A Survey of the Gene Repertoire of Gigaspora rosea Unravels Conserved Features among Glomeromycota for Obligate Biotrophy

Abstract

Arbuscular mycorrhizal (AM) fungi are a diverse group of soil fungi (Glomeromycota) that form the most ancient mutualistic association termed AM symbiosis with a majority of land plants, improving their nutrition uptake and resistance to stresses. In contrast to their great ecological implications, the knowledge of the molecular biological mechanisms involved is still scant, partly due to the limited genomic resources available. Here, we describe the gene repertoire of a new AM fungus Gigaspora rosea (Diversisporales). Among the 86332 non-redundant virtual transcripts assembled, 15346 presented similarities with proteins in the Refseq database and 10175 were assigned with GO terms. KOG and Interpro domain annotations clearly showed an enrichment of genes involved in signal transduction in G. rosea. KEGG pathway analysis indicates that most primary metabolic processes are active in G. rosea. However, as for Rhizophagus irregularis, several metabolic genes were not found, including the fatty acid synthase (FAS) gene. This finding supports the hypothesis that AM fungi depend on the lipids produced by their hosts. Furthermore, the presence of a large number of transporters and 100s of secreted proteins, together with the reduced number of plant cell wall degrading enzymes could be interpreted as an evolutionary adaptation to its mutualistic obligate biotrophy. The detection of meiosis-related genes suggests that G. rosea might use a cryptic sexual process. Lastly, a phylogeny of basal fungi clearly shows Glomeromycota as a sister clade to Mucoromycotina, not only to the Mucorales or Mortierellales. The characterization of the gene repertoire from an AM fungal species belonging to the order of Diversisporales and its comparison with the gene sets of R. irregularis (Glomerales) and Gigaspora margarita (Diversisporales), reveal that AM fungi share several features linked to mutualistic obligate biotrophy. This work contributes to lay the foundation for forthcoming studies into the genomics of Diversisporales, and also illuminates the utility of comparing gene repertoires of species from Diversisporales and other clades of Glomeromycota to gain more insights into the genetics and evolution of this fungal group.

Trade-Offs in Arbuscular Mycorrhizal Symbiosis: Disease Resistance, Growth Responses and Perspectives for Crop Breeding

“…AMF are lipid auxotrophs, and accordingly, lipids are transferred from the host plant to AMF to sustain AM colonization [126][127][128], which requires action of the glycerol-3-phosphate acyltransferase enzyme Required for Arbuscular Mycorrhization 2 (RAM2) [129]. Jiang et al (2017) showed that plant fatty acids are also transferred to the powdery mildew pathogen, Golovinomyces cichoracerum (DC.)…”

Arbuscular Mycorrhizal Symbiosis Requires a Phosphate Transceptor in the Gigaspora margarita Fungal Symbiont

“…In addition, the RNA-seq data analysis coupled with gene expression profiling show that both G. margarita and Gigaspora rosea consist of multiple distinct SPX domaincontaining proteins ( Salvioli et al, 2016 andTang et al, 2016), indicative of the existence of potential Pi sensors in AM fungi to respond to cellular Pi levels through binding inositol polyphosphate in eukaryotes (Wild et al, 2016) and adapting to fluctuation of available phosphate. Thus, a major goal in this field will be to unravel a potential master cellular Pi sensor controlling AM fungal Pi homeostasis during symbiosis.…”

The plasma membrane proteome of Medicago truncatula roots as modified by arbuscular mycorrhizal symbiosis

“…It is noteworthy that Medtr4g097510 is one of the 12 lipid biosynthetic genes only expressed in AM symbiotic hosts (Bravo et al 2016). This suggests that, similarly to the thioesterase FatM, the ketoacyl-acyl carrier reductase KAR, and the ketoacyl-ACP synthase KAS II (Bravo et al 2017;Jiang et al 2017), the PMassociated enoyl-(acyl carrier) reductase may contribute to supply FAs to the AM symbiont which cannot synthetize C16:0 FAs Tang et al 2016). In support of this idea, the beta-hydroxyacyl-(acyl-carrier-protein) dehydratase FabZ (Medtr4g094265) that leads to the synthesis of palmitate (C16:0) was only detected in the PM fraction of AM roots (Table S1).…”