Friend or foe? Evolutionary history of glycoside hydrolase family 32 genes encoding for sucrolytic activity in fungi and its implications for plant-fungal symbioses.
BACKGROUND
Many 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.


RESULTS
We 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.


CONCLUSIONS
We 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.
Parrent
Jeri Lynn
JL
Department of Forest Mycology and Pathology, Swedish University of Agricultural Sciences, Box 7026, Ulls väg 26a, SE 750 07 Uppsala, Sweden. jparrent@umich.edu
James
Timothy Y
TY
Vasaitis
Rimvydas
R
Taylor
Andrew Fs
AF
D004271:DNA, Fungal / Q000235:genetics; D019143:Evolution, Molecular; D005658:Fungi / Q000201:enzymology / Q000235:genetics*; D016681:Genome, Fungal; D005810:Multigene Family; D009699:N-Glycosyl Hydrolases / Q000235:genetics*; D010802:Phylogeny; D010944:Plants / Q000382:microbiology; D017422:Sequence Analysis, DNA; D013395:Sucrose / Q000378:metabolism*; D013559:Symbiosis
D004271:DNA, Fungal; D013395:Sucrose; D009699:N-Glycosyl Hydrolases