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CI presents a range of symptoms that vary depending on the commodities affected. These symptoms include color shading, surface pitting, surface browning, and water-soaking. Additionally, CI affects the inner appearance, causing symptoms such as water succulence, internal browning (IB), and flesh translucence or jelly-like consistency[1]. Exposing the CI vegetables and fruits to room temperature triggers the manifestation of the symptoms listed in Table 1. Some vegetables and fruits, such as papaya, mango, gourd, tomato, cucumber, and okra, exhibit contrasting symptoms of CI between their exocarp and mesocarp due to the adhesive nature of the flesh and peel derived from the ovary wall. When stored at low temperatures, cucumbers exhibit distinct visual characteristics such as a water-soaked patch and subsequent surface pitting collapse. The mesocarp of the cucumber exhibits a translucent coloration, whereas the exocarp darkens and turns green. The variation in the response of vegetables and fruits to CI, specifically between the peel and pulp[3] is depicted in Fig. 1.
Table 1. Critical temperature, CI response and symptoms of some tropical horticultural commodities.
Horticultural
commodityCritical temperature
( °C)CI response
(+)Symptoms Ref. External Internal Banana 13−15 + Skin-darkening Poor ripening [6] Mango 13−15 + Senescent spotting, brown skin Poor ripening [7] Papaya 13 + + Surface pitting Water-soaking [8] Pineapple - Queen 11−13 + ++ Pink bract of fruitlets Internal browning [9] - Smooth cayenne 13 + Non-response Internal browning Ripe tomato 14 + Surface pitting Excessive softening, water soaking, aroma loss [10] Asparagus 0−2 + Dull, grey-green, limp tips [11,12] Bean 7 + Pitting and russeting [11] Eggplant 7 ++ Surface scald, Seed blackening [11] Gourd 10−13 ++ Surface pitting and browning Seed browning [3,11,12] Cucumber 8−10 ++ Surface pitting Water soaking [11,12] Zucchini 0 + Surface pitting [12] Summer squash 5−10 + Surface pitting and fungal rot Breakdown [13] Gac fruit 10−13 + Fruit shriveling, water soaking peel Water leathery like mesocarp and aril [14] Chili 7 + Surface pitting Placenta and seed browning [15] Okra 8−10 + Surface pitting Seed browning [16,17] Chinese kale 4−8 + Water soaking peel [18] Sweet basil 12 ++ Leaf browning, necrosis, decay, and leaf abscission [19] Holy basil 12 ++ Browning spots and water soaking leaves [20] Lemon basil 12 ++ Leaf blackening [5] (+) degree of susceptibility to CI. Figure 1.
Internal structure of immature sponge gourd fruit (left) and visual appearance of immature sponge gourd fruit stored at (a) 25 °C and (b) 5 °C[3].
Mature leaves of sweet basil (Ocimum basilicum L.) stored at 4 °C developed a severity of CI browning symptoms (Fig. 2) with higher levels of polyphenol oxidase (PPO) and lipoxygenase (LOX) activities, resulting in an increase in malondialdehyde (MDA) content compared to the young leaves[4]. Wongsheree et al.[5] reported that mature lemon basil (Ocimum × citriodourum) leaves, having higher LOX, suffered more severe CI than young leaves when stored at 4 °C.
Figure 2.
Chilling injury symptoms generated on young leaves of holy basil (upper right) and sweet basil (below right) during 4 °C storage, compared to non-chilled leaves (left).
CI closely relates to the assessment of fruit maturity. Mango, papaya, banana, pineapple, and corn, ranging from immature to mature stages, possess the potential to serve as vegetables for food ingredients. Green bananas are susceptible to low temperatures. This sensitivity manifests itself as surface pitting and browning on the banana peel. When the fruit is returned to its normal temperature, the ripening process is complete. Blackheart as an internal browning (IB) is a form of CI in the field when maturing in winter. Meanwhile, IB can develop in the core and the surrounding flesh of pineapple fruit stored at 10−15 °C for a week in 'Queen' and 2 weeks in 'Smooth Cayenne' group. The observation of enhanced pink coloration on the upper surface of crown leaves and in the grooves of fruitlets suggests a correlation between the external appearance of pineapple fruit and the production of IB[11]. Cultivars '73−50' and 'Gold' were explicitly developed to reduce IB vulnerability in Hawaii, USA. Although the 'Gold' pineapple fruit is more resistant to IB, it is more susceptible to fruit rot than the 'Smooth Cayenne'[21].
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Cucumber, gourd, mango, and banana are examples of fruits that have separate peel and flesh. Certain types of fruit flesh, such as aril developed from parts of the seed (integument or funiculus), exhibit a distinct response to low temperatures compared to the peel. In many fruits, the peel developed from the ovary wall typically signifies indications of CI before in the flesh.
Basils' CI symptoms were generally characterized by leaf blackening and brown spots on the leaves (Fig. 2). The symptoms began with the dysfunction of oil glands on lemon basil leaves, which progressed to a blackening mark[22]. Several lines of sweet basil produce volatile phenylpropane oils (eugenol and chavicol derivatives) that accumulate in the leaves in specialized structures known as peltate and capitate glands. The peltate glands serve as phenylpropene class defense tissues[23]. The dysfunction of these oil glands could lead to imbalanced intermediates that cause visual browning spots. CI can be induced inside the fruits of some vegetables, such as eggplant, guard, and chili. When stored at low temperatures, the seeds' IB and discoloration initially occur when the exocarps appear normal. In gac fruit, storage at 4 °C induces the tissue collapse of the mesocarp and aril[14].
