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Phloem exudate metabolic content reflects the response to water deficit stress in pea plants (Pisum sativum L.)
Abstract
Drought stress impacts the quality and yield of Pisum sativum. Here we show how short periods of limited water availability during the vegetative stage of pea alters phloem sap content and how these changes are connected to strategies used by plants to cope with water deficit. We have investigated metabolic content of phloem sap exudates and explored how this reflects P. sativum physiological and developmental responses to drought. Our data shows that drought is accompanied by phloem‐mediated redirection of the components that are necessary for cellular respiration and proper maintenance of carbon / nitrogen balance during stress. The metabolic content of phloem sap reveals a shift from anabolic to catabolic processes as well as the developmental plasticity of pea plants subjected to drought. Our study underlines the importance of phloem mediated transport for plant adaptation to unfavourable environmental conditions. We also show that phloem exudate analysis can be used as a useful proxy to study stress responses in plants. We propose that the decrease in oleic acid content within phloem sap could be considered as a potential marker of early signalling events mediating drought response.
... Numerous studies have shown that the transportation of amino acids between source and sink tissues is influenced by genotype, relative capacity between source and sink, and external environment (Hunt et al. 2010;Nam et al. 2022;Sakamoto et al. 2022). A study on 17 maize varieties found significant differences in the content of Pro, Asn, and His in the secretion of the phloem of different strains (Yesbergenova-Cuny et al. 2016); Other studies found that drought stress significantly increased the content of amino acids such as Pro, Glu, Ala, and GABA (γ-aminobutyric acid) in the secretion of the phloem (Blicharz et al. 2021;Liu et al. 2013). Research on grapes found that the peak amino acid content in the secretion of the phloem occurs during vigorous growth stages such as flowering and fruit setting (Gourieroux et al. 2016). ...
The weighted gene co-expression network analysis and antisense oligonucleotide-mediated transient gene silencing revealed that CsAAP6 plays an important role in amino acid transport during tea shoot development.
Nitrogen transport from source to sink is crucial for tea shoot growth and quality formation. Amino acid represents the major transport form of reduced nitrogen in the phloem between source and sink, but the molecular mechanism of amino acid transport from source leaves to new shoots is not yet clear. Therefore, the composition of metabolites in phloem exudates collected by the EDTA-facilitated method was analyzed through widely targeted metabolomics. A total of 326 metabolites were identified in the phloem exudates with the richest variety of amino acids and their derivatives (93), accounting for approximately 39.13% of the total metabolites. Moreover, through targeted metabolomics, it was found that the content of glutamine, glutamic acid, and theanine was the most abundant, and gradually increased with the development of new shoots. Meanwhile, transcriptome analysis suggested that the expression of amino acid transport genes changed significantly. The WGCNA analysis identified that the expression levels of CsAVT1, CsLHTL8, and CsAAP6 genes located in the MEterquoise module were positively correlated with the content of amino acids such as glutamine, glutamic acid, and theanine in phloem exudates. Reducing the CsAAP6 in mature leaves resulted in a significant decrease in the content of glutamic acid, aspartic acid, alanine, leucine, asparagine, glutamine, and arginine in the phloem exudates, indicating that CsAAP6 played an important role in the source to sink transport of amino acids in the phloem. The research results will provide the theoretical basis and genetic resources for the improvement of nitrogen use efficiency and tea quality.
... The transmission of chemical signals from the roots to shoots through the xylem flow to affect growth, reproduction time and stomatal function is an integral part of the plant's initial responses to water scarcity (Li et al., 2021). Blicharz et al. (2021) reported that pea plants could manage their growth in water-deficient conditions by altering the content of phloem exudate. Their study showed that the decline in oleic acid content in the phloem sap occurs before the soil reaches the point of wilting, which can be a potential indicator of early signalling events in response to drought (Table 4). ...
