The RING-finger ubiquitin E3 ligase TaPIR1 targets TaHRP1 for degradation to suppress chloroplast function

• Published in: Nature communications Vol. 15; no. 1; pp. 6905 - 17
• Main Authors: Zhang, Rongrong, Wu, Yu, Qu, Xiangru, Yang, Wenjuan, Wu, Qin, Huang, Lin, Jiang, Qiantao, Ma, Jian, Zhang, Yazhou, Qi, Pengfei, Chen, Guoyue, Jiang, Yunfeng, Zheng, Youliang, Wang, Xiaojie, Wei, Yuming, Xu, Qiang
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 12.08.2024; Nature Publishing Group; Nature Portfolio
• Subjects: 631/326/193; 631/449/1734; 631/449/2169; 82/80; 82/83; Accumulation; Arabidopsis - genetics; Arabidopsis - immunology; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Binding sites; Biodegradation; Chloroplasts; Chloroplasts - metabolism; Degradation; Disease resistance; Disease Resistance - genetics; Gene expression; Gene Expression Regulation, Plant; Histidine; Humanities and Social Sciences; Lysine; Microorganisms; multidisciplinary; Nicotiana - genetics; Nicotiana - metabolism; Photosynthesis; Plant Diseases - genetics; Plant Diseases - immunology; Plant Diseases - microbiology; Plant immunity; Plant Immunity - genetics; Plants, Genetically Modified; Promoter Regions, Genetic - genetics; Proteolysis; Reactive Oxygen Species - metabolism; Regulatory mechanisms (biology); Resistance factors; Science; Science (multidisciplinary); Stripe rust; Transcription factors; Transcription Factors - genetics; Transcription Factors - metabolism; Ubiquitin-protein ligase; Ubiquitin-Protein Ligases - genetics; Ubiquitin-Protein Ligases - metabolism; Ubiquitination; Wheat
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-51249-1

Chloroplasts are key players in photosynthesis and immunity against microbial pathogens. However, the precise and timely regulatory mechanisms governing the control of photosynthesis-associated nuclear genes (PhANGs) expression in plant immunity remain largely unknown. Here we report that TaPIR1, a Pst -induced RING-finger E3 ubiquitin ligase, negatively regulates Pst resistance by specifically interacting with TaHRP1, an atypical transcription factor histidine-rich protein. TaPIR1 ubiquitinates the lysine residues K 131 and K 136 in TaHRP1 to regulate its stability. TaHRP1 directly binds to the TaHRP1-binding site elements within the PhANGs promoter to activate their transcription via the histidine-rich domain of TaHRP1. PhANGs expression induces the production of chloroplast-derived ROS. Although knocking out TaHRP1 reduces Pst resistance, TaHRP1 overexpression contributes to photosynthesis, and chloroplast-derived ROS production, and improves disease resistance. TaPIR1 expression inhibits the downstream activation of TaHRP1 and TaHRP1-induced ROS accumulation in chloroplasts. Overall, we show that the TaPIR1-mediated ubiquitination and degradation of TaHRP1 alters PhANGs expression to disrupt chloroplast function, thereby increasing plant susceptibility to Pst . Wheat E3 ubiquitin ligase TaPIR1-mediated ubiquitination and degradation of an atypical transcription factor TaHRP1 alters PhANGs expression to disrupt chloroplast function and ROS accumulation, increasing plant susceptibility to wheat stripe rust.