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Metabolomics pattern of roots under control (normoxia) or waterlogging (hypoxia) conditions (grey and blue shades, respectively). (a) Heat map showing significant metabolites (p<0.0005, i.e. Bonferroni threshold; two-way ANOVA) with a hierarchical clustering on left (Pearson correlation). The two main groups are framed and numbered (group 1 framed in blue: metabolites decreasing under waterlogging; group 2 framed in red: metabolites increasing under waterlogging). (b) Score plot of Metabolomics pattern of roots under control (normoxia) or waterlogging (hypoxia) conditions (grey and blue shades, respectively). (a) Heat map showing significant metabolites (p < 0.0005, i.e. Bonferroni threshold; two-way ANOVA) with a hierarchical clustering on left (Pearson correlation). The two main groups are framed and numbered (group 1 framed in blue: metabolites decreasing under waterlogging; group 2 framed in red: metabolites increasing under waterlogging). (b) Score plot of the multivariate analysis by O2PLS demonstrating the very good sample discrimination. (c) Volcano plot showing best discriminating metabolites (control vs. waterlogging) with the p-value (y-axis) and the loading in the O2PLS (x-axis). The horizontal dash-dotted line represents the Bonferroni threshold (0.0005). The two best discriminating features under waterlogging are an increase in γ-aminobutyrate (GABA) and a decrease in raffinose. (d) Relative metabolic ratios: aminoadipate-to-lysine (left) and putrescine-to-ornithine (right). For both, the difference between waterlogging and control conditions is significant (p < 0.01, Welch).
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Root oxygen deficiency that is induced by flooding (waterlogging) is a common situation in many agricultural areas, causing considerable loss in yield and productivity. Physiological and metabolic acclimation to hypoxia has mostly been studied on roots or whole seedlings under full submergence. The metabolic difference between shoots and roots duri...
Citations
... Transient flooding may not significantly impact plant growth but can trigger the expression of anaerobic response genes and alter related metabolites in plants, including but not limited to starch, sucrose, and amino acids. Following flooding stress, starch, sugar, and phenolics in Medicago truncatula leaves are significantly up-regulated [56]. The flooding stress experiments conducted on soybean seedlings demonstrated that the submergence leads to the accumulation of citrate, succinate, fumarate, alanine, and gamma-aminobutyric acid. ...
... Genes encoding enzymes involved in mannose metabolism were also up-regulated post-flooding. Similar results have been previously identified in waterlogged Medicago plants [56]. The accumulation levels of serine, phenylalanine, N-Acetyl-L-valine, and proline, which are derivatives of 3-phosphoglycerate, phosphoenolpyruvate, pyruvate, and 2-oxoglutarate, respectively, exhibited varying degrees of increase under flooding stress. ...
Abiotic stress, including flooding, seriously affects the normal growth and development of plants. Mulberry (Morus alba), a species known for its flood resistance, is cultivated worldwide for economic purposes. The transcriptomic analysis has identified numerous differentially expressed genes (DEGs) involved in submergence tolerance in mulberry plants. However, a comprehensive analyses of metabolite types and changes under flooding stress in mulberry remain unreported. A non-targeted metabolomic analysis utilizing liquid chromatography-tandem mass spectrometry (LC-MS/MS) was conducted to further investigate the effects of flooding stress on mulberry. A total of 1,169 metabolites were identified, with 331 differentially accumulated metabolites (DAMs) exhibiting up-regulation in response to flooding stress and 314 displaying down-regulation. Pathway enrichment analysis identified significant modifications in many metabolic pathways due to flooding stress, including amino acid biosynthesis and metabolism and flavonoid biosynthesis. DAMs and DEGs are significantly enriched in the Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways for amino acid, phenylpropanoid and flavonoid synthesis. Furthermore, metabolites such as methyl jasmonate, sucrose, and D-mannose 6-phosphate accumulated in mulberry leaves post-flooding stress. Therefore, genes and metabolites associated with these KEGG pathways are likely to exert a significant influence on mulberry flood tolerance. This study makes a substantial contribution to the comprehension of the underlying mechanisms implicated in the adaptation of mulberry plants to submergence.
