Conserved Proteins of the RNA Interference System in the Arbuscular Mycorrhizal Fungus Rhizoglomus irregulare Provide New Insight into the Evolutionary History of Glomeromycota

Abstract

Horizontal gene transfer (HGT) is an important mechanism in the evolution of many living organisms particularly in Prokaryotes where genes are frequently dispersed between taxa. Although, HGT has been reported in Eukaryotes, its accumulative effect and its frequency has been questioned. Arbuscular mycorrhizal fungi (AMF) are an early diverged fungal lineage belonging to phylum Glomeromycota, whose phylogenetic position is still under debate. The history of AMF and land plant symbiosis dates back to at least 460 Ma. However, Glomeromycota are estimated to have emerged much earlier than land plants. In this study, we surveyed genomic and transcriptomic data of the model arbuscular mycorrhizal fungus Rhizoglomus irregulare (synonym Rhizophagus irregularis) and its relatives to search for evidence of HGT that occurred during AMF evolution. Surprisingly, we found a signature of putative HGT of class I ribonuclease III protein-coding genes that occurred from autotrophic cyanobacteria genomes to R. irregulare. At least one of two HGTs was conserved among AMF species with high levels of sequence similarity. Previously, an example of intimate symbiosis between AM fungus and cyanobacteria was reported in the literature. Ribonuclease III family enzymes are important in small RNA regulation in Fungi together with two additional core proteins (Argonaute/piwi and RdRP). The eukaryotic RNA interference system found in AMF was conserved and showed homology with high sequence similarity in Mucoromycotina, a group of fungi closely related to Glomeromycota. Prior to this analysis, class I ribonuclease III has not been identified in any eukaryotes. Our results indicate that a unique acquisition of class I ribonuclease III in AMF is due to a HGT event that occurred from cyanobacteria to Glomeromycota, at the latest before the divergence of the two Glomeromycota orders Diversisporales and Glomerales.

Genome and evolution of the arbuscular mycorrhizal fungus Diversispora epigaea (formerly Glomus versiforme) and its bacterial endosymbionts

“…Of these, HGT of ribonuclease III was also reported recently in R . irregularis (Lee et al ., ). Most HGT genes were expressed in both fungal spores and extraradical hyphae, and some of them seem to be highly expressed in the spores (Fig.…”

Fungal community analysis in seawater of the Mariana Trench as estimated by Illumina HiSeq

“…Glomeromycota, also called arbuscular mycorrhizal fungi, are typical fungal symbionts colonizing the roots of vascular plants and widely-spread on land. 27 Recently, the phylum Glomeromycota has been also detected in marine environments, including Arctic, marine sediments, 3 and hydrothermal ecosystems. 28 And it was not detected in the Mariana Trench in previous reports.…”

Different Genetic Sources Contribute to the Small RNA Population in the Arbuscular Mycorrhizal Fungus Gigaspora margarita

“…With regards to the RdRp, we found six proteins in G. margarita, more than the one to five generally possessed by non-AMF (Chang et al, 2012;Chen et al, 2015). In our previous work we reported 21 RdRp in R. irregularis, although Lee et al (2018), using more stringent annotation criteria, only reported three.…”

“…Recent surveys of two AMF genomes allowed a first characterization of the RNAi components (DCL, AGO-like, and RdRp) in this group of obligate biotrophs (Lee et al, 2018;Silvestri et al, 2019). These works highlighted that the two analyzed AMF, R. irregularis and R. clarus, are equipped with a RNAi machinery characterized by 26-40 AGO-like, 3-21 RdRp, and 1-2 DCL proteins.…”

“…The RNAi machinery and the sRNA populations in AMF have been characterized only in the model AMF species Rhizophagus irregularis (Lee et al, 2018;Silvestri et al, 2019). The availability of the full genome sequence of Gigaspora margarita (Venice et al, 2019) offered the possibility to explore how conserved are RNAi features in AMF.…”