Drought is increasingly frequent in the context of climate change and is considered a major constraint for crop yield. Water scarcity can impair growth, disturb plant water relations and reduce water use efficiency. Pea (Pisum sativum) is a temperate grain legume rich in protein, fibre, micronutrients and bioactive compounds that can benefit human health. In reducing pea yield because of drought, the intensity and duration of stress are critical. This review describes several drought resistance mechanisms in pea based on morphology, physiology and biochemical changes during/after the water deficit period. Drought tolerance of pea can be managed by adopting strategies such as screening, breeding and marker‐assisted selection. Therefore, various biotechnological approaches have led to the development of drought‐tolerant pea cultivars. Finally, the main objective of the current research is to point out some useful traits for drought tolerance in peas and also, mention the methods that can be useful for future studies and breeding programmes.
... This phenomenon can be partially explained by a decrease in the photosynthetic rate (reduction in CO2 consumption) and an increase in the metabolic CO2 production during stress. Our observations suggested that plants reduced water loss by limiting transpiration and attempted to cope with reduced energy production (the decrease in photosynthetic intensity) by increasing their catabolic processes and redistributing carbon [37]. Osmotic adjustment is an important mechanism of drought tolerance that helps retain water in plant tissues despite a low water potential [38]. ...
Research on mitigating the effects of water scarcity by applying silicon to perennial grasses is still insufficient. This study was conducted to investigate the effect of spring and summer droughts and silicon applications on gas exchange parameters; the morphometric characteristics of root systems; and the biomass distribution of Festulolium braunii, Festuca arundinacea, and Lolium perenne cultivars. Plants were treated with a drought during the tillering phase once a year (during spring or summer regrowth) for 21 days. Foliar nutrition with silicon was applied twice under the drought conditions. Grasses in a pot experiment were cut three times during vegetation. The plants that were exposed to the drought had lower values of the gas exchange parameters than those that were well watered. The beneficial effect of silicon was related to the reduction of excessive water loss through transpiration during the spring drought. Under the drought and silicon applications, the water use efficiency, root dry mass, and length increased compared to the control. Moreover, silicon increased the proportion of both the finer and thicker roots in F. braunii and L. perenne, while the distribution of the root diameter changed least in the more resistant F. arundinacea. Silicon also reduced the carbon content in the roots and increased root carbon accumulation. Our results indicated that Si may help perennial forage grasses cope better with drought stress. This was due to the allocation of carbon to the roots to develop the fine root network, increasing the length and root biomass and improving the water use efficiency.
... In seven-day-old pea seedlings, an earlier accumulation of sucrose was observed in roots than in epicotyl after 24 h of dehydration, followed by an accumulation of galactinol and raffinose (RFOs family) in both organs (Lahuta et al., 2014). Therefore, drought stress increases the content of sucrose, glucose, and sugar alcohol in the phloem sap of pea to sustain osmotic potential, water content and transport, and maintain cell metabolism (Blicharz et al., 2021) (Table 1). Thus, water deficit response induces metabolic modifications, some of which are linked to source/sink relationships (Lemoine et al., 2013). ...
Grain legumes are major food crops cultivated worldwide for their seeds with high nutritional content. To answer the growing concern about food safety and protein autonomy, legume cultivation must increase in the coming years. In parallel, current agricultural practices are facing environmental challenges, including global temperature increase and more frequent and severe episodes of drought stress. Crop yield directly relies on carbon allocation and is particularly affected by these global changes. We review the current knowledge on source‐sink relationships and carbon resource allocation at all developmental stages, from germination to vegetative growth and seed production in grain legumes, focusing on pea (Pisum sativum). We also discuss how these source‐sink relationships and carbon fluxes are influenced by biotic and abiotic factors. Major agronomic traits, including seed yield and quality, are particularly impacted by drought, temperatures, salinity, waterlogging or pathogens and can be improved through the promotion of beneficial soil microorganisms or through optimized plant carbon resource allocation. Altogether, our review highlights the need for a better understanding of the cellular and molecular mechanisms regulating carbon fluxes from source leaves to sink organs, roots and seeds. These advancements will further improve our understanding of yield stability and stress tolerance and contribute to the selection of climate‐resilient crops. This article is protected by copyright. All rights reserved.