... For example PAs are increased due to water deficit [8][9][10] or water excess [11,12]. However, a decline in PAs after such water stresses is also reported [13][14][15]. Our results show that contrasting water supply caused differential response in the endogenous polyamines ( Fig. 1-4). ...
Drought and waterlogging are environmental stress factors that havoc normal plant growth and development. Polyamines are plant growth regulators, which participate in plant growth and development, as well as in the physiological responses to stress conditions. The polyamines fractions were evaluated in triticale plants pretreated with the selective herbicide Serrate®, and exposed to drought or waterlogging for 7 days. The herbicide applied alone provoked a slight decrease in polyamine content. A decrease of polyamine content was found also after drought, while waterlogging provoked an increase in polyamine levels. These data correlate with plant fitness and phenotype characteristics of treated seedlings. Our data provide new information about the role of plant polyamines in the physiological responses of triticale plants to water stress after herbicide application.
... (b) When flooding stress and a second stress induce opposing responses, for example, reduced as opposed to increased plant growth, the response of either of the stresses might be dominant over the other when stresses are combined, or an intermediate response is manifested. Lothier et al., 2020;Mustroph et al., 2010). Most prominently, energy generation via mitochondrial electron transport chain (mtETC) and oxidative phosphorylation are reduced due to O 2 being less available as a terminal electron acceptor (Millar et al., 2011). ...
Current climate change brings with it a higher frequency of environmental stresses, which occur in combination rather than individually leading to massive crop losses worldwide. In addition to, for example, drought stress (low water availability), also flooding (excessive water) can threaten the plant, causing, among others, an energy crisis due to hypoxia, which is responded to by extensive transcriptional, metabolic and growth‐related adaptations. While signalling during flooding is relatively well understood, at least in model plants, the molecular mechanisms of combinatorial flooding stress responses, for example, flooding simultaneously with salinity, temperature stress and heavy metal stress or sequentially with drought stress, remain elusive. This represents a significant gap in knowledge due to the fact that dually stressed plants often show unique responses at multiple levels not observed under single stress. In this review, we (i) consider possible effects of stress combinations from a theoretical point of view, (ii) summarize the current state of knowledge on signal transduction under single flooding stress, (iii) describe plant adaptation responses to flooding stress combined with four other abiotic stresses and (iv) propose molecular components of combinatorial flooding (hypoxia) stress adaptation based on their reported dual roles in multiple stresses. This way, more future emphasis may be placed on deciphering molecular mechanisms of combinatorial flooding stress adaptation, thereby potentially stimulating development of molecular tools to improve plant resilience towards multi‐stress scenarios.
... In the case of Medicago truncatula, root flooding declined the level of raffinose, sucrose, hexoses and pentoses. The leaves, by contrast, were characterized by the increase in sugars and sugar derivatives [51]. The investigation of the effect of the O 2 concentration (21, 2 and 0%) on sunflower (Helianthus annuus) showed that oxygen deficiency caused the increase in sucrose and fructose levels in the leaves, but that of glucose was decreased [52]. ...
Oxygen deficiency is an environmental challenge which affects plant growth, the development and distribution in land and aquatic ecosystems, as well as crop yield losses worldwide. The capacity to exist in the conditions of deficiency or the complete lack of oxygen depends on a number of anatomic, developmental and molecular adaptations. The lack of molecular oxygen leads to an inhibition of aerobic respiration, which causes energy starvation and the acceleration of glycolysis passing into fermentations. We focus on systemic metabolic alterations revealed with the different approaches of metabolomics. Oxygen deprivation stimulates the accumulation of glucose, pyruvate and lactate, indicating the acceleration of the sugar metabolism, glycolysis and lactic fermentation, respectively. Among the Krebs-cycle metabolites, only the succinate level increases. Amino acids related to glycolysis, including the phosphoglycerate family (Ser and Gly), shikimate family (Phe, Tyr and Trp) and pyruvate family (Ala, Leu and Val), are greatly elevated. Members of the Asp family (Asn, Lys, Met, Thr and Ile), as well as the Glu family (Glu, Pro, Arg and GABA), accumulate as well. These metabolites are important members of the metabolic signature of oxygen deficiency in plants, linking glycolysis with an altered Krebs cycle and allowing alternative pathways of NAD(P)H reoxidation to avoid the excessive accumulation of toxic fermentation products (lactate, acetaldehyde, ethanol). Reoxygenation induces the downregulation of the levels of major anaerobically induced metabolites, including lactate, succinate and amino acids, especially members of the pyruvate family (Ala, Leu and Val), Tyr and Glu family (GABA and Glu) and Asp family (Asn, Met, Thr and Ile). The metabolic profiles during native and environmental hypoxia are rather similar, consisting in the accumulation of fermentation products, succinate, fumarate and amino acids, particularly Ala, Gly and GABA. The most intriguing fact is that metabolic alterations during oxidative stress are very much similar, with plant response to oxygen deprivation but not to reoxygenation.
