Clathrin light chains negatively regulate plant immunity by hijacking the autophagy pathway

Authors: LAN, HU-JIAO - Zhejiang Normal University; RAN, JIE - Zhejiang Normal University; WANG, WEN-XU - Zhejiang Normal University; ZHANG, LEI - Zhejiang Normal University; WU, NI-NI - Zhejiang Normal University; ZHAO, YA-TING - Zhejiang Normal University; HUANG, MIN-JUN - Zhejiang Normal University; NI, MIN - Zhejiang Normal University; LIU, FENG - Chinese Academy Of Sciences; CHENG, NINGHUI - Children'S Nutrition Research Center (CNRC); Nakata, Paul; PAN, JIANWEI - Lanzhou University; WHITHAM, STEVEN - Iowa State University; BAKER, BARBARA - University Of California Berkeley; LIU, JIAN-ZHONG - Zhejiang Normal University

Submitted to: Plant Communications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/28/2024
Publication Date: 4/30/2024
Citation: Lan, H., Ran, J., Wang, W., Zhang, L., Wu, N., Zhao, Y., Huang, M., Ni, M., Liu, F., Cheng, N., Nakata, P.A., Pan, J., Whitham, S.A., Baker, B.J., Liu, J. 2024. Clathrin light chains negatively regulate plant immunity by hijacking the autophagy pathway. Plant Communications. 5(8). Article 100937. https://doi.org/10.1016/j.xplc.2024.100937.
DOI: https://doi.org/10.1016/j.xplc.2024.100937

Interpretive Summary: Plant pathogens often infect crop plants resulting in reduced yields, quality, and profitability. Thus, scientists have been avidly searching for ways to increase the plant's immunity to these pathogens. In this study we investigate the role of the genes encoding Clathrin in plant immunity. Gene silencing studies revealed that a reduction in two genes that encode components of Clathrin resulted in an activation of plant defenses against certain bacterial and fungal pathogens. This finding suggests that Clathrin plays a negative role in plant immunity. Genetic and biochemical studies also revealed that the loss of Clathrin impaired the process by which the cell recycles some of its cellular components for reuse. Thus, there appears to be a link between the loss of this recycling process and the increase in plant immunity against certain bacterial and fungal pathogens. It is our hope that by studying this complex process of plant immunity we will gain a level of understanding that will allow us to eventually design strategies to combat plant pathogens and improve the yields, quality, and profitability of crop plants.

Technical Abstract: The crosstalk between clathrin-mediated endocytosis (CME) and the autophagy pathway has been reported in mammals; however, the interconnection of CME with autophagy has not been established in plants. Here, we report that the Arabidopsis CLATHRIN LIGHT CHAIN (CLC) subunit 2 and 3 double mutant, clc2-1 clc3-1, phenocopies Arabidopsis AUTOPHAGY-RELATED GENE (ATG)mutants in both autoimmunity and nutrient sensitivity. Accordingly, the autophagy pathway is significantly compromised in the clc2-1 clc3-1 mutant. Interestingly, multiple assays demonstrate that CLC2 directly interacts with ATG8h/ATG8i in a domain-specific manner. As expected, both GFP-ATG8h/GFP-ATG8i and CLC2-GFP are subjected to autophagic degradation, and degradation of GFP-ATG8h is significantly reduced in the clc2-1 clc3-1 mutant. Notably, simultaneous knockout of ATG8h and ATG8i by CRISPR-Cas9 results in enhanced resistance against Golovinomyces cichoracearum, supporting the functional relevance of the CLC2–ATG8h/8i interactions. In conclusion, our results reveal a link between the function of CLCs and the autophagy pathway in Arabidopsis.