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

Abstract

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. Few plant metabolic fluxes are readily accessible to routine measurement. The major exceptions to this are fluxes involving gas exchange, such as respiration and photosynthesis. Measurements of respiratory gas exchange (i.e. mitochondrial oxygen uptake or CO 2 release in the absence of photorespiration) are useful from a metabolic perspective because they can be interpreted in terms of the underlying carbon fluxes and the generation of ATP by oxidative phosphorylation (Sweetlove et al., 2013). The biochemical reactions of respiration that produce CO 2 and lead to oxygen consumption are well understood (Plaxton and Podestá, 2006;Sweetlove et al., 2010;Millar et al., 2011;Tcherkez et al., 2012). The stoichiometries of the reactions and the connections between them are known, which provides us with a metabolic map of respiration that includes glycolysis, the oxidative pentose phosphate pathway, the citric acid cycle, the mitochondrial electron transport chain (mETC), ATP synthase, and several other surrounding reactions. In plants, carbohydrates are the dominant respiratory substrates, whereas lipids are rarely respired (Plaxton and Podestá, 2006). Carbohydrate oxidation proceeds via organic acids, which serve many purposes in plant...

Predicting dark respiration rates of wheat leaves from hyperspectral reflectance

“…Wheat leaf R dark varied enormously, irrespective of how it was expressed. The sevenfold variation in wheat leaf R dark_LA reported here is higher than the modest twofold reported by Scafaro et al () for wheat and by O'Leary et al () for Arabidopsis ( Arabidopsis thaliana L.). It is comparable with the tenfold variation for 899 species covering plant functional types from the Arctic to the tropics (Atkin et al, ).…”

“…These could include (a) the abundance of sugars, organic acids and adenylates (ATP and ADP); (b) abundance of respiratory enzymes with distinct spectral properties; or (c) aspects of mitochondrial mass or lipid composition. Both leaf starch and sugar content are correlated with R dark (Noguchi, ; O'Leary et al, ; Peraudeau et al, ), and they have both been estimated from hyperspectral reflectance within the range reported in this study (Curran, ; Ramirez et al, ). Cytochrome c oxidase (COX) a respiratory protein complex in the mitochondrial respiratory chain also exhibits spectral characteristics (Appaix et al, ; Mason, Nicholls, & Cooper, ).…”

“…Hyperspectral reflectance characteristics of leaves have been used to predict LMA, leaf N, and photosynthetic traits. Extending this approach to predict R dark seemed plausible given that R dark scales with LMA (Wright et al, ), leaf N (Reich et al, ; Reich, Walters, Ellsworth, et al, ; Ryan, ; Wright et al, ), and photosynthesis (Bouma, De Visser, Van Leeuwen, De Kock, & Lambers, ; O'Leary et al, ). Although the prediction of R dark could in part be related to N or LMA, in our study, clear and simple correlations were not evident (Figure a,b).…”

Core principles which explain variation in respiration across biological scales

“…For example, in wheat, pea and spinach grown in a controlled environment, leaf night‐time respiration correlates strongly with carbohydrate concentration amassed during the previous photosynthetic period, suggesting that respiratory substrate supply controls respiration (Azcon‐Bieto et al ., ). However, the size of the carbohydrate reserve also regulates the rate of sucrose export during the course of the night, which itself is a major ATP demand, causing supply and demand to be linked (Bouma et al ., ; O'Leary et al ., ). Each tissue will experience its own set of linked supply and demand conditions which will determine its respiration rate.…”

“…Respiration is greatly affected by numerous environmental conditions, with respiration rates sometimes responding to change in a predictable fashion, as with temperature (Atkin et al ., ), but often responding in a currently unpredictable way, as with increased atmospheric CO 2 (Dusenge et al ., ). Lastly, even in intraspecies comparisons, leaf respiratory rates varied two‐fold among natural Arabidopsis accessions grown under common laboratory conditions (O'Leary et al ., ) or in wheat lines grown in a common environment (Scafaro et al ., ). These observations illustrate the large scope of research on differences in respiratory rate.…”