Intra‐isolate genome variation in arbuscular mycorrhizal fungi persists in the transcriptome

Abstract

Arbuscular mycorrhizal fungi (AMF) are heterokaryotes with an unusual genetic makeup. Substantial genetic variation occurs among nuclei within a single mycelium or isolate. AMF reproduce through spores that contain varying fractions of this heterogeneous population of nuclei. It is not clear whether this genetic variation on the genome level actually contributes to the AMF phenotype. To investigate the extent to which polymorphisms in nuclear genes are transcribed, we analysed the intra‐isolate genomic and cDNA sequence variation of two genes, the large subunit ribosomal RNA (LSU rDNA) of Glomus sp. DAOM‐197198 (previously known as G. intraradices) and the POL1‐like sequence (PLS) of Glomus etunicatum. For both genes, we find high sequence variation at the genome and transcriptome level. Reconstruction of LSU rDNA secondary structure shows that all variants are functional. Patterns of PLS sequence polymorphism indicate that there is one functional gene copy, PLS2, which is preferentially transcribed, and one gene copy, PLS1, which is a pseudogene. This is the first study that investigates AMF intra‐isolate variation at the transcriptome level. In conclusion, it is possible that, in AMF, multiple nuclear genomes contribute to a single phenotype.

Mitochondrial Genome Rearrangements in Glomus Species Triggered by Homologous Recombination between Distinct mtDNA Haplotypes

“…Despite the fact that these symbioses contribute to important services in natural, agricultural and reclaimed ecosystems (Gianinazzi et al 2010), the species richness, community structure and functional diversity of AMF is not well understood (Wehner et al 2010) due to a lack of reliable molecular tools. The intra-isolate genetic diversity of nuclear DNA and RNA sequences observed in AMF (Sanders et al 1995; Kuhn et al 2001; Pawlowska and Taylor 2004; Mathimaran et al 2008; Stockinger et al 2009; Boon et al 2010), has made it difficult to determine evolutionary relatedness at high levels of resolution (i.e., between genetically similar species and/or isolates).…”

Allelic Differences within and among Sister Spores of the Arbuscular Mycorrhizal Fungus Glomus etunicatum Suggest Segregation at Sporulation

“…Indeed, numerous studies confirm that alleles can vary within and between AMF isolates and sister spores, with evidence coming from rRNA genes (rDNA) [19-24], protein-coding genes [20,22,25-28], and even from the transcriptome [22,29]. …”

“…A similar experiment was performed for the protein-coding gene BiP [30]. Furthermore, a large discrepancy between copy number per nucleus and allele number per isolate indicated that, for Large Subunit (LSU) rDNA, allele variants were partitioned between and not within nuclei in the same isolate [22]. Finally, Ehinger et al [31,32] found genotypic and phenotypic variation after clonal growth of spores over three successive generations, likely with corresponding variation in fitness [32].…”

Genome diversity in arbuscular mycorrhizal fungi

“…Pawlowska and Taylor [20] found that 13 variants of the PLS1 gene (POL1-like, but probably a pseudogene [21]) were all inherited by all spores that they examined in C. etunicatum, and argued that every nucleus must have all the variants because such stability would be very unlikely if each variant were carried by an independently inherited nucleus. This argument loses force if the inheritance is not entirely independent, which could be the case if each nucleus carried several (but not all) variant loci, or if nuclei were mutually interdependent; anastomosis could also stem the loss of variation.…”

“…By contrast, most of the studies of nuclear diversity have involved other isolates, which may be very different. Indeed, many studies [20][21][22]30] concern Claroideoglomus, which has been diverging from Rhizophagus for almost 500 million years [8], so may differ in fundamental ways. The studies of diversity in R. irregularis have not used DAOM197198 but other, potentially less 'domesticated', isolates, and in some cases have deliberately enhanced variation through anastomosis [23,25 ,31].…”