Clathrin Light Chains negatively regulate plant immunity by hijacking the autophagy pathway

Hu-Jiao Lan; Jie Ran; Wen-Xu Wang; Lei Zhang; Ni-Ni Wu; Ya-Ting Zhao; Min-Jun Huang; Min Ni; Feng Liu; Ninghui Cheng; Paul A Nakata; Jianwei Pan; Steven A Whitham; Barbara J Baker; Jian-Zhong Liu

doi:10.1016/j.xplc.2024.100937

Clathrin Light Chains negatively regulate plant immunity by hijacking the autophagy pathway

Plant Commun. 2024 Apr 30:100937. doi: 10.1016/j.xplc.2024.100937. Online ahead of print.

Authors

Hu-Jiao Lan¹, Jie Ran¹, Wen-Xu Wang¹, Lei Zhang¹, Ni-Ni Wu¹, Ya-Ting Zhao¹, Min-Jun Huang¹, Min Ni¹, Feng Liu², Ninghui Cheng³, Paul A Nakata³, Jianwei Pan⁴, Steven A Whitham⁵, Barbara J Baker⁶, Jian-Zhong Liu⁷

Affiliations

¹ Zhejiang Provincial Key Laboratory of Biotechnology on Specialty Economic Plants, Zhejiang Normal University, Jinhua 321004, China.
² Lushan Botanical Garden, Chinese Academy of Sciences, Jiujiang 332000, China.
³ U.S. Department of Agriculture-Agricultural Research Service, Children's Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, Houston, Texas 77030.
⁴ College of Life Sciences, Lanzhou University, Lanzhou 730000, China.
⁵ Department of Plant Pathology and Microbiology, Iowa State University, Ames, Iowa 50011.
⁶ Department of Plant and Microbial Biology, University of California, and Plant Gene Expression Center, U.S. Department of Agriculture-Agricultural Research Service, Berkeley, Berkeley, CA 94720, USA.
⁷ Zhejiang Provincial Key Laboratory of Biotechnology on Specialty Economic Plants, Zhejiang Normal University, Jinhua 321004, China; Institute of Plant Genetics and Developmental Biology, College of Chemistry and Life Sciences, Zhejiang Normal University, Jinhua 321004, China. Electronic address: jzliu@zjnu.cn.

PMID: 38693694
DOI: 10.1016/j.xplc.2024.100937

Abstract

The crosstalk between clathrin-mediated endocytosis (CME) and autophagy pathway has been reported in mammals. However, the interconnection of CME with autophagy has not been established in plants. In this report, we showed that Arabidopsis CLATHRIN LIGHT CHAIN (CLC) subunit 2 and 3 double mutant, clc2-1 clc3-1, phenocopied the Arabidopsis AUTOPHAGY-RELATED GENE (ATG) mutants both in auto-immunity and nutrient sensitivity. Accordingly, the autophagy pathway was significantly compromised in the clc2-1 clc3-1 mutant. Interestingly, we demonstrated with multiple assays that CLC2 directly interacted with ATG8h/ATG8i in a domain-specific manner. As expected, both GFP-ATG8h/GFP-ATG8i and CLC2-GFP were subjected to autophagic degradation and the degradation of GFP-ATG8h was significantly reduced in the clc2-1 clc3-1 mutant. Notably, simultaneously knocking out ATG8h and ATG8i by the CRISPR/CAS9 resulted in an enhanced resistance against Golovinomyces cichoracearum, supporting the functional relevance of the CLC2-ATG8h/8i interactions. In conclusion, our results uncovered a link between the function of CLCs and the autophagy pathway in Arabidopsis.

Keywords: autophagy; cell death; clathrin light chain; clathrin-mediated endocytosis; immunity; senescence.