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During postgerminative seedling establishment, reserves stored during seed filling are mobilized to provide energy and carbon for the growing seedling until autotrophic growth is possible. A plastid isoform of triose phosphate isomerase (pdTPI) plays a crucial role in this transition from heterotrophic to autotrophic growth. A T-DNA insertion in Ar...
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... determine tissue-specific expression, a pair of primers was designed to amplify a 122-bp fragment from At2g21170.1 and a 95-bp fragment from At2g21170.2. The At2g21170.1 form was expressed in roots, leaves, stems, flowers, and siliques, with highest expression in leaves and flowers (see Supplemental Figure 2 online). By contrast, At2g21170.2 ...
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... from 5-d-old seedlings were examined by light and electron microscopy. No apparent difference in cell size was observed between pdtpi and the wild type (Figures 2A and 2B). The number of chloroplasts per cell was much lower in pdtpi compared with the wild type (9.5 6 3.0 chloroplasts versus 4.4 6 0.9 for the wild type and pdtpi [n = 23], respectively) (Figures 2A and 2B). ...
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... apparent difference in cell size was observed between pdtpi and the wild type (Figures 2A and 2B). The number of chloroplasts per cell was much lower in pdtpi compared with the wild type (9.5 6 3.0 chloroplasts versus 4.4 6 0.9 for the wild type and pdtpi [n = 23], respectively) (Figures 2A and 2B). The reduced number and size of chloroplasts may account for the pale-green color of the pdtpi cotyledon. ...
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... reduced number and size of chloroplasts may account for the pale-green color of the pdtpi cotyledon. Examination of chloroplast membrane ultrastructure revealed portions of pdtpi chloroplasts contain prolamella bodies, a structure that typically exists in etioplasts ( Figure 2H). Etioplasts are found in white or pale-yellow etiolated leaves and dark-adapted, green tissues. ...
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... are found in white or pale-yellow etiolated leaves and dark-adapted, green tissues. The plastoglobule, a lipoprotein subcompartment, is significantly larger in the mutant compared with the wild type ( Figure 2H). In comparison, wild-type chloroplasts have developed stacked grana and unstacked stroma thylakoid membranes (Fig- ure 2G). ...
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... plastoglobule, a lipoprotein subcompartment, is significantly larger in the mutant compared with the wild type ( Figure 2H). In comparison, wild-type chloroplasts have developed stacked grana and unstacked stroma thylakoid membranes (Fig- ure 2G). These observations suggest that chloroplast differentiation in pdtpi is delayed during the early stages of the greening process. ...
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... observations suggest that chloroplast differentiation in pdtpi is delayed during the early stages of the greening process. In accordance with its changing structure, pdtpi accumulates fewer starch granules in the chloroplast stroma compared with the wild type ( Figures 2E and 2F), suggesting that photosynthetic capacity in pdtpi is compromised. ...
Citations
... These proteins provide energy and carbon through the breakdown of carbohydrates and other nutrients. Storage reserves are activated during seedling growth until autotrophic growth is supported [24]. Through glycolysis, the citric acid cycle, and β-oxidation, these enzymes support the pathways that catalyze the production of ATP, thereby providing energy to the developing plant seedling. ...
Physiological maturity impacts seed quality through various mechanisms including vigor, desiccation tolerance, dormancy induction, synthesis of raw materials (including seed storage proteins), and the reorganization of metabolisms. Peanut seed development can be classified into seven classes with four incremental stages per class. Based on the mesocarp color, the final three stages are commonly referred to as “orange”, “brown”, and “black”. In 2017, freshly harvested pods from one genotype of runner market-type peanuts grown under conventional practices were obtained from the University of Georgia research facility. The pods were removed from the plant material and ‘pod blasted’ to reveal the mesocarp. After separation, the remainder of the pod outer layer was removed, and the seeds were segregated for proteomic analysis. The raw peanuts were analyzed by bottom-up LC-MS/MS proteomics, which was conducted by the Proteomics Resource Center at the Rockefeller University, to identify the significant protein composition differences in each maturity class. The proteomic data revealed differentially expressed proteins as a function of maturity class with multiple functions including plant defense, metabolism, cell signaling, nutrient accumulation, and packaging. Understanding the processes needed for seed maturation will enable peanut scientists to evaluate the traits needed for robust germination, hardiness of the seed in response to disease, and nutrient quality.
