A lncRNA fine-tunes salicylic acid biosynthesis to balance plant immunity and growth

Ningkun Liu; Yanzhuo Xu; Qi Li; Yuxin Cao; Dechang Yang; Shasha Liu; Xiaokang Wang; Yingjie Mi; Yang Liu; Chenxi Ding; Yan Liu; Yong Li; Yao-Wu Yuan; Ge Gao; Jinfeng Chen; Weiqiang Qian; Xiaoming Zhang

doi:10.1016/j.chom.2022.07.001

A lncRNA fine-tunes salicylic acid biosynthesis to balance plant immunity and growth

Cell Host Microbe. 2022 Aug 10;30(8):1124-1138.e8. doi: 10.1016/j.chom.2022.07.001. Epub 2022 Jul 30.

Authors

Ningkun Liu¹, Yanzhuo Xu¹, Qi Li², Yuxin Cao³, Dechang Yang⁴, Shasha Liu¹, Xiaokang Wang³, Yingjie Mi⁵, Yang Liu¹, Chenxi Ding⁶, Yan Liu¹, Yong Li⁷, Yao-Wu Yuan⁸, Ge Gao⁴, Jinfeng Chen⁹, Weiqiang Qian¹⁰, Xiaoming Zhang¹¹

Affiliations

¹ State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, China.
² State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.
³ State Key Laboratory of Protein and Plant Gene Research, School of Advanced Agricultural Sciences, Peking University, Beijing 100871, China.
⁴ State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences, BIOPIC & ICG, and Center for Bioinformatics, Peking University, Beijing 100871, China.
⁵ State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; Department of Life Sciences, Henan Normal University, Xinxiang, Henan 453007, China.
⁶ State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; College of Life Sciences, Hebei University, Baoding, Hebei 071002, China.
⁷ College of Life Sciences, Northeast Agricultural University, Harbin, Heilongjiang 150038, China.
⁸ Department of Ecology and Evolutionary Biology, University of Connecticut, 75 North Eagleville Road, Unit 3043, Storrs, CT 06269, USA.
⁹ State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China. Electronic address: chenjinfeng@ioz.ac.cn.
¹⁰ State Key Laboratory of Protein and Plant Gene Research, School of Advanced Agricultural Sciences, Peking University, Beijing 100871, China. Electronic address: wqqian@pku.edu.cn.
¹¹ State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China; CAS Center for Excellence in Biotic Interactions, University of Chinese Academy of Sciences, Beijing 100049, China. Electronic address: zhangxm@ioz.ac.cn.

PMID: 35908550
DOI: 10.1016/j.chom.2022.07.001

Abstract

Constitutive activation of plant immunity is detrimental to plant growth and development. Here, we uncover the role of a long non-coding RNA (lncRNA) in fine-tuning the balance of plant immunity and growth. We find that a lncRNA termed salicylic acid biogenesis controller 1 (SABC1) suppresses immunity and promotes growth in healthy plants. SABC1 recruits the polycomb repressive complex 2 to its neighboring gene NAC3, which encodes a NAC transcription factor, to decrease NAC3 transcription via H3K27me3. NAC3 activates the transcription of isochorismate synthase 1 (ICS1), a key enzyme catalyzing salicylic acid (SA) biosynthesis. SABC1 thus represses SA production and plant immunity via decreasing NAC3 and ICS1 transcriptions. Upon pathogen infection, SABC1 is downregulated to derepress plant resistance to bacteria and viruses. Together, our findings reveal lncRNA SABC1 as a molecular switch in balancing plant defense and growth by modulating SA biosynthesis.

Keywords: H3K27me3; ICS1; NAC3; SABC1; bacteria; chromatin loop; lncRNA; plant immunity and growth balance; salicylic acid; viruses.

MeSH terms

Arabidopsis Proteins* / genetics
Arabidopsis Proteins* / metabolism
Arabidopsis* / microbiology
Gene Expression Regulation, Plant
Plant Diseases
Plant Immunity / physiology
Plants / genetics
RNA, Long Noncoding* / genetics
Salicylic Acid

Substances

Arabidopsis Proteins
RNA, Long Noncoding
Salicylic Acid