SR45a plays a key role in enhancing cotton resistance to Verticillium dahliae by alternative splicing of immunity genes

• Published in: The Plant journal : for cell and molecular biology 2024-07, Vol.119 (1), p.137-152
• Main Authors: Liu, Fujie, Cai, Sheng, Dai, Lingjun, Ai, Nijiang, Feng, Guoli, Wang, Ningshan, Zhang, Wenli, Liu, Kang, Zhou, Baoliang
• Format: Article
• Language: English
• Subjects: Alternative splicing; Alternative Splicing - genetics; Ascomycota - physiology; Cellular stress response; Chitin; Cotton; Diploids; Disease Resistance - genetics; Gene expression; Gene Expression Regulation, Plant; Gene regulation; Gene silencing; Genes; Gossypium - genetics; Gossypium - immunology; Gossypium - microbiology; Immune response; Immunity; Kinases; Plant Diseases - genetics; Plant Diseases - immunology; Plant Diseases - microbiology; plant immunity; Plant Immunity - genetics; Plant Proteins - genetics; Plant Proteins - metabolism; Proteomes; RNA-binding protein; RNA-mediated interference; Splicing factors; splicing regulating factor; SR protein; Transcriptomes; Verticillium; Verticillium dahliae; Verticillium wilt
• ISSN: 0960-7412; 1365-313X; 1365-313X
• DOI: 10.1111/tpj.16750

SUMMARY Alternative splicing (AS) of pre‐mRNAs increases the diversity of transcriptome and proteome and plays fundamental roles in plant development and stress responses. However, the prevalent changes in AS events and the regulating mechanisms of plants in response to pathogens remain largely unknown. Here, we show that AS changes are an important mechanism conferring cotton immunity to Verticillium dahliae (Vd). GauSR45a, encoding a serine/arginine‐rich RNA binding protein, was upregulated expression and underwent AS in response to Vd infection in Gossypium australe, a wild diploid cotton species highly resistant to Vd. Silencing GauSR45a substantially reduced the splicing ratio of Vd‐induced immune‐associated genes, including GauBAK1 (BRI1‐associated kinase 1) and GauCERK1 (chitin elicitor receptor kinase 1). GauSR45a binds to the GAAGA motif that is commonly found in the pre‐mRNA of genes essential for PTI, ETI, and defense. The binding between GauSR45a and the GAAGA motif in the pre‐mRNA of BAK1 was enhanced by two splicing factors of GauU2AF35B and GauU1‐70 K, thereby facilitating exon splicing; silencing either AtU2AF35B or AtU1‐70 K decreased the resistance to Vd in transgenic GauSR45a Arabidopsis. Overexpressing the short splicing variant of BAK1GauBAK1.1 resulted in enhanced Verticillium wilt resistance rather than the long one GauBAK1.2. Vd‐induced far more AS events were in G. barbadense (resistant tetraploid cotton) than those in G. hirsutum (susceptible tetraploid cotton) during Vd infection, indicating resistance divergence in immune responses at a genome‐wide scale. We provided evidence showing a fundamental mechanism by which GauSR45a enhances cotton resistance to Vd through global regulation of AS of immunity genes. Significance Statement We found PTI‐ and ETI‐associated genes underwent genome‐wide AS in the immune response to Vd in cotton and SR45a collaborated with splicing factors U2AF35B and U1‐70K to regulate AS of immune‐associated genes. Our results provide evidence showing that SR45a may play a central role in the regulation of AS of plant immunity genes in response to Vd invasion, and thus deepen our insights into the mechanisms of VW resistance in cotton.