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The C4 cycle and beyond: diverse metabolic adaptations accompany dual-cell photosynthetic functions in Setaria
Proteomic and kinetic analyses disclose metabolic strategies involving chloroplastic, mitochondrial, and peroxisomal proteins to maintain an optimal performance of the C4 cycle. Abstract C4 photosynthesis is typically characterized by the spatial compartmentalization of the photosynthetic reactions...
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Published in: | Journal of experimental botany 2021-12, Vol.72 (22), p.7876-7890 |
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Main Authors: | , , , , , , , |
Format: | Article |
Language: | English |
Subjects: | |
Citations: | Items that this one cites Items that cite this one |
Online Access: | Get full text |
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Summary: | Proteomic and kinetic analyses disclose metabolic strategies involving chloroplastic, mitochondrial, and peroxisomal proteins to maintain an optimal performance of the C4 cycle.
Abstract
C4 photosynthesis is typically characterized by the spatial compartmentalization of the photosynthetic reactions into mesophyll (M) and bundle sheath (BS) cells. Initial carbon fixation within M cells gives rise to C4 acids, which are transported to the BS cells. There, C4 acids are decarboxylated so that the resulting CO2 is incorporated into the Calvin cycle. This work is focused on the study of Setaria viridis, a C4 model plant, closely related to several major feed and bioenergy grasses. First, we performed the heterologous expression and biochemical characterization of Setaria isoforms for chloroplastic NADP-malic enzyme (NADP-ME) and mitochondrial NAD-malic enzyme (NAD-ME). The kinetic parameters obtained agree with a major role for NADP-ME in the decarboxylation of the C4 acid malate in the chloroplasts of BS cells. In addition, mitochondria-located NAD-ME showed regulatory properties that could be important in the context of the operation of the C4 carbon shuttle. Secondly, we compared the proteomes of M and BS compartments and found 825 differentially accumulated proteins that could support different metabolic scenarios. Most interestingly, we found evidence of metabolic strategies to insulate the C4 core avoiding the leakage of intermediates by either up-regulation or down-regulation of chloroplastic, mitochondrial, and peroxisomal proteins. Overall, the results presented in this work provide novel data concerning the complexity of C4 metabolism, uncovering future lines of research that will undoubtedly contribute to the expansion of knowledge on this topic. |
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ISSN: | 0022-0957 1460-2431 |
DOI: | 10.1093/jxb/erab381 |