... The accumulation of homoserine, but not asparagine, in pea leaves under drought has been shown previously [39,51]. It is possible that the drought-induced changes in homoserine, asparagine, and glutamine content were due to a disruption of phloem transport [52,70]. ...
The metabolic re-arrangements of peas (Pisum sativum L.) under soil drought and re-watering are still not fully explained. The search for metabolic markers of the stress response is important in breeding programs, to allow for the selection drought-resistant cultivars. During the present study, changes in the polar metabolite content in pea plant shoots were measured under repeated short-term soil drought and subsequent re-watering. A gas chromatograph, equipped with a mass spectrometer (GC-MS), was used for the metabolite profiling of pea plants during their middle stage of vegetation (14–34 days after sowing, DAS). The major changes occurred in the concentration of amino acids and some soluble carbohydrates. Among them, proline, γ-aminobutyric acid (GABA), branched-chain amino acids, hydroxyproline, serine, myo-inositol, and raffinose were accumulated under each soil drought and decreased after re-watering. Besides, the obtained results show that the first drought/re-watering cycle increased the ability of pea plants to restore a metabolic profile similar to the control after the second similar stress. The accumulation of proline seems to be an important part of drought memory in pea plants. However, confirmation of this suggestion requires metabolite profiling studies on a broader spectrum of pea cultivars.
... , P. persica Rieger 2002, Morandi et al. 2008) A. thaliana (Aguayo et al. 2013, Nosarzewski et al. 2012 Transport evidence P. cerasus , M. domestica , Watari et al. 2004 P. major (Fu et al. 2011, Ramsperger-Gleixner et al. 2004), A. thaliana (Klepek et al. 2005), gramineae crops (Kong et al. 2020) Pinitol Presence in tissues Eucaliptus sp., Acacia sp. (Merchant et al. 2006) L. decidua, P. mariana, P. abies, P. sylvestris , Gallinger and Gross 2018, Merchant et al. 2006, Simard et al. 2013 Glycine max (Streeter et al. 2001) Presence in phloem sap B. papyrifera (Shi et al. 2020) P. abies, Abies alba, P. sylvestris, L. deciduas (Gallinger and Gross 2018); P. pinaster (Devaux et al. 2009) Medicago sativa (Campbell et al. 1984), P. sativum (Blicharz et al. 2021), Lupinus angustifolius (Merchant 2012) ...
Plants constitute 80% of the biomass on earth, and almost two thirds of this biomass is found in wood. Wood formation is a carbon demanding process and relies on carbon transport from photosynthetic tissues. Thus, understanding the transport process is of major interest for understanding terrestrial biomass formation. Here we review the molecules and mechanisms used to transport and allocate carbon in trees. Sucrose is the major form in which carbon is transported, found in the phloem sap of all so far investigated tree species. However, in several tree species sucrose is accompanied by other molecules, notably polyols and the raffinose family of oligosaccharides. We describe the molecules that constitute each of these transport groups, and their distribution across different tree species. Further, we detail the metabolic reactions for their synthesis, the mechanisms by which trees load and unload these compounds in and out of the vascular system, and how they are radially transported in the trunk and finally catabolized during wood formation. We also address a particular carbon recirculation process between phloem and xylem that occurs in trees during the annual cycle of growth and dormancy. A search of possible evolutionary drivers behind the diversity of C carrying molecules in trees reveals no consistent differences in carbon transport mechanisms between angiosperm and gymnosperm trees. Furthermore, the distribution of C forms across species suggests that climate related environmental factors will not either explain the diversity of carbon transport forms. However, the consideration of C transport mechanisms in relation to tree-rhizosphere coevolution deserves further attention. To conclude the review, we identify possible future lines of research in this field.
