Reciprocal recombination genomic signatures in the symbiotic arbuscular mycorrhizal fungi Rhizophagus irregularis

Abstract

Arbuscular mycorrhizal fungi (AMF) are part of the most widespread fungal-plant symbiosis. They colonize at least 80% of plant species, promote plant growth and plant diversity. These fungi are multinucleated and contain either one or two haploid nuclear genotypes (monokaryon and dikaryon) identified by the alleles at a putative mating-type locus. This taxon has been considered as an ancient asexual scandal because of the lack of observable sexual structures. Despite identification of a putative mating-type locus and functional activation of genes related to mating when two isolates co-exist, it remains unknown if the AMF life cycle involves a sexual or parasexual stage. We used publicly available genome sequences to test if Rhizophagus irregularis dikaryon genomes display signatures of sexual reproduction in the form of reciprocal recombination patterns, or if they display exclusively signatures of parasexual reproduction involving gene conversion. We used short-read and long-read sequence data to identify nucleus-specific alleles within dikaryons and then compared them to orthologous gene sequences from related monokaryon isolates displaying the same putative MAT-types as the dikaryon. We observed that the two nucleus-specific alleles of the dikaryon A5 are more related to the homolog sequences of monokaryon isolates displaying the same putative MAT-type than between each other. We also observed that these nucleus-specific alleles displayed reciprocal recombination signatures. These results confirm that dikaryon and monokaryon isolates displaying the same putative MAT-type are related in their life-cycle. These results suggest that a genetic exchange mechanism, involving reciprocal recombination in dikaryon genomes, allows AMF to generate genetic diversity.

Purifying Selection and Persistent Polymorphism among Nuclei in the Multinucleate Arbuscular Mycorrhizal (AM) Fungi

“…Previous studies have proposed mixing of different nuclei, i.e. nucleotypes, as a result of hyphal fusion (Giovannetti, Azzolini, and Citernesi 1999;Bever and Wang 2005), potentially followed by recombination events identified using polymorphic markers (Vandenkoornhuyse, Leyval, and Bonnin 2001;Gandolfi et al 2003) and sequencing data (Chen, Mathieu, et al 2018;Mateus et al 2022), although these predictions are sensitive to filtering and whether repeat regions are included or not (Auxier and Bazzicalupo 2019). In our study, we detected no was not certified by peer review) is the author/funder.…”

Rethinking asexuality: the enigmatic case of functional sexual genes inLepraria(Stereocaulaceae)

“…Much more common are cases such as the basidiomycete fungus Pseudozyma [16] and AMF Glomus [11], where genomes are found to contain complete and seemingly functional complements of core meiotic genes. Presence does not necessarily prove use in meiosis, but evidence for recombination has been found in AMF genera Glomus and Rhizophagus [81, 82].…”

Evolution of unexpected diversity in a putative mating type locus and its correlation with genome variability reveals likely asexuality in the model mycorrhizal fungus Rhizophagus irregularis

“…However, this was questioned by Auxier and Bazzicalupo [22] who suggested that these may be artefacts. A re-analysis of the data from Chen, et al [21] also detected a small number of potential recombination sites between nuclei [23]. Sperschneider, et al [24] conducted similar analyses with phased genome assemblies of dikaryon isolates and could not detect reciprocal recombination between co-existing nuclei.…”