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Intercellular signaling across plasmodesmata in vegetable species

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  • The formation of edible organs and stress adaption are two major focuses of the studies on vegetable species. The regulation of these two processes often involves cell-to-cell signaling. In most plants, including vegetable species, intercellular signaling can be delivered by mobile regulators that traffic through a channel called plasmodesmata connecting almost all cells. A large number of transcription factors and RNAs have been discovered to move across plasmodesmata (called the symplastic way) to travel a short-range or a long-distance. This symplastic transport of signaling molecules has emerged to be an important regulation of a wide range of developmental and physiological processes. Callose deposition to plasmodesmata is a key step controlling the plasmodesmata permeability in many cell types. Here we summarize the recent progress in our understanding of plasmodesmata-mediated signaling in plants.
  • With the development of the world economy, people's lifestyles have changed dramatically, and long-term high-intensity work has put many people's bodies in a sub-healthy state. The increasing incidence of various chronic diseases has not only put enormous pressure on society's healthcare systems but also caused endless suffering to people[1]. Therefore, people's demands on the functionality and safety of food are increasing, and it has become the consensus of people that 'not just eating enough, but more importantly eating well'.

    Rice is the staple food for more than half of the world's population and the main economic source for a large number of rural people[2]. However, due to the rising cost of rice cultivation, farmers are gaining less and less economic benefits from growing rice, which seriously undermines their incentive to grow rice and poses a serious threat to world food security. Increasing the added value of rice not only helps to increase farmers' income but also helps to ensure world food security. The presence of a large number of functional ingredients in rice makes it possible to increase the added value of rice, and functional rice has therefore been widely noticed.

    Functional rice refers to rice containing certain specific components that play a regulatory and balancing role in human physiological functions in addition to the nutrients necessary for human growth and development in the endosperm, embryo, and rice bran. They can increase human physiological defense mechanisms, prevent certain diseases, help recovery, delay aging, and boost physical strength and energy levels[3]. Rice is a staple food for more than half of the world's population[4], and its functional components have a great potential to be exploited for human welfare. Using functional rice as a carrier to address health problems and realize 'medicine-food homology' is an excellent motivation for promoting functional rice. The current typical functional rice is introduced in this paper. It also summarizes the breeding and cultivation technologies of functional rice.

    Rice has a high glycemic index. Its long-term consumption leads to obesity, diabetes, and colon disease in many people[5]. However, the consumption of rice rich in resistant starch (RS) can greatly reduce the risk of these diseases[6]. Therefore, breeding rice varieties with high RS content has attracted considerable attention from breeders in various countries. However, the variability of RS content between different rice varieties is low, and there are few germplasm resources available for selection, thus making it challenging to breed rice varieties with high RS content using traditional breeding methods. Combining traditional and modern molecular breeding techniques can greatly improve the successful production of high RS rice breeds. Nishi et al.[7] selected a high RS rice variety EM10 by treating fertilized egg cells of Kinmaze with N-methyl-N-nitrosourea. However, its yield was very low, and it was not suitable for commercial production. Wada et al.[8] crossed 'Fukei 2032' and 'EM129' as parents and selected Chikushi-kona 85, a high RS rice variety with a higher yield than EM10. Miura et al.[9] bred ultra-high RS BeI-BEIIB double mutant rice by crossing the Abe I and Abe IIB mutant strains, and the content of RS in the endosperm reached 35.1%. Wei et al.[10] found that the simultaneous inhibition of starch branching enzyme (SBE) genes SBEIIb and SBEI in Teqing by antisense RNA could increase the RS content in rice to 14.9%. Zhu et al.[11] used RNAi technology to inhibit the expression of SBEI and SBEII genes in rice, which increased the content of RS in rice endosperm from 0 to 14.6 %. Zhou et al.[6] found that rice RS formation is mainly controlled by soluble starch synthase (SSIIA). However, its regulation is dependent on the granule-bound starch synthase Waxy (Wx), and SSIIA deficiency combined with high expression of Wxa facilitates the substantial accumulation of RS in the rice. The results of Tsuiki et al.[12] showed that BEIB deficiency was the main reason for the increased accumulation of RS in rice. Itoh et al.[13] developed new mutant rice lines with significantly higher levels of RS in rice by introducing genes encoding starch synthase and granule-bound starch synthase in the rice into the BEIB-deficient mutant line be2b.

    The accumulation of anthocyanins/proanthocyanidins in the seed coat of the rice grain gives brown rice a distinct color[14]. Most common rice varieties lack anthocyanins in the seed coat, and so far, no rice variety with colored endosperm in its natural state has been identified. However, Zhu et al.[15] bred rice with purple endosperm using transgenic technology. Red rice contains only proanthocyanidins, while black and purple rice contain anthocyanidins and proanthocyanidins[16]. Red seed coat of rice was found to be controlled by the complementary effects of two central effect genes Rc and Rd. The loss of function of the Rc gene prevented the synthesis of proanthocyanidins, while the Rd gene could enhance the effect of the Rc gene in promoting proanthocyanidins synthesis[17]. Purple seed coat color is controlled by two dominant complementary genes Pb and Pp. Pb determines the presence or absence of seed coat color, and Pp determines the depth of seed coat color[18]. In addition, phycocyanin synthesis is also regulated by transcription factors such as MYB, bHLH, HY5, and WD40[14], but the exact regulatory mechanism is not clear. Colored rice is rich in bioactive components, such as flavonoids, phenolic acids, vitamin E (VE), glutelin, phytosterols, and phytic acid (PA). It also contains large amounts of micronutrients such as Ca, Fe, Zn, and Se[19], and has a much higher nutritional and health value than ordinary white rice. In addition, Zhu et al.[20] successfully developed rice with enriched astaxanthin in the endosperm by introducing the genes sZmPSY1, sPaCrtI, sCrBKT, and sHpBHY. This achievement has laid a solid foundation for the further development of functional rice industry.

    Giant embryo rice refers to rice varieties whose embryo volume is more than twice that of ordinary rice[21]. Rice embryo contains more nutrients than the endosperm; therefore, the nutritional value of giant embryo rice greatly exceeds that of ordinary rice. Studies have found that the levels of γ-aminobutyric acid (GABA), essential amino acids, VE, γ-oryzanol, phenols, and trace elements in giant embryo rice are considerably higher than that in ordinary rice[21]. Satoh & Omura[22] used the chemical mutagen N-methyl-N-nitrosourea to treat the fertilized egg cells of the rice variety Kinmaze to obtain a 'giant embryo' mutant. The mutants’ embryo occupied 1/4–1/3 of the rice grain volume and was 3–4 times larger than normal rice embryo[23]. Its GABA content increased dramatically after the rice was soaked in water. Maeda et al.[24] crossed the giant embryo mutant EM40 of Kinmaze with the high-yielding variety Akenohoshi to produce the giant embryo rice variety 'Haiminori'. The embryo size of 'Haiminori' is 3–4 times that of ordinary rice, and the GABA content of its brown rice is 3–4 times higher than that of 'Nipponbare' and 'Koshihikari' after soaking for four hours in water. A few genes that can regulate the size of rice embryos have been identified, and GE is the first identified rice giant embryo gene[25]. Nagasawa et al.[26] found that the loss of GE gene function resulted in enlarged embryos and smaller endosperm in rice. Lee et al.[27] found that the inhibition of LE gene expression by RNAi technology could lead to embryo enlargement in rice, but the regulatory mechanism remains to be investigated.

    Protein is the second most crucial nutrient in rice, accounting for 7–10% of the grain weight, and glutenin accounts for 60%–80% of the total protein content in rice grains[28]. Compared to other proteins, glutenin is more easily digested and absorbed by the body[29]. Therefore, higher glutenin content in rice can improve its nutritional value. However, people with renal disease (a common complication of diabetes) have impaired protein metabolism, and consumption of rice with lower glutelin content can help reduce their protein intake and metabolic burden[30]. Japanese breeders treated Nihonmasari with the chemical mutagen ethyleneimine and selected the low-glutelin rice mutant NM67[31]. Iida et al.[31] developed a new rice variety LGC-1 (Low glutelin content-1) with a glutelin content of less than 4% by backcrossing the NM67 mutant with the original variety 'Nihonmasari'. According to Miyahara[32], the low glutelin trait in LGC-1 is controlled by a single dominant gene Lgc-1 located on chromosome 2. Subsequently, Nishimura et al.[33] produced two rice varieties, 'LGC Katsu' and 'LGC Jun' with lower glutelin content by crossing LGC1 with a mutant line Koshikari (γ-ray induction) lacking 26 kDa globulin (another easily digestible protein).

