Regulation of Sugar and Storage Oil Metabolism by Phytochrome during De-etiolation

• Published in: Plant physiology (Bethesda) 2020-02, Vol.182 (2), p.1114-1129
• Main Authors: Kozuka, Toshiaki, Sawada, Yuji, Imai, Hiroyuki, Kanai, Masatake, Hirai, Masami Yokota, Mano, Shoji, Uemura, Matsuo, Nishimura, Mikio, Kusaba, Makoto, Nagatani, Akira
• Format: Article
• Language: English
• Subjects: Arabidopsis - enzymology; Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis - radiation effects; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Chromatography, High Pressure Liquid; Cotyledon - metabolism; Cotyledon - radiation effects; Cotyledon - ultrastructure; Etiolation - genetics; Etiolation - radiation effects; Glyoxylates - metabolism; Glyoxysomes - metabolism; Glyoxysomes - radiation effects; Light; Lipid Droplets - metabolism; Lipid Droplets - radiation effects; Metabolome - radiation effects; Metabolomics; Microscopy, Electron, Transmission; Mutation; Phytochrome A - genetics; Phytochrome A - metabolism; Phytochrome B - genetics; Phytochrome B - metabolism; Seedlings - metabolism; Seedlings - radiation effects; Sugars - metabolism; Thylakoids - metabolism; Thylakoids - ultrastructure; Triglycerides - metabolism
• ISSN: 0032-0889; 1532-2548
• DOI: 10.1104/pp.19.00535

Exposure of dark-grown (etiolated) seedlings to light induces the heterotrophic-to-photoautotrophic transition (de-etiolation) processes, including the formation of photosynthetic machinery in the chloroplast and cotyledon expansion. Phytochrome is a red (R)/far-red (FR) light photoreceptor that is involved in the various aspects of de-etiolation. However, how phytochrome regulates metabolic dynamics in response to light stimulus has remained largely unknown. In this study, to elucidate the involvement of phytochrome in the metabolic response during de-etiolation, we performed widely targeted metabolomics in Arabidopsis ( ) wild-type and phytochrome A and B double mutant seedlings de-etiolated under R or FR light. The results revealed that phytochrome had strong impacts on the primary and secondary metabolism during the first 24 h of de-etiolation. Among those metabolites, sugar levels decreased during de-etiolation in a phytochrome-dependent manner. At the same time, phytochrome upregulated processes requiring sugars. Triacylglycerols are stored in the oil bodies as a source of sugars in Arabidopsis seedlings. Sugars are provided from triacylglycerols through fatty acid β-oxidation and the glyoxylate cycle in glyoxysomes. We examined if and how phytochrome regulates sugar production from oil bodies. Irradiation of the etiolated seedlings with R and FR light dramatically accelerated oil body mobilization in a phytochrome-dependent manner. Glyoxylate cycle-deficient mutants not only failed to mobilize oil bodies but also failed to develop thylakoid membranes and expand cotyledon cells upon exposure to light. Hence, phytochrome plays a key role in the regulation of metabolism during de-etiolation.