Precursor processing by SBT3.8 and phytosulfokine signaling contribute to drought stress tolerance in Arabidopsis

Abstract

Increasing drought stress poses a severe threat to agricultural productivity. Plants, however, evolved numerous mechanisms to cope with such environmental stress. Here we report that the stress-induced production of a peptide signal contributes to stress tolerance. The expression of phytosulfokine (PSK) peptide precursor genes, and transcripts of three subtilisin-like serine proteases, SBT1.4, SBT3.7 and SBT3.8 were found to be up-regulated in response to osmotic stress. Stress symptoms were enhanced in sbt3.8 loss-of-function mutants and could be alleviated by PSK treatment. Osmotic stress tolerance was improved in plants overexpression the precursor of PSK1 (proPSK1) or SBT3.8 resulting in higher fresh weight and improved lateral root development in the transgenic compared to wild-type plants. We further showed that SBT3.8 is involved in the biogenesis of the bioactive PSK peptide. ProPSK1 was cleaved by SBT3.8 at the C-terminus of the PSK pentapeptide. Processing by SBT3.8 depended on the aspartic acid residue adjacent to the cleavage site. ProPSK1 processing was impaired in the sbt3.8 mutant. The data suggest that increased expression in response to osmotic stress followed by the post-translational processing of proPSK1 by SBT3.8 leads to the production of PSK as a peptide signal for stress mitigation.

The PSY Peptide Family—Expression, Modification and Physiological Implications

“…Out of these 56 SBTs, a single one encodes a phytaspase, possessing extreme aspartate specificity [ 55 ]. This aspartate-dependent protease, SBT3.8, has recently been shown to be involved in the biogenesis of both PSK and RGF peptide, yielding the active peptides, cleaved at their N-terminal site [ 26 , 56 ]. Tyrosine-sulfated and non-sulfated RGF6s were cleaved by SBT3.8 at similar rates, indicating that sulfation of the tyrosine upstream of the aspartate motif does not affect processing activity [ 26 ].…”

TPST-dependent and -independent regulation of root development and signaling by PSK LRR receptor kinases in Arabidopsis

“…The hps7 mutant displayed a similar root hair phenotype as tpst-1 that was exaggerated by phosphate starvation with root hair formation extending toward the tip close to the meristem revealing a link between TPST-dependent signaling in nutrient stress adaptation. Support for a broader contribution of sulfated peptide signaling in abiotic stress responses comes from recent reports on the role for PSK in mediating osmotic stress tolerance (Stührwohldt et al , 2021).…”

“…An unusual precursor protein is PSK1 that is flanked by Asp at both sites of the mature peptide. We could recently show that the C-terminal Asp is cleaved by Arabidopsis SBT3.8 to release the active C-terminus (Stührwohldt et al , 2021).…”

“…Zhang et al (2018) showed that PSK signals the Auxin-dependent immune responses in tomato after infection with the necrotrophic fungus Botrytis cinerea . Recent studies also revealed a role of PSK signaling in osmotic and drought stress adaptation (Schönhof et al , 2020; Stührwohldt et al , 2021).…”

Plant proteases: from molecular mechanisms to functions in development and immunity

“…In order to survive and reproduce, plants, in addition to biotic invaders, also have to endure and overcome abiotic stress conditions. Stührwohldt et al (2021) explore the role of a serine protease subtilase SBT3.8 for production of a peptide hormone, which contributes to stress tolerance. They show that during stress, the precursor of the phytosulfokine peptide hormone is processed by SBT3.8 to enhance drought resistance in Arabidopsis.…”