).

    In 2021, SH and SC respiration rates were more comparable at 0.5 and 10 °C, but at 5 °C, SH respiration rates were higher than SC at the 3-4 and 4-5 colour levels while SC cherries showed a higher respiration rate when assessed at 5 °C compared to the SH cherries at the 5-6 colour level (Table 6). SH respiration rates in 2021 were consistent at 0.5 and 10 °C for all colour levels (Table 6). However, at 5 °C SH cherries at the 5-6 colour level had the lowest respiration rate for all three of the colour levels and the SH cherries at the 3-4 colour level showed the highest respiration rate. This occurred in both 2018 and 2021 (Table 6). The respiration rates of SC cherries were not affected by colour level when assessed at 0.5 °C, but at the 5 °C respiration rate assessment temperature, 2018 SC cherries at 5-6 colour level had lower respiration values (Table 6), while 2021 SC cherries at the 4-5 colour level showed a lower respiration rate value (Table 6). Comparing colour levels, SL cherries at the 5-6 colour level had the highest respiration rates at 0.5 and 10 °C (Table 6). However, at 5 °C, all SL colour levels had comparable respiration values (Table 6). Further, in 2021, all cultivars at 0.5 °C assessment temperature showed respiration rates that were comparable between all colour levels except for SL 5-6. This respiration rate value was significantly higher than the respiration rates measured for the SL 3-4 and 4-5 colour levels and was also higher than the respiration rates determined for SH and SC at the 5-6 colour level. Interestingly, the respiration rate assessed at 0.5 °C for SL at the 5-6 colour level was not significantly different than the respiration rate assessed at 5 °C for SL at the 5-6 colour level (Table 6).

    To further discuss the results presented above, a main source of decreasing TA values in cherries is high respiratory activity[11]. Therefore, linking flavour quality, which is affected by TA levels, to differences in respiration rates is reasonable. Higher respiration rate assessment temperatures were related to higher respiration rates of cherries as seen in Table 6, which was not unexpected and again points to the importance of keeping temperature near 0.5 °C during storage. Additionally, the temperature cherries experience during a growing season affects the respiration rate of the harvested fruit, as Ross et al.[1] found the average temperature and the average high temperature measured in an orchard was positively correlated with the cherry respiration rate at both 5 and 10 °C. Therefore, understanding factors that impact respiration rate, and ensuring cherries are harvested under conditions that ensure a low respiration rate is of significant importance. Table 6 (2021 data) suggests the colour level with the lowest respiration rates for SC cherries is 4-5, which is supported by previous work[1]. While Table 6 (2018 data) suggests the 5-6 colour level gives the lowest respiration rates for SC cherries. When this information is combined with the TA value data, the peak TA values for SC cherries occurs at the 4-5 level and 5-6 colour levels. SH cherries showed that for respiration rate assessed at 0.5 °C, the colour level with the consistently lowest respiration rate was 3-4, but at the 5 °C respiration rate assessment temperature, which is a more abusive temperature, the 5-6 colour level showed the lowest respiration rate in both 2018 and 2021. The highest TA values were seen at the 5-6 colour level for SH cherries. SL cherries show highest TA values at the 3-4 and 4-5 colour level in the 2019 growing year, but insufficient respiration rate data is available in 2019 to comment further. However, the data in Tables 14 indicate that colour is not a reliable indicator of maturity and/or flavor quality. Cherries of the same colour may differ in DM, SS and TA due to cultivar and growing conditions. Figure 1 shows that not all cherries at the same colour level are at the same DM both within and between cultivars. There is a range of DM values for each cultivar in the 3-4, 4-5, and 5-6 colour ranges. However, it is noted the distribution of DM shifted to the right (higher levels) in the 5-6 colour cherries. The work of Palmer et al.[25] and Toivonen et al.[6] have indicated the importance of DM as a fruit quality metric. The implications of colour, DM, and respiration rate results on flavour quality and DM standards are discussed below.

    Associations between colour and DM at harvest with sweet cherry flavour quality attributes and respiration rates were statistically examined using Pearson's correlation coefficient from all available data over all growing years to investigate whether there may be colour/DM levels that are associated with lower respiration rates (Table 7) and could be indicative of when harvest should be performed (i.e. maturity). It was found that colour at harvest was positively correlated with SS at harvest and SS after storage (r = 0.845, p ≤ 0.0005, and r = 0.684, p ≤ 0.005, respectively). Colour at harvest was also positively correlated with DM at harvest (r = 0.768, p ≤ 0.0005). This was expected as darker cherries of a certain cultivar are generally more developed or mature; sugar content (main contributor to DM) and TA increases upon fruit development[1,6,22]. Neither colour or DM at harvest were correlated with SS/TA ratio at harvest or after storage (Table 7). Over all cultivars, no correlation was seen between respiration rate at any assessment temperature and colour level (Table 7). No significant correlations were found between respiration rate assessed at 0.5 and 10 °C and DM (Table 7). A significant negative correlation (r = −0.514, p ≤ 0.025) was found between respiration rate at 5 °C and DM. It was speculated that a correlation between respiration rate and DM was not observed when assessed at 0.5 °C, as this temperature is very low and effectively slows metabolic activity regardless of physiological status of the cherry. No observed correlation between respiration rate assessed at 10 °C and DM was speculated to be due to 10 °C being such an abusive temperature that even physiologically healthy cherries show elevated respiration rates when stored at 10 °C, and likely experienced increased flavour quality deterioration, which could be tested by measuring SS and TA values. Over all cultivars at 5 °C, cherries with lower DM tended to have higher respiration rates, and may be susceptible to more rapid quality deterioration at non-ideal temperatures such as 3−5 °C, which can be encountered in the cherry industry, particularly during export shipping (personal communication, Dr. Peter Toivonen, May, 2021). This points to the importance of good temperature control during storage and diverting lower DM cherries to the domestic and/or rapid consumption market vs export market. Colour was not correlated with TA, while DM at harvest was positively correlated with TA at harvest and upon storage (Table 7), which is relevant for flavour quality. These results indicate that DM has a greater influence on flavour quality attributes than cherry colour.

    Table 7.  Correlations between colour and dry matter at harvest with sweet cherry flavour quality attributes and respiration rate.
    Relationship assessed for Sweetheart*,
    Staccato, and Sentennial**
    cultivars over 2018, 2019,
    and 2021 growing seasons
    Pearson's
    correlation
    coefficient
    Significance
    level
    (p value)
    Colour correlated with
    Soluble solids at harvest r = +0.845 p ≤ 0.0005
    Soluble solids at 28-d storage r = +0.684 p ≤ 0.005
    Dry matter at harvest r = +0.768 p ≤ 0.0005
    Dry matter correlated with
    Soluble solids at harvest r = +0.871 p ≤ 0.0005
    Soluble solids at 28-d storage r = +0.776 p ≤ 0.0005
    Colour at harvest r = +0.769 p ≤ 0.0005
    Titratable acidity at harvest r = +0.439 p ≤ 0.05
    Titratable acidity at 28 d storage r = +0.398 p ≤ 0.10
    Respiration rate at 5 °C r = −0.514 p ≤ 0.025
    Insignificant correlations
    Colour and titratable acidity at harvest r = +0.099 p = 0.696
    Colour and titratable acidity at 28 d storage r = +0.100 p = 0.692
    Colour and soluble solids to titratable
    acidity ratio at harvest
    r = +0.218 p = 0.383
    Colour and soluble solids to titratable
    acidity ratio at 28 d storage
    r = +0.073 p = 0.774
    Colour and respiration rate at 0.5 °C r = +0.252 p = 0.364
    Colour and respiration rate at 5 °C r = −0.206 p = 0.462
    Colour and respiration rate at 10 °C r = +0.084 p = 0.766
    Dry matter and soluble solids to titratable
    acidity ratio at harvest
    r = −0.135 p = 0.595
    Dry matter and soluble solids to titratable
    acidity ratio at 28 d storage
    r = −0.227 p = 0.365
    Dry matter and respiration rate at 0.5 °C r =−0.125 p = 0.657
    Dry matter and respiration rate at 10 °C r = −0.181 p = 0.519
    *Only 2018 and 2019 growing season data available; **only 2019 growing season data available.
     | Show Table
    DownLoad: CSV

    Further, specific cultivar respiration rate and DM relationships were also examined (data not shown). For SH cherries, a negative correlation was determined between respiration rate assessed at 5 °C and DM (p ≤ 0.1), yet this correlation was not seen for SL cherries. Based on statistical parameters SC cherries only showed a negative correlation between respiration rate assessed at 5 °C and DM if a higher p value > 0.1 was used which signifies evidence is not strong enough to suggest a relationship exists. Nevertheless, the statistically significant negative correlation between respiration rate assessed at 5 °C and DM over all cultivars was identified (Table 7).