... Consequently, both seed germination and seedling establishment are essential for subsequent plant development. It is worth noting that both processes are powered by energy stored in the seed itself [4]. Seedling establishment has traditionally been studied as part of the germination process. ...
Zelkova schneideriana Hand.-Mazz is a valuable ornamental tree and timber source, whose seedling breeding and large-scale cultivation are restricted by low seed germination and seedling rates. The regulatory mechanisms underlying seed germination and seedling establishment in Z. schneideriana remain unknown. This study conducted metabolomic and transcriptomic analyses of seed germination and seedling establishment in Z. schneideriana. Regular expression of genes and metabolite levels has been observed in plant hormone signal transduction, starch and sucrose metabolism, linoleic acid metabolism, and phenylpropanoid biosynthesis. The reduction in abscisic acid during seed germination may lead to seed release from dormancy. After the seed is released from dormancy, the metabolic levels of auxin, cytokinins, brassinolide, and various sugars are elevated, and they are consumed in large quantities during the seedling establishment stage. Linoleic acid metabolism is gradually activated during seedling establishment. Transcriptome analysis showed that a large number of genes in different metabolic pathways are upregulated during plant establishment, and material metabolism may be accelerated during seedling establishment. Genes regulating carbohydrate metabolism are altered during seed germination and seedling establishment, which may have altered the efficiency of carbohydrate utilization. In addition, the syntheses of lignin monomers and cellulose have different characteristics at different stages. These results provide new insights into the complex mechanisms underlying seed germination and seedling establishment in Z. schneideriana and other woody plants.
... Mutations in TPI's plastid form in Arabidopsis result in chlorotic leaves and almost no growth after ten weeks of evaluation because of the accumulation of methylglyoxal, which is twice that of the wild type. As a result, the transition from heterotrophic to autotrophic growth is delayed (Chen & Thelen, 2010). Moreover, TPI has cysteine residues similar to the GAPB subunit of the GAPDH enzyme. ...
... Methylglyoxal (MG) is the main sugar derivative generated from glycolysis, and it is indirectly regulated by triose phosphate isomerase (TPI). MG accumulation can cause toxic damage to cell functioning and proliferation (Chen and Thelen, 2010). MG alters the structures and stabilities of amino acids and nucleic acids, in terms of protein carbonylation, it leads to the formation of advanced glycation end-products (AGEs) (Allaman et al., 2015;Li et al., 2017;Fu et al., 2021). ...
... High sugar content is coupled with excessive accumulation of MG and AGEs that negatively a ects leaf development in Arabidopsis seedlings (Borysiuk et al., 2018). The Arabidopsis triose phosphate isomerase mutant pdtpi shows reduced TPI activity and high levels of MG accumulation, leading to severe stunting and chlorosis in leaves of seedlings together with defective chloroplast morphology (Chen and Thelen, 2010). However, the e ects of MG and AGEs on leaf senescence have not been reported yet. ...
Drought-induced leaf senescence is related to high sugar levels, which bears resemblance to the syndrome of diabetes in human. However, the underlying mechanisms of plant diabetes on carbon imbalance in maize and corresponding detoxification strategy have not been well-understood. Here, we investigate the regulatory mechanism of exogenous MG on plant diabetes under drought stress through foliar spraying application during grain-filling stage. Results demonstrated that exogenous MG delayed leaf senescence and promoted photoassimilation, thereby retrieving 14% drought-induced yield loss. Transcriptome and metabolite analyses revealed that drought increased sugar accumulation in leaf with inhibition of sugar transporters facilitating phloem loading. This led to disequilibrium of glycolysis and over-accumulation of endogenous MG. Contrarily, exogenous MG upregulated glycolytic flux and glyoxalase system catabolizing endogenous MG and advanced glycation end-products, ultimately alleviating plant diabetes. Besides, the genes facilitating anabolism and catabolism of trehalose-6-phosphate were promoted and suppressed by drought, respectively, whereas exogenous MG reversed this effect, implying trehalose-6-phosphate signaling in plant diabetes mediation. Moreover, exogenous MG activated phenylpropanoid biosynthetic pathway, promoting lignin and phenol contents for resilience. Collectively, our findings support that exogenous MG activates the defense-related pathway to alleviate the toxicity derived from plant diabetes, thereby maintaining leaf function and yield production under drought.
