The C4 cycle and beyond: diverse metabolic adaptations accompany dual-cell photosynthetic functions in Setaria

CALACE, PAULA; TONETTI, TOMÁS; MARGARIT, EZEQUIEL; FIGUEROA, CARLOS M; LOBERTTI, CARLOS; ANDREO, CARLOS S; GERRARD WHEELER, MARIEL C; SAIGO, MARIANA

JOURNAL OF EXPERIMENTAL BOTANY

OXFORD UNIV PRESS

Año: 2021 vol. 72 p. 7876 - 7890

0022-0957

C4 photosynthesis is typically characterised by the spatial compartmentalisation 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. In the first place, 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 of NADP-ME in the decarboxylation of the C4 acid malate in the chloroplasts of BS cells. Besides, mitochondria-located NAD-ME showed regulatory properties that could be important in the context of the operation of the C4 carbon shuttle. In the second place, 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.Artículo elegido como editor´s choice of the issue.