    Although colour was positively correlated with DM (Table 7), a higher colour may not necessarily indicate a low respiration rate as no significant correlation was observed between colour and respiration rate at any assessment temperature when examined over all cultivars over the growing years tested. Although this highlights the importance of DM in overall quality rather than colour, the data presented thus far suggests certain cultivars achieve different optimal DM values or ranges at maturity that are related to quality retention. In general, higher DM is positive, but is there an upper limit/threshold in terms of higher respiration rate. The lack of correlation between respiration rate assessed at 5 °C and DM for SC and SL cherries seems to indicate a lower optimal DM level for these cultivars compared to SH cherries, as a negative correlation between respiration rate assessed at 5 °C and DM was observed for SH cherries. Again, non-ideal temperatures such as 3−5 °C, can be encountered in the cherry industry, particularly during export shipping, which makes these results extremely relevant to help ensure cherry growers deliver high quality fruit for the export market.

    In 2018, the respiration rate at 5 °C was lowest at the 4-5 and 5-6 colour levels for SH cherries, and the average DM values were ~22% and 25%, respectively. Information from Table 6 shows that 38% of SH fruit were in the 22.5% DM bin indicating the highest percentage of SH cherries at the 4-5 colour level had a DM of 21% to 22.5% while 26% of SH cherries at the 5-6 colour level resided in the 25.5% DM bin indicating the highest percentage of cherries at this colour level had a DM of 24% to 25.5%. For SH cherries in 2021, the lowest respiration rate at 5 °C was at the 5-6 colour level and average DM value was ~23.6%. Information from Table 6 shows that 30% of SH at the 5-6 colour level resided in 24% DM bin indicating the highest percentage of SH cherries at this colour level had a dry mater of 22.5% to 24%. For 2018 SH cherries, titratable acidity, which is important for flavour quality, was highest at the 5-6 colour level where respiration rate assessed at 5 °C was lower. These results imply, that at maturity, cherries tend to a certain DM value or range that corresponds to reduced respiratory activity and promotes quality retention, and would therefore be considered optimal. Based on this data (lower respiration rate (2018 and 2021) and peak TA (2018)), an optimal DM range for SH may be between 22.5%−25% DM or around 23% DM. This optimal DM corresponded to cherries in the 4-5 colour level (21.9%) in 2018, and in the 5-6 colour level (25.2%, 23.6% respectively) in 2018 and 2021.

    2018 respiration rate (assessed at 5 °C) was lowest at the 5-6 colour level for SC cherries and the average DM value was ~22%, respectively. Information from Table 6 shows that 50% of SC cherries resided in the 22.5% DM bin indicating the highest percentage of SC cherries at the 5-6 colour level had a DM of 21% to 22.5% The 2021 respiration rate (assessed at 5 °C) was lowest for SC cherries at the 4-5 colour level and average DM value was ~22% while the highest respiration rate was measured at the 5-6 colour level and the average DM value was ~23.0%. Information from Table 6 shows that 24% and 20% of SC cherries resided in each the 21% and 22.5% DM bins, respectively, indicating the highest percentage of SC cherries at the 4-5 colour level had a DM of 19.5% to 22.5%. For 2021 SC cherries, TA was higher at the 4-5 colour levels, where respiration rate assessed at 5 °C was lowest. Again, these results imply that at maturity cherries tends to a certain DM value or range (optimal) that corresponds to reduced respiratory activity and promotes quality retention. Based on this data (lower respiration rate (2018 and 2021) and peak TA (2018 and 2021)) an optimal DM range for SC may be between 19.5%−22.5% DM or around 22% DM. This optimal DM corresponded to cherries in the 4-5 colour level (22.0%) in 2021, and in the 5-6 colour level (22.4%) in 2018. The data also shows the optimal DM range for SH cherries is higher than the optimal DM range for SC cherries.

    In 2021, for the SL cherries, all colour levels showed the same respiration rate (assessed at 5 °C) and average DM values were 20.5%, 22.6% and 23.5% for the 3-4, 4-5 and 5-6 colour levels, respectively. Information from Table 6 shows that SL cherries at both the 4-5 and 5-6 colour levels, 28% and 24% of the cherries resided in the 22.5% and 24% DM bins indicting the highest percentage of cherries at these colour stages ranged from 21% to 24% DM. For SL, based on the one year of respiration data (2021), determining optimum DM was not as clear. At lower storage temperature (0.5 °C), lower average DM (20.5%−22.6% vs 23.5%) maintained lower respiration rates, but at higher storage temperature (5 and 10 °C) respiration rate did not appear to be affected by DM level. These lower DM values occurred at the 3-4 and 4-5 colour levels.

    Available DM, TA and respiration rate data as discussed suggests the optimal DM range for SH may be between 22.5%−25% DM or around 23% and an optimal dry matter range for SC may be between 19.5%−22.5% DM or around 22% DM, The histogram data over all growing years does further strengthen the justification for suggesting different optimal DM values for different cultivars (Fig. 1). The data over all growing years shows higher proportions of cherries in the 24 % DM bin for SH cherries at the 5-6 colour level which indicated highest proportion of cherries with a DM of 22.5% to 24%. The SC cherries at the 5-6 colour level showed the highest proportion of cherries in the 22.5% DM bin, which indicates the highest percentage of cherries have a DM of 21% to 22.5%; again these DM ranges have been suggested as optimal DM values based on previously discussed respiration data.

    In psychology self-actualization is a concept regarding the process by which an individual reaches their full potential[31]. The data suggests that sweet cherries self-actualize, with the majority of cherries reaching maturity with a DM range that promotes quality retention during storage when growing conditions are favourable. This optimal DM range is different for different cultivars, and growing conditions would be expected to influence the rate and/or ability of this 'self-actualization', as this work and our previous research has shown that environmental factors are correlated with these important quality characteristics[1]. Placing highest importance on distribution of DM levels at the 5-6 colour levels (Fig. 1) is justified as the cherries are the most physiologically mature and will likely exhibit the highest proportion of cherries with optimal DM; however, the optimal DM can occur at other colour ranges and should be used as the primary indicator of maturity. Maturity at harvest is the most important factor that determines storage-life and final fruit quality assweet cherries produce very small quantities of ethylene and do not respond to ethylene treatment; they need to be picked when fully ripe to ensure good flavour quality[32]. It is noted the CTFIL colour standard series goes up to colour level 7, yet a balance needs to be reached between flavour quality optimization vs other quality parameters such as firmness and stem pull force. Supplementary Tables S1S6 provide values of the quality parameters of firmness, stem pull force, stem shrivel, stem browning, pebbling and pitting levels at harvest and after storage for the SH, SC and SL cherries. All of these cherry cultivars exhibited good quality attributes at the 5-6 colour level, as well as lighter colour ranges.

    It is noted that the development of DM standards for different cultivars is a novel concept. This work was positioned as field work that collected cherry data for three cultivars over three growing years in adjacent orchards using the same management practices. Equipment constraints limited respiration rate data collection. As such absolute optimal DM values and/or ranges could not be determined nor was the goal of this study. The goal of this work was to further the concept that different cultivars may reach maturity at different DM levels, which would result in lower respiration rates and higher TA levels at harvest, and after storage, achieving enhanced quality retention. In this regard, absolute optimal DM would be the DM achievable by a cherry cultivar that maximizes flavour attributes and minimizes respiration under ideal conditions. In reality, the absolute optimal DM may or may not be reached during a growing season depending on environmental conditions and orchard management practices; however, cherry cultivars will reach a DM that will be optimal for the growing conditions at harvest maturity, as the present research demonstrates. Developing definitive DM standards to determine optimal harvest points for different cultivars under different environmental conditions should be a direction of research to be further pursued to ensure cherry quality, particularly for cherries subjected to longer term storage and/or cherries destined for the overseas export market.

