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

PAULA CALACE; TOMAS TONETTI; EZEQUIEL MARGARIT; FIGUEROA, CARLOS M.; CARLOS LOBERTTI; CARLOS S. ANDREO; MARIEL C GERRARD WHEELER; MARIAN SAIGO

JOURNAL OF EXPERIMENTAL BOTANY

OXFORD UNIV PRESS

Año: 2021

0022-0957

C4 photosynthesis is typically characterized by the spatial compartmentalization of the photosynthetic reactions intomesophyll (M) and bundle sheath (BS) cells. Initial carbon fixation within M cells gives rise to C4 acids, which aretransported to the BS cells. There, C4 acids are decarboxylated so that the resulting CO2 is incorporated into theCalvin cycle. This work is focused on the study of Setaria viridis, a C4 model plant, closely related to several majorfeed and bioenergy grasses. First, we performed the heterologous expression and biochemical characterization ofSetaria 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 malatein the chloroplasts of BS cells. In addition, mitochondria-located NAD-ME showed regulatory properties that couldbe important in the context of the operation of the C4 carbon shuttle. Secondly, we compared the proteomes ofM and BS compartments and found 825 differentially accumulated proteins that could support different metabolicscenarios. Most interestingly, we found evidence of metabolic strategies to insulate the C4 core avoiding the leakageof 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, uncoveringfuture lines of research that will undoubtedly contribute to the expansion of knowledge on this topic.