    Vitamin A (VA) is one of the essential nutrients for the human body[34]. However, rice, a staple food, lacks VA, leading to a VA deficiency in many people. β-carotene is a precursor for VA synthesis and can be effectively converted into VA in the human body[35]. Therefore, breeding rice varieties rich in β-carotene has attracted the attention of breeders in various countries. Ye et al.[36] simultaneously transferred phytoene synthase (psy), phytoene desaturase (crt I), and lycopene β-cyclase (lcy) genes into rice using the Agrobacterium-mediated method and produced the first generation of golden rice with a β-carotene content of 1.6 µg·g−1 in the endosperm. However, due to the low content of β-carotene in rice, it is difficult to meet the human body's demand for VA. To increase β-carotene content in rice, Paine et al.[37] introduced the phytoene synthase (psy) gene from maize and the phytoene desaturase (crt I) gene from Erwinia into rice. They obtained the second generation of golden rice with 37 µg g−1 of β-carotene in the endosperm, with nearly 23-fold increase in β-carotene content compared to the first generation of golden rice.

    Fe and Zn are essential trace elements for human beings. The contents of Fe and Zn in common rice are about 2 μg·g−1 and 16 μg·g−1, respectively[38], which are far from meeting human needs. In 2004, to alleviate micronutrient deficiencies among underprivileged people in developing countries, the Consultative Group on International Agricultural Research launched the HarvestPlus international collaborative program for improving Fe, Zn, and β-carotene levels in staple crops, with breeding targets of 13 μg·g−1 and 28 μg·g−1 for Fe and Zn in rice, respectively. Masuda et al.[39] found that expression of the nicotianamine synthase (NAS) gene HvNAS in rice resulted in a 3-fold increase in Fe and a 2-fold increase in Zn content in polished rice. Trijatmiko et al.[38] overexpressed rice OsNAS2 gene and soybean ferritin gene SferH-1 in rice, and the Fe and Zn content in polished rice of rice variety NASFer-274 reached 15 μg·g−1 and 45.7 μg·g−1, respectively. In addition, it has been found that increasing Fe intake alone does not eliminate Fe deficiency but also decreases the amount of Fe absorption inhibitors in the diet or increases the amount of Fe absorption enhancers[40]. The negatively charged phosphate in PA strongly binds metal cations, thus reducing the bioavailability of Fe and Zn in rice[41], while the sulfhydryl group in cysteine binds Fe, thereby increasing the absorption of non-heme Fe by the body[42]. To improve the bioavailability of Fe and Zn, Lucca et al.[40] introduced a heat-tolerant phytase (phyA) gene from Aspergillus fumigatus into rice and overexpressed the cysteine-rich protein gene (rgMT), which increased the content of phytase and cysteine residues in rice by 130-fold and 7-fold, respectively[40].

    The functional quality of rice is highly dependent on germplasm resources. Current functional rice breeding mainly adopts transgenic and mutagenic technologies, and the cultivated rice varieties are mainly enriched with only one functional substance and cannot meet the urgent demand by consumers for rice enriched with multiple active components. The diversity of rice active components determines the complexity of multifunctional rice breeding. In order to cultivate multifunctional rice, it is necessary to strengthen the application of different breeding technologies. Gene polymerization breeding is a crop breeding technology that can polymerize multiple superior traits that have emerged in recent years, mainly including traditional polymerization breeding, transgenic polymerization breeding, and molecular marker-assisted selection polymerization breeding.

    The transfer of beneficial genes in different species during traditional polymeric breeding is largely limited by interspecific reproductive isolation, and it is challenging to utilize beneficial genes between different species effectively. Gene transfer through sexual crosses does not allow accurate manipulation and selection of a gene and is susceptible to undesirable gene linkage, and in the process of breed selection, multiple backcrosses are required[43]. Thus, the period of selecting target plants is long, the breeding cost is high, and the human resources and material resources are costly[44]. Besides, it is often difficult to continue the breakthrough after a few generations of backcrossing due to linkage drag. Thus, there are significant limitations in aggregating genes by traditional breeding methods[45].

    Transgenic technology is an effective means of gene polymerization breeding. Multi-gene transformation makes it possible to assemble multiple beneficial genes in transgenic rice breeding rapidly and can greatly reduce the time and workload of breeding[46]. The traditional multi-gene transformation uses a single gene transformation and hybridization polymerization method[47], in which the vector construction and transformation process is relatively simple. However, it is time-consuming, laborious, and requires extensive hybridization and screening efforts. Multi-gene-based vector transformation methods can be divided into two major categories: multi-vector co-transformation and multi-gene single vector transformation[47]. Multi-vector co-transformation is the simultaneous transfer of multiple target genes into the same recipient plant through different vectors. The efficiency of multi-vector co-transformation is uncertain, and the increase in the number of transforming vectors will increase the difficulty of genetic screening, resulting in a reduced probability of obtaining multi-gene co-transformed plants. Multi-gene single vector transformation constructs multiple genes into the T-DNA region of a vector and then transfers them into the same recipient plant as a single event. This method eliminates the tedious hybridization and backcrossing process and solves the challenges of low co-transformation frequency and complex integration patterns. It can also avoid gene loss caused by multi-gene separation and recombination in future generations[47]. The transgenic method can break through the limitations of conventional breeding, disrupt reproductive isolation, transfer beneficial genes from entirely unrelated crops to rice, and shorten the cycle of polymerizing target genes significantly. However, there are concerns that when genes are manipulated, unforeseen side effects may occur, and, therefore, there are ongoing concerns about the safety of transgenic crops[48]. Marker-free transgenic technology through which selective marker genes in transgenic plants can be removed has been developed. This improves the safety of transgenic crops, is beneficial to multiple operations of the same transgenic crop, and improves the acceptance by people[49].

    Molecular marker-assisted selection is one of the most widely used rice breeding techniques at present. It uses the close linkage between molecular markers and target genes to select multiple genes directly and aggregates genes from different sources into one variety. This has multiple advantages, including a focused purpose, high accuracy, short breeding cycle, no interference from environmental conditions, and applicability to complex traits[50]. However, few genes have been targeted for the main effect of important agronomic traits in rice, and they are mainly focused on the regulation of rice plant type and the prevention and control of pests and diseases, and very few genes related to the synthesis of active components, which can be used for molecular marker-assisted selection are very limited. Furthermore, the current technical requirements and costs for analyzing and identifying DNA molecular markers are high, and the identification efficiency is low. This greatly limits the popularization and application of functional rice polymerization breeding. Therefore, to better apply molecular marker-assisted selection technology to breed rice varieties rich in multiple active components, it is necessary to construct a richer molecular marker linkage map to enhance the localization of genes related to functional substance synthesis in rice[51]. Additionally, it is important to explore new molecular marker technologies to improve efficiency while reducing cost.

    It is worth noting that the effects of gene aggregation are not simply additive. There are cumulative additive effects, greater than cumulative epistatic effects, and less than cumulative epistatic effects among the polymerization genes, and the effects are often smaller than the individual effect. Only with a clearer understanding of the interaction between different QTLs or genes can functional rice pyramiding breeding be carried out reasonably and efficiently. Except for RS and Se, other active components of rice mainly exist in the rice bran layer, and the content of active components in the endosperm, the main edible part, is extremely low. Therefore, cultivating rice varieties with endosperm-enriched active components have broad development prospects. In addition, because crops with high quality are more susceptible to pests and diseases[52], the improvement of rice resistance to pests and diseases should be considered during the polymerization breeding of functional rice.

    The biosynthesis of active components in rice is influenced by rice varieties but also depends on cultivation management practices and their growth environment.