    The present work is not the first to point to the importance of DM and cherry flavour retention, as an anecdotal report[33] indicated that SH cherries should be harvested at a DM of no higher than 20% or the fruit will lose both sugar and acidity more rapidly during shipping storage. Although this DM value is lower than the DM recommended for SH in the current work, it indicates the importance of DM level and flavour quality in relation to a specific cultivar. The differences between optimal DM for flavour retention in our work and the anecdotal report signifies the complexity of determining DM standards and the impact of growing year/environmental conditions and orchard management practices on optimal DM. Growers will continue to face these complex issues but the present work provides valuable information to growers regarding DM standards for three cultivars.

    It must be noted again that development of absolute DM standards for different cherry cultivars requires more study under rigorous controlled environmental conditions. Additionally, given the impact of environmental conditions on optimal DM, cultivars of interest must be studied over many growing years and orchard conditions to collect a robust data set. Nevertheless, the present research indicates that SH, SC, and SL cultivars have different dry matter values at maturity. The data also shows the DM range for SH cherries at maturity is higher than the DM range for SC cherries at maturity and that for SL, lower DM levels maintained lower respiration rates at lower temperatures, potentially improving ability to maintain quality after harvest.

    Overall, this research showed that DM was a better indicator of flavour quality than colour, as DM was related to both sugars and TA, while colour was only related to sugar. Therefore, this work identified that colour may not be a reliable indicator of maturity and/or flavor quality. This work indicated that cherries of the same colour may differ in DM, SS, and TA due to cultivar type and growing conditions as influenced by growing year. Relative humidity encountered by cherries during the growing season was negatively correlated with TA and higher growing temperatures were positively correlated with TA. This work discovered that sweet cherries may self-actualize, in that when growing conditions are favourable, DM levels may tend towards a certain level at maturity (optimal DM) resulting in superior flavour quality attributes and lower respiration, allowing cherries to reach their full quality potential and ensure quality retention in storage. Therefore, optimal DM can be reached at maturity despite colour. Remaining challenges include development of DM standards for various sweet cherry cultivars and further understanding the impact of growing conditions to better allow for self-actualization and prediction of the optimal DM under those conditions to optimize timing of harvest from year-to-year. Nevertheless, this research based on field work for three sweet cherry cultivars over three growing years, indicated an optimal DM range for SH between 22.5%−25% DM and an optimal DM range for SC between 19.5%−22.5% DM. Interestingly, under the same field conditions, the optimal DM range for SH cherries was higher than the optimal DM range for SC cherries. More analysis is required for determining optimal DM for SL, but the initial data indicates DM in the range of 20.5% to 22.6% maintained lower respiration rates at lower temperature potentially improving ability to maintain quality after harvest.

    The authors confirm contribution to the paper as follows: study conception and design: Ross KA, DeLury NC, Fukumoto L; data collection: Ross KA, DeLury NC, Fukumoto L; analysis and interpretation of results: Ross KA, DeLury NC, Fukumoto L; draft manuscript preparation: Ross KA, DeLury N, Fukumoto L, Forsyth JA. All authors reviewed the results and approved the final version of the manuscript.

    The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

    We are grateful to the BC Cherry Association for financial support of this research project. We acknowledge Manon Gentes, Gillian Beaudry, and Duncan Robinson for their technical assistance. We are grateful to Brenda Lannard for providing her expertise on using the Felix F750 handheld spectrometer (Felix Instruments, Inc.) to obtain dry matter values and obtaining respiration data. Kelly A. Ross would like to thank and acknowledge Dr. Peter Toivonen for his mentorship, valuable scientific discussions and consistently kind support.

  • The authors declare that they have no conflict of interest.

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  • Cite this article

    Wang G, Wang L, Yu M, Wu D, Lu L, et al. 2024. Continuous monoculture of Xanthoceras sorbifolia Bunge leads to continuous cropping challenges due to fungal pathogen accumulation and reduced beneficial bacteria abundance. Fruit Research 4: e040 doi: 10.48130/frures-0024-0034
    Wang G, Wang L, Yu M, Wu D, Lu L, et al. 2024. Continuous monoculture of Xanthoceras sorbifolia Bunge leads to continuous cropping challenges due to fungal pathogen accumulation and reduced beneficial bacteria abundance. Fruit Research 4: e040 doi: 10.48130/frures-0024-0034

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Continuous monoculture of Xanthoceras sorbifolia Bunge leads to continuous cropping challenges due to fungal pathogen accumulation and reduced beneficial bacteria abundance

Fruit Research  4 Article number: e040  (2024)  |  Cite this article

Abstract: Xanthoceras sorbifolium Bunge, a unique oil crop native to northern China, has a long history of cultivation. In this study, X. sorbifolium Bunge was continuously planted in Zibo and Weifang, Shandong Province, to explore the factors that cause a decline in X. sorbifolium Bunge yield and fruit quality after long-term continuous planting. The results showed that the continuous cropping of X. sorbifolium Bunge led to a significant decrease in the biomass of the plant's seedlings, markedly reduced the root activity, and reduced the soil nutrient content. A significant change in the soil microbial community structure was observed after years of X. sorbifolia Bunge monoculture. At the genus level, the relative abundance of soil pathogenic fungi, such as Neocosmospora, Aspergillus, and Penicillium, significantly increased after continuous cropping, with the relative abundance of Neocosmospora increasing significantly in the three study sites. The abundance of common soil bacterial genera, such as Mortierella, Bacillus, and Streptomyces, is significantly lower under continuous cropping than in regular soil. The number of soil-specific bacteria was also reduced. The results showed that the accumulation of fungal pathogens, particularly Neocosmospora, may be the main challenge in the continuous cropping of X. sorbifolium Bunge, as it reduces the abundance of beneficial bacteria, primarily Bacillus, Streptomyces, and Mortierella.

    • Xanthoceras sorbifolium Bunge is a small deciduous tree or shrub of the Xanthoceras genus in the Sapindaceae family. This species is a woody oil tree unique to China and produces excellent raw material for manufacturing biodiesel[1]. In addition, this plant is used to produce high-grade edible oil[2]. The oil content of the seed kernel is high (45.54%−56.26%), and it is rich in unsaturated fatty acids, which has high nutritional value and is beneficial to human health[3]. X. sorbifolia Bunge is rich in phytosterols, tocopherols, fatty acids, and rare organic acids involved in nervous system development[4]. Consequently, X. sorbifolia Bunge oil has extremely high nutritional value and health benefits. The use of this species in various fields has significantly increased the demand for X. sorbifolia Bunge oil. Moreover, this species is an excellent biomass energy source, ornamental tree species, and barren hill greening tree species. Therefore, it is widely cultivated in over ten provinces and cities, such as Inner Mongolia, Shanxi, and Hebei[5]. The cultivation area of X. sorbifolia has increased from 1.33 × 105 to 2.6 × 105 ha due to its significant economic value[68]. However, the monoculture of X. sorbifolium Bunge is adopted without any rotation due to the increasing scarcity of land and the impacts of agricultural industrialization. This practice is prevalent in China, resulting in poor growth after years of continuous planting.

      Continuous planting of crops often leads to the occurrence of replanting diseases. Furthermore, repeated monoculture leads to reduced plant strength, low yield, poor fruit quality, increased risks of pests and diseases, and death of the trees[9]. Wang et al.[10] observed that the Fusarium pathogen caused apple replanting disease in the Bohai Bay area of China. Allelopathic autotoxic substances such as amygdalin and benzoic acid are observed in the soil of aged peach orchards and significantly inhibit the growth of replanted plants[11]. Qin et al.[12] reported that amygdalin, an allelotoxic substance in old cherry orchard soil, significantly inhibits the growth of replanted plants. These findings indicate that the production of allelopathic substances, changes in the soil's physicochemical properties, an imbalance in soil nutrients, and changes in the soil microbial community structure increase the risk of diseases and poor plant growth characteristics[13]. Notably, the replanting challenges are not caused by a change in a single factor but by an interaction between soil, environmental, and plant-related factors[1416]. Soil microorganisms are involved in soil nutrient transformation and soil structure stability, affecting plant growth[17]. Multiple factors cause a decrease in yield and increased risk of diseases in continuously cropped X. sorbifolium Bunge. Notably, replanting challenges in some crops are caused by changes in the soil microbial community, with changes in the soil fungal community structure as the primary factor[18]. The total bacterial abundance decreased under continuous monoculture tobacco, and the soil bacterial community structure changed significantly[19]. Continuous cropping of cucumber increases soil Fusarium abundance and the occurrence of cucumber Fusarium wilt, affecting cucumber production globally[17]. Konjac soft rot caused by Pectinobacillus causes significant losses to Konjac farming annually due to the continuous cultivation of this crop. This bacteria is the main challenge in the Konjac industry worldwide[20]. Li et al. observed that the continuous cropping of peanuts markedly reduced the crop quality and yield. A previous study demonstrated that the accumulation of fungal pathogens in the soil increases the occurrence of continuous cropping diseases in peanuts at the expense of plant-beneficial fungi[21].

