A fungal endophyte induces local cell wall-mediated resistance in wheat roots against take-all disease

• Published in: Frontiers in plant science Vol. 15; p. 1444271
• Main Authors: Chancellor, Tania, Smith, Daniel P, Chen, Wanxin, Clark, Suzanne J, Venter, Eudri, Halsey, Kirstie, Carrera, Esther, McMillan, Vanessa, Canning, Gail, Armer, Victoria J, Hammond-Kosack, Kim E, Palma-Guerrero, Javier
• Format: Journal Article
• Language: English
• Published: Switzerland Frontiers Media S.A 18.09.2024
• Subjects: cell-wall modifications; fungal biocontrol; Plant Science; root endophyte; root pathogen; wheat defences; wheat root transcriptome; fungal biocontrol; root pathogen; root endophyte; wheat defences; wheat root transcriptome; cell-wall modifications
• ISSN: 1664-462X; 1664-462X
• DOI: 10.3389/fpls.2024.1444271

Take-all disease, caused by the Ascomycete fungus , is one of the most important root diseases of wheat worldwide. The fungus invades the roots and destroys the vascular tissue, hindering the uptake of water and nutrients. Closely related non-pathogenic species in the family, such as , occur naturally in arable and grassland soils and have previously been reported to reduce take-all disease in field studies. However, the mechanism of take-all protection has remained unknown. Here, we demonstrate that take-all control is achieved via local but not systemic host changes in response to prior root colonisation. A time-course wheat RNA sequencing analysis revealed extensive transcriptional reprogramming in -colonised tissues, characterised by a striking downregulation of key cell wall-related genes, including genes encoding cellulose synthases (CESA), and xyloglucan endotransglucosylase/hydrolases (XTH). In addition, we characterise the root infection biologies of and in wheat. We investigate the ultrastructure of previously described "subepidermal vesicles" (SEVs), dark swollen fungal cells produced in wheat roots by non-pathogenic , but not by pathogenic We show that SEVs share key characteristics of fungal resting structures, containing a greater number of putative lipid bodies and a significantly thickened cell wall compared to infection hyphae. We hypothesise that SEVs are fungal resting structures formed due to halted hyphal growth in the root cortex, perhaps as a stress response to locally induced wheat defence responses. In the absence of take-all resistant wheat cultivars or non-virulent strains, studying closely related non-pathogenic provides a much needed avenue to elucidate take-all resistance mechanisms in wheat.