... The effects of waterlogging on plant trunks are poorly understood because they have rarely been studied. However, it is clear that waterlogging responses do not occur only in plants' roots and may differ between parts of the plant, giving rise to tissue-or organ-specific expression patterns (Ellis et al., 1999;Kreuzwieser et al., 2009;Mustroph et al., 2014;Lothier et al., 2020). ...
... Although the roots exhibit a strong waterlogging response, responses in other organs also warrant study because systemic signals allow plants to respond to stress at the whole-plant level rather than merely at the local or cellular level (Zandalinas et al., 2020;Omary et al., 2023). Accordingly, there are numerous research publications have elucidated organ-specific waterlogging responses in other plants (Ellis et al., 1999;Mustroph et al., 2009;Hsu et al., 2011;Mustroph et al., 2014;Lothier et al., 2020;Cao et al., 2022) marked the necessity to investigate waterlogging responses in other parts of oil palm as well. ...
... The carbon metabolism (ath01200) and carbon fixation (ath00710) pathways, which are both related to sugar metabolism, were also significantly enriched. This suggests that waterlogging induces increased starch and sucrose degradation to maintain a constant carbohydrate supply to waterlogged plants (Parent et al., 2008;Mustroph et al., 2009;Kreuzwieser and Rennenberg, 2014;Planchet et al., 2017;Cui et al., 2019;Lothier et al., 2020). Similar findings were obtained in an earlier transcriptomic study on oil palm seedlings, supporting our results (Nuanlaong et al., 2020). ...
Global warming-induced climate change causes significant agricultural problems by increasing the incidence of drought and flooding events. Waterlogging is an inevitable consequence of these changes but its effects on oil palms have received little attention and are poorly understood. Recent waterlogging studies have focused on oil palm seedlings, with particular emphasis on phenology. However, the transcriptomic waterlogging response of mature oil palms remains elusive in real environments. We therefore investigated transcriptomic changes over time in adult oil palms at plantations over a two-year period with pronounced seasonal variation in precipitation. A significant transcriptional waterlogging response was observed in the oil palm stem core but not in leaf samples when gene expression was correlated with cumulative precipitation over two-day periods. Pathways and processes upregulated or enriched in the stem core response included hypoxia, ethylene signaling, and carbon metabolism. Post-waterlogging recovery in oil palms was found to be associated with responses to heat stress and carotenoid biosynthesis. Nineteen transcription factors (TFs) potentially involved in the waterlogging response of mature oil palms were also identified. These data provide new insights into the transcriptomic responses of planted oil palms to waterlogging and offer valuable guidance on the sensitivity of oil palm plantations to future climate changes.
... Increase in GABA, polyols (glycerol and inositol), and organic acids (citrate, aconitate, and malate) and decrease in many amino acids, TCA cycle, and nitrogen metabolism were reported in sunflower and oil palm (Cui et al. 2019b). GC-MS analysis in Medicago showed that GABA, polyols, and polyamines like spermidine levels are increased, and raffinose and xylose levels are decreased significantly (Lothier et al. 2020). Prolonged waterlogging induces accumulation of toxic metabolites like ethanol, hydrogen peroxide, and lactic acid, which finally leads to cell senescence and plant death (Zhang et al. 2017). ...