      Increased occurrence of diseases and pests in continuous monoculture farming[22] has prompted the development of various strategies, such as chemical treatments, crop variety selection, and biological control methods, to increase crop yields and minimize continuous cropping challenges[2326]. Examples include using beneficial microorganisms for biological control and the application of Rhizobia and arbuscular mycorrhizal fungi (AMF) to mitigate replanting diseases in various crops and enhance crop yield[27]. Bacillus cereus WL08 effectively breaks down the autotoxic substances of pinellia, significantly improving the photosynthesis, growth, yield, and quality of the plant[28]. Ceratobasidum stevensi effectively increases the watermelon growth rate, enhances the activity of key defense enzymes, modulates the soil microbiome, and alleviates watermelon repeated cropping challenges[29]. However, the failure to effectively prevent continuous cropping challenges is mainly due to a lack of understanding of the underlying mechanisms. X. sorbifolium Bunge is an important oil woody crop. However, only a few studies have explored the challenges associated with the replanting of X. sorbifolium Bunge.

      In this study, the effects of continuous planting of X. sorbifolium Bunge on soil physicochemical properties and soil microbial community structure in different areas was examined. The purpose of this study is to analyze the relative abundance and structure of soil microbial community after continuous planting of X. sorbifolia Bunge in high-throughput sequencing, with a single planting site as the control, and to further explore the mechanism of yield reduction caused by continuous cropping obstacles of X. sorbifolium.

    • The experimental materials were collected from Xilao Village (36°99' N, 118°28'E), Fenghuang Town, Linzi District, Zibo City, Shandong Province (China), the altitude is 69 m; Hengdi Village, Changyi City, Weifang City (36°99' N, 119°39' E), the altitude is 55 m; and Meiyu Village, Huiqu Town, Anqiu City, Weifang City (36°27' N, 119°01' E), the altitude is 23 m, during the cropping season in 2022. Red Xanthoceras sorbifolium varieties were used for the experiments.

    • Anqiu, Weifang (AQ), Linzi, Zibo (LZ), and Changyi, Weifang (CY) were selected as the study sites. Twenty-year-old Red X. sorbifolium orchards continuously planted Red X. sorbifolium seedlings were used as the cropping samples (AQCK, LZCK, and CYCK). The land adjacent to the old orchards, without Red X. sorbifolium seedlings was used as the control group (AQ, LZ, and CY). The continuous cropping and control treatments were compared separately for each region. Healthy 3–4-leaves seedlings exhibiting consistent growth and no pests or diseases were transplanted in mid-April, with 20 replicates per treatment used for each study site[30]. The roots of the seedlings were washed before planting to minimize the presence of microorganisms in the roots.

      Three plants were randomly selected for each treatment to represent three biological replicates. Topsoil within 30 cm of the trunk was removed by digging 0–5 cm deep, lightly attached to roots removed, tightly attached soil collected with a sterile bristle brush, and filtered out of the soil impurities with a 2 mm screen. Subsequently, the soil samples were divided into three portions[30]. Two portions of the samples were stored at 4 °C and −80 °C. Using fresh samples stored at −80°C for soil DNA extraction, high throughput sequencing. The third portion was air-dried to determine soil physicochemical properties and evaluation of soil-related indicators. The plant tissue samples were stored under low-temperature conditions in liquid nitrogen during the study to ensure the tissue activity was effectively preserved.

    • Sampling was conducted in May, June, and July. During sampling, the plant height and stem diameter of the plants were measured using a tape measure and a Vernier caliper, respectively.

    • The 2,3,5-triphenyltetrazolium chloride (TTC) method was used to evaluate the seedling root activity. The procedure for assessment of root activity was adopted from a study by Liu et al.[31].

    • Soil organic matter was evaluated using the organic potassium dichromate volumetric method. The contents of ammonium nitrogen and nitrate nitrogen (NH4+-N and NO3-N) were assessed using the CaCl2 extraction flow injection analyzer method. The level of available phosphorus (P2O5) was determined by the molybdenum–antimony resistance colorimetric method. The amount of available potassium (K2O) was evaluated with flame spectrophotometry. Soil physicochemical properties were evaluated following methods described by Bao[32].

    • Total DNA was extracted from each soil sample using the E.Z.N.A. Soil DNA Kit (Omega Bio-tek Inc., Norcross, GA, USA) according to the manufacturer's protocols. The quality of soil DNA extraction was detected by 1% agarose gel electrophoresis, and the samples were sent to Majorbio Bio-pharma Technology Co., Ltd. (Shanghai, China) for testing. High-throughput sequencing was performed to explore soil fungi and bacteria structure and abundance. Amplification was performed using universal primers 338F/806R and ITS1F/ITS2R for bacteria and fungi. Soil microbial community structure analysis was conducted following methods described by Bennett et al. and Wang et al.[33,34].

    • All data were expressed as the mean ± standard deviation of three replicates. Microsoft Excel was used for data processing. Graphs were generated using GraphPad Prism 8.0 (San Diego, CA 92108, USA). Statistical analysis was conducted using SPSS 26.0 software. T-test or one-way ANOVA was used to explore differences between the groups. p < 0.05 indicated statistically significant differences between groups.

    • The results showed that the biomass of X. sorbifolium Bunge was significantly lower in seedlings planted in soils from areas under repeated cropping compared to those grown in soil under regular cropping (Fig. 1). The plant height and stem diameter of the seedlings planted in July, August, and September in the AQ region were significantly inhibited by continuous cropping compared to the control group.

      Figure 1. 

      Effects of continuous cropping on seedling biomass of X. sorbifolium Bunge planted in different regions. A t-test was used to determine the significant differences between the two treatment groups. Data in the box plots are expressed as mean ± SE. AQ: Untreated soil in Anqiu; AQCK: Continuous planting of X. sorbifolium Bunge in Anqiu; LZ: Untreated soil in Linzi; LZCK: Continuous planting of X. sorbifolium Bunge in Linzi; CY: Untreated soil in Changyi; CYCK: Continuous planting of X. sorbifolium Bunge in Changyi. Significant differences are presented as follows: * 0.01 ≤ p < 0.05, ** 0.001 < p ≤0.01, and *** p ≤ 0.001.

    • The results demonstrated that the root activity of the X. sorbifolium Bunge planted in continuous cropping soil was significantly lower compared to plants planted in regular cropping soil (Table 1). The AQ, LZ, and CY soils exhibited significantly higher root activity than the continuous cropping soil. The root activity of seedlings planted in the regular soil was significantly different compared to that of seedlings planted in continuous cropping soil in the CY region. The root activity of the seedlings planted in continuous cropping soil in the CY region decreased by 57.8% compared to the seedlings in the regular soil.

      Table 1.  Root activity of crown fruit in different regions.

