Abstract
BackgroundArbuscular mycorrhizal fungi (AMF) are members of the phylum Glomeromycota, an early divergent fungal lineage that forms symbiotic associations with the large majority of land plants. These organisms are asexual obligate biotrophs, meaning that they cannot complete their life cycle in the absence of a suitable host. These fungi can exchange genetic information through hyphal fusions (i.e. anastomosis) with genetically compatible isolates belonging to the same species. The occurrence of transient mitochondrial length-heteroplasmy through anastomosis between geographically distant Rhizophagus irregularis isolates was previously demonstrated in single spores resulting from crossing experiments. However, (1) the persistence of this phenomenon in monosporal culture lines from crossed parental isolates, (2) its correlation with nuclear exchanges and (3) the potential mechanisms responsible for mitochondrial inheritance are still unknown. Using the AMF model organism R. irregularis, we tested whether the presence of a heteroplasmic state in progeny spores was linked to the occurrence of nuclear exchanges and whether the previously observed heteroplasmic state persisted in monosporal in vitro crossed-culture lines. We also investigated the presence of a putative mitochondrial segregation apparatus in Glomeromycota by identifying proteins similar to those found in other fungal groups.ResultsWe observed the occurrence of biparental inheritance both for mitochondrial and nuclear markers tested in single spores obtained from crossed-isolates. However, only one parental mitochondrial DNA and nuclear genotype were recovered in each monosporal crossed-cultures, with an overrepresentation of certain mitochondrial haplotypes. These results strongly support the presence of a nuclear-independent mitochondrial segregation mechanism in R. irregularis. Furthermore, a nearly complete set of genes was identified with putative orthology to those found in other fungi and known to be associated with the mitochondrial segregation in Saccharomyces cerevisiae and filamentous fungi.ConclusionsOur findings suggest that mitochondrial segregation might take place either during spore formation or colony development and that it might be independent of the nuclear segregation machinery. We present the basic building blocks for a better understanding of the mitochondrial inheritance process and segregation in these important symbiotic fungi. The comprehension of these processes is of great importance since it has been shown that different segregated lines of the same isolate can have variable effects on the host plant.Electronic supplementary materialThe online version of this article (doi:10.1186/s12866-016-0627-5) contains supplementary material, which is available to authorized users.
Highlights
Arbuscular mycorrhizal fungi (AMF) are members of the phylum Glomeromycota, an early divergent fungal lineage that forms symbiotic associations with the large majority of land plants
The 34 monosporal crossed-culture lines genotyped by quantitative polymerase chain reaction (qPCR) approach presented only one parental mitochondrial DNA (mtDNA) haplotype
The Department of Agriculture (DAOM)-197198 haplotype dominated when it was combined with the DAOM234328 haplotype, the latter was not detected in any monosporal culture lines
Summary
Arbuscular mycorrhizal fungi (AMF) are members of the phylum Glomeromycota, an early divergent fungal lineage that forms symbiotic associations with the large majority of land plants These organisms are asexual obligate biotrophs, meaning that they cannot complete their life cycle in the absence of a suitable host. The benefits to plants provided by this association with AMF could be enhanced by the manipulation of the fungal partner genetics, as demonstrated by Angelard et al [5] and Colard et al [6], using the model organism Rhizophagus irregularis In both studies, through the exchange of nuclear genetic information via hyphal fusion, in vitro crossed-culture lines and segregated culture lines were generated. A previous study showed that AMF mtDNAs and nuclei migrate massively into spores during their formation [15], but the fate of each parental haplotype following crosses needs to be investigated
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