Plant cells are capable of uptaking exogenous organic substances. This inherited trait allows the development of heterotrophic cell cultures in various plants. The most common of them are Nicotiana tabacum and Arabidopsis thaliana. Plant cells are widely used in academic studies and as factories for valuable substance production. The repertoire of compounds supporting the heterotrophic growth of plant cells is limited. The best growth of cultures is ensured by oligosaccharides and their cleavage products. Primarily, these are sucrose, raffinose, glucose and fructose. Other molecules such as glycerol, carbonic acids, starch, and mannitol have the ability to support growth occasionally, or in combination with another substrate. Culture growth is accompanied by processes of specialization, such as elongation growth. This determines the pattern of the carbon budget. Culture ageing is closely linked to substrate depletion, changes in medium composition, and cell physiological rearrangements. A lack of substrate leads to starvation, which results in a decrease in physiological activity and the mobilization of resources, and finally in the loss of viability. The cause of the instability of cultivated cells may be the non-optimal metabolism under cultural conditions or the insufficiency of internal regulation.
Nitrogen transport from source to sink is crucial for tea shoots growth and quality formation. Amino acid represents the major transport form of reduced nitrogen in the phloem between source and sink, but the molecular mechanism of amino acid transport from source leaves to new shoots is not yet clear. Therefore, the composition of metabolites in phloem exudates collected by the EDTA-facilitated method was analyzed through widely-targeted metabolomics. A total of 326 metabolites were identified in the phloem exudates with the richest variety of amino acids and their derivatives (93), accounting for approximately 39.13% of the total metabolites. Moreover, through targeted metabolomics, it was found that the content of glutamine, glutamic acid, and theanine was the most abundant, and gradually increased with the development of new shoots. Meanwhile, transcriptome analysis suggested that the expression of amino acid transport genes changed significantly. The WGCNA analysis identified that the expression levels of CsAVT1 , CsLHTL8 , and CsAAP6 genes located in the MEterquoise module were positively correlated with content of amino acids such as glutamine, glutamic acid, and theanine in phloem exudates. Reducing the CsAAP6 in mature leaves resulted in a significant decrease in the content of glutamic acid, aspartic acid, alanine, leucine, asparagine, glutamine, arginine in the phloem exudates, indicating that CsAAP6 played an important role in the source to sink transport of amino acids in the phloem. The research results will provide the theoretical basis and genetic resources for the improvement of nitrogen use efficiency and tea quality.
This study evaluates a novel handheld sensor technology coupled with pattern recognition to provide real-time screening of several soybean traits for breeders and farmers, namely protein and fat quality. We developed predictive regression models that can quantify soybean quality traits based on near-infrared (NIR) spectra acquired by a handheld instrument. This system has been utilized to measure crude protein, essential amino acids (lysine, threonine, methionine, tryptophan, and cysteine) composition, total fat, the profile of major fatty acids, and moisture content in soybeans (n = 107), and soy products including soy isolates, soy concentrates, and soy supplement drink powders (n = 15). Reference quantification of crude protein content used the Dumas combustion method (AOAC 992.23), and individual amino acids were determined using traditional protein hydrolysis (AOAC 982.30). Fat and moisture content were determined by Soxhlet (AOAC 945.16) and Karl Fischer methods, respectively, and fatty acid composition via gas chromatography-fatty acid methyl esterification. Predictive models were built and validated using ground soybean and soy products. Robust partial least square regression (PLSR) models predicted all measured quality parameters with high integrity of fit (RPre ≥ 0.92), low root mean square error of prediction (0.02–3.07%), and high predictive performance (RPD range 2.4–8.8, RER range 7.5–29.2). Our study demonstrated that a handheld NIR sensor can supplant expensive laboratory testing that can take weeks to produce results and provide soybean breeders and growers with a rapid, accurate, and non-destructive tool that can be used in the field for real-time analysis of soybeans to facilitate faster decision-making.