      AQ
      (μgTTF·g−1·h−1)
      LZ
      (μgTTF·g−1·h−1)
      CY
      (μgTTF·g−1·h−1)
      T1 13.46 ± 0.68** 14.59 ± 1.68* 15.73 ± 0.50***
      CK 7.40 ± 0.54 7.21 ± 0.83 6.64 ± 0.50
      A t-test was used to determine the significant differences between the two treatment groups. Data in the table are expressed as mean ± SE. T1 represents untreated soil; CK denotes continuous planting of X. sorbifolium Bunge. Significant differences are presented as follows: * 0.01 ≤ p < 0.05, ** 0.001 < p ≤ 0.01, and *** p ≤ 0.001.
    • Analysis of the soil physicochemical properties in the three regions showed that continuous cropping of X. sorbifolium Bunge significantly reduced the available potassium content in the soil (Table 2). Notably, the available potassium levels in the CY area showing the most significant decline, with a 49.82% decrease compared to the regular soil. The three regions exhibited a reduction in available phosphorus content, with the most significant decrease observed in the AQ area at 43.63%. Notably, the difference in the amount of available phosphorus between the two treatment groups in the CY area was not significant. The contents of nitrate nitrogen and ammonium nitrogen decreased significantly in the three regions. Continuous cropping of X. sorbifolium Bunge significantly decreased the soil nitrogen content compared to the regular soil. The soil organic matter content decreased significantly after years of X. sorbifolium Bunge planting. The most significant decrease in soil organic matter content was observed under continuous cropping in the LZ area, with a 27.54% decrease compared to the regular soil.

      Table 2.  Soil physicochemical properties in different areas.

      Treatment Organic matter
      (g·kg−1)
      Nitrate nitrogen
      (mg·kg−1)
      Ammonium nitrogen
      (mg·kg−1)
      Available phosphorus
      (mg·kg−1)
      Available potassium
      (mg·kg−1)
      AQ 10.58 ± 0.20* 1.23 ± 0.00** 0.09 ± 0.00** 1.13 ± 0.06*** 16.79 ± 0.11***
      AQCK 9.47 ± 0.19 0.23 ± 0.01 0.06 ± 0.00 0.75 ± 0.01 14.56 ± 0.56
      LZ 11.62 ± 0.20*** 0.32 ± 0.01*** 0.10 ± 0.00** 0.10 ± 0.01** 15.13 ± 0.09**
      LZCK 8.42 ± 0.37 0.14 ± 0.00 0.08 ± 0.00 0.86 ± 0.01 13.54 ± 0.17
      CY 10.59 ± 0.19** 0.27 ± 0.01** 0.09 ± 0.01*** 1.24 ± 0.03* 12.81 ± 0.03***
      CYCK 9.34 ± 0.07 0.17 ± 0.01 0.08 ± 0.01 1.06 ± 0.03 8.50 ± 0.20
      A t-test was used to determine the significant differences between the two treatment methods. Data in the table are expressed as mean ± SE. AQ: Untreated soil in Anqiu; AQCK: continuous planting of X. sorbifolium Bunge in Anqiu; LZ: Untreated soil in Linzi; LZCK: Continuous planting of X. sorbifolium Bunge in Linzi; CY: Untreated soil in Changyi; CYCK: Continuous planting of X. sorbifolium Bunge in Changyi. Significant differences are denoted as follows: * 0.01 ≤ p < 0.05, ** 0.001 < p ≤ 0.01, and *** p ≤ 0.001.
    • The soil enzyme activities significantly differed between the regular soil and continuous cropping soil in the three regions. AQ, LZ, and CY soils exhibited a significant decrease in urease activity under continuous cropping compared to the regular soil (Fig. 2ac). The urease activity under the continuous cropping treatment in the CY region was significantly (29.20%) lower compared to the regular cropping soil. Soil sucrase activity was significantly lower under the continuous cropping treatment in the three regions, with 18.24%, 22.55%, and 31.03% decreases compared to the regular cropping soil (Fig. 2df). The phosphatase activity was significantly lower under the continuous cropping treatment compared to the regular soil. The continuously cropped X. sorbifolium Bunge induced the most significant decrease in soil phosphatase activity in the CY area, with a 32.73% decrease relative to the regular soil (Fig. 2gi). Catalase activity decreased after the continuous cropping of X. sorbifolium Bunge compared to the regular soil treatment (Fig. 2jl).

      Figure 2. 

      Soil enzyme activities in different regions. AQ: Untreated soil in Linzi; AQCK: Continuous planting of X. sorbifolium Bunge in Linzi; LZ: Untreated soil in Cangyi; LZCK: Continuous planting of X. sorbifolium Bunge in Cangyi; CY: Untreated soil in Anqiu; CYCK: Continuous planting of X. sorbifolium Bunge in Anqiu. T-test analysis was conducted to determine the significant differences between the two treatment methods. Data are expressed as mean ± SE. Significant differences are represented as follows: * 0.01 ≤ p < 0.05, ** 0.001 < p ≤ 0.01, and *** p ≤ 0.001.

    • The compositions of bacterial genera with relative abundances greater than 0.5% were evaluated (Fig. 3a, d). Continuous cropping of X. sorbifolium Bunge in the AQ area significantly affected the horizontal relative abundance of soil bacteria. The average relative abundance of Bacillus, Streptomyces, and Blastococcus in the soil decreased significantly, whereas the relative abundance of Gaiella, Rubrobacter, and Arthrobacter increased significantly after continuous cropping of X. sorbifolium. The average relative abundance of Aeromicrobium (p < 0.05) and Lysobacter (p < 0.05) in the AQCK group significantly increased compared to the AQ treatment (Fig. 3e). The average relative abundance of Chujaibacter (p < 0.001) decreased significantly after continuous cropping of X. sorbifolium Bunge. The abundance of Bacillus (p < 0.05), Streptomyces (p < 0.05), Rubrobacter (p < 0.05), and Amycolatopsis (p < 0.05) also decreased significantly in the AQCK group relative to the AQ treatment.

      Figure 3. 

      Effects of continuous cropping of X. sorbifolium Bunge on soil bacterial community structure in the AQ area. (a) Horizontal abundance analysis of bacterial genera; (b) PCoA plot showing the distribution of bacteria genera; (c) Venn diagram showing the distribution of bacterial species; (d) A heat map showing the bacterial community composition; (e) Bacterial community differences at the genus level between the treatment groups. AQ: Untreated soil in Anqiu; AQCK: Continuous planting of X. sorbifolium Bunge in Anqiu.

      Venn diagram analysis (Fig. 3c) of soil microorganisms showed that the number of soil bacterial OTU species changed after continuous planting of crown fruit. The results showed 31 endemic species in the regular soil and 77 unique bacterial species were observed under the continuous cropping treatment. The soil bacterial OTU profile markedly changed after continuous cropping.

      PCoA of the soil bacteria (Fig. 2b) showed that the continuous cropping soil treatment formed a distinct cluster away from the AQCK treatment, exhibiting different quadrants. These findings indicate that the continuous cropping treatment significantly changed the diversity of the soil bacterial community compared to the control treatment. The PC1 and PC2 values were 31.84% and 29.78%, explaining 61.62% of the bacterial diversity differences.

    • The continuous planting of X. sorbifolium Bunge in the AQ region significantly affected the soil fungal community (Fig. 4ae). Aspergillus genus exhibited the highest abundance in the AQ region, followed by Solicoccozyma, Chaetomium, Mortierella, and Penicillium (Fig. 4a). The abundances of Aspergillus, Fusarium, Penicillium, and Neocosmospora were significantly higher in the continuous cropping soil compared to the regular soil. Conversely, the relative abundances of Mortierella, Kernia, Solicoccozyma, and Coniochaeta were higher in the AQCK treatment than in the AQ treatment. The results demonstrated that the average relative abundance of some soil fungi genus decreased significantly after continuous cropping, whereas the average relative abundance of Mortierella increased significantly (p < 0.05; Fig. 4e). The relative abundances of Coniochaeta (p < 0.05) and Trichoderma (p < 0.05) were significantly higher in the AQCK treatment relative to the AQ treatment. At the phylum level, the relative abundance of Ascomycota, Monoblepharomycota, and Glomeromycota decreased significantly after continuous cropping relative to the regular soil treatment (Fig. 4d).

      Figure 4. 

      Effects of continuous cropping of X. sorbifolium Bunge on soil fungal community structure in the AQ area. (a) Horizontal abundance of fungi at the genus level; (b) PCoA plot illustrating fungi distribution under the two treatments; (c) Venn diagram showing the distribution of fungal OTU species; (d) A heat map showing fungal community composition; (e) Differences in the fungal horizontal community between the two treatment groups. AQ: Untreated soil in Anqiu; AQCK: Continuous planting of X. sorbifolium Bunge in Anqiu.