    Environmental conditions have a greater effect on protein content than genetic forces[53]. Both light intensity and light duration affect the synthesis and accumulation of active components in rice. Low light intensity in the early stage of rice growth is not conducive to the accumulation of glutelin in rice grains but favors the accumulation of amylose, while the opposite is true in the late stage of rice growth[54]. Low light intensity during the grain-filling period reduces the accumulation of total flavonoids in rice[55] and decreases Fe ions' movement in the transpiration stream and thereby the transport of Fe ions to rice grains[56]. An appropriate increase in light intensity is beneficial to the accumulation of flavonoids, anthocyanins, and Fe in rice, but the photostability of anthocyanins is poor, and too much light will cause oxidative degradation of anthocyanins[57]. Therefore, functional rice is best cultivated as mid-late rice, which would be conducive to accumulating active components in rice.

    The temperature has a great influence on the synthesis of active components in rice. An appropriate increase in the temperature is beneficial to the accumulation of γ-oryzanol[58] and flavonoids[59] in rice. A high temperature during the grain-filling period leads to an increase in glutelin content in rice[60], but an increase in temperature decreases the total phenolic content[61]. The results regarding the effect of temperature on the content of PA in rice were inconsistent. Su et al.[62] showed that high temperatures during the filling period would increase the PA content, while Goufo & Trindade[61] reported that the increase in temperature would reduce the PA content. This may be due to the different growth periods and durations of temperature stress on rice in the two studies. The synthesis of anthocyanins/proanthocyanidins in colored rice requires a suitable temperature. Within a certain range, lower temperatures favor the accumulation of anthocyanins/proanthocyanidins in rice[63]. Higher temperatures will lead to degradation, and the thermal stability of proanthocyanidins being higher than that of anthocyanins[64]. In addition, cold or heat stress facilitates GABA accumulation in rice grains[65]. Therefore, in actual production, colored rice and low-glutelin rice are best planted as late rice, and the planting time of other functional rice should be determined according to the response of its enriched active components to temperature changes.

    Moderate water stress can significantly increase the content of glutelin[66] and GABA[67] in rice grains and promote the rapid transfer of assimilation into the grains, shorten the grain filling period, and reduce the RS content[68]. Drought stress can also induce the expression of the phytoene synthase (psy) gene and increase the carotenoid content in rice[69]. Soil moisture is an important medium in Zn diffusion to plant roots. In soil with low moisture content, rice roots have low available Zn, which is not conducive to enriching rice grains with Zn[70]. Results from studies on the effect of soil water content on Se accumulation in rice grains have been inconsistent. Li et al.[71] concluded that flooded cultivation could significantly increase the Se content in rice grains compared to dry cultivation. However, the results of Zhou et al.[72] showed that the selenium content in rice grains under aerobic and dry-wet alternative irrigation was 2.44 and 1.84 times higher than that under flood irrigation, respectively. This may be due to the forms of selenium contained in the soil and the degree of drought stress to the rice that differed between experiments[73]. In addition, it has been found that too much or too little water impacts the expression of genes related to anthocyanin synthesis in rice, which affects the accumulation of anthocyanins in rice[74]. Therefore, it is recommended to establish different irrigation systems for different functional rice during cultivation.

    Both the amount and method of nitrogen application affect the accumulation of glutelin. Numerous studies have shown that both increased and delayed application of nitrogen fertilizer can increase the accumulation of lysine-rich glutelin to improve the nutritional quality of rice (Table 1). However, this improvement is not beneficial for kidney disease patients who cannot consume high glutelin rice. Nitrogen stress can down-regulate the expression of ANDs genes related to the anthocyanins biosynthesis pathway in grains, resulting in a decrease in anthocyanins synthesis[55]. Increased nitrogen fertilizer application can also increase the Fe, Zn, and Se content in rice[75,76]. However, some studies have found that increased nitrogen fertilizer application has no significant effect on the Fe content of rice[77], while other studies have shown that increased nitrogen fertilizer application will reduce the Fe content of rice[78]. This may be influenced by soil pH and the form of the applied nitrogen fertilizer. The lower the soil pH, the more favorable the reduction of Fe3+ to Fe2+, thus promoting the uptake of Fe by rice. Otherwise, the application of ammonium fertilizer can improve the availability of soil Fe and promote the absorption and utilization of Fe by rice. In contrast, nitrate fertilizer can inhibit the reduction of Fe3+ and reduce the absorption of Fe by rice[79].

    Table 1.  Effect of nitrogen fertilizer application on glutelin content of rice.
    SampleN level
    (kg ha−1)
    Application timeGlutelin content
    (g 100 g−1)
    References
    Rough rice05.67[66]
    270Pre-transplanting : mid tillering : panicle initiation : spikelet differentiation = 2:1:1:16.92
    300Pre-transplanting : mid tillering : panicle initiation : spikelet differentiation = 5:2:2:16.88
    Brown rice05.35[83]
    90Pre-transplanting : after transplanting = 4:16.01
    Pre-transplanting : after transplanting = 1:16.60
    180Pre-transplanting : after transplanting = 4:16.53
    Pre-transplanting : after transplanting = 1:17.29
    270Pre-transplanting : after transplanting = 4:17.00
    Pre-transplanting : after transplanting = 1:17.66
    Rough rice05.59[84]
    187.5Pre-transplanting : after transplanting = 4:16.47
    Pre-transplanting : after transplanting = 1:16.64
    300Pre-transplanting : after transplanting = 4:17.02
    Pre-transplanting : after transplanting = 1:17.14
    Polished rice03.88[85]
    90Pre-transplanting : tillering : booting = 2:2:14.21
    180Pre-transplanting : tillering : booting = 2:2:14.43
    270Pre-transplanting : tillering : booting = 2:2:16.42
    360Pre-transplanting : tillering : booting = 2:2:14.87
    Brown rice09.05[86]
    120Flowering22.14
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    Appropriate application of phosphorus fertilizer is beneficial in promoting the translocation of Fe and Zn from leaves to rice grains, thus increasing the content in rice grains[80]. However, the excessive application of phosphate fertilizer will reduce the availability of Fe and Zn in soil, resulting in less uptake by the roots and a lower content in the rice grains[81]. The content of PA in rice increased with a higher phosphorus fertilizer application rate[80]. Increasing the phosphorus fertilizer application rate would increase the values of [PA]/[Fe] and [PA]/[Zn] and reduce the effectiveness of Fe and Zn in rice[80]. Currently, there are few studies on the effect of potassium fertilization on the synthesis of active components in rice. Available studies report that increased application of nitrogen fertilizer can increase the Zn content in rice[82]. Therefore, the research in this area needs to be strengthened.

    Because the iron in soil mainly exists in the insoluble form Fe3+, the application of iron fertilizer has little effect on rice biofortification[87]. There are different opinions about the effect of Zn fertilizer application methods. Phattarakul et al.[88] believed that foliar spraying of Zn fertilizer could significantly improve the Zn content in rice grains. Jiang et al.[89] concluded that most of the Zn accumulated in rice grains were absorbed by the roots rather than from the reactivation of Zn in leaves. In contrast, Yuan et al.[90] suggested that soil application of Zn fertilizer had no significant effect on Zn content in rice grains. The different results may be affected by the form of zinc fertilizer applied and the soil conditions in the experimental sites. Studies have found that compared with the application of ZnEDTA and ZnO, zinc fertilizer in the form of ZnSO4 is most effective for increasing rice's Zn[70]. In addition, the application of zinc fertilizer reduces the concentration of PA in rice grains[70].

    The form of selenium fertilizer and the method and time of application will affect the accumulation of Se in rice grains. Regarding selenium, rice is a non-hyperaccumulative plant. A moderate application of selenium fertilizer can improve rice yield. However, the excessive application can be toxic to rice, and the difference between beneficial and harmful supply levels is slight[91]. Selenite is readily adsorbed by iron oxide or hydroxide in soil, and its effectiveness in the soil is much lower than selenite[92]. In addition, selenate can migrate to the roots and transfer to rice shoots through high-affinity sulfate transporters. In contrast, selenite is mainly assimilated into organic selenium in the roots and transferred to the shoots in smaller amounts[93]. Therefore, the biological effectiveness of Se is higher in selenate-applied soil than in selenite application[94] (Table 2). Zhang et al.[95] found that the concentration of Se in rice with soil application of 100 g Se ha-1 was only 76.8 μg·kg-1, while the concentration of Se in rice with foliar spray of 75 g Se ha-1 was as high as 410 μg·kg-1[73]. However, the level of organic selenium was lower in rough rice with foliar application of selenium fertilizer compared to soil application[96], while the bioavailability of organic selenium in humans was higher than inorganic selenium[97]. Deng et al.[73] found that the concentrations of total selenium and organic selenium in brown rice with selenium fertilizer applied at the full heading stage were 2-fold higher than those in brown rice with selenium fertilizer applied at the late tillering stage (Table 2). Although the application of exogenous selenium fertilizer can rapidly and effectively increase the Se content of rice (Table 2), it can easily lead to excessive Se content in rice and soil, which can have adverse effects on humans and the environment. Therefore, breeding Se-rich rice varieties is a safer and more reliable way to produce Se-rich rice. In summary, functional rice production should include the moderate application of nitrogen and phosphorus fertilizer and higher levels of potassium fertilizer, with consideration to the use of trace element fertilizers.

