Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold‐regulated gene expression with modifications in metabolite content

Kaplan, Fatma; Kopka, Joachim; Sung, Dong Yul; Zhao, Wei; Popp, Mick; Porat, Ron; Guy, Charles L.

doi:10.1111/j.1365-313x.2007.03100.x

Cited by 445 publications

(395 citation statements)

References 67 publications

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“…In response to acute temperature shock, plants mobilize starch at time when biosynthesis would be expected (e.g., in the middle of the light period), resulting in the accumulation of maltose, the major starch catabolite, and of its deriving sugars (Usadel et al, 2008a;Purdy et al, 2013;Guy, 2005, 2004;Sitnicka and Orzechowski, 2014;Yano et al, 2005;Kaplan et al, 2007). Similar rearrangements of starch metabolism are observed when plants are subject to short periods of oxidative or osmotic stress (Scarpeci and Valle, 2008;Zanella et al, 2016;Valerio et al, 2011;Geigenberger et al, 1997).…”

Section: Introductionmentioning

confidence: 68%

Regulation of Leaf Starch Degradation by Abscisic Acid Is Important for Osmotic Stress Tolerance in Plants

et al. 2016

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Starch serves functions that range over a timescale of minutes to years, according to the cell type from which it is derived. In guard cells, starch is rapidly mobilized by the synergistic action of b-AMYLASE1 (BAM1) and a-AMYLASE3 (AMY3) to promote stomatal opening. In the leaves, starch typically accumulates gradually during the day and is degraded at night by BAM3 to support heterotrophic metabolism. During osmotic stress, starch is degraded in the light by stress-activated BAM1 to release sugar and sugar-derived osmolytes. Here, we report that AMY3 is also involved in stress-induced starch degradation. Recently isolated Arabidopsis thaliana amy3 bam1 double mutants are hypersensitive to osmotic stress, showing impaired root growth. amy3 bam1 plants close their stomata under osmotic stress at similar rates as the wild type but fail to mobilize starch in the leaves. 14 C labeling showed that amy3 bam1 plants have reduced carbon export to the root, affecting osmolyte accumulation and root growth during stress. Using genetic approaches, we further demonstrate that abscisic acid controls the activity of BAM1 and AMY3 in leaves under osmotic stress through the AREB/ABF-SnRK2 kinase-signaling pathway. We propose that differential regulation and isoform subfunctionalization define starch-adaptive plasticity, ensuring an optimal carbon supply for continued growth under an ever-changing environment.

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Section: Introductionmentioning

confidence: 68%

Regulation of Leaf Starch Degradation by Abscisic Acid Is Important for Osmotic Stress Tolerance in Plants

et al. 2016

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“…Organic acids, TCA intermediates and its related enzymes are decreased under cold stress in an opposite way to i.e. Arabidopsis which tends to activate these pathways (97). Furthermore, on the contrary to other plants in which starch is quickly depleted under stress situations most probably for the conversion into other sugars (19), in C. reinhardtii starch is constantly accumulated.…”