      A Venn diagram based on the abundance of soil microorganisms showed that the number of OTU species of soil fungi was significantly affected after continuous planting of X. sorbifolium Bunge (Fig. 4c). The results revealed 336 endemic species in the regular soil and 468 species of unique fungi species in the AQCK treatment. Notably, 28.21% more endemic fungi were observed under the continuous cropping treatment relative to the AQ treatment.

      PCoA showed that the fungi under the continuous cropping soil treatment clustered distantly from the regular soil treatment and in different quadrants (Fig. 4b). This finding indicates that the continuous cropping soil treatment significantly changed the structure and composition of the soil fungal community compared with the control treatment. The values of PC1 and PC2 were 51.30% and 24.61%, explaining 75.91% of the fungal diversity difference between the groups.

    • Continuous cropping of X. sorbifolium Bunge significantly changed the community structure and abundance of soil bacteria and microorganisms in LZ. At the genus level, Bacillus, Gaiella, and Streptomyces were the dominant genera with significantly higher relative abundance under the continuous cropping soil treatment compared to the regular soil. The abundance of Norank_f_geminicoccaceae and Solirubrobacter was lower in the LZ treatment than in the LZCK treatment (Fig. 5a). Further analysis showed that the abundance of Gaiella (p < 0.05) and MnD1 (p < 0.05) were significantly higher in the continuous cropping soil than in the regular soil (Fig. 5e). In addition, the relative abundances of Blastococcus (p < 0.001), Sphingomonas (p < 0.01), and Solirubirobacter were significantly higher in the continuous cropping soil than in the regular soil. At the phylum-level analysis, the relative abundances of Fibrobacterota, Sumerlaeota, and Patescibacteria in the LZCK treatment were significantly lower compared to the LZ treatment (Fig. 5d). Conversely, the relative abundances of Dependentiae, Methylomirabilota, and Acidobacteriota were significantly higher in the regular cropping soil relative to the LZCK treatment (Fig. 5d).

      Figure 5. 

      Effect of continuous cropping of X. sorbifolium Bunge on soil bacterial community structure in the LZ area. (a) Horizontal abundance of bacterial genera; (b) Bacterial PCoA illustrating the distribution of bacteria genera under the two treatments; (c) Venn diagram analysis showing differences in bacterial species under the two treatments; (d) A heat map showing bacterial community composition under the two treatments; (e) Community differences at the bacterial genus level between the two groups. LZ: Untreated soil in Linzi; LZCK: Continuous planting of X. sorbifolium Bunge in Linzi.

      Venn diagram analysis revealed that the continuous cropping of X. sorbifolium significantly changed the soil fungal OTU species, with the endemic bacteria increasing by 30.16% under the continuous cropping soil relative to the control treatment in the LZ region (Fig. 5c).

      PCoA demonstrated a significant distance between the soil bacteria under the regular soil treatment and the continuous cropping treatment, with bacteria under the two treatments clustering in different quadrants (Fig. 5b). These findings indicate that the continuous cropping treatment significantly changed the diversity of the soil bacteria community compared to the regular soil treatment. The value for PC1 was 50.99%, whereas the PC2 value was 20.69%, explaining 71.68% of the bacterial diversity difference.

    • The soil fungal microbial community structure in the fungus LZ region changed significantly after long-term continuous cropping of X. sorbifolium Bunge. Chaetomium, Neocosmospora, Mortierella, Humicola, and Penicillium were the most abundant fungi genera in the soil samples from LZ (Fig. 6a). At the genus level, the relative abundance of Neocosmopora, Humicola, Penicillium, and Pyrenochaetopsis was significantly higher in the continuous cropping soil than in the LZ treatment. The relative abundance of Mortierella and Solicoccozyma was significantly higher in the regular cropping soil than in the LZCK (Fig. 6a). T-test analysis showed that the relative abundance of Mortierella (p < 0.05) and Acremonium (p < 0.01) was significantly higher in the regular cropping soil than in the LZCK treatment. Conversely, the relative abundance of Neocosmopora (p < 0.01), Humicola (p < 0.05), and Penicillium (p < 0.05) was lower in the regular cropping soil compared to the LZCK treatment. At the phylum level, the relative abundances of Ascomycota, Basidiomycota, and Chytridiomycota were significantly higher under the LZCK treatment than in the LZ treatment (Fig. 6d).

      Figure 6. 

      Effects of continuous cropping of X. sorbifolium Bunge on soil fungal community structure in the LZ area. (a) Horizontal abundance of fungi at the genus level; (b) PCoA showing fungal distribution; (c) Venn diagram analysis of fungal OTU species; (d) A heat map showing fungal community composition under the two treatments; (e) Differences in fungal horizontal community between two treatment groups. LZ: Untreated soil in Linzi; LZCK: Continuous planting of X. sorbifolium Bunge in Linzi.

      Venn diagram analysis showed that the continuous cropping of X. sorbifolium Bunge significantly influenced the number of soil fungal species in the LZ region. The relative abundance of fungal species increased by 28.63% in the continuous cropping soil compared with the regular soil. PCoA of the soil fungi revealed that the LZ treatment clustered distantly from the LZCK treatment and in different quadrants (Fig. 6b). These results indicate that the LZCK treatment significantly changed the diversity of the soil fungi community compared with the LZ treatment. The values of PC1 and PC2 were 61.08% and 20.25%, explaining 81.33% of the fungal diversity differences.

    • At the genus level, the bacterial community structure and abundance exhibited significant differences between the regular cropping soil and continuous cropping soil in the CY region. The relative abundance of Bacillus, Sporomonas, and Streptomyces was significantly higher in the CY treatment compared to the CYCK treatment. Notably, Bacillus, Sporomonas, and Streptomyces were the most dominant genera in the CY area. The t-test results showed that the relative abundance of Bacillus (p < 0.05), Streptomyces (p < 0.01), and _TK10 (p < 0.01) was significantly higher under the CY treatment than in the CYCK treatment. At the phylum level, the relative abundance of Armatimonadota increased, whereas Deferrisomatota abundance decreased in the CYCK treatment relative to the regular cropping soil (Fig. 7d).

      Figure 7. 

      Effect of continuous cropping of X. sorbifolia Bunge on soil bacterial community structure in the CY area. (a) Horizontal abundance and distribution of bacterial genera; (b) PCoA plot showing bacterial distribution under the two treatments; (c) Venn diagram analysis of bacterial species distribution; (d) A heat map showing bacterial community composition; (e) Community differences at the bacterial genus level between the two treatment groups. CY: Untreated soil in Changyi; CYCK: Continuous planting of X. sorbifolium Bunge in Changyi.

      PCoA of the soil bacteria demonstrated that the bacteria under the CYCK treatment clustered away from the CY treatment and in different quadrants (Fig. 7b). This finding indicates that the CYCK treatment significantly changed the diversity of the soil bacterial community compared to the control. PC1 and PC2 values were 53.61% and 17.71%, explaining 71.32% of the bacterial diversity difference. Venn diagram analysis showed that the number of unique species in the soil bacterial community decreased significantly after the continuous cropping of X. sorbifolium Bunge, exhibiting a 59.84% decrease compared to the regular soil (Fig. 7c).

    • The classification results showed that Tausonia, Neocosmospora, Mortierella, Penicillium, and Solicoccozyma were the top five fungal genera in the CY area. The relative abundance of these genera was significantly lower in the CYCK treatment compared to the CY treatment (Fig. 8a). The relative abundance of Talaromycetes was markedly higher (p < 0.001) in the CYCK treatment compared to the abundance in the regular soil. The relative abundances of Clonostachys (p < 0.01), Chordomyces (p < 0.05), and Mrakia (p < 0.05) genera were significantly higher in abundance in the CYCK treatment compared to the regular soil. At the phylum level, the relative abundance of Cladosporium and Glomus was lower under the CY treatment than the CYCK treatment. Conversely, the relative abundance of Ascomycota and Mortierellomycota increased significantly in the CY treatment than the CYCK treatment (Fig. 8d).

      Figure 8. 

      Effects of continuous cropping of X. sorbifolium Bunge on soil fungal community structure in CY area. (a) Relative abundance of fungi under the two treatments; (b) PCoA plot showing the fungal distribution under the two treatments; (c) Venn diagram showing the distribution of fungal OTU species; (d) A heat map showing fungal community composition in the two groups; (e) Differences in the fungal horizontal community between the two treatment groups. CY: Untreated soil in Changyi; CYCK: Continuous planting of X. sorbifolium Bunge in Changyi.

