A Snapshot of the Trehalose Pathway During Seed Imbibition in Medicago truncatula Reveals Temporal- and Stress-Dependent Shifts in Gene Expression Patterns Associated With Metabolite Changes

Macovei, Anca; Pagano, Andrea; Cappuccio, Michela; Gallotti, Lucia; Dondi, Daniele; Araújo, Susana de Sousa; Fevereiro, Pedro; Balestrazzi, Alma

doi:10.3389/fpls.2019.01590

Cited by 10 publications

(9 citation statements)

References 87 publications

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“…For example, when it is exogenously applied, trehalose changes the enzymes involved in the accumulation of storage carbohydrates in photosynthetic tissues as well as its gene expression (including the induction of AGPase genes found in Arabidopsis [ 7 ]), and increases the drought tolerance and biomass yield [ 8 – 10 ]. In addition, previous study have revealed that the trehalose pathway is involved in the early stages of seed germination in Medicago truncatula during seed imbibition with water or stress agents (polyethylene glycol and sodium chloride), the trehalose was significantly reduced during seed absorption was measured by HPLC (high performance liquid chromatography), indicating that trehalose may be an energy source rather than an osmotic protector [ 11 ]. Moreover, The ramosa3 mutant of Zea mays have significantly reduced trehalose and results excessive branching [ 12 , 13 ].…”

Section: Introductionmentioning

confidence: 99%

Genome-wide analysis of trehalose-6-phosphate phosphatases (TPP) gene family in wheat indicates their roles in plant development and stress response

Ding

et al. 2022

BMC Plant Biol

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Background Trehalose-6-phosphate phosphatases genes (TPPs) are involved in the development and stress response of plants by regulating the biosynthesis of trehalose, though little is currently known about TPPs in common wheat (Triticum aestivum L.). Results In this study, we performed a genome-wide identification of the TPP gene family in common wheat, and identified a total of 31 TaTPP genes. These were subdivided into six subfamilies based on the phylogenetic relationships and the conservation of protein in six monocot and eudicot plants. The majority of TPP genes were represented by 2–3 wheat homoalleles (named TaTPPX_ZA, TaTPPX_ZB, or TaTPPX_ZD), where Z is the location on the wheat chromosome of the gene number (X). We also analyzed the chromosomal location, exon-intron structure, orthologous genes, and protein motifs of the TaTPPs. The RNA-seq data was used to perform an expression analysis, which found 26 TaTPP genes to be differentially expressed based on spatial and temporal characteristics, indicating they have varied functions in the growth and development of wheat. Additionally, we assessed how the promoter regulatory elements were organized and used qRT-PCR in the leaves to observe how they were expressed following ABA, salt, low tempreture, and drought stress treatments. All of these genes exhibited differential expression against one or more stress treatments. Furthermore, ectopic expression of TaTPP11 in Arabidopsis exhibited a phenotype that delayed plant development but did not affect seed morphology. Conclusions TaTPPs could serve important roles in the development and stress response in wheat. These results provide a basis for subsequent research into the function of TaTPPs.

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Section: Introductionmentioning

confidence: 99%

Genome-wide analysis of trehalose-6-phosphate phosphatases (TPP) gene family in wheat indicates their roles in plant development and stress response

Ding

et al. 2022

BMC Plant Biol

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“…Sucrose and starch are used to fuel the Krebs cycle to produce ATP/NADH and as substrates for biosynthesis during the process of dormancy release and germination, including for the synthesis of DNA and cell walls. The increase in the contents of some sugars during seed imbibition indicates the need for an increased energy supply [ 41 ]. Our results showed that starch and sucrose metabolism was a significantly enriched pathway in seeds treated with GA 3 and the main metabolites that exhibited increased levels in the hulled and de-hulled seeds treated with GA 3 were α-D-glucose-1P, D-fructose, D-glucose and α-D-glucose-6P, which may eventually participate in glycolysis, the TCA cycle or the pentose phosphate pathway.…”

Section: Discussionmentioning

confidence: 99%

“…In addition, 3 DEGs encoding α-trehalase ( treh ) were upregulated, hydrolysing trehalose to glucose. A study on Medicago truncatula showed that the trehalose content decreased during seed imbibition and may be an important energy source compared to osmoprotectants [ 41 ]. A study on some fungal species also observed decreased trehalose content during spore germination [ 52 ].…”

Section: Discussionmentioning

confidence: 99%

Integrated Analysis of the Transcriptome and Metabolome Revealed Candidate Genes Involved in GA3-Induced Dormancy Release in Leymus chinensis Seeds

