Remodeled respiration in ndufs4 with low phosphorylation efficiency suppresses Arabidopsis germination and growth and alters control of metabolism at night

Respiratory oxidative phosphorylation is a cornerstone of cellular metabolism in aerobic multicellular organisms. Theefficiency of this process is generally assumed to be maximized, but the presence of dynamically regulated nonphosphorylatingbypasses implies that plants can alter phosphorylation efficiency and can benefit from lowered energy generation duringrespiration under certain conditions. We characterized an Arabidopsis (Arabidopsis thaliana) mutant, ndufs4 (for NADHdehydrogenase [ubiquinone] fragment S subunit 4), lacking complex I of the respiratory chain, which has constitutivelylowered phosphorylation efficiency. Through analysis of the changes to mitochondrial function as well as whole cell transcriptsand metabolites, we provide insights into how cellular metabolism flexibly adapts to reduced phosphorylation efficiency andwhy this state may benefit the plant by providing moderate stress tolerance. We show that removal of the single proteinsubunit NDUFS4 prevents assembly of complex I and removes its function from mitochondria without pleiotropic effects onother respiratory components. However, the lack of complex I promotes broad changes in the nuclear transcriptome governinggrowth and photosynthetic function. We observed increases in organic acid and amino acid pools in the mutant, especially atnight, concomitant with alteration of the adenylate content. While germination is delayed, this can be rescued by application ofgibberellic acid, and root growth assays of seedlings show enhanced tolerance to cold, mild salt, and osmotic stress.We discussthese observations in the light of recent data on the knockout of nonphosphorylating respiratory bypass enzymes that showopposite changes in metabolites and stress sensitivity. Our data suggest that the absence of complex I alters the adenylatecontrol of cellular metabolism.