Combined loss of mitochondrial MDH1 and NAD-malic enzyme impairs Arabidopsis growth and photosynthesis under energy-limiting conditions

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Abstract
Malate is a central metabolite in plant energy metabolism and biosynthesis and a major carrier of carbon and reducing equivalents between chloroplasts, the cytosol, and mitochondria. Here, we combined reverse genetics with multiple complementary approaches to investigate how disruption of the major mitochondrial malate-converting enzymes affects plant performance under different environmental conditions. We generated two independent mutant lines (mdh1 me1 me2) lacking the predominant mitochondrial malate dehydrogenase isoform MDH1 and both subunits of NAD-dependent malic enzyme (NAD-ME), ME1 and ME2. Growth under contrasting photoperiods and irradiances revealed a conditional phenotype that was most pronounced under short-day/low-light condition. Under this condition, the mutants exhibited impaired growth and photosynthetic performance, accompanied by cytosolic redox imbalance and altered chloroplast ultrastructure. Transfer experiments demonstrated that this phenotype was reversible and determined by the prevailing growth conditions: plants initially grown under short days and low light recovered in newly formed leaves after transfer to long-day/normal-light condition, whereas the reciprocal transfer reproduced the growth impairment in newly formed leaves. Transcriptomic and proteomic analyses revealed dawn-associated perturbations in photosynthetic and redox homeostasis, characterized by reduced investment in chloroplast translation and photosynthetic machinery alongside enhanced proteome maintenance, photoprotection and repair, and iron/ROS homeostasis. Branched-chain amino acids also accumulated in the mutants at the end of the night under low light. Together, these results show that the combined loss of mitochondrial MDH1 and NAD-ME causes a reversible, light-regime-dependent impairment of Arabidopsis growth and photosynthetic performance, highlighting the importance of the simultaneous contribution of both the MDH1 and NAD-ME systems to mitochondrial malate conversion when photosynthetic energy input is limited.