Drought, hot temperatures, salinity, and rising carbon dioxide levels all have an impact on plant development that creates a significant challenge for agricultural production. Concerns about the consequences of climate change on natural resources, diversification, and global food security have made this a prominent topic. Environmental stress adaptation in plants necessitates significant modifications in the “-omic” architecture. In this chapter, we present a summary of stress adaptation's physiological and molecular mechanisms, emphasizing how proteins, metabolites, and genes change in responses to single and multiple environmental stressors. We explored the importance that “omics” research, in combination with systems biology methodologies, could serve in research considerations for plants that appear to be unable to adapt, along with those that can resist anthropogenic global warming.
... As shown in Fig. 2a, there was an approximately 4.5-fold increase in proline content in roots after waterlogging for 13 days. The accumulation of proline in response to waterlogging is mediated by stimulation of synthesis, loss of feedback inhibition, and the inhibition of xylem transfer (Olgun et al. 2008;Lothier et al. 2020). ...
... In addition, although waterlogging stress was shown to decrease the photosynthetic rate in balloon flower, the sucrose, fructose, and glucose contents were greater in the leaves of waterlogged plants than in those of the control plants (Fig. 2c). In Medicago truncatula, the phloem loading rate was reduced by waterlogging stress (Lothier et al. 2020), indicating that the accumulation of sugar in leaves of waterlogged balloon flower should be mediated by the inhibition of sugar transport via the phloem. Under waterlogged conditions, sugars are required for the formation of new adventitious roots, which contain more aerenchyma than primary roots (Visser and Voesenek 2005;Qi et al. 2020). ...
Unlabelled:
Waterlogging stress is a major limiting factor resulting in stunted growth and loss of crop productivity, especially for root crops. However, physiological responses to waterlogging have been studied in only a few plant models. To gain insight into how balloon flower (Platycodon grandiflorus (Jacq.) A. DC) responds to waterlogging stress, we investigate changes to sucrose metabolism combined with a physiological analysis. Although waterlogging stress decreased the photosynthetic rate in balloon flower, leaves exhibited an increase in glucose (ninefold), fructose (4.7-fold), and sucrose (2.1-fold), indicating inhibition of sugar transport via the phloem. In addition, roots showed a typical response to hypoxia, such as the accumulation of proline (4.5-fold higher than in control roots) and soluble sugars (2.1-fold higher than in control roots). The activities and expression patterns of sucrose catabolizing enzymes suggest that waterlogging stress leads to a shift in the pathway of sucrose degradation from invertase to sucrose synthase (Susy), which consumes less ATP. Furthermore, we suggest that the waterlogging-stress-induced gene PlgSusy1 encodes the functional Susy enzyme, which may contribute to improving tolerance in balloon flower to waterlogging. As a first step toward understanding the waterlogging-induced regulatory mechanisms in balloon flower, we provide a solid foundation for further understanding waterlogging-induced alterations in source-sink relationships.
Supplementary information:
The online version contains supplementary material available at 10.1007/s12298-023-01310-y.
... Recently, metabolomics analyses of cucumber plants subjected to phosphorus deficiency have shown important changes in phloem sap metabolome, not only in carbohydrates (galactitol, fructose) but also in organic acids (e.g., oxalate, citrate, fatty acids) along with nitrogenous compounds (e.g., ethanolamine, 4-aminobutyrate and pyroglutamate) [67]. Metabolomics analyses of phloem sap exudates during root waterlogging have found a change in the sugar to organic acid ratio, suggesting (i) a crucial role of the balance between loading in shoots and unloading in roots for sap composition and (ii) potentially, a negative feedback of metabolite accumulation in phloem sap onto shoot metabolism, such as sugar interconversions and respiration [106]. ...
Phloem sap transport is essential for plant nutrition and development since it mediates redistribution of nutrients, metabolites and signaling molecules. However, its biochemical composition is not so well-known because phloem sap sampling is difficult and does not always allow extensive chemical analysis. In the past years, efforts have been devoted to metabolomics analyses of phloem sap using either liquid chromatography or gas chromatography coupled with mass spectrometry. Phloem sap metabolomics is of importance to understand how metabolites can be exchanged between plant organs and how metabolite allocation may impact plant growth and development. Here, we provide an overview of our current knowledge of phloem sap metabolome and physiological information obtained therefrom. Although metabolomics analyses of phloem sap are still not numerous, they show that metabolites present in sap are not just sugars and amino acids but that many more metabolic pathways are represented. They further suggest that metabolite exchange between source and sink organs is a general phenomenon, offering opportunities for metabolic cycles at the whole-plant scale. Such cycles reflect metabolic interdependence of plant organs and shoot–root coordination of plant growth and development.