Reactive oxygen species (ROS) as CI triggers
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Various physiological stresses can produce ROS in different forms, as outlined in Table 2. Low-temperature exposure triggers redox reactions that generate oxygen species (O2·−)[24]. Oxygen radicals are commonly produced through electron transport chains during photosynthesis and respiration. The presence of a dysfunctional electron in ROS can efficiently cause damage to macromolecules such as proteins, lipids, and DNA/RNA. The membrane-lipid bilayer of cells and organelles represents a pivotal piece of evidence. Reactive oxygen species are conveyed across cellular boundaries via hydrogen peroxide (H2O2) with the assistance of superoxide dismutase (SOD), which encompasses both iron-dependent SOD (Fe-SOD) and manganese-dependent SOD (Mn-SOD). Hydrogen peroxide is transported to neighboring cells and acts as a signal transduction molecule. Nevertheless, H2O2 is unstable and undergoes the Fenton reaction, which converts it into a highly reactive hydroxyl radical (HO·−) and a hydroxide ion (HO−). This reaction has the potential to degrade the integrity of membrane lipids, resulting in detrimental alterations in fluidity and permeability.
Table 2. General ROS produced in plant cells under low temperature storage.
Form Name Form Name O2·− Superoxide radical 1O2 Singlet oxygen OH· Hydroxy radical H2O2 Hydrogen peroxide RO· Alkoxyl radical ROO· Alkylperoxyl radical ROOH Alkylhydroperoxide ClO− Hypochlorite ion Fe5+O Periferryl ion Fe4+O Ferryl ion NO· Nitric oxide Cellular localization of CI
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CI causes an impairment of membrane function, resulting in an elevation in permeability. The cellular membrane consists of phospholipid bilayers, wherein hydrophilic heads are oriented toward the solute, and hydrophobic tails are oriented toward each other. This phenomenon complicates the transportation of the solute. The saturation or unsaturation of fatty acids in the membrane component is a determining factor. Fatty acids react differently at different low temperatures. Plants possess defensive mechanisms in the form of antioxidants, which serve the purpose of scavenging free radicals through the presence of various enzymes found in different cellular compartments. The cytosol contains enzymes such as Cu-SOD, Zn-SOD, monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR), glutathione reductase (GTR), and glutathione peroxidase (GTP). Mn-SOD and GTR are found in the mitochondria, while Cu-SOD, Zn-SOD, Fe-SOD, ascorbate peroxidase (APX), MDHAR, DHAR, and GTR are present in the chloroplast. Lastly, catalase (CAT) is found on the peroxisome (Fig. 3).
Tropical vegetables and fruits are more susceptible to cold temperatures than temperate ones. CI was previously believed to occur through a membrane phase transition, specifically from a semi-liquid state to a solid state. However, the current phase transition results in an exceedingly high amount of energy that is unattainable to produce within living cells. Conversely, cellular injury leads to the production of CI, which is evidenced by the release of electrolytes. Consequently, research has been conducted to examine the etiology of membrane injury.
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We thank Dr. Panipa Youryon from King Mongkut's Institute of Technology Ladkrabang and Dr. Surisa Phornvillay from the University of Malaysia Sarawak for their valuable contributions to certain CI photographs.
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About this article
Cite this article
Wongs-Aree C, Aschariyaphotha W, Palapol Y, Bodhipadma K, Noichinda S. 2024. Structural membrane alterations in tropical horticultural crops under postharvest chilling stress. Vegetable Research 4: e016 doi: 10.48130/vegres-0024-0013
Structural membrane alterations in tropical horticultural crops under postharvest chilling stress
- Received: 09 January 2024
- Accepted: 15 April 2024
- Published online: 03 June 2024
Abstract: Optimal storage temperatures are essential for preserving vegetables' quality. Tropical plants, meanwhile, have a significant vulnerability to low temperatures, yet the majority of vegetables are farmed within tropical climates. Low temperatures can cause oxidative stress in vegetables, resulting in a condition known as 'chilling injury' (CI). The symptoms may manifest as visible external traits, including color shading, surface pitting, surface browning, and water soaking. Conversely, CI can alter internal changes such as water succulence, internal browning, and flesh translucence. Additionally, CI potentially triggers abnormal metabolic processes, resulting in atypical ripening or the development of an unpleasant odor. Reactive oxygen species (ROS) that occur during oxidative stress at low temperatures first harm the membrane of organelles and subsequently damage macromolecules like proteins, lipids, and DNA/RNA. Therefore, visual signs of cellular damage indicate the advanced stage of damage after membrane transition. The tolerant plant generally contains more polyunsaturated fatty acids (PUFA) than monounsaturated fatty acids (MUFA) in its cellular membrane. All damaging cells display an imbalance between ROS and the scavenging systems, including chemical compounds and enzymatic cycles. Inducing antioxidant systems is essential for preserving the quality of chilled vegetables. Therefore, when the cells reach the advanced stages of CI development, specifically after membrane leakage, they are unable to recover and will progress to the final stage of CI, exhibiting phenotypic CI symptoms.