Abstract
Pathogenic fungi drastically affect plant health and cause significant losses in crop yield and quality. In spite of their impact, little is known about the carbon sources used by these fungi in planta and about the fungal transporters importing sugars from the plant-fungus interface. Here, we report on the identification and characterization of MELIBIOSE TRANSPORTER1 (MBT1) from the hemibiotrophic fungus Colletotrichum graminicola (teleomorph Glomerella graminicola), the causal agent of leaf anthracnose and stalk rot disease in maize (Zea mays). Functional characterization of the MBT1 protein in baker's yeast (Saccharomyces cerevisiae) expressing the MBT1 cDNA revealed that α-D-galactopyranosyl compounds such as melibiose, galactinol, and raffinose are substrates of MBT1, with melibiose most likely being the preferred substrate. α-D-glucopyranosyl disaccharides like trehalose, isomaltose, or maltose are also accepted by MBT1, although with lower affinities. The MBT1 gene shows low and comparable expression levels in axenically grown C. graminicola and upon infection of maize leaves both during the initial biotrophic development of the fungus and during the subsequent necrotrophic phase. Despite these low levels of MBT1 expression, the MBT1 protein allows efficient growth of C. graminicola on melibiose as sole carbon source in axenic cultures. Although Δmbt1 mutants are unable to grow on melibiose, they do not show virulence defects on maize.
Highlights
Pathogenic fungi drastically affect plant health and cause significant losses in crop yield and quality
Raffinose hydrolysis was mediated by cell wall-bound invertases (a-D-Glcp-1,2b-D-Fruf; Roitsch and Gonzalez, 2004; Vargas et al, 2009), but of the resulting products, only Fru was taken up by the plant cells whereas melibiose accumulated in the medium
BLAST searches with a-glucoside transporter (AGT) sequences from baker’s yeast and other fungi in the National Center for Biotechnology Information trace archives and in the C. graminicola genome database identified five genes for proteins with significant homology to known or putative AGT transporters
Summary
Pathogenic fungi drastically affect plant health and cause significant losses in crop yield and quality. When Bringhurst et al (2001) studied the activity of a galactoside-sensing a-galactosidase-GFP construct in the transgenic soil bacterium Sinorhizobium meliloti in the presence of root washes from different legume species, they observed strong GFP fluorescence in S. meliloti Qualitative analyses of these root washes identified legume-derived secreted raffinose and stachyose (a-D-Galp-1,6-a-D-Galp-1,6-a-D-Glcp-1,2-b-D-Fruf) as the inducing compounds, suggesting that these oligosaccharides are secreted to feed rhizosphere symbionts. While biotrophic fungi only penetrate the cell wall of their host but not the plasma membrane to grow extracellularly, fungi exhibiting a necrotrophic lifestyle invade the plant cell and kill the host by secretion of toxins or by generating reactive oxygen species (Mendgen and Hahn, 2002; Horbach et al, 2011) Depending on their lifestyle, pathogens have access to different carbon sources. It is important to note that biotrophic fungi have fewer genes encoding cell walldegrading enzymes (Kamper et al, 2006) and cause only minimal cell wall damage during the infection process (Mendgen and Deising, 1993)
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