The D-galacturonic acid catabolic pathway genes differentially regulate virulence and salinity response in Sclerotinia sclerotiorum

• Published in: Fungal genetics and biology Vol. 145; p. 103482
• Main Authors: Wei, Wei, Pierre-Pierre, Nickisha, Peng, Hao, Ellur, Vishnutej, Vandemark, George J., Chen, Weidong
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.12.2020
• Subjects: Ascomycota - genetics; Ascomycota - metabolism; Cell wall; Cell Wall - metabolism; Fungal pathogen; Fungal Proteins - genetics; Gene Expression Regulation, Fungal; Glycine max - genetics; Glycine max - metabolism; Hexuronic Acids - metabolism; Metabolic Networks and Pathways - genetics; Metabolism - genetics; Pectin catabolism; Plant Diseases - genetics; Plant Diseases - microbiology; Salt tolerance; Solanum lycopersicum - genetics; Solanum lycopersicum - microbiology; Virulence; White mold; Fungal pathogen; Salt tolerance; White mold; Pectin catabolism; Virulence; Cell wall
• ISSN: 1087-1845; 1096-0937
• DOI: 10.1016/j.fgb.2020.103482

•D-galacturonic acid catabolic enzymes in S. sclerotiorum have versatile functions.•These enzymes enhance virulence via degrading pectin components in host cell wall.•As secreted proteins, these enzymes reduce S. sclerotiorum tolerance to salt stress.•SsGAR2 has an additional function of promoting S. sclerotiorum cell wall integrity. Sclerotinia sclerotiorum causes white mold disease on a wide range of economically important crops such as soybean, canola, tomato, pea and sunflower. As one of the most successful plant pathogens, S. sclerotiorum has the unique ability of adapting to various environmental conditions and effectively suppressing or evading plant defense. Notably, S. sclerotiorum secretes an array of plant cell-wall degrading enzymes (CWDEs) to macerate host cell wall and utilizes the liberated monosaccharides and oligosaccharides as nutrients. One of the major plant cell wall constituents is polygalacturonic acid in pectin, with D-galacturonic acid being the most abundant component. In this research, we identified four S. sclerotiorum genes that encode the enzymes for the D-galacturonic acid catabolism, namely Ssgar1, Ssgar2, Sslgd1 and Sslga1. Gene-knockout mutants were created for all four catabolic genes. When cultured on pectin as the alternative carbon source, Sslgd1- and Sslga1-deletion mutants and Ssgar1/Ssgar2 double deletion mutants exhibited significantly reduced growth. The D-galacturonic acid catabolic genes are transcriptionally induced by either polygalacturonic acid in the culture media or during host infection. Virulence tests of the knockout mutants revealed that Ssgar2, Sslgd1 and Sslga1 all facilitated the effective colonization of S. sclerotiorum to the leaves of soybean and pea, but not of tomato which has the lowest D-galacturonic acid contents in its leaves. In addition to their positive roles in virulence, all four enzymes negatively affect S. sclerotiorum tolerance to salt stress. SsGAR2 has an additional function in tolerance to Congo Red, suggesting a potential role in cell wall stability of S. sclerotiorum. This study is the first report revealing the versatile functions of D-galacturonic acid catabolic genes in S. sclerotiorum virulence, salinity response and cell wall integrity.