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Photorespiration differs among Arabidopsis thaliana ecotypes and is correlated with photosynthesis.

ABSTRACT: A greater understanding of natural variation in photosynthesis will inform strategies for crop improvement by revealing overlooked opportunities. We use Arabidopsis thaliana ecotypes as a model system to assess (i) how photosynthesis and photorespiration covary and (ii) how mesophyll conductance influences water use efficiency (WUE). Phenotypic variation in photorespiratory CO2 efflux was correlated with assimilation rates and two metrics of photosynthetic capacity (i.e. VCmax and Jmax); however, genetic correlations were not detected between photosynthesis and photorespiration. We found standing genetic variation-as broad-sense heritability-for most photosynthetic traits, including photorespiration. Genetic correlation between photosynthetic electron transport and carboxylation capacities indicates that these traits are genetically constrained. Winter ecotypes had greater mesophyll conductance, maximum carboxylation capacity, maximum electron transport capacity, and leaf structural robustness when compared with spring ecotypes. Stomatal conductance varied little in winter ecotypes, leading to a positive correlation between integrated WUE and mesophyll conductance. Thus, variation in mesophyll conductance can modulate WUE among A. thaliana ecotypes without a significant loss in assimilation. Genetic correlations between traits supplying energy and carbon to the Calvin-Benson cycle are consistent with biochemical models, suggesting that selection on either of these traits would improve all of them. Similarly, the lack of a genetic correlation between photosynthesis and photorespiration suggests that the positive scaling of these two traits can be broken.

SUBMITTER: Tomeo NJ

PROVIDER: S-EPMC6184796 | biostudies-literature | 2018 Oct

REPOSITORIES: biostudies-literature

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Photorespiration differs among Arabidopsis thaliana ecotypes and is correlated with photosynthesis.

Tomeo Nicholas J NJ Rosenthal David M DM Rosenthal David M DM

Journal of experimental botany 20181001 21

A greater understanding of natural variation in photosynthesis will inform strategies for crop improvement by revealing overlooked opportunities. We use Arabidopsis thaliana ecotypes as a model system to assess (i) how photosynthesis and photorespiration covary and (ii) how mesophyll conductance influences water use efficiency (WUE). Phenotypic variation in photorespiratory CO2 efflux was correlated with assimilation rates and two metrics of photosynthetic capacity (i.e. VCmax and Jmax); however ...[more]

PMID: 30053111

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Project description:Photorespiration recovers carbon that would be otherwise lost following the oxygenation reaction of rubisco and production of glycolate. Photorespiration is essential in plants and recycles glycolate into usable metabolic products through reactions spanning the chloroplast, mitochondrion, and peroxisome. Catalase in peroxisomes plays an important role in this process by disproportionating H2O2 resulting from glycolate oxidation into O2 and water. We hypothesize that catalase in the peroxisome also protects against nonenzymatic decarboxylations between hydrogen peroxide and photorespiratory intermediates (glyoxylate and/or hydroxypyruvate). We test this hypothesis by detailed gas exchange and biochemical analysis of Arabidopsis thaliana mutants lacking peroxisomal catalase. Our results strongly support this hypothesis, with catalase mutants showing gas exchange evidence for an increased stoichiometry of CO2 release from photorespiration, specifically an increase in the CO2 compensation point, a photorespiratory-dependent decrease in the quantum efficiency of CO2 assimilation, increase in the 12CO2 released in a 13CO2 background, and an increase in the postillumination CO2 burst. Further metabolic evidence suggests this excess CO2 release occurred via the nonenzymatic decarboxylation of hydroxypyruvate. Specifically, the catalase mutant showed an accumulation of photorespiratory intermediates during a transient increase in rubisco oxygenation consistent with this hypothesis. Additionally, end products of alternative hypotheses explaining this excess release were similar between wild type and catalase mutants. Furthermore, the calculated rate of hydroxypyruvate decarboxylation in catalase mutant is much higher than that of glyoxylate decarboxylation. This work provides evidence that these nonenzymatic decarboxylation reactions, predominately hydroxypyruvate decarboxylation, can occur in vivo when photorespiratory metabolism is genetically disrupted.

Project description:BackgroundLow temperature leads to major crop losses every year. Although several studies have been conducted focusing on diversity of cold tolerance level in multiple phenotypically divergent Arabidopsis thaliana (A. thaliana) ecotypes, genome-scale molecular understanding is still lacking.ResultsIn this study, we report genome-scale transcript response diversity of 10 A. thaliana ecotypes originating from different geographical locations to non-freezing cold stress (10°C). To analyze the transcriptional response diversity, we initially compared transcriptome changes in all 10 ecotypes using Arabidopsis NimbleGen ATH6 microarrays. In total 6061 transcripts were significantly cold regulated (p < 0.01) in 10 ecotypes, including 498 transcription factors and 315 transposable elements. The majority of the transcripts (75%) showed ecotype specific expression pattern. By using sequence data available from Arabidopsis thaliana 1001 genome project, we further investigated sequence polymorphisms in the core cold stress regulon genes. Significant numbers of non-synonymous amino acid changes were observed in the coding region of the CBF regulon genes. Considering the limited knowledge about regulatory interactions between transcription factors and their target genes in the model plant A. thaliana, we have adopted a powerful systems genetics approach- Network Component Analysis (NCA) to construct an in-silico transcriptional regulatory network model during response to cold stress. The resulting regulatory network contained 1,275 nodes and 7,720 connections, with 178 transcription factors and 1,331 target genes.ConclusionsA. thaliana ecotypes exhibit considerable variation in transcriptome level responses to non-freezing cold stress treatment. Ecotype specific transcripts and related gene ontology (GO) categories were identified to delineate natural variation of cold stress regulated differential gene expression in the model plant A. thaliana. The predicted regulatory network model was able to identify new ecotype specific transcription factors and their regulatory interactions, which might be crucial for their local geographic adaptation to cold temperature. Additionally, since the approach presented here is general, it could be adapted to study networks regulating biological process in any biological systems.

Dataset Information

Photorespiration differs among Arabidopsis thaliana ecotypes and is correlated with photosynthesis.

Publications

Photorespiration differs among Arabidopsis thaliana ecotypes and is correlated with photosynthesis.

Similar Datasets

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