Pepper SUMO E3 ligase CaDSIZ1 enhances drought tolerance by stabilizing the transcription factor CaDRHB1

Abstract

Summary Small ubiquitin‐like modifier (SUMO) conjugation (SUMOylation) is a reversible post‐translational modification associated with protein stability and activity, and modulates hormone signaling and stress responses in plants. Previously, we reported that the pepper dehydration‐responsive homeobox domain transcription factor CaDRHB1 acts as a positive modulator of drought response. Here, we show that CaDRHB1 protein stability is enhanced by SUMO E3 ligase Capsicum annuum DRHB1‐interacting SAP and Miz domain (SIZ1) (CaDSIZ1)‐mediated SUMOylation in response to drought, thereby positively modulating abscisic acid (ABA) signaling and drought responses. Substituting lysine (K) 138 of CaDRHB1 with arginine reduced CaDSIZ1‐mediated SUMOylation, indicating that K138 is the principal site for SUMO conjugation. Virus‐induced silencing of CaDSIZ1 promoted CaDRHB1 degradation, suggesting that CaDSIZ1 is involved in drought‐induced SUMOylation of CaDRHB1. CaDSIZ1 interacted with and facilitated SUMO conjugation of CaDRHB1. CaDRHB1, mainly localized in the nucleus, but also in the cytoplasm in the SUMOylation mimic state, suggesting that SUMOylation of CaDRHB1 promotes its nuclear export, leading to cytoplasmic accumulation. Moreover, CaDSIZ1‐silenced pepper plants were less sensitive to ABA and considerably sensitive to drought stress, whereas CaDSIZ1‐overexpressing plants displayed ABA‐hypersensitive and drought‐tolerant phenotypes. Collectively, our data indicate that CaDSIZ1‐mediated SUMOylation of CaDRHB1 functions in ABA‐mediated drought tolerance.

Pepper U‐Box E3 ubiquitin ligase 24, CaPUB24, negatively regulates drought stress response

“…Based on the potential association of CaPUB24 with various abiotic stresses, particularly drought stress (Figure 1C), we sought to elucidate the biological function of CaPUB24 in response to drought stress. For this investigation, we adopted the TRV‐based VIGS system (Burch‐Smith et al, 2004, Senthil‐Kumar and Mysore, 2014), which has been previously reported as an efficient strategy for gene silencing in pepper plants (Baek et al, 2021, Jeong et al, 2021, Joo et al, 2022, Bae et al, 2023, Jeong et al, 2023). We selected a suitable VIGS site using the SGN web tool (Fernandez‐Pozo et al, 2015) and generated CaPUB24 ‐silenced pepper plants using the TRV2: CaPUB24 construct.…”

Roles of the pepper JAZ protein CaJAZ1‐03 and its interacting partner RING‐type E3 ligase CaASRF1 in regulating ABA signaling and drought responses

“…In this study, we identified the pepper JAZ gene transpirational water loss (Schroeder et al, 2001). Several studies have suggested that stomatal opening and closure critically influence drought sensitivity and tolerance (Joo et al, 2022;Xu et al, 2021).…”

“…Under drought stress conditions, plants rapidly synthesize ABA in various organs, which subsequently enhances stomatal closure, inhibiting transpirational water loss (Schroeder et al, 2001). Several studies have suggested that stomatal opening and closure critically influence drought sensitivity and tolerance (Joo et al, 2022; Xu et al, 2021).…”

Crop Resistance Mechanisms to Alleviate Climate Change-Related Stress

“…The differently ubiquitinated proteins under high temperatures are enriched in a wide range of molecular functions Pengyan et al, 2020). Sumoylation can be stimulated in plants under heat (Miller et al, 2010;Miller et al, 2013;Hendriks and Vertegaal, 2016;Rytz et al, 2018;Han et al, 2021) or drought stress (Catala et al, 2007;Miura et al, 2009;Castro et al, 2012;Wu et al, 2016;Joo et al, 2022) and largely depends on SUMO E3 ligase SAP AND MIZ1 DOMAIN-CONTAINING LIGASE 1 (SIZ1). SIZ1 facilitates conjugation of SUMO to protein substrates, and positively regulates plant heat tolerance and acquired thermotolerance (Yoo et al, 2006;Kim et al, 2017;Rytz et al, 2018).…”