Nitric oxide induces monosaccharide accumulation through enzyme S‐nitrosylation

• Published in: Plant, cell and environment Vol. 40; no. 9; pp. 1834 - 1848
• Main Authors: Zhang, Zhong‐Wei, Luo, Sha, Zhang, Gong‐Chang, Feng, Ling‐Yang, Zheng, Chong, Zhou, Yang‐Hong, Du, Jun‐Bo, Yuan, Ming, Chen, Yang‐Er, Wang, Chang‐Quan, Liu, Wen‐Juan, Xu, Xiao‐Chao, Hu, Yong, Bai, Su‐Lan, Kong, Dong‐Dong, Yuan, Shu, He, Yi‐Kun
• Format: Journal Article
• Language: English
• Published: United States Wiley Subscription Services, Inc 01.09.2017
• Subjects: Accumulation; Adenosine diphosphate; Adenosine Diphosphate Glucose - metabolism; Adenosine Triphosphate - metabolism; Arabidopsis - drug effects; Arabidopsis - enzymology; Arabidopsis - metabolism; ATP; ATP synthase; ATP Synthetase Complexes - metabolism; Biosynthesis; Catabolism; Coenzyme A; Defects; Dehydrogenase; Dehydrogenases; Enzymes; Flowering; Fructose; Glucose; Glycolysis; Glycolysis - drug effects; Metabolism; monosaccharide catabolism; Monosaccharides; Monosaccharides - metabolism; Mutation - genetics; Nitric oxide; Nitric Oxide - pharmacology; Nitrosation; Oxidation; Oxidation-Reduction; Phenotype; Physiological effects; Plant Development - drug effects; Plant growth; Plant Roots - anatomy & histology; Plant Roots - drug effects; Plant Roots - metabolism; Plant Shoots - drug effects; Plant Shoots - metabolism; Plants (botany); polysaccharide synthesis; Pyruvate Dehydrogenase Complex - metabolism; Pyruvic acid; Solubility; Starch; Starch - metabolism; starch granule; Sucrose; Sucrose - pharmacology; Sugar; Supplements; Sweetness; Thioctic Acid - analogs & derivatives; Thioctic Acid - metabolism; Uridine Diphosphate Glucose - metabolism; polysaccharide synthesis; monosaccharide catabolism; starch granule
• ISSN: 0140-7791; 1365-3040
• DOI: 10.1111/pce.12989

Nitric oxide (NO) is extensively involved in various growth processes and stress responses in plants; however, the regulatory mechanism of NO‐modulated cellular sugar metabolism is still largely unknown. Here, we report that NO significantly inhibited monosaccharide catabolism by modulating sugar metabolic enzymes through S‐nitrosylation (mainly by oxidizing dihydrolipoamide, a cofactor of pyruvate dehydrogenase). These S‐nitrosylation modifications led to a decrease in cellular glycolysis enzymes and ATP synthase activities as well as declines in the content of acetyl coenzyme A, ATP, ADP‐glucose and UDP‐glucose, which eventually caused polysaccharide‐biosynthesis inhibition and monosaccharide accumulation. Plant developmental defects that were caused by high levels of NO included delayed flowering time, retarded root growth and reduced starch granule formation. These phenotypic defects could be mediated by sucrose supplementation, suggesting an essential role of NO‐sugar cross‐talks in plant growth and development. Our findings suggest that molecular manipulations could be used to improve fruit and vegetable sweetness. The physiological effects of NO can be largely reversed by high‐level (either exogenous or endogenous) sucrose treatments. Nitric oxide significantly inhibits polysaccharide synthesis (by S‐nitrosylation of ATP synthase and therefore decreasing ATP, ADP‐glucose and UDP‐glucose levels) and monosaccharide catabolism by modulating sugar metabolic enzymes (including pyruvate dehydrogenase) through S‐nitrosylation. Therefore, cellular monosaccharides (glucose and fructose) accumulated substantially after NO treatments, which enhanced plant's sweetness.