... In Arabidopsis thaliana, the plastid TPI isoform (pdTPI) does not affect the expression level and enzymatic activity of the cytosolic TPI (Chen and Thelen, 2010a,b). Inhibiting pdTPI in Arabidopsis thaliana reduced TPI activity, resulting in a severely stunted and chlorotic seedling that accumulated DHAP, glycerol, glycerol-3-phosphate and methylglyoxal, but had reduced levels of GAP (Chen and Thelen, 2010b). The reduced number and size of chloroplasts and the shortage of carbon intermediates may account for the pale-green colour of the pdtpi cotyledons (Chen and Thelen, 2010b); however, in pdTPI-antisense rice (Oryza sativa), plant growth was not affected, whereas the overexpression of pdTPI only marginally improved photosynthesis to a level insufficient to improve biomass production in rice (Suzuki et al., 2022a,b). ...
... Inhibiting pdTPI in Arabidopsis thaliana reduced TPI activity, resulting in a severely stunted and chlorotic seedling that accumulated DHAP, glycerol, glycerol-3-phosphate and methylglyoxal, but had reduced levels of GAP (Chen and Thelen, 2010b). The reduced number and size of chloroplasts and the shortage of carbon intermediates may account for the pale-green colour of the pdtpi cotyledons (Chen and Thelen, 2010b); however, in pdTPI-antisense rice (Oryza sativa), plant growth was not affected, whereas the overexpression of pdTPI only marginally improved photosynthesis to a level insufficient to improve biomass production in rice (Suzuki et al., 2022a,b). In pdTPI-antisense rice lines, the pool sizes of both GAP and DHAP decreased to 60%-70% of those in the wild-type (WT) plants. ...
... pdTPI has two splice variants (At2g21170.1 and At2g21170.2) in Arabidopsis (Chen and Thelen, 2010b). The At2g21170.2 ...
Heat stress causes dysfunction of the carbon‐assimilation metabolism. As a member of Calvin–Benson–Bassham (CBB) cycle, the chloroplast triose phosphate isomerases (TPI) catalyse the interconversion of glyceraldehyde 3‐phosphate (GAP) and dihydroxyacetone phosphate (DHAP). The tomato ( Solanum lycopersicum ) genome contains two individual SlTPI genes, Solyc10g054870 and Solyc01g111120, which encode the chloroplast‐located proteins SlTPI1 and SlTPI2, respectively. The tpi1 and tpi2 single mutants had no visible phenotypes, but the leaves of their double mutant lines tpi1tpi2 had obviously reduced TPI activity and displayed chlorotic variegation, dysplasic chloroplasts and lower carbon‐assimilation efficiency. In addition to altering carbon metabolism, proteomic data showed that the loss of both SlTPI1 and SlTPI2 severely affected photosystem proteins, reducing photosynthetic capacity. None of these phenotypes was evident in the tpi1 or tpi2 single mutants, suggesting that SlTPI1 and SlTPI2 are functionally redundant. However, the two proteins differed in their responses to heat stress; the protein encoded by the heat‐induced SlTPI2 showed a higher level of thermotolerance than that encoded by the heat‐suppressed SlTPI1 . Notably, heat‐induced transcription factors, SlWRKY21 and SlHSFA2/7, which negatively regulated SlTPI1 expression and positively regulated SlTPI2 expression, respectively. Our findings thus reveal that SlTPI1 and SlTPI2 have different thermostabilities and expression patterns in response to heat stress, which have the potential to be applied in thermotolerance strategies in crops.
... However, overloading of hexoses in cells enhanced the carbon metabolism resulting in producing unavoidably cytotoxic by-product MG from glycolysis and Calvin cycle (Takagi et al., 2014;Li, 2016). Exogenous MG precursors G3P in Arabidopsis wild type decrease the chlorophyll content similar to pdtpi mutant which was tended to overproduce MG (Chen and Thelen, 2010). Therefore, these negative progressions and phenomena were referred to as plant diabetes in previous studies Takagi et al., 2014). ...