Plant phenotyping platforms offer automated, fast scoring of traits that simplify the selection of varieties that are more competitive under stress conditions. However, indoor phenotyping methods are frequently based on the analysis of plant growth in individual pots. We present a reproducible indoor phenotyping method for screening young barley populations under water stress conditions and after subsequent rewatering. The method is based on a simple read-out of data using RGB imaging, projected canopy height, as a useful feature for indirectly following the kinetics of growth and water loss in a population of barley. A total of 47 variables including 15 traits and 32 biochemical metabolites measured (morphometric parameters, chlorophyll fluorescence imaging, quantification of stress-related metabolites; amino acids and polyamines, and enzymatic activities) were used to validate the method. The study allowed the identification of metabolites related to water stress response and recovery. Specifically, we found that cadaverine (Cad), 1,3-aminopropane (DAP), tryptamine (Tryp), and tyramine (Tyra) were the major contributors to the water stress response, whereas Cad, DAP, and Tyra, but not Tryp, remained at higher levels in the stressed plants even after rewatering. In this work, we designed, optimized and validated a non-invasive image-based method for automated screening of potential water stress tolerance genotypes in barley populations. We demonstrated the applicability of the method using transgenic barley lines with different sensitivity to drought stress showing that combining canopy height and the metabolite profile we can discriminate tolerant from sensitive genotypes. We showed that the projected canopy height a sensitive trait that truly reflects other invasively studied morphological, physiological, and metabolic traits and that our presented methodological setup can be easily applicable for large-scale screenings in low-cost systems equipped with a simple RGB camera. We believe that our approach will contribute to accelerate the study and understanding of the plant water stress response and recovery capacity in crops, such as barley.
Organic (e.g., sugars and amino acids) and inorganic (e.g., K+, Na+, PO42−, and SO42−) solutes are transported long-distance throughout plants. Lateral movement of these compounds between the xylem and the phloem, and vice versa, has also been reported in several plant species since the 1930s, and is believed to be important in the overall resource allocation. Studies of Arabidopsis thaliana have provided us with a better knowledge of the anatomical framework in which the lateral transport takes place, and have highlighted the role of specialized vascular and perivascular cells as an interface for solute exchanges. Important breakthroughs have also been made, mainly in Arabidopsis, in identifying some of the proteins involved in the cell-to-cell translocation of solutes, most notably a range of plasma membrane transporters that act in different cell types. Finally, in the future, state-of-art imaging techniques should help to better characterize the lateral transport of these compounds on a cellular level. This review brings the lateral transport of sugars and inorganic solutes back into focus and highlights its importance in terms of our overall understanding of plant resource allocation.
Plants grow and reproduce within a highly dynamic environment that can see abrupt changes in conditions, such as light intensity, temperature, humidity, or interactions with biotic agents. Recent studies revealed that plants can respond within seconds to some of these conditions, engaging many different metabolic and molecular networks, as well as rapidly altering their stomatal aperture. Some of these rapid responses were further shown to propagate throughout the entire plant via waves of reactive oxygen species (ROS) and Ca²⁺ that are possibly mediated through the plant vascular system. Here, we propose that the integration of these signals is mediated through pulses of gene expression that are coordinated throughout the plant in a systemic manner by the ROS/Ca⁺² waves.
