S-acylation of a non-secreted peptide controls plant immunity via secreted-peptide signal activation

• Published in: EMBO reports 2024-02, Vol.25 (2), p.489-505
• Main Authors: Li, Wenliang, Ye, Tushu, Ye, Weixian, Liang, Jieyi, Wang, Wen, Han, Danlu, Liu, Xiaoshi, Huang, Liting, Ouyang, Youwei, Liao, Jianwei, Chen, Tongsheng, Yang, Chengwei, Lai, Jianbin
• Format: Article
• Language: English
• Subjects: Acylation; Arabidopsis - metabolism; Arabidopsis Proteins - metabolism; Biomedical and Life Sciences; EMBO19; EMBO30; EMBO37; Life Sciences; Peptides - metabolism; Plant Immunity; Plants - metabolism; Protein Kinases - metabolism
• ISSN: 1469-3178; 1469-221X; 1469-3178
• DOI: 10.1038/s44319-023-00029-x

Small peptides modulate multiple processes in plant cells, but their regulation by post-translational modification remains unclear. ROT4 (ROTUNDIFOLIA4) belongs to a family of Arabidopsis non-secreted small peptides, but knowledge on its molecular function and how it is regulated is limited. Here, we find that ROT4 is S-acylated in plant cells. S-acylation is an important form of protein lipidation, yet so far it has not been reported to regulate small peptides in plants. We show that this modification is essential for the plasma membrane association of ROT4. Overexpression of S-acylated ROT4 results in a dramatic increase in immune gene expression. S-acylation of ROT4 enhances its interaction with BSK5 (BRASSINOSTEROID-SIGNALING KINASE 5) to block the association between BSK5 and PEPR1 (PEP RECEPTOR1), a receptor kinase for secreted plant elicitor peptides (PEPs), thereby activating immune signaling. Phenotype analysis indicates that S-acylation is necessary for ROT4 functions in pathogen resistance, PEP response, and the regulation of development. Collectively, our work reveals an important role for S-acylation in the cross-talk of non-secreted and secreted peptide signaling in plant immunity. Synopsis S-acylation of the non-secreted peptide ROT4 is essential for its membrane localization and function in plant cells. S-acylation of ROT4 enhances its association with BSK5 to activate immune signaling mediated by plant elicitor peptides. S-acylation is important for the plasma membrane localization of the non-secreted plant peptide ROT4. The upregulation of plant immune genes mediated by ROT4 requires its S-acylation. S-acylation of ROT4 increases its association with BSK5 for activation of plant elicitor peptide signaling. S-acylation is necessary for the function of ROT4 in plant immunity and in pathogen resistance. S-acylation of the non-secreted peptide ROT4 is essential for its membrane localization and function in plant cells. S-acylation of ROT4 enhances its association with BSK5 to activate immune signaling mediated by plant elicitor peptides.