Abstract
BackgroundMany fungi are obligate biotrophs of plants, growing in live plant tissues, gaining direct access to recently photosynthesized carbon. Photosynthate within plants is transported from source to sink tissues as sucrose, which is hydrolyzed by plant glycosyl hydrolase family 32 enzymes (GH32) into its constituent monosaccharides to meet plant cellular demands. A number of plant pathogenic fungi also use GH32 enzymes to access plant-derived sucrose, but less is known about the sucrose utilization ability of mutualistic and commensal plant biotrophic fungi, such as mycorrhizal and endophytic fungi. The aim of this study was to explore the distribution and abundance of GH32 genes in fungi to understand how sucrose utilization is structured within and among major ecological guilds and evolutionary lineages. Using bioinformatic and PCR-based analyses, we tested for GH32 gene presence in all available fungal genomes and an additional 149 species representing a broad phylogenetic and ecological range of biotrophic fungi.ResultsWe detected 9 lineages of GH32 genes in fungi, 4 of which we describe for the first time. GH32 gene number in fungal genomes ranged from 0–12. Ancestral state reconstruction of GH32 gene abundance showed a strong correlation with nutritional mode, and gene family expansion was observed in several clades of pathogenic filamentous Ascomycota species. GH32 gene number was negatively correlated with animal pathogenicity and positively correlated with plant biotrophy, with the notable exception of mycorrhizal taxa. Few mycorrhizal species were found to have GH32 genes as compared to other guilds of plant-associated fungi, such as pathogens, endophytes and lichen-forming fungi. GH32 genes were also more prevalent in the Ascomycota than in the Basidiomycota.ConclusionWe found a strong signature of both ecological strategy and phylogeny on GH32 gene number in fungi. These data suggest that plant biotrophic fungi exhibit a wide range of ability to access plant-synthesized sucrose. Endophytic fungi are more similar to plant pathogens in their possession of GH32 genes, whereas most genomes of mycorrhizal taxa lack GH32 genes. Reliance on plant GH32 enzyme activity for C acquisition in these symbionts supports earlier predictions of possible plant control over C allocation in the mycorrhizal symbiosis.
Highlights
Many fungi are obligate biotrophs of plants, growing in live plant tissues, gaining direct access to recently photosynthesized carbon
By reconstructing the history of Glycoside hydrolase family 32 (GH32) genes throughout fungi we addressed the following questions: 1) does GH32 gene presence and abundance positively correlate with a plant pathogenic ecological strategy; 2) do mycorrhizal, endophytic, and lichenic fungi typically possess or lack GH32 genes? Within plant-associated fungi we hypothesize that GH32 gene presence may be negatively correlated with the degree of mutualism and its presence or absence may serve as a general marker for the sign of interaction between a plant and a fungus
GH32 Gene phylogeny from fungal genome data Seventy-six genomes from five fungal phyla were queried for GH32 gene presence: 9 Basidiomycota, 62 Ascomycota, 2 Zygomycota, 1 Chytridiomycota and 2 microsporidia
Summary
Many fungi are obligate biotrophs of plants, growing in live plant tissues, gaining direct access to recently photosynthesized carbon. All Fungi are heterotrophic organisms, and the majority of fungal species rely solely upon plant tissues to meet their carbon (C) demands. Sucrose is cleaved by extracellular invertase enzymes into equimolar concentrations of glucose and fructose. These monosaccharide molecules are imported into plant cells via transport proteins and used either to meet cellular energy demands or as substrates for synthesizing other carbohydrate-containing storage molecules. Increased invertase enzyme activity and the resultant decline in sucrose concentrations in sink tissues is intimately tied to phloem unloading and carbon allocation in the plant [3,4]
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