SUMOylation of rice DELLA SLR1 modulates transcriptional responses and improves yield under salt stress

Abstract

Author Contributions: 15 NMG participated in the conception of research, executed most experiments, and 16 wrote the article with contributions from all authors. TF did protein interaction 17 experiments. MTGR characterized SUMO-protease rice lines. CCM analysed data 18 and completed the writing. MAAR purified recombinant proteins. PMB analysed RNA 19 seq. MMO supervised experiments and analysed results. IAA conceived original 20 project, supervised experiments, and finalised the article. 31 32 Short title (50 characters): SUMOylation of rice SLR1 increases salt tolerance 33 34 ABSTRACT 35 DELLA proteins modulate GA signalling and are major regulators of plant plasticity to 36 endure stress. DELLAs are mostly regulated at the post-translational level, and their 37 activity relies on the interaction with upstream regulators and transcription factors 38 (TFs). SUMOylation is a post-translational modification (PTM) capable of changing 39protein interaction and found to influence DELLA activity in Arabidopsis. We 40 determined that SUMOylation of the single rice DELLA SLENDER RICE1 (SLR1) 41 occurs in a lysine residue different from the one identified in Arabidopsis 42 REPRESSOR OF GA (RGA), which suggests differential DELLA regulation by 43SUMOylation in monocots and dicots. Remarkably, artificially increasing 44 SUMOylated SLR1 (SUMO1SLR1) levels attenuated the penalty of salt stress on 45 plant yield. Gene expression analysis revealed that the overexpression of 46 SUMOylated SLR1 regulates key dioxygenases that modulate active GA levels, 47namely GA20ox2 and GA2ox3, which could partially explain the sustained 48 productivity upon salt stress imposition. Besides, SLR1 SUMOylation blocked the 49 interaction with the growth regulator YAB4, which may fine-tune GA20ox2 50 expression. Mechanistically, we propose that SLR1 SUMOylation disrupts the 51 interaction with members of several transcription factor families to modulate gene 52 expression. We found that SLR1 SUMOylation represents a novel mechanism 53 modulating DELLA activity, which attenuates the impact of stress on plant 54 performance. 55 56 gibberellin 58 59 One sentence summary: Rice plants show increased yield under salt stress when 60 its gibberellin transcriptional regulator DELLA protein is artificially SUMOylated.

Recurrent Selection with Low Herbicide Rates and Salt Stress Decrease Sensitivity of Echinochloa colona to Imidazolinone

“…Different herbicides and stresses, such as salinity, affect morphological, biochemical, physiological, and molecular attributes in crops and weeds [10,[46][47][48][49][50]. Different responses at different biological levels have been studied in cultivated rice under salt stress [51][52][53]. However, there is little information about weed behavior under these conditions, and the weed response to a combination of herbicide and salinity stresses, which could be imprinted into the genome of succeeding generations.…”

Understanding and Exploiting Post-Translational Modifications for Plant Disease Resistance

“…However, DELLA stabilisation causes high DELLA levels and reduced fertility [264]. Rice DELLA SLR1 also undergoes SUMOylation, which alters its interaction with specific transcription factors to improve abiotic stress tolerance [265]. There is a suggestion that SLR1 SUMOylation may attenuate the penalty of salt stress tolerance on plant yield [265], with the goal of maintaining yield and disease resistance under pathogen stress in rice, which would be interesting to explore.…”

“…Rice DELLA SLR1 also undergoes SUMOylation, which alters its interaction with specific transcription factors to improve abiotic stress tolerance [265]. There is a suggestion that SLR1 SUMOylation may attenuate the penalty of salt stress tolerance on plant yield [265], with the goal of maintaining yield and disease resistance under pathogen stress in rice, which would be interesting to explore. In addition, mutation of the SIM site in GID1 in rice or Arabidopsis could be manipulated to fine-tune DELLA degradation [263].…”

Regulation of DELLA Proteins by Post-translational Modifications

“…A recent study revealed that the rice SLR1 was SUMOylated at K2 but not at K60 (the position equivalent to K65 in RGA), suggesting that DELLA SUMOylation operates differently in monocots and eudicots. In turn, SLR1 can be deSUMOyated by the FUG1 SUMO protease ( Gonçalves et al. 2020 ).…”

“…2A ). Rice plants overexpressing SUMO–SLR1 displayed improved tolerance to salt stress and altered expression of genes involved in the defense response and in GA metabolism ( Gonçalves et al. 2020 ).…”