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

Abstract

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.

The role of carbon in fungal nutrient uptake and transport

“…1), which is broken down by plant derived acid invertase 19,20 or sucrose synthase 21 into hexoses which the fungus takes up via a high affinity monosaccharide transporter. 22 AM fungi are unable to use sucrose as a C source 23 so they induce the expression of the plant acid invertase in the mycorrhizal Plant uptake transporters of the DP are downregulated in mycorrhizal roots, 13,14 and the MP can represent the main uptake pathway even in plants in which no positive growth benefit is observed. 15 Whether the suppression of the DP in mycorrhizal roots is a host driven or a fungal mediated response is not known.…”

Enigmatic Sebacinales

“…Sucrose from host plants is mostly hydrolyzed by fungal plant parasites into their monosaccharides by glycosyl hydrolase family 32 enzymes (GH32). Genes for such enzymes were lacking in 46 basidiomycetous ECM fungi, with the remarkable exception of Sebacina incrustans (Parrent et al 2009), but they were present in 16 of 54 surveyed non-mycorrhizal Agaricomycetes. A putatively secreted sucrase was identified in the genome draft of P. indica, suggesting a wide-spread distribution of the enzyme in the Sebacinales ).…”

The Role of the Mycorrhizal Symbiosis in Nutrient Uptake of Plants and the Regulatory Mechanisms Underlying These Transport Processes

“…It is generally accepted that in contrast to phytopathogenic fungi or ericoid mycorrhizal fungi, AM and ECM fungi are not able to use sucrose as a carbon source, and that they take up simpler sugars, such as glucose or fructose, from the mycorrhizal interface. The presence of invertase genes in fungal genomes is correlated with the nutritional mode and in contrast to other plant-associated fungi, such as pathogens, or endophytes, there are no indications that AM or ECM fungi possess invertase genes [44] or have invertase activity [30]. Consequently, mycorrhizal fungi rely on the invertase activity of the host in the interfacial apoplast for sucrose hydrolysis.…”