      PCoA of the relative abundance of soil fungi showed distinct clustering of the fungi under CY treatment at different quadrants from the CYCK treatment (Fig. 8b). These results indicate that the CYCK treatment significantly changed the diversity of the soil fungi community compared with the CY treatment. The PC1 and PC2 values were 56.69% and 17.16%, explaining 73.85% of the fungal diversity difference. Venn diagram analysis of the soil OTU level revealed significant differences in fungal microbial species between the two treatments, with only 280 common microbial species (Fig. 8c).

    • The influence of continuous cropping on soil microbial communities was primarily reflected in the weakening of interactions between microbial communities. The effect of continuous cropping of X. sorbifolium Bunge on soil microbial interactions was explored by constructing a microbial co-occurrence network (Fig. 9). Co-occurrence network analysis showed that different phyla in the same family appeared in different co-occurrence networks, indicating that they exhibit different relative abundances and play different network roles. Co-occurrence network analysis of soil bacteria demonstrated that Proteobacteria accounted for a higher proportion and played a more significant role in the interaction network (Fig. 9a). Notably, the proportion of Proteobacteria in soil increased significantly after the continuous cropping of X. sorbifolium Bunge, and the interactions across the bacterial communities at the phylum levels were closer. The abundance ratio of Gammaproteobacteria, Myxococcia, Chloroflexia, and other bacteria decreased after continuous cropping, with decreased interactions. Co-occurrence network analysis of soil fungi demonstrated that Basidiomycetes was the most dominant soil microbial phyla before and after the continuous cropping of X. sorbifolium Bunge (Fig. 9b). However, after continuous cropping, the interactions of the soil fungal communities became closer, the abundance of fungi increased, and the abundance of Mortierellomycota decreased. In addition, the importance of Mortierellomycota in the interactions of soil fungi decreased after continuous cropping.

      Figure 9. 

      Soil microbial OTU co-occurrence network ((a) bacteria, (b) fungi) for the continuously cropped X. sorbifolium Bunge based on Spearman's coefficient. Each point represents a genus, the color indicates the bacterial or fungal phylum, and the size of the point represents the relative abundance. T: Untreated soil; CK: Continuous planting of X. sorbifolium Bunge. Species information with an absolute value of correlation coefficient greater than or equal to 0.6, p < 0.05 for the two treatment conditions is displayed.

    • Bacterial RDA showed that (Fig. 10a), with soil physicochemical properties as influencing factors, RDA1 accounted for 34.85% of the explanatory weight ratio, whereas RDA2 accounted for 26.10%. Available potassium (AK) had a greater explanatory weight in explaining the composition of the bacterial community in the regular cropping soil used for planting X. sorbifolium Bunge. All soil physicochemical properties were positively correlated with the soil bacterial community. In addition, all soil physicochemical properties exhibited a positive correlation with the bacterial community structural changes under the regular cropping soil. OTU4225, OTU4751, OTU5234, and OTU5023, the strains used to demonstrate the changes in soil physicochemical properties, showed a significant correlation between soil physicochemical properties and soil bacterial communities. Fungal RDA demonstrated that the explanatory weight ratio of RDA1 was 30.75% and RDA2 was 23.73% (Fig. 10b). The findings revealed that the soil physicochemical properties significantly influenced the distribution of soil fungal communities under continuous cropping of X. sorbifolium Bunge in the AQ and CY regions. Soil physicochemical properties were negatively correlated with soil fungal microbial communities. OTU998, OTU1086, OTU1102, OTU935, and OTU1011 represented the response strains to the changes in soil physicochemical properties. These strains showed significant correlation between soil physicochemical properties and soil fungal communities.

      Figure 10. 

      A scatter diagram of RDA of X. sorbifolium Bunge continuous cropping. (a) RDA of the correlation between soil physicochemical properties and soil bacterial community; (b) RDA of the correlation between soil physicochemical properties and soil fungal community; (c) The relationships between soil physicochemical properties and strains representing soil microbial community changes. SOM: organic matter, NH4: Ammonium nitrogen, NO3: Nitrate nitrogen , AP: Available phosphorus, AK: Available potassium. Different colors in the heat map represent positive and negative correlation, color depth represents positive and negative correlation, and asterisks in color blocks represent the significance level. * 0.01 ≤ p < 0.05, ** 0.001 < p ≤ 0.01, *** p ≤ 0.001.

    • Correlation analysis was conducted to explore the relationship between the abundance of microorganisms and the change in the soil physicochemical properties (Fig. 10c). Analysis of the soil fungal community showed that the abundance of Silicocozyma was positively correlated with the level of available potassium (AK). Conversely, the abundance of Mortierella was negatively correlated with ammonium nitrogen (NH4+-N) level. The abundance of Neocosmospora was positively correlated with soil nitrate nitrogen (NO3-N) content and organic matter (SOM) amount. Analysis of soil bacterial community revealed that the levels of ammonium nitrogen, NO3-N, and SOM were negatively correlated with the abundance of Pseudohodoplanes and A4b.

    • Correlation analysis was conducted to explore the relationship between the core microorganisms and plant biomass index. Analysis of the bacterial microbial community revealed that the abundance of Streptosporangium was significantly positively correlated with the biomass of X. sorbifolium Bunge in the three locations (Fig. 11a). The relative abundance of Streptosporangium was significantly correlated with the stem diameter of X. sorbifolium Bunge. Correlation analysis of the fungal microbial community demonstrated that the abundance of Mortierella was positively correlated with the biomass of X. sorbifolium Bunge and positively correlated with the stem diameter of X. sorbifolium Bunge (Fig. 11b). Conversely, significant negative correlations were observed between the relative abundances of Neocosmospora, Phialemoniopsis, Aspergillus, and the biomass of X. sorbifolium Bunge in the three places. Notably, the change in the relative abundance of Neocosmospora had a significantly higher influence on the change in X. sorbifolium biomass.

      Figure 11. 

      Correlation between rhizosphere microbial abundance and X. sorbifolia biomass under continuous cropping. (a) Correlation between the biomass of X. sorbifolium Bunge and soil bacterial community; (b) Correlation between the biomass of X. sorbifolium Bunge and soil fungal community. Different colors in the heat map represent positive and negative correlation; color depth represents positive and negative correlation; * in color blocks represents statistical significance. * 0.01 ≤ p < 0.05, ** 0.001 < p ≤ 0.01, *** p ≤ 0.001; (c) The relationships between soil indicator microorganisms and plant biomass indicators. Pearson correlation coefficient indicates the linear correlation between two random variables. The value of R ranges from −1~1, with R > 0 denoting a positive correlation and R < 0 representing a negative correlation. The p value represents the significance of the correlation degree.

      Correlation analysis was conducted to explore the relationship between the plant height in July and the abundance of Streptosporangium and Neocosmopora. The results showed a significant negative correlation between the height of X. sorbifolium Bunge and the abundance of Neocosmospora, with a correlation coefficient of −0.9979 (Fig. 11d). Conversely, a positive correlation was observed between Streptosporangium and the height of X. sorbifolium Bunge, with a correlation coefficient of 0.9969, indicating a positive relationship between (Fig. 11c).

    • Successive crop planting often leads to the occurrence of continuous cropping diseases, which result in weakened plant growth, reduced nutrient absorption and decreased yield[3435]. Long-term single monoculture of coffee changes the soil pH, reduces the organic matter content, and significantly decreases the abundance of soil bacteria and fungi, affecting coffee production[36]. Continuous monoculture of wheat, corn, and soybeans reduce organic carbon and nitrogen contents in the soil, significantly affecting the crop yield[37]. Moreover, long-term continuous cropping of cotton induces significant changes in the soil physicochemical properties, with dysregulated levels of soil nitrogen, phosphorus, and potassium, and a decrease in soil enzyme activity within a short period (1 to 10 years), significantly affecting crop production[38]. In this study, the continuous cropping of X. sorbifolium Bunge significantly reduced the plant height and stem diameter and inhibited the root activity of plant seedlings. The physicochemical properties of various soils have changed, and the contents of available nutrients such as nitrate nitrogen, ammonium nitrogen, available phosphorus, and available potassium have decreased. The amount of nutrients directly available to plants depends on the community structure and corresponding functions of soil microorganisms. As the main source of plant nutrients, soil microorganisms can effectively promote the turnover of soil organic matter[39]. Therefore, due to the decrease of available nutrients of soil plants, the growth of X. sorbifolia Bunge is slowed down and the resistance is reduced, which leads to continuous cropping obstacles.