    Table 2.  Effect of selenium fertilizer application on the selenium content of rice.
    SampleSe level (g Se ha−1)Selenium fertilizer formsApplication methodSe content (μg·g−1)References
    Rough rice00.002[98]
    18SeleniteFoliar spray at full heading0.411
    Polished rice00.071[99]
    20SeleniteFoliar spray at full heading0.471
    20SelenateFoliar spray at full heading0.640
    Rough rice75SeleniteFoliar spray at late tillering0.440[73]
    75SeleniteFoliar spray at full heading1.290
    75SelenateFoliar spray at late tillering0.780
    75SelenateFoliar spray at full heading2.710
    Polished rice00.027[100]
    15SeleniteFoliar spray at full heading0.435
    45SeleniteFoliar spray at full heading0.890
    60SeleniteFoliar spray at full heading1.275
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    The content of many active components in rough rice is constantly changing during the development of rice. It was found that the content of total flavonoids in brown rice increased continuously from flowering stage to dough stage and then decreased gradually[101]. The γ-oryzanol content in rice decreased by 13% from milk stage to dough stage, and then gradually increased to 60% higher than milk stage at full maturity[101]. The results of Shao et al.[102] showed that the anthocyanin content in rice reached its highest level at two weeks after flowering and then gradually decreased. At full ripeness, and the anthocyanins content in brown rice was only about 50% of the maximum level. The content of total phenolics in rice decreased with maturity from one week after flowering to the fully ripe stage, and the loss of total phenolics reached more than 47% by the fully ripe stage. In contrast, the content of total phenolics in black rice increased with maturity[102]. Moreover, RS content in rough rice decreases during rice maturation[68]. Therefore, the production process of functional rice should be timely and early harvested to obtain higher economic value.

    Pests and diseases seriously impact the yield and quality of rice[103]. At present, the two most effective methods to control pests and diseases are the use of chemical pesticides and the planting of pest and disease-resistant rice varieties. The use of chemical pesticides has greatly reduced the yield loss of rice. However, excessive use of chemical pesticides decreases soil quality, pollutes the environment, reduces soil biodiversity[104], increases pest resistance, and aggravates the adverse effects of pests and diseases on rice production[105]. It also increases residual pesticide levels in rice, reduces rice quality, and poses a severe threat to human health[106].

    Breeding pest and disease-resistant rice varieties are among the safest and effective ways to control rice pests and diseases[107]. In recent years, many pest and disease resistance genes from rice and microorganisms have been cloned[47]. Researchers have used these genes to breed rice varieties resistant to multiple pests and diseases through gene polymerization breeding techniques. Application in production practices delivered good ecological and economic benefits[108].

    Green pest and disease control technologies must consider the synergies between rice and water, fertilizer, and pest and disease management. In this regard, the rice-frog, rice-duck, and other comprehensive rice production models that have been widely used in recent years are the most representative. These rice production models significantly reduced chemical pesticide usage and effectively controlled rice pests and diseases[109]. The nutritional imbalance will reduce the resistance of rice to pests and diseases[110]. Excessive application of nitrogen fertilizer stimulates rice overgrowth, protein synthesis, and the release of hormones, increasing its attractiveness to pests[111]. Increased soluble protein content in rice leaves is more conducive to virus replication and increases the risk of viral infection[112]. Increasing the available phosphorus content in the soil will increase crop damage by pests[113], while insufficient potassium supply will reduce crop resistance to pests and diseases[114]. The application of silica fertilizer can boost the defense against pests and diseases by increasing silicon deposition in rice tissue, inducing the expression of genes associated with rice defense mechanisms[115] and the accumulation of antifungal compounds in rice tissue[116]. The application of silica fertilizer increases the release of rice volatiles, thereby attracting natural enemies of pests and reducing pest damage[117]. Organic farming increases the resistance of rice to pests and diseases[118]. In addition, rice intercropping with different genotypes can reduce pests and diseases through dilution and allelopathy and changing field microclimate[119].

    In conclusion, the prevention and control of rice pests and diseases should be based on chemical and biological control and supplemented by fertilizer management methods such as low nitrogen, less phosphorus, high potassium and more silicon, as well as agronomic measures such as rice-aquaculture integrated cultivation, organic cultivation and intercropping of different rice varieties, etc. The combined use of multiple prevention and control measures can improve the yield and quality of functional rice.

    Functional rice contains many active components which are beneficial to maintaining human health and have high economic and social value with broad market prospects. However, the current development level of the functional rice industry is low. The development of the functional rice requires extensive use of traditional and modern polymerization breeding techniques to cultivate new functional rice varieties with endosperm that can be enriched with multiple active components and have broad-spectrum resistance to pests and diseases. It is also important to select suitable planting locations and times according to the response characteristics of different functional rice active components to environmental conditions.

    This work is supported by the National Natural Science Foundation of China (Project No. 32060430 and 31971840), and Research Initiation Fund of Hainan University (Project No. KYQD(ZR)19104).

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

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  • Cite this article

    Li M, Niu X, Li S, Li Q, Fu S, et al. 2023. Intercellular signaling across plasmodesmata in vegetable species. Vegetable Research 3:22 doi: 10.48130/VR-2023-0022
    Li M, Niu X, Li S, Li Q, Fu S, et al. 2023. Intercellular signaling across plasmodesmata in vegetable species. Vegetable Research 3:22 doi: 10.48130/VR-2023-0022

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Intercellular signaling across plasmodesmata in vegetable species

Vegetable Research  3 Article number: 22  (2023)  |  Cite this article

Abstract: The formation of edible organs and stress adaption are two major focuses of the studies on vegetable species. The regulation of these two processes often involves cell-to-cell signaling. In most plants, including vegetable species, intercellular signaling can be delivered by mobile regulators that traffic through a channel called plasmodesmata connecting almost all cells. A large number of transcription factors and RNAs have been discovered to move across plasmodesmata (called the symplastic way) to travel a short-range or a long-distance. This symplastic transport of signaling molecules has emerged to be an important regulation of a wide range of developmental and physiological processes. Callose deposition to plasmodesmata is a key step controlling the plasmodesmata permeability in many cell types. Here we summarize the recent progress in our understanding of plasmodesmata-mediated signaling in plants.

    • First visualized by Robert Hooke in 1665, cells had long been regarded as individual units of a whole organism. Whether the cell represents an autonomous entity was a question that had been a subject of debate in 19th Century. The observation of intercellular bridges and plasmodesmata supports the idea that the cellular structure forms the protoplasmic continuity, highlighting the importance of reciprocal interaction of cells within a multicellular organism. As a pioneering cell biologist, Wilson wrote in 1923, "it is the 'organism as a whole' and a 'property of the system as such' "[1], almost all plant cells are connected by the intercellular channel called plasmodesmata (PD)[2].

      Primary PD is a straight channel-like structure, as small as 30-50 nm in diameter, connecting two neighboring plant cells[3,4]. A major component of this channel is an endoplasmic reticulum (ER) derived central membranous strands called desmotubles, which form presumably through trapping ER strands in the cell plate during cytokinesis[5,6]. In between the desmotubule and flanking plasma membrane is the cytosolic space called cytoplasmic sleeve[7,8]. Components including cytoskeletons, a GPI-anchor protein and PD localizing proteins (PDLP) have been suggested to participate in the organization and function of plasmodesmata[9, 10].

