Alternative splicing of a potato disease resistance gene maintains homeostasis between growth and immunity

Authors: SUN, BIYING - Nanjing Agricultural University; HUANG, JIE - Nanjing Agricultural University; KONG, LIANG - Nanjing Agricultural University; GAO, CHUYUN - Nanjing Agricultural University; ZHAO, FEI - Nanjing Agricultural University; SHEN, JIAYONG - Nanjing Agricultural University; WANG, TIAN - Nanjing Agricultural University; LI, KANGPING - Nanjing Agricultural University; WANG, LUYAO - Nanjing Agricultural University; WANG, YUANCHAO - Nanjing Agricultural University; Halterman, Dennis; DONG, SUOMENG - Nanjing Agricultural University

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/18/2024
Publication Date: 6/28/2024
Citation: Sun, B., Huang, J., Kong, L., Gao, C., Zhao, F., Shen, J., Wang, T., Li, K., Wang, L., Wang, Y., Halterman, D.A., Dong, S. 2024. Alternative splicing of a potato disease resistance gene maintains homeostasis between growth and immunity. The Plant Cell. 36(9):3729-3750. https://doi.org/10.1093/plcell/koae189.
DOI: https://doi.org/10.1093/plcell/koae189

Interpretive Summary: Microorganisms that cause plant diseases present a substantial burden to agriculture through yield losses due to plant stress, costs associated with disease control, and efforts to detect infections and limit disease epidemics. Plant breeders are interested in the identification and incorporation of simply inherited genes that confer robust resistance to diseases. These resistance (R) genes typically encode proteins that recognize the presence of very specific pathogen molecules, termed effectors, resulting in the activation of defense responses. Introduction of R genes into plants can confer a high level of disease resistance, but improper expression of R genes can cause plant stress leading to yield losses. Our work has determined the molecular mechanisms involved in expression of the R gene RB, which confers resistance to potato late blight. Under normal plant growth, expression RB is reduced to avoid plant stress. However, RB expression changes during pathogen infection to allow the plant to become resistant. Our understanding of the molecular mechanisms involved in proper RB gene expression will allow us to improve the deployment of RB into cultivated potato to avoid plant stress associated yield losses, which will impact the potato industry. Our work will also impact the deployment of other R genes in order to ensure proper expression to confer resistance and balance this with risks associated with potential yield losses.

Technical Abstract: Plants possess an innate immune system against pathogens. The intracellularly localized receptors called nucleotide-binding, leucine-rich repeat receptors (NLRs) recognize pathogen-derived effector proteins to trigger the immune response. The expression level of NLRs is precisely modulated in multifaceted ways. Alternative splicing (AS) plays a vital role in NLR expression modulation. However, modulation of NLR AS by the pathogen is not well documented. Here we report that the potato (Solanum tuberosum) NLR gene RB undergoes alternative splicing of its intron, resulting in two transcripts. During normal growth RB mainly exists as intron-retained transcript RB_IR, which results in translation of a truncated R protein. During infection, P. infestans induces AS of RB to promote intron splicing, increasing the abundance of RB_CDS, which encodes a full-length, active R protein. Additionally, we demonstrate that effector IPI-O1 directly interacts with splicing factor CWC15, causing CWC15 re-localization from the nucleoplasm to the nucleolus and nuclear speckles. Silencing of CWC15 compromises the RB splicing ratio and RB-mediated immunity. Our study indicates that resistance gene RB encodes an NLR receptor, whose expression level is precisely mediated via AS to differentiate normal plant growth from the defense response. This effector recognition strategy provides a way to utilize an intron to control resistance gene activation upon infection and avoid plant stress associated with autoimmunity when the pathogen is absent.