The serine-threonine protein kinase Snf1 orchestrates the expression of plant cell wall-degrading enzymes and is required for full virulence of the maize pathogen Colletotrichum graminicola

• Published in: Fungal genetics and biology 2024-03, Vol.171, p.103876-103876, Article 103876
• Main Authors: de Oliveira Silva, Alan, Fernando Devasahayam, Bennet Rohan, Aliyeva-Schnorr, Lala, Glienke, Chirlei, Deising, Holger B.
• Format: Article
• Language: English
• Subjects: Cell wall-degrading enzymes; Colletotrichum graminicola; Plant invasion; Serine-threonine protein kinase; SNF1; Virulence factor; Xylanases; Zea mays
• ISSN: 1087-1845; 1096-0937
• DOI: 10.1016/j.fgb.2024.103876

•Colletotrichum graminicola differentiates a pressurized infection cell called an appressorium to invade the cell.•While the role of force in appressorial penetration is established the role of cell wall-degrading enzymes is poorly understood.•We identified and characterized the SNF1 homolog of C. graminicola. Δsnf1 mutants showed reduced growth on polymeric carbon sources.•Microscopy revealed reduced efficacies in appressorial penetration and formation of unusual medusa-like biotrophic hyphae by Δsnf1 mutants.•Severe and moderate virulence reductions were observed on intact and wounded leaves, respectively.•RNA-sequencing showed that Snf1 controls more than 2,500 genes in necrotrophic hyphae, many of which encode cell wall-degrading enzymes.•The data presented show that SNF1 is a global regulator of gene expression and is required for full virulence. Colletotrichum graminicola, the causal agent of maize leaf anthracnose and stalk rot, differentiates a pressurized infection cell called an appressorium in order to invade the epidermal cell, and subsequently forms biotrophic and necrotrophic hyphae to colonize the host tissue. While the role of force in appressorial penetration is established (Bechinger et al., 1999), the involvement of cell wall-degrading enzymes (CWDEs) in this process and in tissue colonization is poorly understood, due to the enormous number and functional redundancy of these enzymes. The serine/threonine protein kinase gene SNF1 identified in Sucrose Non-Fermenting yeast mutants mediates de-repression of catabolite-repressed genes, including many genes encoding CWDEs. In this study, we identified and functionally characterized the SNF1 homolog of C. graminicola. Δsnf1 mutants showed reduced vegetative growth and asexual sporulation rates on media containing polymeric carbon sources. Microscopy revealed reduced efficacies in appressorial penetration of cuticle and epidermal cell wall, and formation of unusual medusa-like biotrophic hyphae by Δsnf1 mutants. Severe and moderate virulence reductions were observed on intact and wounded leaves, respectively. Employing RNA-sequencing we show for the first time that more than 2,500 genes are directly or indirectly controlled by Snf1 in necrotrophic hyphae of a plant pathogenic fungus, many of which encode xylan- and cellulose-degrading enzymes. The data presented show that Snf1 is a global regulator of gene expression and is required for full virulence.