      More recently, sphingolipids were found to affect the pore size of plasmodesmata[11]. Interestingly, analysis of Physcomitrium patens plasmodesmata proteome suggested the enrichment of cell-wall located proteins including EXORDIUM-family members and xyloglucan transglycosylases in plasmodesmata[12]. In particular, this study identified callose-degrading glycolyl hydrolase family 17 (GHL17) proteins as an abundant PD protein family[12], suggesting the potentially conserved plasmodesmata regulation by callose (will be further discussed later in this review) over the evolution.

      Smaller molecules, ions and metabolic substance can all pass through PD by diffusion. Other micro-molecules including proteins and RNAs are thought to transverse PD via active transport[1115]. Mobile molecules can move across PD via either the cytoplasmic sleeve, or through the desmotubule (in lumen or lateral diffusion in the desmotubule membrane), or via diffusion in the flanking plasma membrane[16,17]. In support of these hypotheses, it was found that the interference of the membrane structure affected PD permeability[17]. In old tissues, plant cells further produce secondary PD that is normally branched and complex in shape. Localized cell wall modification could be involved in secondary PD formation, and the complexity of this type of PD is correlated with reduced PD permeability[18,19]. Nevertheless,the detailed mechanism and the exact roles of secondary PD during development are still far from clear. Interestingly, multiple types of PD were found at grafted wounds, suggesting that different PD types could have distinct functions[20]. In this review, we focus on our current understanding of cell-to-cell signaling across plasmodesmata.

    • The observation of cell-to-cell movement of large molecules initially arose from the micro-injection of fluorescent dye in plant tissues[2124]. The first endogenous protein exhibiting the intercellular mobility is KNOTTED1 (KN1), a homeodomain protein essential for maintenance of the shoot apical meristem (SAM) in maize[25,26]. Recently, the ribosomal RNA-processing protein 44A (AtRRP44A) was shown to mediate the cell-to-cell trafficking of KN1[27]. Since then, a large number of transcription factors were identified in plants that can move between tissues and cells to provide positional instruction during plant development[21]. These mobile regulators can traffic across just a few cell layers to function locally or over a long distance to affect global developmental change.

      One of the central questions in organogenesis is how to spatiotemporally maintain stem cells and specify cell fates. In SAM, WUSCHEL (WUS) is expressed in the organizing center of shoot apical meristem, but the protein moves to the layer1 and 2 (L1 & 2) of shoot apical meristem where WUS triggers CLAVATA 3 (CLV3) expression, which in turn inhibits WUS transcription in L1 and L2 layer[28,29]. With this WUS-CLV3 feedback loop, plants can maintain the stem cell population in proper size in SAM. With the similar strategy, plants maintain the root stem cell niche via WOX5-CLE40 loop, in which WOX5 traffics from quiescent center (QC) to columella stem cell (CSC) to repress the cell differentiation[30]. In Arabidopsis, SHOOT MERISTEMLESS (STM) and ARABIDOPSIS KNOTTED-LIKE (KNAT1)/BREVIPEDICELLUS (BP) are two homologs of the KN1 gene, previously described to be mobile in maize SAM. When driven by an L1 specific promoter, STM and KNAT1 were observed to move from the L1 layer into the inner cell layers of the SAM[31,32]. In addition, KNAT1 was able to pass the interface between cortex and epidermis in Arabidopsis when mis-expressed by a mesophyll specific promoter[33].

      In embryogenesis, TARGET OF MONOPTEROS 7 (TMO7), encoding a bHLH transcription factor, is essential for hypophysis, the founder cell for forming root apex during post-embryonic growth. TMO7 is transcribed in embryonic cells while the TMO7-GFP fusion can be detected in the neighboring hypophysis, indicating a non-cell-autonomy of this regulator[34,35]. In post-embryonic growth, intercellular movement of transcriptional factors regulates a variety of developmental aspects ranging from root radial patterning to root hair and trichome initiation. These mobile regulators including SHORT-ROOT (SHR), CAPRICE (CPC), TRANSPARENT TESTA GLABRA 1 (TTG1), GLABRA 3 (GL3), ENHANCER OF TRY AND CPC 3 (ETC3)/ TRIPTYCHON (TRY), UBIQUITIN-SPECIFIC PROTEASE (UBP1) have been well reviewed previously[15,21]. A previous screen estimated that around 15% of transcriptional factors in roots can move between cells[36]. In contrast, we only have limited understanding of the functionality of these mobile proteins.

      Recently, more mobile transcriptional factors have been identified (summarized in Table 1). Two closely related AT-hook family members, AT-HOOK MOTIF NUCLEAR LOCALIZED PROTEIN 3 (AHL3) and AHL4, were shown to interact in vivo and regulate the boundaries between the procambium and xylem[37]. Interestingly, their interaction seemed to be required for their intercellular trafficking. A SHR target, SCL23 displays a bidirectional radial spread and long-range movement into meristem in Arabidopsis roots. Through direct interaction, SCL23 controls movement of SHR and participate in endodermal specification in the root meristem[38].

      Table 1.  Summary of the mobile transcription factors identified in plants.

      Mobile TFsFunctionMoves from:toReference
      HY5Root growth and N uptakeShoot-to-rootChen et al. (2016)[41]
      DWARF14Regulate the development of AMsThrough phloem into axillary meristems (AMs)Kameoka et al. (2016)[139]
      BdMUTEBdMUTE is required for subsidiary cell formationGMCs to neighboring cell filesRaissig et al. (2017)[97]
      SPCHStomatal cell fateCell-to-cell diffusion in the leaf epidermis of chorusGuseman et al. (2010)[96]
      AN3Leaf developmentFrom the mesophyll to the epidermis in leavesKawade et al. (2013)[140]
      WUSMeristem maintenanceFrom the organizing centre to L1, L2 layersYadav et al. (2011)[28]
      KN1/STMMeristem maintenanceBroadly in the SAMKim et al. (2003)[31], 2005[32]
      PLT2Longitudinal root zonationLongitudinally from the root meristem forming a gradientMahonen et al. (2014)[141]; Galinha et al. (2007)[142]
      SHRRoot radial patterning and RAM maintenanceWithin Stele; Stele into endodermis, QC, CEI and CEDKoizumi et al. (2011)[44], Nakajima et al. (2001)[78]
      AHL3/AHL4Xylem specificationFrom procambium cells to the xylemZhou et al. (2013)[37]
      WOX5Stem cell maintenanceQC to CSCPi et al. (2015)[30]
      TMO7Recruitment of the hypophysisEmbryo into the upper cell of suspensorSchlereth (2010)[34]; Lu et al. (2018)[35]
      Cyp1Root growthFrom leaves to root in tomatoSpiegelman et al. (2015)[143]
      UBP1Transition from cell division to elongationStele and LRC to cells into transition/elongation zoneTsukagoshi et al. (2010)[144]
      SCL23Endodermal cell fateBidirectional radial spread and movement into meristemLong et al. (2015)[38]
      TTG1Trichome patterningAtrichoblasts into trichome initials
      CPCTrichome patterning, root hair initiationTrichome initials into Atrichoblasts; non-root hair cell into root hair cellWester et al. (2009)[90]
      GL3/EGL3Root hair initiationRoot hair cell into non-root hair cellKang et al. (2013)[91]

      Besides the local regulation, transcriptional factors were also found to traffic long-distance between organs to direct global developmental transition in plants in Fig 1. An early example is the detection of FLOWERING LOCUS T (FT) trafficking from leaves where it is synthesized in response to day length, to the SAM to trigger flowering[39,40]. Recently, a light-activated transcriptional factor, ELONGATED HYPOCOTYL 5 (HY5) was shown to move via phloem from shoot-to-root. This translocation of HY5 was proposed to mediate light-activated root growth and N uptake from the soil to balance photosynthetic carbon fixation in the leaf[41].

      Figure 1. 

      Mobile proteins and RNAs in plant development and stress response. The mobile regulators participate widely in the development of different organs (as illustrated). They can travel short-range to regulate local tissue patterning or long-distance to transduce systemic signaling. Gray arrow: phloem-based long-distance movement. WUS and STM regulate SAM maintenance; SPCH, BdMUTE, AN3, TTG1, GL3 and CPC are involved in epidermal patterning. In roots, PLT2, SHR, AtDof4.1, AHL3/AHL4, WOX5, TMO7, UBP1 and SCL23 govern a variety of processes including cell division, radial patterning, stem cell maintenance and developmental transition. Long-distance signaling regulators such as FT and HY5 can traffic from leaves to SAM to promote flowering, and from shoot to root to regulate root growth and nitrate uptake respectively. Environmental stresses can induce PD closure. Small RNAs including miR399d, 827 and 2111 move from aerial parts to roots in response to phosphate starvation.