      High-throughput sequencing provides qualitative and semi-quantitative information on the composition and abundance of the soil microbial communities and reveals more taxonomic groups of soil fungi compared to conventional methods[40]. The present study revealed that continuous cropping of X. sorbifolium Bunge leads to continuous cropping diseases, inhibiting plant growth. Significant differences in the soil microbial community structure were observed under the different planting systems. Analysis of 16S rRNA gene sequencing data demonstrated that the planting sequence of peanuts changes the soil microbial community[19]. However, studies have not explored the effects of continuous cropping of X. sorbifolium Bunge on soil microbial community structure. Continuous cropping of this species in three areas significantly decreased the relative abundance of Ascomycetes and Basidiomycetes compared to the regular cropping soil. Conversely, the relative abundance of Mucor, Cladosporium, and Glomus significantly increased after continuous cropping. These results show that, at the phylum level, the fungal community structure is similar across different locations and soil types.

      Changes in fungal microbial community structure in plant rhizosphere, caused by fungal pathogens, are the main challenge in the continuous cropping of various plants. For example, continuous cropping of peas leads to the occurrence of soil fungi and oomycetes, forming a pathogen complex. At the genus level, the abundance of Ascomycota, Basidiomycota, Phoma, Podospora Pseudaleuria Veronaea in the rhizosphere of diseased peas is correlated with plant morbidity[41]. Analysis of successive poplar planting demonstrated changes in the composition, diversity, and structure of the soil fungal community. In addition, the abundance of pathogenic fungi was significantly higher after successive poplar planting compared to non-continuous cropping soil, significantly affecting poplar growth[42]. The abundance of Candida, Hypocrea, and Sistotrema increased significantly after continuous cropping of Andrographis paniculate. Moreover, the community structure of root fungi changed significantly compared to non-continuous cropping, leading to a decrease in Andrographis paniculata yield and challenges in continuous cropping[43]. In this study, the relative abundance of common soil fungi such as Fusarium, Chaetomium and Pseudosclerotium changed significantly after continuous cropping of X. sorbifolia Bunge. These findings imply that the instability of the rhizosphere fungal community structure caused by the continuous cropping of X. sorbifolia Bunge is the leading cause of the continuous cropping challenges of this plant.

      The relative abundance of other primary pathogens in the continuous cropping soil did not change. Degens et al. observed a significant positive correlation between the abundance of Phoma sp. in peas and the severity of diseases[44]. Moreover, continuous cultivation of Panax Notoginseng increases the risk of root infection by pathogenic bacteria. Previous findings indicate that Leotiomycetes, Cylindrocarpon, Fusarium, and Mycocentrospora are potential pathogens that prevent the continuous cultivation of Panax notoginseng[45]. These microorganisms are obligate pathogens, so they are dominant in roots rather than inhabiting the soil, leading to plant diseases. The present research results are consistent with findings from previous research that an increase in Neocosmospora abundance is a significant factor that limits the continuous cropping of X. sorbifolium Bunge. Neocosmospora was identified as the dominant pathogenic fungus in this study. This fungus typically inhabits soil, plant debris, living wood, or grass matrix and is occasionally observed in water and air[46]. Consequently, it may be the primary pathogen that causes continuous cropping diseases in X. sorbifolium Bunge farms.

      The relative abundance of Operational Taxonomic Unit (OTU) identified as Mortierella, Talaromyces, and Solicoccozyma in the continuously cropped X. sorbifolium Bunge field was significantly lower than in the control field. Moreover, the abundance of Mortierella in the three study sites was negatively correlated with continuously cropped X. sorbifolium Bunge. These fungi have been used as soil biocontrol strategies for bacteria. Previous findings report that Mortierella transforms nutrients, promotes crop growth, improves soil quality, and prevents soil degradation[47]. Talaromyces produces secondary compounds with a significant broad-spectrum antibacterial activity and is widely used in the agricultural industry[48]. Some species with a low abundance, including Penicillium, Mucor, and Burkholderia, are involved in nutrient transformation and promoting crop growth in the rhizosphere of continuously cropped tobacco plants. Notably, these species are negatively correlated with the relative abundance of continuously cropped tobacco pathogens[49]. Researchers inoculated rhizobia and endophytic fungi in the continuous cropping of Panax notoginseng. They observed increased diversity of Ascomycota, Zygomycota, and Basidiomycota, subsequently alleviating the challenges associated with the continuous cropping of this plant[45].

      In this study, the bacterial community structure in the soil of X. sorbifolium Bunge also changed substantially after continuous cropping. The relative abundances of Bacillus, Blastococcus, Solirurobacter, Dependentiae, Methylomirabilota, and Acidobacteriota were negatively correlated with continuous cropping. Conversely, the relative abundances of Blastococcus, Solirurobacter, and Dependentiae increased under regular cropping. Previous studies report that soil bacteria undergo significant changes under continuous cropping[50]. Continuous cropping of cotton leads to a decline in the abundance of beneficial bacteria such as Actinomycetes, Acidobacteriota, Sessilebacteria, and nitrifying bacteria in the soil[51]. Dynamic changes are observed in the abundance and diversity of beneficial bacteria during the continuous planting of peanuts. These findings demonstrate that bacterial populations, especially beneficial ones, can be used to minimize continuous cropping diseases[52]. Pearson correlation analysis of all categories showed that the abundances of Actinomycetes, Basidiomycetes, Bacteroides, Verruca, and fungi were negatively correlated with the disease index (DI) of vanilla after continuous cropping[53]. These findings imply a decline in the abundance of beneficial microorganisms may occur under the monoculture of continuous cropping of X. sorbifolium Bunge, ultimately reducing the biological inhibition of other regular soil microorganisms on continuous cropping diseases.

      In summary, the results of this study show that the continuous monoculture of X. sorbifolium Bunge leads to slow growth, reduced vitality, and low yield, resulting in continuous cropping diseases. Among them, the soil microbial community changed, and the relative abundance of pathogenic fungi including Neocosmospora and Alternaria is the main reason for the continuous cropping obstacle of X. sorbifolia. Hence, continuous cropping diseases can be mitigated by changing the soil microbial community structure. These findings provide insights for formulating strategies for the prevention and control of replanting diseases. Soil fumigation and disinfection should be adopted to reduce fungal pathogens, optimize microbial community structure, and prevent continuous cropping diseases.

      • This research was supported by The Improved Variety Program of Shandong Province of China (2020LZGC0904).

      • The authors confirm contribution to the paper as follows: study conception and design: Zhao Y, Lv J; data collection: Wang G; analysis and interpretation of results: Wang G, Wang L, Yu M, Wu D, Lu L, Xie X; draft manuscript preparation: Wang G, Wang L, Yu M, Wu D, Lu L, Xie X. All authors reviewed the results and approved the final version of the manuscript.

      • The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.

      • The authors declare that they have no conflict of interest.

      • # Authors contributed equally: Gongshuai Wang, Lei Wang

      • Copyright: © 2024 by the author(s). Published by Maximum Academic Press, Fayetteville, GA. This article is an open access article distributed under Creative Commons Attribution License (CC BY 4.0), visit https://creativecommons.org/licenses/by/4.0/.
    Figure (11)  Table (2) References (53)
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    Wang G, Wang L, Yu M, Wu D, Lu L, et al. 2024. Continuous monoculture of Xanthoceras sorbifolia Bunge leads to continuous cropping challenges due to fungal pathogen accumulation and reduced beneficial bacteria abundance. Fruit Research 4: e040 doi: 10.48130/frures-0024-0034
    Wang G, Wang L, Yu M, Wu D, Lu L, et al. 2024. Continuous monoculture of Xanthoceras sorbifolia Bunge leads to continuous cropping challenges due to fungal pathogen accumulation and reduced beneficial bacteria abundance. Fruit Research 4: e040 doi: 10.48130/frures-0024-0034

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