Zhang

Wang

et al. 2021

IJMS

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Leymus chinensis is a perennial forage grass that has good palatability, high yield and high feed value, but seed dormancy is a major problem limiting the widespread cultivation of L. chinensis. Here, we performed transcriptomic and metabolomic analysis of hulled and de-hulled seeds of L. chinensis treated with or without GA3 to investigate the changes in gene and metabolites associated with dormancy release induced by GA3. The germination test revealed that the optimum concentration of GA3 for disruption of L. chinensis seed dormancy was 577 μM. A total of 4327 and 11,919 differentially expressed genes (DEGs) and 871 and 650 differentially abundant metabolites were identified in de-hulled and hulled seeds treated with GA3, respectively, compared with seeds soaked in sterile water. Most of the DEGs were associated with starch and sucrose metabolism, protein processing in the endoplasmic reticulum, endocytosis and ribosomes. Furthermore, isoquinoline alkaloid biosynthesis, tyrosine metabolism, starch and sucrose metabolism, arginine and proline metabolism, and amino sugar and nucleotide sugar metabolism were significantly enriched pathways. Integrative analysis of the transcriptomic and metabolomic data revealed that starch and sucrose metabolism is one of the most important pathways that may play a key role in providing carbon skeletons and energy supply for the transition of L. chinensis seeds from a dormant state to germination by suppressing the expression of Cel61a, egID, cel1, tpsA, SPAC2E11.16c and TPP2, enhancing the expression of AMY1.1, AMY1.2, AMY1.6 and GLIP5, and inhibiting the synthesis of cellobiose, cellodextrin, and trehalose while promoting the hydrolysis of sucrose, starch, cellobiose, cellodextrin, and trehalose to glucose. This study identified several key genes and provided new insights into the molecular mechanism of seed dormancy release induced by GA3 in L. chinensis. These putative genes will be valuable resources for improving the seed germination rate in future breeding studies.

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“…Several other experimental evidences support the regulatory role of these genes not only in stress conditions but also during development and in plant–microbe interactions. Thus, PvTPS9 was proposed to be a crucial modulator of Tre metabolism in symbiotic nodules and whole common bean plants ( Barraza et al, 2016 ); OsTPP7 promoted early seed vigor by its regulation of Suc levels during germination under anoxic stress vigor ( Kretzschmar et al, 2015 ); MtTPS7 and MtTPS10 were identified as early markers of the seed response to osmotic stress in Medicago truncatula ( Macovei et al, 2019 ); class II TPS genes were associated with high-temperature stress resistance in Moringa oleifera ( Lin et al, 2018 ); carbon starvation strongly induced the expression of TPS7 and TPS11 during early kiwi fruit development ( Nardozza et al, 2020 ), and TPS6, TPS7, and TPS11 were identified as yield-related traits in wheat ( Lyra et al, 2020 ). In this context, the extensive neutral-to-negative effect that the defoliation stress had on the expression of the AhTPS6, 7, 8 , and 9 genes in all organs examined, at FL, suggests that these genes might be essential to ensure an efficient recovery from defoliation in A. cruentus .…”

Section: Discussionmentioning

confidence: 99%

Highest Defoliation Tolerance in Amaranthus cruentus Plants at Panicle Development Is Associated With Sugar Starvation Responses

Cisneros-Hernández

Vargas‐Ortiz²,

Sánchez-Martínez³

et al. 2021

Front. Plant Sci.

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Defoliation tolerance (DT) in Amaranthus cruentus is known to reach its apex at the panicle emergence (PE) phase and to decline to minimal levels at flowering (FL). In this study, defoliation-induced changes were recorded in the content of non-structural carbohydrates and raffinose family oligosaccharides (RFOs), and in the expression and/or activity of sugar starvation response-associated genes in plants defoliated at different vegetative and reproductive stages. This strategy identified sugar-starvation-related factors that explained the opposite DT observed at these key developmental stages. Peak DT at PE was associated with increased cytosolic invertase (CI) activity in all organs and with the extensive induction of various class II trehalose-phosphate synthase (TPS) genes. Contrariwise, least DT at FL coincided with a sharp depletion of starch reserves and with sucrose (Suc) accumulation, in leaves and stems, the latter of which was consistent with very low levels of CI and vacuolar invertase activities that were not further modified by defoliation. Increased Suc suggested growth-inhibiting conditions associated with altered cytosolic Suc-to-hexose ratios in plants defoliated at FL. Augmented cell wall invertase activity in leaves and roots, probably acting in a regulatory rather than hydrolytic role, was also associated with minimal DT observed at FL. The widespread contrast in gene expression patterns in panicles also matched the opposite DT observed at PE and FL. These results reinforce the concept that a localized sugar starvation response caused by C partitioning is crucial for DT in grain amaranth.

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A Snapshot of the Trehalose Pathway During Seed Imbibition in Medicago truncatula Reveals Temporal- and Stress-Dependent Shifts in Gene Expression Patterns Associated With Metabolite Changes

Cited by 10 publications

References 87 publications

Genome-wide analysis of trehalose-6-phosphate phosphatases (TPP) gene family in wheat indicates their roles in plant development and stress response

Genome-wide analysis of trehalose-6-phosphate phosphatases (TPP) gene family in wheat indicates their roles in plant development and stress response

Integrated Analysis of the Transcriptome and Metabolome Revealed Candidate Genes Involved in GA3-Induced Dormancy Release in Leymus chinensis Seeds

Highest Defoliation Tolerance in Amaranthus cruentus Plants at Panicle Development Is Associated With Sugar Starvation Responses

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