... In the past, numerous metabolomics investigations were conducted in various crop systems after waterlogging stress to uncover possible metabolites and their function in waterlogging stress tolerance. For example, in Medicago truncatula after waterlogging stress, a metabolomics technique was used which unveiled a greater accumulation of numerous metabolites, such as sugars, organic acid, aromatics, glycine, alanine, glutamine, and lysine, that may play a critical role in stress tolerance [150]. Similarly, in G. max, three key metabolites, such as pyruvate, NADH2, and glycine, and gamma-aminobutyric acid, succinate, and citrate were found abundantly after waterlogging stress [151]. ...
Soil flooding has emerged as a serious threat to modern agriculture due to the rapid global warming and climate change, resulting in catastrophic crop damage and yield losses. The most detrimental effects of waterlogging in plants are hypoxia, decreased nutrient uptake, photo-synthesis inhibition, energy crisis, and microbiome alterations, all of which result in plant death. Although significant advancement has been made in mitigating waterlogging stress, it remains largely enigmatic how plants perceive flood signals and translate them for their adaptive responses at a molecular level. With the advent of multiomics, there has been significant progress in understanding and decoding the intricacy of how plants respond to different stressors which have paved the way towards the development of climate-resistant smart crops. In this review, we have provided the overview of the effect of waterlogging in plants, signaling (calcium, reactive oxygen species, nitric oxide, hormones), and adaptive responses. Secondly, we discussed an insight into past, present, and future prospects of waterlogging tolerance focusing on conventional breeding, transgenic, multiomics, and gene-editing approaches. In addition, we have also highlighted the importance of panomics for developing waterlogging-tolerant cultivars. Furthermore, we have discussed the role of high-throughput phenotyping in the screening of complex waterlog-ging-tolerant traits. Finally, we addressed the current challenges and future perspectives of water-logging signal perception and transduction in plants, which warrants future investigation.
... Previous studies have utilized tolerant plant varieties to study the role of metabolites in enabling plants to withstand harsh environmental conditions. This approach is done with meticulous care, as the use of tolerant plant varieties provides valuable information about how plants respond metabolically to environmental stress (Lothier et al., 2020). Metabolites carries signals and move in intra and inter-cellular environments and are directly or in directly involved in the growth and development as well as defense (Evans, 2003). ...
Background
Flooding is a major stress factor impacting watermelon growth and production globally. Metabolites play a crucial role in coping with both biotic and abiotic stresses.
Methods
In this study, diploid (2X) and triploid (3X) watermelons were investigated to determine their flooding tolerance mechanisms by examining physiological, biochemical, and metabolic changes at different stages. Metabolite quantification was done using UPLC-ESI-MS/MS and a total of 682 metabolites were detected.
Results
The results showed that 2X watermelon leaves had lower chlorophyll content and fresh weights compared to 3X. The activities of antioxidants, such as superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT), were higher in 3X than in 2X. 3X watermelon leaves showed lower O2 production rates, MDA, and hydrogen peroxide (H2O2) levels in response to flooding, while higher ethylene production was observed. 3X had higher levels of dehydrogenase activity (DHA) and ascorbic acid + dehydrogenase (AsA + DHA), but both 2X and 3X showed a significant decline in the AsA/DHA ratio at later stages of flooding. Among them, 4-guanidinobutyric acid (mws0567), an organic acid, may be a candidate metabolite responsible for flooding tolerance in watermelon and had higher expression levels in 3X watermelon, suggesting that triploid watermelon is more tolerant to flooding.
Conclusion
This study provides insights into the response of 2X and 3X watermelon to flooding and the physiological, biochemical, and metabolic changes involved. It will serve as a foundation for future in-depth molecular and genetic studies on flooding response in watermelon.
