Sorbitol dehydrogenase aids grain-fill and integrates carbohydrate metabolism with redox in the hypoxic maize endosperm

Abstract Extreme low oxygen is typical of microenvironments inside developing grains, thus requiring metabolic adaptations to hypoxia. Potential contributions from sorbitol dehydrogenase (SDH) are tested here for maize (Zea mays) since the reversible reaction (fructose + NADH ↔ sorbitol + NAD+) can balance both redox state and metabolism during assimilate import into kernels. To do so, we developed and analyzed maize sdh1 mutants and over-expression lines. Dysfunction of Sdh1 decreased seed weight by 17%, impaired starch accumulation, and enhanced levels of glucose, fructose, and sucrose. Redox balance in the inner endosperm was also disrupted (NADH and NADPH levels rose) and adenylate energy charge (AEC) decreased. Moreover, genes responsive to oxidative stress were upregulated in mutant kernels. In contrast, Sdh1-OE lines rescued the small-grain phenotype without exceeding wild-type kernel size. Metabolite profiles of mutant and Sdh1-OE kernels revealed reciprocal levels for sucrose, hexoses, and key points of redox sensitivity and C/N balance. Results are distinct from the classical involvement of sorbitol in long distance transport (as in apples) and its contribution to desiccation tolerance in diverse species. Rather, our analyses support a two-fold contribution by an SDH-modulated sorbitol reservoir that 1) aids redox balance in the hypoxic endosperm by storing excess reductant and 2) minimizes fructose levels that can otherwise inhibit sucrose import, metabolism, and signaling pathways. Collective evidence reveals a previously unrecognized role for sorbitol and SDH in kernel-fill that integrates carbohydrate metabolism and redox balance in the low-oxygen endosperm of this developing grain.