      Considering the size of transcriptional factors, PD seems to be the most possible way for the intercellular translocation. With an iclas3m system (described in detail in a later part of this review) that blocked the PD between stele and endodermis, SHR intercellular transport was terminated[3]. Another piece of evidence supporting PD transport of transcriptional factors is the blocked movement of TMO7 from meristematic cells into the root cap in the cals3-2d, a mutant in which PD is restricted by over-accumulated callose[35]. To get access to PD, transcriptional factors could exploit intracellular apparatus including microtubules and endomembrane delivery system[42,43]. Besides, an unknown function protein named SHR INTERACTING EMBRYONIC LETHAL (SIEL) was shown to interact with a number of mobile transcriptional factors and the mutation of this gene seemed to reduce SHR intercellular movement[44]. As SIEL partially localized to endosomes, it was proposed that this protein could function as a 'shuttle' to facilitate delivery of mobile transcriptional factors. In addition, some facilitating proteins have also been identified. After passing through PD, a few mobile proteins including APS KINASE 1 (KN1), SHOOT MERISTEMLESS (STM) and TRANSPARENT TESTA GLABRA 1 (TTG1) were discovered to associate with a group of type II chaperonin complexes consisting of CHAPERONIN CONTAINING T-COMPLEX POLYPEPTIDE-1 SUBUNIT 7 and 8 (CCT7 & CCT8), which facilitate the movement possibly by promoting the protein refolding after the PD cross-over[27].

      Although no specific domain has been identified that accounts for intercellular mobility, the cell-to-cell transport of transcriptional factors seemed to be protein sequence-dependent. Homeodomain (HD) and the helical domains have been shown to be necessary and sufficient for PD-mediated transport of KN1. Unlike this, three conserved domains (HD, WUS-box, and EAR-like domain) in WUS are not required for its movement. Instead, WUS mobility seems to be controlled by a non-conserved sequence between the HD domain and WUS-box[29]. Despite triple GFP Tag impaired TMO7 movement, protein size did not seem to be the primary determinant of intercellular transport. Instead, TMO7 was found to move in a sequence-dependent manner, and both nuclear residence and protein modification are important for TMO7 mobility[35]. In two other mobile transcriptional factors, CPC and SHR, the mobility relied on multiple regions within the proteins. In addition, the mobility of these two proteins seemed to be associated with the subcellular distribution in both the cytoplasm and the nucleus.

      In addition to transcriptional factors, small RNAs also participate in transcriptional regulation of diverse developmental and physiological events in plants. Small RNAs are 21−24 nt long and can be generally divided into siRNAs and miRNAs[45]. Small RNAs function either through degrading target genes by near-perfect complementarity, or via transcriptional silencing by histone modification and DNA methylation[4650]. Small RNAs were often regarded as the long-distance signals as the initial efforts dissecting their mobility exploited the grafting system in which mutants defective in small RNAs biogenesis were included. Facilitated by high-throughput sequencing techniques, researchers identified a large number of mobile siRNAs that can traffic from shoot to root presumably via phloem. Besides siRNA, a large number of miRNAs were discovered to traffic in phloem exudates over long distance. Low-phosphate induced miR399s exhibited a shoot-to-root movement to repress downstream targets including PHO2 in the root[51]. Similarly,miR399d, miR827 and miR2111 were all found in grafting experiments to relocate from aerial parts to roots in response to phosphate starvation[52]. During rhizobial infection, miR2111 functioned as long-distance signals to post-transcriptionally regulate symbiosis suppressor TOO MUCH LOVE in roots[53]. miR395 can also translocate from wild-type scions to rootstocks of the miRNA processing mutant hen1-1 to target the APS gene[54]. In addition, both miR156 and miR172 have been confirmed as potentially phloem-mobile miRNAs that regulate tuber formation[5557].

      In grafting system, only small RNAs transporting from shoot-to-root via phloem could be analyzed. Other approaches that allow for the comparison between the expression areas and in situ RNA distribution patterns may help the identification of small RNAs acting locally as non-cell autonomous signals. To establish adaxial–abaxial leaf polarity, a member of Trans-acting small interfering RNA (ta-siRNA) family forms a gradient across the leaves by intercellular diffusion. This diffusion-driven pattern of ta-siRNA shapes the expression pattern of AUXIN RESPONSE FACTOR3 (ARF3), an abaxial determinant gene. Another small RNA, miR390 was proved to regulate the leaf polarity by the cell-to-cell movement from vasculature and pith region below the shoot apical meristem to the vegetative apex[54]. In addition, miRNA165/166 were discovered to move from the endodermis into the stele to regulate the xylem cell fate[58]. Moreover, miR394 was shown to regulate stem cell maintenance in SAM by the PD-mediated movement from L1 to inner cell layers to repress LEAF CURLING RESPONSIVENESS (LCR) expression[59].

      In addition to siRNA and miRNA, mRNAs have also been found to travel beyond the cells in which they are expressed in Fig 1. In addition to the early example of mobile mRNAs of KN1, potato sucrose transporter SUC1 mRNA was also confirmed to be mobile. In grafting experiments, a number of mRNAs were found to travel, such as FT, FVE and AGL24 in Arabidopsis[60], Aux/IAA in melon and Arabidopsis[61], PP16 and NACP in pumpkin[62,63], BEL5 and POTH1 in potato, SLR/IAA14 in apple[64], PFP-T6 and PS in tomato[65] (summarized in Table 2). Recently, Luo et al. developed a fluorescence-based mRNA labeling system to identify mobile mRNAs targeted to PD[66]. Their analyses revealed that only mobile rather than not non-mobile mRNAs were selectively targeted to PD, providing further evidence for PD mediated transport of mRNAs. Interestingly, using a Nicotiana benthamiana/tomato heterograft system, Xia et al. found some mRNAs have bidirectional mobility between shoots and roots. In addition, forced expression of non-mobile mRNAs in the companion cells did not confer the mobility[6771]. Thus, the movement of mRNA is likely an actively regulated process. Moreover, a large number of graft-transmissible mRNAs have been identified by high throughput sequencing in a variety of species including Arabidopsis, tobacco, grape, cucumber and tomato[6772].

      Table 2.  List of mobile RNAs with functions in organ development.

      Mobile factorFunctionMoves from: toReference
      mRNA
      KN1SAM maintenanceinjected cell to neighbouring cellsLucas et al. (1995)[26]
      SUC1Sucrose transportcompanion cells to sieve elementsKuhn et al. (1999)[145]
      FT1Flowering inductionLeaf to SAMLu et al. (2012)[60]
      Aux/IAA18Root developmentLeaf to rootNotaguchi et al. (2012)[61]
      PP16RNA transportPhloem to shoot apexXoconostle-Cazares et al. (1999)[62]
      NACPMeristem maintenancePhloem to shoot apexRuiz-Medrano et al. (1999)[146]
      StBEL5Tuber formationLeaf to rootBanerjee et al. (2009)[147]
      POTH1Leaf developmentLeaf to rootMahajan et al. (2012)[148]
      SLR/IAA14Lateral root formationShoot to rootKanehira et al. (2010)[64]
      PFP-T6Leaf developmentLeaf to leaf primordiaKim et al. (2001)[65]
      PSPathogen resistanceShoot to root and vice versaZhang et al. (2018)[149]
      GAILeaf developmenthost to parasiteRoney et al. (2007) [150]; David-Schwartz et al. (2008)[151]
      ATCFloral initiationLeaf to flower apicesHuang et al. (2012)[152]
      FVEfloral regulatorsRoot to SAMYang and Yu (2010)[153]
      AGL24floral regulatorsRoot to SAMYang and Yu (2010)[153]
      siRNA
      ta-siRNAEstablishment of leaf polaritythe adaxial to the abaxial side of the leafChitwood et al. (2009)[154]
      hc-siRNADNA methylationShoot to rootBaldrich et al. (2016)[155]
      miRNA
      miR165/166Xylem specificationendodermis into the steleCarlsbecker et al. (2010)[58]
      miR390Leaf polarityvasculature and pith region below the SAM to SAMChitwood et al. (2009)[154]
      miR394Meristem maintenanceL1 to inner layers in the shoot meristemKnauer et al. (2013)[59]
      miR395Sulfate homeostasisgraft unionsBuhtz et al. (2010)[54]
      miR399dPhosphate homeostasisshoot to root and vice versaPant et al. (2008)[156]; Lin et al. (2008)[51]
      miR172regulate tuber formationLeaf to rootMartin et al. (2009)[55]
      miR2111Phosphate homeostasis;
      Rhizobial infection;
      shoot to root and vice versaHuen et al. (2017)[52];
      Tsikou et al. (2018)[53]
      miR827Phosphate homeostasisshoot to root and vice versaHuen et al. (2017)[52]
    • A plant organ is usually composed of morphologically and functionally different cell types in different positions. Small molecules can move between cells and across plasmodesmata, which mediates crucial intercellular communication for the growth and development of plant tissues and organs. For example, a plant root is composed of concentrically arranged cell layers with epidermis, cortex, endodermis, and stele locating from outside to inside[73]. This anatomic arrangement highlights the regulation of tissue patterning instructed by positional information, often through the exchange of signaling molecules between cells. A number of developmental processes including root radial patterning, root hair initiation and trichome formation, have emerged as the model system for studying tissue patterning in plants.

