Photorespiratory serine hydroxymethyltransferase 1 activity impacts abiotic stress tolerance and stomatal closure

• Published in: Plant, cell and environment cell and environment, 2019-09, Vol.42 (9), p.2567-2583
• Main Authors: Liu, Yanpei, Mauve, Caroline, Lamothe‐Sibold, Marlène, Guérard, Florence, Glab, Nathalie, Hodges, Michael, Jossier, Mathieu
• Format: Article
• Language: English
• Subjects: abiotic stress; Abscisic Acid - metabolism; Arabidopsis - enzymology; Arabidopsis - genetics; Arabidopsis - growth & development; Arabidopsis Proteins - metabolism; Biochemistry, Molecular Biology; Botanics; Carbon Dioxide; Cell Respiration; Dehydration; Drought; Droughts; Genetic Complementation Test; Glycine; Glycine Hydroxymethyltransferase - metabolism; Life Sciences; Metabolism; Mitochondria; Mutation; Oxygenase; Phenotypes; Phosphorylation; photorespiration; Photosynthesis; Plant Stomata - physiology; Plants, Genetically Modified; Polyamines; Proline; protein phosphorylation; Proteins; Salt Tolerance - genetics; Salts; Serine; SHMT1; Stomata; Stress; Stress, Physiological; Vegetal Biology
• ISSN: 0140-7791; 1365-3040
• DOI: 10.1111/pce.13595

The photorespiratory cycle is a crucial pathway in photosynthetic organisms because it removes toxic 2‐phosphoglycolate made by the oxygenase activity of ribulose‐1,5‐bisphosphate carboxylase/oxygenase and retrieves its carbon as 3‐phosphoglycerate. Mitochondrial serine hydroxymethyltransferase 1 (SHMT1) is an essential photorespiratory enzyme converting glycine to serine. SHMT1 regulation remains poorly understood although it could involve the phosphorylation of serine 31. Here, we report the complementation of Arabidopsis thaliana shm1‐1 by SHMT1 wild‐type, phosphorylation‐mimetic (S31D) or nonphophorylatable (S31A) forms. All SHMT1 forms could almost fully complement the photorespiratory growth phenotype of shm1‐1; however, each transgenic line had only 50% of normal SHMT activity. In response to either a salt or drought stress, Compl‐S31D lines showed a more severe growth deficiency compared with the other transgenic lines. This sensitivity to salt appeared to reflect reduced SHMT1‐S31D protein amounts and a lower activity that impacted leaf metabolism leading to proline underaccumulation and overaccumulation of polyamines. The S31D mutation in SHMT1 also led to a reduction in salt‐induced and ABA‐induced stomatal closure. Taken together, our results highlight the importance of maintaining photorespiratory SHMT1 activity in salt and drought stress conditions and indicate that SHMT1 S31 phosphorylation could be involved in modulating SHMT1 protein stability. Serine hydroxymethyltransferase 1 (SHMT1) regulation is poorly understood although it could involve the phosphorylation of serine 31. Complementation of Arabidopsis thaliana shm1‐1 by SHMT1 wild‐type, phosphorylation‐mimetic (S31D) or nonphophorylatable (S31A) forms revealed that Compl‐S31D lines were more sensitive to salt and drought stress and exhibited a reduction in salt‐induced and ABA‐induced stomatal closure. The increased stress sensitivity of SHMT1‐S31D was linked to a lower photorespiratory‐dependent SHMT1 activity arising from a phosphorylation‐mimetic decrease in SHMT1 protein stability.