CaSWC4 regulates the immunity-thermotolerance tradeoff by recruiting CabZIP63/CaWRKY40 to target genes and activating chromatin in pepper

Abstract

Pepper (Capsicum annuum) responds differently to high temperature stress (HTS) and Ralstonia solanacearum infection (RSI) but employs some shared transcription factors (TFs), such as CabZIP63 and CaWRKY40, in both cases. How the plant activates and balances these distinct responses, however, was unclear. Here, we show that the protein CaSWC4 interacts with CaRUVBL2 and CaTAF14b and they all act positively in pepper response to RSI and thermotolerance. CaSWC4 activates chromatin of immunity or thermotolerance related target genes of CaWRKY40 or CabZIP63 by promoting deposition of H2A.Z, H3K9ac and H4K5ac, simultaneously recruits CabZIP63 and CaWRKY40 through physical interaction and brings them to their targets (immunity- or thermotolerance-related genes) via binding AT-rich DNA element. The above process relies on the recruitment of CaRUVBL2 and TAF14 by CaSWC4 via physical interaction, which occurs at loci of immunity related target genes only when the plants are challenged with RSI, and at loci of thermotolerance related target genes only upon HTS. Collectively, our data suggest that CaSWC4 regulates rapid, accurate responses to both RSI and HTS by modulating chromatin of specific target genes opening and recruiting the TFs, CaRUVBL2 and CaTAF14b to the specific target genes, thereby helping achieve the balance between immunity and thermotolerance.

The cAMP-dependent phosphorylation footprint in response to heat stress

“…In A. thaliana, SWC4 is associated with the SWR1 and the NuA4 acetyltransferase complexes which both have a role in the epigenetic regulation (Espinosa-Cores et al 2020 ; Willhoft and Wigley 2020 ). Recently, it has been demonstrated in pepper that SWC4 affects the responses to both pathogen infection and HS and does so by modulating chromatin of specific target genes (Cai et al 2022 ). We therefore propose that cAMP-dependent phosphorylation of SWC4 may contribute to altered responses of the cAMP-depleted cells, both in response to HS and pathogens (Paradiso et al 2020 ; Sabetta et al 2019 ).…”

A 14-3-3 Protein Ca16R Acts Positively in Pepper Immunity against Ralstonia solanacearum by Interacting with CaASR1

“…Bacterial wilt caused by Ralstonia solanacearum is one of the most important soil-borne diseases in the production of pepper and other solanaceous crops, especially in tropical or subtropical regions, causing heavy loss in the productivity of these crops [25,26]. According to our previous studies, transcription factors including CaWRKY27b [27], CaWRKY28 [28], CaWRKY40 [29], CabZIP23 [30], CabZIP63 [30], CaNAC2c [31], and CaNAC029 [31], as well as other proteins such as CaCDPK29 [27] and chromatin remodeling-related CaSWC4 [32], are involved and constitute regulatory networks in pepper immunity against R. solanacearum and also participate in pepper thermotolerance. CaWRKY40 and CabZIP23 act crucially in this network, with CaWRKY40 being directly regulated by CabZIP23, to activate pepper immunity and thermotolerance that are distinct in their nature.…”

The OsSGS3-tasiRNA-OsARF3 module orchestrates abiotic-biotic stress response trade-off in rice

“…In pepper ( Capsicum annuum ), the NAC-type transcription factor NAC DOMAIN CONTAINING PROTEIN 2c (CaNAC2c) coordinately regulates immunity and thermotolerance through its differential subcellular localization and interacting proteins 14 . A chromatin remodeling modulator CaSWC4 modulates the immunity-thermotolerance trade-off by recruiting transcription factors CabZIP63 and CaWRKY40 15 . AVRPPHB SUSCEPTIBLE 3 (PBS3), an acyl-adenylate/thioester-forming enzyme, balances plant immunity, salt stress responses and phyllosphere bacterial communities to maintain plant fitness through abscisic acid (ABA)-SA crosstalk under combined biotic and abiotic stresses 16 .…”