Drought-induced leaf senescence is related to high sugar levels in leaves, photosynthesis inhibition, and ultimate yield loss. This physiological phenomenon in leaves bears resemblance to the symptom of diabetes in human disease. However, the underlying mechanisms of plant diabetes on carbon imbalance in maize leaf and corresponding detoxification strategy have not been well understood. In this study, we demonstrated that foliar application of exogenous methylglyoxal (MG) delayed leaf senescence and promoted photoassimilation, retrieved 14% yield loss induced by drought stress during grain filling stage. Transcriptome and metabolite analysis revealed that drought increased sugar accumulation in leaf with inhibition of sugar transporters facilitating phloem loading. This further lead to disequilibrium of glycolysis and over-accumulation of endogenous MG. Contrarily, exogenous MG significantly upregulated glycolytic flux and glyoxalase system catabolizing endogenous MG and advanced glycation end products toxicity, ultimately alleviating plant diabetes. Besides, the genes facilitating anabolism and catabolism of trehalose- 6-phosphate were promoted and suppressed by drought, respectively, whereas exogenous MG reversed the effect. Moreover, exogenous MG activated phenylpropanoid biosynthetic pathway, likely promoting cell structural integrity. Collectively, these results suggest that exogenous MG alleviates the toxic effect from drought-induced sugar accumulation and activates the defense-related pathway, thereby maintaining leaf function and yield production.
Highlight
Exogenous methylglyoxal stimulates glycolytic flux and glyoxalase system, providing a potential insight to alleviate plant diabetes under drought condition.
... Methylglyoxal (MG) is the main sugar derivative that is generated from glycolysis and indirectly regulated by triose phosphate isomerase (TPI). MG accumulation can cause toxic damage to cell functioning and proliferation (Chen and Thelen, 2010). MG alters the structures and stabilities of amino acids and nucleic acids, leading to the formation of advanced end glycation products (AGEs), in terms of protein carbonylation (Allaman et al., 2015;Li et al., 2017;Fu et al., 2021). ...
... The mutant pdtpi in Arabidopsis resulted in reduction of TPI activity and high-level MG accumulation, leading to severe stunting and chlorosis in seedling leaf. The author proposed that chloroplast morphology is defective in pdtpi possibly attributed to MG toxicity (Chen and Thelen, 2010). Nonetheless, the effects of MG and AGEs on leaf senescence have not been reported yet. ...
Drought-induced leaf senescence is related to high sugar levels in leaves, photosynthesis inhibition, and ultimate yield loss. This physiological phenomenon in leaves bears resemblance to the symptom of diabetes in human disease. However, the underlying mechanisms of plant diabetes on carbon imbalance in maize leaf and corresponding detoxification strategy have not been well understood. In this study, we demonstrated that foliar application of exogenous methylglyoxal (MG) delayed leaf senescence and promoted photoassimilation, retrieved 14% yield loss induced by drought stress during grain filling stage. Transcriptome and metabolite analysis revealed that drought increased sugar accumulation in leaf with inhibition of sugar transporters facilitating phloem loading. This further lead to disequilibrium of glycolysis and over-accumulation of endogenous MG. Contrarily, exogenous MG significantly upregulated glycolytic flux and glyoxalase system catabolizing endogenous MG and advanced glycation end products toxicity, ultimately alleviating plant diabetes. Besides, the genes facilitating anabolism and catabolism of trehalose-6-phosphate were promoted and suppressed by drought, respectively, whereas exogenous MG reversed the effect, revealing that trehalose-6-phosphate metabolism or signaling may contribute to MG-delayed leaf senescence under drought. Moreover, exogenous MG increased the activation of phenylpropanoid biosynthetic pathways, likely promoting cell structural integrity. Collectively, these results suggest that exogenous MG alleviates the toxic effect from drought-induced excessive sugar accumulation and activates the defense-related pathway, thereby maintaining leaf function and yield production.
... Genetic dissection of the lipid bilayer composition provides essential in vivo evidence for the role of individual lipid species in membrane function [14]. Lipidomics are increasingly applied to study pathway perturbations in various settings that implicate dysregulation in lipid metabolism [26,27], leading to a novel understanding of the connections between lipids and phenotypes [26,[28][29][30]. To offer additional insights about the in vivo role of the FAD4 gene and 16:1t-PG, we generated FAD4-overexpressing plants (OX-FAD4s). ...
A unique feature of plastid phosphatidylglycerol (PG) is a trans-double bond specifically at the sn-2 position of 16C fatty acid (16:1t- PG), which is catalyzed by FATTY ACID DESATURASE 4 (FAD4). To offer additional insights about the in vivo roles of FAD4 and its product 16:1t-PG, FAD4 overexpression lines (OX-FAD4s) were generated in Arabidopsis thaliana Columbia ecotype. When grown under continuous light condition, the fad4-2 and OX-FAD4s plants exhibited higher growth rates compared to WT control. Total lipids were isolated from Col, fad4-2, and OX-FAD4_2 plants, and polar lipids quantified by lipidomic profiling. We found that disrupting FAD4 expression altered prokaryotic and eukaryotic PG content and composition. Prokaryotic and eukaryotic monogalactosyl diacylglycerol (MGDG) was up-regulated in OX-FAD4 plants but not in fad4-2 mutant. We propose that 16:1t-PG homeostasis in plastid envelope membranes may coordinate plant growth and stress response by restricting photoassimilate export from the chloroplast.