Plants respond to drought stress through the ABA dependent and independent pathways, which in turn modulate transcriptional regulatory hubs. Here, we employed Illumina RNA-Seq to analyze a total of 18 cDNA libraries from leaves, sap, and roots of papaya plants under drought stress. Reference and de novo transcriptomic analyses identified 8,549 and 6,089 drought-responsive genes and unigenes,
respectively. Core sets of 6 and 34 genes were simultaneously up- or down-regulated, respectively, in all stressed samples. Moreover, GO enrichment analysis revealed that under moderate drought stress,
processes related to cell cycle and DNA repair were up-regulated in leaves and sap; while responses to abiotic stress, hormone signaling, sucrose metabolism, and suberin biosynthesis were up-regulated in
roots. Under severe drought stress, biological processes related to abiotic stress, hormone signaling, and oxidation-reduction were up-regulated in all tissues. Moreover, similar biological processes were
commonly down-regulated in all stressed samples. Furthermore, co-expression network analysis revealed three and eight transcriptionally regulated modules in leaves and roots, respectively. Seventeen stress-related TFs were identified, potentially serving as main regulatory hubs in leaves and roots. Our findings provide insight into the molecular responses of papaya plant to drought, which could contribute to the improvement of this important tropical crop.
Developmental plasticity, defined as the capacity to respond to changing environmental conditions, is an inherent feature of plant growth. Recent studies have brought the phloem tissue, the quintessential conduit for energy metabolites and inter-organ communication, into focus as an instructive developmental system. Those studies have clarified long-standing questions about essential aspects of phloem development and function, such as the pressure flow hypothesis, mechanisms of phloem unloading, and source–sink relationships. Interestingly, plants with impaired phloem development show characteristic changes in body architecture, thereby highlighting the capacity of the phloem to integrate environmental cues and to fine-tune plant development. Therefore, understanding the plasticity of phloem development provides scenarios of how environmental stimuli are translated into differential plant growth. In this Review, we summarize novel insights into how phloem identity is established and how phloem cells fulfil their core function as transport units. Moreover, we discuss possible interfaces between phloem physiology and development as sites for mediating the plastic growth mode of plants.
Vascular plants respond to various environmental stresses by integrating and transmitting environmental information perceived by roots and leaves, respectively. Long-distance signaling plays a crucial role in plant adaptation to and subsequent survival to severe environmental conditions. Recent studies have elucidated that various mobile molecules, such as small proteins, peptides, RNAs, metabolites, and second messengers, transmit extracellular stimuli from sensing tissues to target organs. Plants have unique and complex mechanisms for accurately connecting various organs despite the lack of a nervous system. In this short review, we summarize the current knowledge of plant molecules involved in long-distance signaling for optimal growth and stress response, with special focus on mobile peptides.
Soil drying causes leaf rolling in rice, but the relationship between leaf rolling and drought tolerance has historically confounded selection of drought tolerant genotypes. In this study on tropical japonica and aus diversity panels (170‐220 genotypes), the degree of leaf rolling under drought was more affected by leaf morphology than by stomatal conductance, leaf water status, or maintenance of shoot biomass and grain yield. A range of canopy temperature and leaf rolling (measured as change in normalized difference vegetation index (ΔNDVI)) combinations were observed among aus genotypes, indicating that some genotypes continued transpiration while rolled. Association mapping indicated co‐location of genomic regions for leaf rolling score and ΔNDVI under drought with previously reported leaf rolling genes and gene networks related to leaf anatomy. The relatively subtle variation across these large diversity panels may explain the lack of agreement of this study with earlier reports that used small numbers of genotypes that were highly divergent in hydraulic traits driving leaf rolling differences. This study highlights the large range of physiological responses to drought among rice genotypes, and emphasizes that drought response processes should be understood in detail before incorporating them into a varietal selection program.
Rapid, long-distance signaling in plants
A plant injured on one leaf by a nibbling insect can alert its other leaves to begin anticipatory defense responses. Working in the model plant Arabidopsis , Toyota et al. show that this systemic signal begins with the release of glutamate, which is perceived by glutamate receptor–like ion channels (see the Perspective by Muday and Brown-Harding). The ion channels then set off a cascade of changes in calcium ion concentration that propagate through the phloem vasculature and through intercellular channels called plasmodesmata. This glutamate-based long-distance signaling is rapid: Within minutes, an undamaged leaf can respond to the fate of a distant leaf.
Science , this issue p. 1112 ; see also p. 1068