Arabidopsis RING‐type E3 ubiquitin ligase XBAT35.2 promotes proteasome‐dependent degradation of ACD11 to attenuate abiotic stress tolerance

Abstract

Plants employ multiple mechanisms to cope with a constantly changing and challenging environment, including using the ubiquitin proteasome system (UPS) to alter their proteome to assist in initiating, modulating and terminating responses to stress. We previously reported that the ubiquitin ligase XBAT35.2 mediates the proteasome-dependent degradation of Accelerated Cell Death 11 (ACD11) to promote pathogen defense. Here, we demonstrate roles for XBAT35.2 and ACD11 in abiotic stress tolerance. As seen in response to pathogen infection, abiotic stress stabilizes XBAT35.2 and the abundance of ACD11 rose consistently with increasing concentrations of abscisic acid (ABA) and salt. Surprisingly, exposure to ABA and salt increased the stability of ACD11, and the overexpression of ACD11 improves plant survival of salt and drought stress, suggesting a role for ACD11 in promoting tolerance. Prolonged exposure to high concentrations of ABA or salt resulted in ubiquitination and the proteasome-dependent degradation of ACD11, however. The stress-induced turnover of ACD11 requires XBAT35.2, as degradation is slowed in the absence of the E3 ubiquitin ligase. Consistent with XBAT35.2 mediating the proteasome-dependent degradation of ACD11, the loss of E3 ubiquitin ligase function enhances the tolerance of salt and drought stress, whereas overexpression increases sensitivity. A model is presented where, upon the perception of abiotic stress, ACD11 abundance increases to promote tolerance. Meanwhile, XBAT35.2 accumulates and in turn promotes the degradation of ACD11 to attenuate the stress response. The results characterize XBAT35.2 as an E3 ubiquitin ligase with opposing roles in abiotic and biotic stress. Keywords: abiotic stress tolerance, abscisic acid (ABA), ubiquitin proteasome system (UPS), RING-type E3 ubiquitin ligase, XBAT35 (for XB3 ortholog 5 in Arabidopsis thaliana), regulated protein degradation.

The E3 ligase XBAT35 mediates thermoresponsive hypocotyl growth by targeting ELF3 for degradation in Arabidopsis

“…XBAT35 is involved in plant thermomorphogenesis XBAT35 belongs to a small E3 ubiquitin ligase gene family that is involved in abiotic stress responses, apical hook curvature and lateral root development in Arabidopsis (Nodzon et al, 2004;Carvalho et al, 2012;Liu et al, 2017;Li et al, 2020;Yu et al, 2020). We obtained several gene-edited loss-of-function mutant alleles of XBAT35 (Figure S1), and checked their thermoresponsive hypocotyl phenotypes.…”

The deubiquitinases UBP12 and UBP13 integrate with the E3 ubiquitin ligase XBAT35.2 to modulate VPS23A stability in ABA signaling

“…5), likely promoting the deubiquitination and stabilization of VPS23A, which seems to contradict with the promoted degradation of VPS23A under ABA stimulation. Considering that VPS23A stability is modulated by the E3 ligase XBAT35.2, a previous study reported that ABA treatment also stabilizes XBAT35.2 (52). Hence, we surmised whether the increased amount of UBP12 and UBP13 could also deubiquitinate and thus stabilize XBAT35.2 to reduce the amount of VPS23A in response to ABA.…”

Alternative splicing regulation appears to play a crucial role in grape berry development and is also potentially involved in adaptation responses to the environment

“…The skipping of the exon-8 has been characterized in Arabidopsis and shown to produce a nuclear localization signal (NLS)-lacking variant, XBAT35.2, consistently localized in the cytoplasm, in contrast with the nuclear localization of the full-length transcript XBAT35.1 [ 44 ]. The E3 ligase isoform XBAT35.2, functioning in the ubiquitin-proteasome system by targeting specific substrates, has been shown to regulate the morphogenesis of Arabidopsis plantlets [ 44 ] and is thought to play dual roles in biotic and abiotic stress responses [ 45 , 46 ]. Interestingly, when Arabidopsis young plants were treated with the phytohormone ABA, the transcription and translation of XBAT35.2 were induced, negatively controlling the tolerance to abiotic stress [ 46 ].…”

“…The E3 ligase isoform XBAT35.2, functioning in the ubiquitin-proteasome system by targeting specific substrates, has been shown to regulate the morphogenesis of Arabidopsis plantlets [ 44 ] and is thought to play dual roles in biotic and abiotic stress responses [ 45 , 46 ]. Interestingly, when Arabidopsis young plants were treated with the phytohormone ABA, the transcription and translation of XBAT35.2 were induced, negatively controlling the tolerance to abiotic stress [ 46 ]. Given the fact that ripening of the grape berry, a non-climacteric fruit, is highly dependent on ABA, the increasing predominance of XBAT35.2 from pré-véraison to mid-ripening could have a particular significance in this context.…”