Metabolite Profiling in <i>Arabidopsis</i><i>thaliana</i> with Moderately Impaired Photorespiration Reveals Novel Metabolic Links and Compensatory Mechanisms of Photorespiration

• Main Authors: Stefan Timm, Adriano Nunes-Nesi, Alexandra Florian, Marion Eisenhut, Katja Morgenthal, Markus Wirtz, Rüdiger Hell, Wolfram Weckwerth, Martin Hagemann, Alisdair R. Fernie, Hermann Bauwe
• Format: Article
• Language: English
• Published: MDPI AG 2021-06-01
• Series: Metabolites
• Subjects: <i>Arabidopsis</i>; photorespiration; hydroxypyruvate reductase; metabolomics; isotope labeling; metabolic acclimation
• Online Access: https://www.mdpi.com/2218-1989/11/6/391

Photorespiration is an integral component of plant primary metabolism. Accordingly, it has been often observed that impairing the photorespiratory flux negatively impacts other cellular processes. In this study, the metabolic acclimation of the <i>Arabidopsis</i><i>thaliana</i> wild type was compared with the hydroxypyruvate reductase 1 (HPR1; <i>hpr1</i>) mutant, displaying only a moderately reduced photorespiratory flux. Plants were analyzed during development and under varying photoperiods with a combination of non-targeted and targeted metabolome analysis, as well as ¹³C- and ¹⁴C-labeling approaches. The results showed that <i>HPR1</i> deficiency is more critical for photorespiration during the vegetative compared to the regenerative growth phase. A shorter photoperiod seems to slowdown the photorespiratory metabolite conversion mostly at the glycerate kinase and glycine decarboxylase steps compared to long days. It is demonstrated that even a moderate impairment of photorespiration severely reduces the leaf-carbohydrate status and impacts on sulfur metabolism. Isotope labeling approaches revealed an increased CO₂ release from <i>hpr1</i> leaves, most likely occurring from enhanced non-enzymatic 3-hydroxypyruvate decarboxylation and a higher flux from serine towards ethanolamine through serine decarboxylase. Collectively, the study provides evidence that the moderate <i>hpr1</i> mutant is an excellent tool to unravel the underlying mechanisms governing the regulation of metabolic linkages of photorespiration with plant primary metabolism.