      In root, the formation of the endodermal cell layer starts from the endodermal and cortex initial cells in root stem cell niche, where two transcriptional factors, SHR and SCARECROW (SCR) promote the expression of CYCD6;1 to allow the switch of cell division pattern from anticlinal to periclinal[7477]. This results in the formation of two distinct layers of cells within the ground tissue, and the role of SHR in specifying the endodermal layer was proposed based on the fact that the endodermal layer was completely absent in shr-2 mutant. Intriguingly, SHR expression is restricted in stele, but the SHR protein is actively transported through PD from stele toward the outside to play non-cell-autonomous roles[78,79]. In the enodermis, SHR directly activates SCR which, in turn, physically binds to SHR to trap this mobile transcription factor in the nucleus of the endodermis, preventing further movement[77]. This mechanism was discovered to be conserved in rice and thus was proposed to be an evolutionarily conserved mechanism defining a single endodermal cell layer in almost all land plants[74]. However, a study on rice SHR homologs suggested that SHR alone is insufficient to determine endodermal cell fate[80]. Consistent with this argument, mis-expression of SHR indicated that SHR ability to confer endodermal identity partially relied on cell lineage and was coordinated by uncharacterized positional information, presumably derived from stele.

      Specific expression of marker genes, as often used previously to determine endodermal cell fate, is sometimes misleading. A prominent feature of the endodermis is the formation of the Casparian Strip (CS), an apoplastic barrier between vascular tissues and outer ground tissues[81]. The presence of functional CS is therefore a better trait for precise evaluation of endodermal identity. Two recent studies revealed that SHR does serves as a master regulator activating a hierarchical downstream network for CS formation[82,83]. The combination of SHR mediated cascade and another independent peptide signal derived from stele forms the minimum set of regulators that program endodermal identity, exemplified by the formation of functional CS[83]. Since both SHR and the peptide are specifically expressed in vascular tissues, CS formation represents the elaborate developmental control by stele-to-endodermis movement of mobile regulators. Besides CS, SHR and its downstream target SCR can activate the expression of miRNA165/166 in the endodermis which in turn moves back to vasculature to repress a class III homeodomain-leucine zipper transcription factors for proper xylem formation[58]. Thus the reciprocal communication between ground tissue and vasculature in root spatially defines the radial patterning in root. In Cardamine, a recent study indicated that a differential spatial distribution of miR165/166 is responsible for forming the extra cortex layer[84]. In addition to roots, miR165/166 also function in other organs including leaf primordial and ovule. By restricting PHB expression in incipient inner integument, miR165/166 promotes the correct ovule patterning[85]. Interestingly, a callose synthase mutant in maize, named tie-dyed2 (tdy-2), affects the development of vasculature, suggesting the mechanism of vascular development directed by intercellular communication (possibly via miR165/166) is likely conserved in crops[86,87]. In addition to roots, plasmodesmata also plays a key role in regulating leaf development, particularly the formation of leaf veins[88].

      Trichomes and root hairs, originating from the epidermis in leaves and roots respectively play important roles in protecting plants from bio/abiotic stresses, and promoting nutrient absorption[89,90]. In Arabidopsis, the initiation of trichomes and root hairs is precisely patterned in epidermis, indicating an essential role of cell-to-cell communication in these processes.

      In trichome initiation, both positive regulator TRANSPARENT TESTA GLABRA (TTG1) and negative regulator ENHANCER OF TRY AND CPC 3 (ETC3) and CAPRICE (CPC) move between cells. In incipient trichome cells, TTG1 protein accumulates through a trapping/depletion mechanism mediated by GLABRA3 (GL3)[91]. On the other hand, the repressor of ETC3 and CPC move into the neighboring non-trichome cells (also regulated by GL3), forming inactivated MYB/bHLH/WD40 to inhibit the development towards trichomes[92]. Recently, PdBG4 has been implicated in regulating PD permeability in Arabidopsis trichome development[93]. In root hairs, CPC serves as a positive regulator and it is trapped in the hair-position root epidermis by interacting with EGL3 and GL3 after the movement[94]. The trn1 mutant is defective in the position-dependent pattern of root hairs and cause the ectopic expression of WER, GL2 and EGL3, suggesting that TRN1 also participates in the position-dependent cell fate determination[95,96].

      Stomata on epidermis are responsible for water and gas exchange between the plants and the environments. The mature stomata structure is produced through successive cell division and differentiation process, with both processes subject to highly spatiotemporal regulation[97]. In a GLUCAN SYNTHASE-LIKE 8 (GSL8) mutant in which normal callose deposition is disrupted, SPCH-GFP diffused to neighboring cells from meristemoids, resulting in excessive proliferation of stomatal-lineage cells. This observation suggests that proper gating of critical regulators, likely through callose regulation, regulates the correct patterning of stomata complex[98]. MUTE, another key transcriptional factor required to terminate asymmetric division and promote the transition of meristemoids to GMCs, was shown in Brachypodium to move from GMCs to neighboring cells to induce the subsidiary cells (SCs) formation[99].

    • Plants respond to stresses often by accumulation of callose, which is negatively correlated with PD permeability in Fig 2. A variety of abiotic stresses have been associated to callose induction, such as cold stress[100,101], wounding[102,103], heat stress[104,105], and heavy metals[106109]. Although detailed mechanism is not entirely clear, callose synthases were found to participate in the callose regulation. In Arabidopsis, there are 12 callose synthase (CalS) family members. When exposed to excess iron, the cals5 and cals12 mutants showed an attenuated callose deposition in phloem, compared to wild type and other cals mutants. This result suggests that cals5 and cals12 may play specific roles in iron stress response in Arabidopsis[110]. In tomato, cold stress has long been known to cause catfacing fruits or malformed fruits by breeders and gardeners. A recent study proved this phenomenon was caused by the restriction of SlWUS intercellular movement via plasmodesmata in floral meristem[101]. The cold induced callose accumulation blocked the plasmodesmata, resulting in the excessive activation of CLV3 and TAG1, and disrupted WUS-CLV3/WUS-TAG1 negative feedback loops[101].

      Figure 2. 

      Regulation of PD permeability by callose. (a) Schematic illustration of regulation of the PD aperture by callose deposition in flanking regions of PD. Induced callose accumulation closes PD permeability and blocks the intercellular movement of transcription factors and small RNAs. (b) The design of ‘icals3m’ system that can inducibly (via estradiol induction cassette) promote callose deposition in specific cell types (via cell-type specific promoters)[128],[138].

      It has been reported that PD regulation serves as an innate defense strategy[111]. Pathogens trigger both pathogen-associated molecular pattern (PAMP) and PAMP-triggered immunity (PTI) systems, which have been reported to induce callose deposition[112]. Upon SMV virus invasion, callose was accumulated in soybean phloem which prevents the virus from traveling long distances[113]. Salicylic acid (SA) is a plant immune signal produced upon pathogen infection, which has also been shown to trigger PD closure and affect symplastic communication. Elevation of SA level seemed to be necessary for the PD response during bacterial infection, and the expression of bacterial derived salicylate hydroxylase (NahG) gene in plants resulted in higher susceptivity to bacteria[113]. Biotic stresses including pathogen infection are known to modulate ROS level and callose abundance in infected regions, which is presumably responsible for the altered PD permeability[114,115].

