Variation in Leaf Respiration Rates at Night Correlates with Carbohydrate and Amino Acid Supply

Plant respiration can theoretically be fueled by and dependent upon an array of central metabolism components; however, which ones are responsible for the quantitative variation found in respiratory rates is unknown. Here, large-scale screens revealed 2-fold variation in nighttime leaf respiration rate (R_N) among mature leaves from an Arabidopsis (Arabidopsis thaliana) natural accession collection grown under common favorable conditions. R_N variation was mostly maintained in the absence of genetic variation, which emphasized the low heritability of R_N and its plasticity toward relatively small environmental differences within the sampling regime. To pursue metabolic explanations for leaf R_N variation, parallel metabolite level profiling and assays of total protein and starch were performed. Within an accession, R_N correlated strongly with stored carbon substrates, including starch and dicarboxylic acids, as well as sucrose, major amino acids, shikimate, and salicylic acid. Among different accessions, metabolite-R_N correlations were maintained with protein, sucrose, and major amino acids but not stored carbon substrates. A complementary screen of the effect of exogenous metabolites and effectors on leaf R_N revealed that (1) R_N is stimulated by the uncoupler FCCP and high levels of substrates, demonstrating that both adenylate turnover and substrate supply can limit leaf R_N, and (2) inorganic nitrogen did not stimulate R_N, consistent with limited nighttime nitrogen assimilation. Simultaneous measurements of R_N and protein synthesis revealed that these processes were largely uncorrelated in mature leaves. These results indicate that differences in preceding daytime metabolic activities are the major source of variation in mature leaf R_N under favorable controlled conditions.