Section: Discussionmentioning

confidence: 99%

Systemic Cold Stress Adaptation of Chlamydomonas reinhardtii

Valledor

Furuhashi

Hanak

et al. 2013

Molecular & Cellular Proteomics

130

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Chlamydomonas reinhardtii is one of the most important model organisms nowadays phylogenetically situated between higher plants and animals (Merchant et al. 2007). Stress adaptation of this unicellular model algae is in the focus because of its relevance to biomass and biofuel production. Here, we have studied cold stress adaptation of C. reinhardtii hitherto not described for this algae whereas intensively studied in higher plants. Toward this goal, high throughput mass spectrometry was employed to integrate proteome, metabolome, physiological and cell-morphological changes during a time-course from 0 to 120 h. These data were complemented with RT-qPCR for target genes involved in central metabolism, signaling, and lipid biosynthesis. Using this approach dynamics in central metabolism were linked to cold-stress dependent sugar and autophagy pathways as well as novel genes in C. reinhardtii such as CKIN1, CKIN2 and a hitherto functionally not annotated protein named CKIN3. Cold stress affected extensively the physiology and the organization of the cell. Gluconeogenesis and starch biosynthesis pathways are activated leading to a pronounced starch and sugar accumulation. Quantitative lipid profiles indicate a sharp decrease in the lipophilic fraction and an increase in polyunsaturated fatty acids suggesting this as a mechanism of maintaining membrane fluidity. The proteome is completely remodeled during cold stress: specific candidates of the ribosome and the spliceosome indicate altered biosynthesis and degradation of proteins important for adaptation to low temperatures. Specific proteasome degradation may be mediated by the observed cold-specific changes in the ubiquitinylation system. Sparse partial least squares regression analysis was applied for protein correlation network analysis using proteins as predictors and Fv/Fm, FW, total lipids, and starch as responses. We applied also Granger causality analysis and revealed correlations between proteins and metabolites otherwise not detectable. Twenty percent of the proteins responsive to cold are uncharacterized proteins. This presents a considerable resource for new discoveries in cold stress biology in alga and plants. Molecular &

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“…5B). Increases of both metabolites as osmoprotectants under stress conditions such as cold, heat, salt, and drought have been well documented (Taji et al, 2002;Kaplan et al, 2004Kaplan et al, , 2007Nishizawa et al, 2008;Sanchez et al, 2008). The high accumulation of these metabolites might be needed to protect the plant cells in the basal region to allow the progression of senescence, presumably to sustain functionality (e.g.…”

Section: Carbon Metabolism During Developmental Senescencementioning

confidence: 99%

Comprehensive Dissection of Spatiotemporal Metabolic Shifts in Primary, Secondary, and Lipid Metabolism during Developmental Senescence in Arabidopsis

et al. 2013

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Developmental senescence is a coordinated physiological process in plants and is critical for nutrient redistribution from senescing leaves to newly formed sink organs, including young leaves and developing seeds. Progress has been made concerning the genes involved and the regulatory networks controlling senescence. The resulting complex metabolome changes during senescence have not been investigated in detail yet. Therefore, we conducted a comprehensive profiling of metabolites, including pigments, lipids, sugars, amino acids, organic acids, nutrient ions, and secondary metabolites, and determined approximately 260 metabolites at distinct stages in leaves and siliques during senescence in Arabidopsis (Arabidopsis thaliana). This provided an extensive catalog of metabolites and their spatiotemporal cobehavior with progressing senescence. Comparison with silique data provides clues to source-sink relations. Furthermore, we analyzed the metabolite distribution within single leaves along the basipetal sink-source transition trajectory during senescence. Ceramides, lysolipids, aromatic amino acids, branched chain amino acids, and stressinduced amino acids accumulated, and an imbalance of asparagine/aspartate, glutamate/glutamine, and nutrient ions in the tip region of leaves was detected. Furthermore, the spatiotemporal distribution of tricarboxylic acid cycle intermediates was already changed in the presenescent leaves, and glucosinolates, raffinose, and galactinol accumulated in the base region of leaves with preceding senescence. These results are discussed in the context of current models of the metabolic shifts occurring during developmental and environmentally induced senescence. As senescence processes are correlated to crop yield, the metabolome data and the approach provided here can serve as a blueprint for the analysis of traits and conditions linking crop yield and senescence.

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Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold‐regulated gene expression with modifications in metabolite content

Cited by 445 publications

References 67 publications

Regulation of Leaf Starch Degradation by Abscisic Acid Is Important for Osmotic Stress Tolerance in Plants

Regulation of Leaf Starch Degradation by Abscisic Acid Is Important for Osmotic Stress Tolerance in Plants

Systemic Cold Stress Adaptation of Chlamydomonas reinhardtii

Comprehensive Dissection of Spatiotemporal Metabolic Shifts in Primary, Secondary, and Lipid Metabolism during Developmental Senescence in Arabidopsis

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