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

Weiwei Cai; Sheng Yang; Ruijie Wu; Yutong Zheng; Shicong He; Lei Shen; Deyi Guan; Shuilin He

doi:10.1371/journal.pgen.1010023

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

PLoS Genet. 2022 Feb 28;18(2):e1010023. doi: 10.1371/journal.pgen.1010023. eCollection 2022 Feb.

Authors

Weiwei Cai^{1

2

3

4}, Sheng Yang^{1

2

3}, Ruijie Wu^{1

2

3}, Yutong Zheng^{1

2

3}, Shicong He^{1

2

3}, Lei Shen^{1

2

3}, Deyi Guan^{1

2

3}, Shuilin He^{1

2

3}

Affiliations

¹ Key Laboratory of Applied Genetics of universities in Fujian Province, Fujian Agriculture and Forestry University, Fuzhou, Fujian, PR China.
² National Education Ministry Key Laboratory of Plant Genetic Improvement and Comprehensive Utilization, Fujian Agriculture and Forestry University, Fuzhou, Fujian, PR China.
³ Agricultural College, Fujian Agriculture and Forestry University, Fuzhou, Fujian, PR China.
⁴ College of of Horticultural Sciences, Zhejiang Agriculture and Forestry University, Hangzhou, Zhejiang, PR China.

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.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Capsicum* / genetics
Chromatin / genetics
Chromatin / metabolism
Disease Resistance / genetics
Gene Expression Regulation, Plant
Gene Silencing
Plant Diseases / genetics
Plant Growth Regulators / metabolism
Plant Immunity / genetics
Plant Proteins / genetics
Plant Proteins / metabolism
Ralstonia solanacearum* / genetics
Ralstonia solanacearum* / metabolism
Thermotolerance*

Substances

Chromatin
Plant Growth Regulators
Plant Proteins

Grants and funding

This work was supported by the National Natural Science Foundation of China (No.31401890, No.31401312) to SLH. This work was supported by the Scientific Research Foundation of the Graduate School of Fujian Agriculture and Forestry University (324-1122yb068) to WWC. This work was supported by the Development Fund Project of Fujian Agriculture and Forestry University (CXZX2016158, CXZX2017548) to SLH. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.