... In Arabidopsis thaliana, carbon metabolism is important for skotomorphogenesis. Triacylglycerol, which is the main form of lipid stored in seeds, is catabolized to yield free fatty acids and glycerol, both of which are ultimately converted to sugars that are required for post-germination seedling growth in darkness (Chen & Thelen, 2010;Liu et al., 2017;O'Neill et al., 2003). A deficiency in galactose synthesis in the Arabidopsis mur3-3 mutant results in the production of dysfunctional xyloglucan. ...
The metabolic networks underlying skotomorphogenesis in seedlings remain relatively unknown. On the basis of our previous study on the folate metabolism in seedlings grown in darkness, the plastidial folylpolyglutamate synthetase gene (AtDFB) T‐DNA insertion Arabidopsis thaliana mutant (atdfb‐3) was examined. Under the nitrate‐sufficient condition, the mutant exhibited deficient folate metabolism and hypocotyl elongation, which affected skotomorphogenesis. Further analyses revealed changes to multiple intermediate metabolites related to carbon and nitrogen metabolism in the etiolated atdfb‐3 seedlings. Specifically, the sugar, polyol, and fatty acid contents decreased in the atdfb‐3 mutant under the nitrate‐sufficient condition, whereas the abundance of various organic acids and amino acids increased. In response to nitrate‐limited stress, multiple metabolites, including sugars, polyols, fatty acids, organic acids, and amino acids, accumulated more in the mutant than in the wild‐type control. The differences in the contents of multiple metabolites between the atdfb‐3 and wild‐type seedlings decreased following the addition of exogenous 5‐F‐THF under both nitrogen conditions. Additionally, the mutant accumulated high levels of one‐carbon metabolites, such as Cys, S‐adenosylmethionine, and S‐adenosylhomocysteine, under both nitrogen conditions. Thus, our data demonstrated that the perturbed folate metabolism in the atdfb‐3 seedlings, which was caused by the loss‐of‐function mutation to AtDFB, probably altered carbon and nitrogen metabolism, thereby modulating skotomorphogenesis. Furthermore, the study findings provide new evidence of the links among folate metabolism, metabolic networks, and skotomorphogenesis.
... However, overloading of hexoses in cells enhanced the carbon metabolism resulting in producing unavoidably cytotoxic by-product MG from glycolysis and Calvin cycle (Takagi et al., 2014;Li, 2016). Exogenous MG precursors G3P in Arabidopsis wild type decrease the chlorophyll content similar to pdtpi mutant which was tended to overproduce MG (Chen and Thelen, 2010). Therefore, these negative progressions and phenomena were referred to as plant diabetes in previous studies Takagi et al., 2014). ...
In maize (Zea mays L.) production, grain-filling stage is a pivotal phase that drought occurring would irreversibly cause leaf senescence and yield loss. Meanwhile, drought induces the disequilibrium of carbohydrates that inevitably produces the toxic substance methylglyoxal (MG) that plays dual roles including cytotoxic metabolite or signaling molecule in plants. However, how exogenous MG influences maize yield formation in response to drought during grain filling remains unknown. In this study, maize plants were exposed to moderate and severe drought conditions from 15 to 28 days after pollination with foliar spraying of MG (0, 15, 25, and 35 mM). Notably, MG application significantly increased kernel number and retrieved yield loss by 14–48% under drought, demonstrating an increased resistance of the plants. Interestingly, high (25–35 mM) and low concentrations (15–25 mM) of MG application under moderate and severe drought performed the highest yield output, respectively. To investigate the mechanisms by which MG enhanced drought resistance, we confirmed that MG application postponed leaf senescence under both drought conditions and significantly improved photosynthesis under severe drought during filling stage. Specifically, MG application escalated the levels of soluble sugar and sucrose while suppressing endogenous MG accumulation by activating glyoxalase system in leaf during the early phase of drought stress and well-watered condition. Collectively, these results demonstrate that exogenous MG application enhances drought tolerance during maize grain filling, possibly through regulation on the homeostasis of endogenous MG and sugars. These findings provide a new approach to secure yield against drought stress in maize production.