      Virus can also regulate the mesenchymal plasmodesmata in tobacco[109] and it was recently reported that ROS-mediated PD closure is controlled by multiple pathways, either in SA- or PDLP5-dependent manners. Change of callose level in biotic stresses is also modulated by callose synthase members[112,113]. SA-dependent PD regulation requires the function of callose synthase1 (CalS1). However, the CalS8 seemed to be more involved in basal and ROS-dependent PD regulation[103]. Callose synthase members have also been widely reported in recent years. CsCalS4 function was identified in pollen development in cucumber, and CsCalS1/8 homologous genes were induced by cucumber fungus and functioned as the key factors in response to biological stress[114]. GhCalS5 and ZmCals were found to promote callose synthesis in cotton and maize in responsive to stresses[116,117].

      In addition, PD-localized proteins also emerged as the regulator of PD aperture during biotic stresses. It was shown that the PD closure triggered by chitin was dependent on the activity of PD-localized receptor-like protein LYM2[111]. Besides, bacterial flagellin could rapidly activate the expression of CML41, a PD-localized Ca2+-binding protein, which is necessary for the induction of callose at PD.

      Callose is the linear polysaccharide that is composed of β-1,3-glucan. It is a component of cell wall and is frequently found to deposit at PD, where it is believed to control the PD permeability during plant development and stress response. It was found the precise developmental transition often relies on the regulation of symplastic continuity. In birch, bud dormancy entry and release are associated with the shift between callose production and turnover. Callose accumulation at PD in the shoot apical and rib meristems can seal off the symplastic communication and promote the bud dormancy[116121]. A period of chilling, however, triggers gibberellin biosynthesis, resulting in increased expression of 1,3-β-glucanases and degradation of callose. Accumulating evidence suggests that callose regulation is actually implicated in a wide range of developmental processes, including seed germination, embryogenesis, cell division, flowering and reproduction[122124]. In tomato, a short period of cold stress is sufficient to induce callose accumulation in floral meristem and blocked intercellular movement of SlWUS, resulting in malformed fruits[101]. In olives, callose deposition, as part of cell wall modification, regulates fruit abscission[114].

      Through a genetic screen for defective vascular development, Vaten et al. (Helariutta group) identified three semi-dominant alleles of CALLOSE SYNTHASE 3 (cals3d) that caused an increase in callose deposition at PD and abnormal plant growth[3,19]. In the root, cals3d mutants all showed aberrant radial patterning and misspecification of the phloem and the xylem. Consistent with these phenotypes, cals3d roots exhibited decreased PD-mediated symplastic movement of free GFP, SHR and miRNA165/66[3,125]. It thus seemed that the identified dominant mutations can substantially enhance the ability of CALS3 to promote callose deposition at PD. By combining these mutations in a vector containing LexA-VP16-ER (XVE)-based estradiol inducible cassette, the Helariutta group designed an elegant tool named as the 'icals3m system'. Driven by specific promoters, this system can potentially be used to temporally manipulate callose at PD and symplastic communication in particular cell types[3,126].

      The initial attempts using this system in vascular tissues and lateral root development proved to be successful[3,125,127]. With specific induction of icals3m system in xylem pole pericycle, Benitez-Alfonso et al. detected a significantly increased number of initiated primordial [126]. Together with the observation of a transient symplastic isolation of the primordium prior to emergence, they confirmed the essential role of callose based symplastic connectivity between pericycle cells, founder cells, and the neighboring tissue during lateral root patterning[122]. More recently, icals3m system was used to dissect the roles of symplastic communication in root apical stem[122]. Driven by an endodermis-specific EN7 promoter, icals3m induced symplastic blockage led to severe root patterning defects, shown by disrupted cell division direction, misspecification of cell fate as well as impaired cell polarity. In root tip, different cell types including endodermis all derived from the root stem cell niche, where QC was believed to repress the differentiation of surrounding stem cells based on an early classic laser ablation experiment carried out in the 1990's[127]. However, icals3m system provides an alternative non-invasive approach to examine the role of QC. With the expression under WOX5 promoter, icals3m system was clearly shown to induce callose specifically in QC[128]. The visible callose signal based on aniline blue staining was detected as quickly as 6 h after the estradiol induction[129]. This icals3m system was further used to study the interaction between root cap and the root meristem[124,128130]. When the symplastic communication between root cap and root meristem was disrupted, developmental defects were observed in both parts: In meristem, stem cell maintenance was affected while in root cap the starch granules, the marker commonly used as an indicator of columella differentiation, disppeared[125]. An earlier study showed that starch granules in columella cells relied on auxin concentration[131]. In this study, short-term disruption of symplastic communication was sufficient to cause defects in stem cells, while it took longer for auxin distribution in root meristem to occur[125]. In fact, plasmodesmata itself can act as the channel for auxin flow[131,132]. Furthermore, icals3m system also was employed in the study of phloem unloading[132]. A phloem pole pericycle specific promoter CalS8 and a companion cell and metaphloem sieve element specific promoter psAPL were both used to drive icals3m to block the connection between different phloem cell types[133]. A direct developmental defects arose from the blocked plasmodesmata in phloem was the reduced growth of axillary buds[50].

      To summarize, callose regulation is a central mechanism to control symlastic communication during plant development. Spatiotemporal expression of icals3m system can be an effective tool to deepen our understanding of the developmental regulation mediated by symplastic signals. The power of this system can be even higher with the combination with other techniques including cell type specific OMICs. The application of this system in vegetable studies would greatly enhance our ability to dissect various aspects of development and physiology in vegetable species ranging from fruit development to stress resistance.

    • Intercellular signaling across plasmodesmata plays crucial roles in a wide range of processes in plants. The currently identified signaling molecules across plasmodesmata are mainly transcription factors and RNAs. However, accumulating evidence suggests that many other signaling pathways including calcium signaling, redox signaling, phosphorylation signaling, and hormone signaling can also function in non-cell-autonamous manner[134136]. As these pathways are often complex and interplay with each other, it is still difficult to unravel such non-cell-autonamous functions. With the advance in high-resolution imaging techniques, such as super-resolution microscopy, researchers will be able to visualize in vivo the action and mobility of the molecular players involved in intercellular signaling[137].

      In addition to visualizing the intercellular mobility of molecules, it is crucial to precisely evaluate the phenotype with a specific intercellular signaling disrupted. Developing cell type specific approaches is the key step and thus identification of promoters with restricted expression in certain cell types is important. Furthermore, abolishing gene function in a specific cell type is a valuable tool for studying intercellular signaling. Previously, cell-specific RNAi was employed but the intercellular mobility of small RNAs prevents the precise evaluation of gene function. Recent rapid development of CRISPR-Cas9 technique has emerged as a powerful tool for this purpose. The combination of cell-specific expression of Cas9 with reporters that allows for visualizing the gene editing in different cells could greatly enhance our ability to precisely evaluate the function of mobile regulators.

      Lastly, to gain a more comprehensive understanding of the plasmodesmata mediated intercellular signaling, it is important to integrate multiple approaches, such as high-resolution imaging, single-cell technique, multi-omics, and computational modeling. Although the cell-to-cell signaling often occurs locally, the impact could be systemic in plants. The complete assessment of plasmodesmata-mediated intercellular signalling, as well as derived tissue- or cell-type-specific techniques, will not only benefit the study of plant development, but also provide the opportunity for future biotechnological renovation of plants.

      • This work was supported by carbon-nitrogen high efficiency grants from Fujian Agriculture and Forestry University (118992201A).

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

      • Copyright: © 2023 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/.
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    Li M, Niu X, Li S, Li Q, Fu S, et al. 2023. Intercellular signaling across plasmodesmata in vegetable species. Vegetable Research 3:22 doi: 10.48130/VR-2023-0022
    Li M, Niu X, Li S, Li Q, Fu S, et al. 2023. Intercellular signaling across plasmodesmata in vegetable species. Vegetable Research 3:22 doi: 10.48130/VR-2023-0022

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