Importation of chloroplast proteins under heat stress is facilitated by their SUMO conjugations

Abstract

Chloroplasts are hypersensitive to heat stress (HS). SUMOylation, a critical posttranslational modification, is conservatively involved in HS responses. However, the functional connection between SUMOylation and chloroplasts under HS remains to be studied.The bioinformatics, biochemistry, and cell biology analyses were used to detect the SUMOylation statuses of Arabidopsis nuclear-encoded chloroplast proteins and the effect of SUMOylation on subcellular localization of these proteins under HS. PSBR, a subunit of photosystem II, was used as an example for a detailed investigation of functional mechanisms.After a global SUMOylation site prediction of nuclear-encoded chloroplast proteins, biochemical data showed that most of the selected candidates are modified by SUMO3 in the cytoplasm. The chloroplast localization of these SUMOylation targets under long-term HS is partially maintained by the SUMO ligase AtSIZ1. The HS-induced SUMOylation on PSBR contributes to the maintenance of its chloroplast localization, which is dependent on its chloroplast importation efficiency correlated to phosphorylation. The complementation analysis provided evidence that SUMOylation is essential for the physiological function of PSBR under HS.Our study illustrated a general regulatory mechanism of SUMOylation in maintaining the chloroplast protein importation during HS and provided hints for further investigation on protein modifications associated with plant organelles under stress conditions.

A genetic module at one locus in rice protects chloroplasts to enhance thermotolerance

“…The process of ubiquitination plays a key role in eliminating denatured proteins and thus improves plants thermotolerance (6,12). Chloroplasts are photosynthetic organelles that also contribute to heat-stress responses (8,10,13,14). Chloroplast proteins damaged by stress need to be rapidly degraded through chloroplastic hydrolases or extraplastidic pathways (26S-proteasome and autophagy), which are well described (15)(16)(17).…”

Chloroplast proteostasis: A story of birth, life, and death

“…Moreover, a recent study indicated that the SUMO modification of various chloroproteins is essential for their precise chloroplast localization under heat stress. At least the Toc33-containing TOC complex is involved in the import of SUMOylated preproteins ( Zheng et al., 2022 ), further indicating that import regulation makes a large contribution to the shifting and rebalancing of chloroplast proteostasis in response to environmental stimuli.…”

The hot science in rice research: How rice plants cope with heat stress

“…SUMOylation is required for the import of nucleus-encoded chloroplast proteins in Arabidopsis under heat stress conditions (Zheng et al, 2022).…”

“…C312) (Mishra et al, 2017), and creeping bentgrass ( Agrostis stolonifera L.) (Li et al, 2013). SUMOylation is required for the import of nucleus‐encoded chloroplast proteins in Arabidopsis under heat stress conditions (Zheng et al, 2022). SUMOylation of the TOC complex, which imports proteins into chloroplasts, was recently reported (Watson et al, 2021).…”