‘The sky is overcast with clouds and the rain is ceaseless‘ in Gitanjali by Rabindranath Tagore.
Mid-Summer: Across Lorraine, this is generally the hottest month of the year, and when most everyone is headed to a beach or the mountains to look for a little respite. No scorching mid-Summer heat this year. Over the week-end, the sky was pouring with rain and the sun never shone from dawn to dusk. It poured with rain the entire night.
Well, I take this opportunity to get back to outstanding papers. The study of GH32 invertases in fungi from Jerri Parent, together with Tim James and Andy Taylor, was worth re-reading. In this BMC Evolutionary Biology paper, they tested for occurrence of the glycosyl hydrolase family 32 (GH32) genes in all available fungal genomes and an additional 149 species representing a broad phylogenetic and ecological range of biotrophic fungi. This GH32 family, containing mostly invertases, is crucial for plant-interacting fungi. Sucrose is the primary metabolite used by most plants to translocate carbon throughout their tissues, and its abundance within plants makes it a valuable carbon source for the many fungi that are obligate plant associates. To acquire the host sucrose, colonizing fungi must possess the necessary enzymes, such as extracellular invertase(s), to split sucrose into its constituent monosaccharides, glucose and fructose.
Ancestral state reconstruction of GH32 gene abundance showed a strong correlation with nutritional mode (saprobic, endophytic, mutualist, pathogenic). Expansion of gene families 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 (e.g. Puccinia graminis), with the notable exception of mycorrhizal taxa (e.g. Laccaria bicolor). 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.
We noticed in our Nature paper the lack of invertase in the ectomycorrhizal L. bicolor suggesting that this symbiont depends on its host plant to provide glucose in exchange for nitrogen. I have checked the presence of the extracellular invertase in our draft genome sequences of L. amethystina and Glomus intraradices, and the 454 transcripts of Lactarius quietus and Pisolithus microcarpus. None of these ECM fungi have a gene coding for this enzyme, whereas the poplar rust, Melampsora larici-populina has two sequences similar to the wheat rust Puccinia graminis GH32s. Intriguingly, the genome of the ectomycorrhizal ascomycete, Tuber melanosporum — the Black Truffe of Perigord — contains a gene encoding a GH32 enzyme, suggesting that the truffle may act as a scavenger instead of being a true mutualist. However, the corresponding transcript is lowly expressed in free-living mycelium, fruiting body and ectomycorrhiza according to our NimbleGen oligoarray and RNA-Seq transcript profilings.
As stressed by Parent et al. “Reliance on plant GH32 enzyme activity for C acquisition in these [ECM] symbionts supports earlier predictions of a general absence of invertase in mycorrhizal fungi, and a highly evolved mutualistic relationship between plants and mycorrhizal fungi, a remarkable scenario in light of the high degree of phylogenetic diversity spanned by mycorrhizal fungal taxa. Whether the plant host is able to detect fungal invertase activity and use such a signal to differentiate antagonistic from mutualistic biotrophic symbionts is a completely speculative, though plausible hypothesis.”
Parrent et al. (2009) Friend or foe? Evolutionary history of glycoside hydrolase family 32 genes encoding for sucrolytic activity in fungi and its implications for plant-fungal symbioses. BMC Evolutionary Biology 9:148 doi:10.1186/1471-2148-9-148.
Photo: Lorraine Big Sky © F Martin