Improved photorespiration has a major impact on the root metabolome of Arabidopsis.

Abstract

Photorespiration is an essential metabolic repair process in oxygenic photosynthesis, as it detoxifies Rubisco's inhibitory oxygenase byproduct, 2-phosphoglycolate (2-PG). It has been demonstrated that improving endogenous photorespiration in C3 plants through enzyme overexpression can enhance photosynthesis and promote plant growth. However, the potential impact of improved photorespiration in leaves on heterotrophic roots remained unexplored. To address this, we conducted a metabolome analysis of Arabidopsis leaves and roots using transgenic lines with enhanced glycine decarboxylase (GDC) activity, achieved by overexpressing the mitochondrial lipoamide dehydrogenase (mtLPD1) subunit. In the leaves, mtLPD1 overexpression primarily resulted in reduced steady-state levels of intermediates associated with photorespiration, the tricarboxylic acid (TCA) cycle, and soluble sugars, while intermediates related to nitrogen metabolism were elevated. In roots, where mtLPD1 expression was unchanged, we observed contrasting accumulation patterns in the transgenic lines compared to the wildtype, including increased levels of photorespiratory and TCA-cycle intermediates. Notably, we also detected elevated amounts of soluble sugars, nitrate, and starch. Phloem exudate analysis revealed altered metabolite profiles in the overexpressors, particularly with respect to photorespiratory intermediates linked to the GDC reaction, as well as soluble sugars and metabolites involved in cellular redox homeostasis. This suggested an increased transport of these metabolites from shoots to roots, thereby altering sink organ metabolism. In summary, we hypothesize that optimizing photorespiration enhances photosynthesis, which leads to an increased export of carbon surplus to heterotrophic tissues. Thus, improving photorespiration may hold potential for increasing yields in beet- and tuber-forming plants.