Iturin and fengycin lipopeptides inhibit pathogenic Fusarium by targeting multiple components of the cell membrane and their regulative effects in wheat

Author:

Yuan Qing‐Song12ORCID,Yang Peng13ORCID,Liu Yi‐Ke4ORCID,Tabl Karim M.15ORCID,Guo Mao‐Wei16ORCID,Zhang Jing‐Bo1ORCID,Wu Ai‐Bo7ORCID,Liao Yu‐Cai1ORCID,Huang Tao8ORCID,He Wei‐Jie1ORCID

Affiliation:

1. College of Plant Science and Technology Huazhong Agricultural University Wuhan 430070 China

2. Resource Institute for Chinese & Ethnic Materia Medica Guizhou University of Traditional Chinese Medicine Guiyang 550025 China

3. Jiangsu Ruihua Agricultural Science and Technology Co. Ltd. Suqian 223800 China

4. Institute of Food Crops, Hubei Academy of Agricultural Sciences/Key Laboratory of Crop Molecular Breeding Ministry of Agriculture and Rural Affairs/Hubei Key Laboratory of Food Crop Germplasm and Genetic Improvement Wuhan 430064 China

5. Agricultural Botany Department, Faculty of Agriculture (Saba Basha) Alexandria University Alexandria 21531 Egypt

6. Grassland Research Institute Chinese Academy of Agricultural Sciences Hohhot 010000 China

7. SIBS‐UGENT‐SJTU Joint Laboratory of Mycotoxin Research, CAS Key Laboratory of Nutrition, Metabolism and Food Safety, Shanghai Institute of Nutrition and Health University of Chinese Academy of Sciences, the Chinese Academy of Sciences Shanghai 200031 China

8. College of Life Science and Technology Huazhong Agricultural University Wuhan 430070 China

Abstract

ABSTRACTBiocontrol microorganisms and their derived metabolites with antagonistic activity represent promising alternatives to chemical fungicides in managing plant pathogens. The lipopeptides (LPs) iturin and fengycin derived from Bacillus amyloliquefaciens S76‐3 exhibit highly inhibitory effects against pathogenic fungi, especially Fusarium graminearum (Fg), the primary pathogen causing Fusarium head blight (FHB) in cereals. However, the specific target of iturin and fengycin in Fg and the underlying mechanism of antagonistic activity remain unclear. Here, global transcriptome sequencing, combined with both genetic and chemical approaches, demonstrates that the LPs exhibit antagonism toward Fg by binding to multiple components in the cell membrane of Fg cells, including ergosterol, phospholipids, glycosylphosphatidylinositol, and ankyrin. Lipopeptides result in cell swelling by inducing cell wall remodeling and osmotic substance glycerol synthesis mediated by cell wall integrity and high‐osmolarity glycerol signaling pathways. Furthermore, we found that LPs can activate the induced systemic resistance in wheat against FHB and deoxynivalenol accumulation. Additionally, LPs were able to promote wheat growth by regulating auxin, cytokinin, and gibberellin signaling pathways while also delaying seed germination through the stimulation of abscisic acid and ethylene signaling pathways. These findings advance knowledge on the underlying mechanism of iturin and fengycin antagonistic activity and provide a new avenue for developing agricultural and clinical broad‐spectrum antifungal agents and identifying plant growth regulators in the future.

Funder

China Postdoctoral Science Foundation

National Natural Science Foundation of China

Publisher

Wiley

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