Evidence for the sexual origin of heterokaryosis in arbuscular mycorrhizal fungi

Ropars, Jeanne; Toro, Kinga Sędzielewska; Noël, Jessica; Pelin, Adrian; Charron, Philippe; Farinelli, Laurent; Marton, Timea; Krüger, Manuela; Fuchs, Jörg; Brachmann, Andreas; Corradi, Nicolas

doi:10.1038/nmicrobiol.2016.33

Cited by 156 publications

(324 citation statements)

References 65 publications

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“…Previous studies have proposed that the heterokaryosity in AMF species drives variable genetic combinations of mycelia 68 . Recent genomic studies, furthermore, discovered signatures of sexual reproduction within the dikaryon-like stage 16,69 . Our hypothesis does not exclude current theories for the genetic and phenotypic plasticity of AMF species (heterokaryosis and sexual reproduction) but proposes a multilayered diversification mechanism leading to their widespread distribution.…”

Section: Resultsmentioning

confidence: 99%

“…Genomic data have been provided for Rhizophagus irregularis DAOM-181602 (=DOAM-197198) 12–14 , Gigaspora rosea 12 , Rhizophagus clarus 15 , and other isolates of R. irregularis 14,16 . These studies revealed potential host-dependent biological pathways 12,17 and candidate genes for plant infection and sexual reproduction 15,16,17 . However, fragmented genome sequences limit the ability to analyze repetitive structures and to distinguish between orthologous and paralogous genes 14 .…”

Section: Introductionmentioning

confidence: 99%

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Evidence of non-tandemly repeated rDNAs and their intragenomic heterogeneity in Rhizophagus irregularis

et al. 2018

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Arbuscular mycorrhizal fungus (AMF) species are some of the most widespread symbionts of land plants. Our much improved reference genome assembly of a model AMF, Rhizophagus irregularis DAOM-181602 (total contigs = 210), facilitated a discovery of repetitive elements with unusual characteristics. R. irregularis has only ten or 11 copies of complete 45S rDNAs, whereas the general eukaryotic genome has tens to thousands of rDNA copies. R. irregularis rDNAs are highly heterogeneous and lack a tandem repeat structure. These findings provide evidence for the hypothesis that rDNA heterogeneity depends on the lack of tandem repeat structures. RNA-Seq analysis confirmed that all rDNA variants are actively transcribed. Observed rDNA/rRNA polymorphisms may modulate translation by using different ribosomes depending on biotic and abiotic interactions. The non-tandem repeat structure and intragenomic heterogeneity of AMF rDNA/rRNA may facilitate successful adaptation to various environmental conditions, increasing host compatibility of these symbiotic fungi.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Evidence of non-tandemly repeated rDNAs and their intragenomic heterogeneity in Rhizophagus irregularis

et al. 2018

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“…Sexual reproduction is unknown but supported by genome evidence (Ropars et al 2016). Asexually formed chlamydospore-like spores are borne terminally, laterally, or intercalary on specialized hyphae.…”

Section: Taxonomymentioning

confidence: 99%

A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data

et al. 2016

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Zygomycete fungi were classified as a single phylum, Zygomycota, based on sexual reproduction by zygospores, frequent asexual reproduction by sporangia, absence of multicellular sporocarps, and production of coenocytic hyphae, all with some exceptions. Molecular phylogenies based on one or a few genes did not support the monophyly of the phylum, however, and the phylum was subsequently abandoned. Here we present phylogenetic analyses of a genome-scale data set for 46 taxa, including 25 zygomycetes and 192 proteins, and we demonstrate that zygomycetes comprise two major clades that form a paraphyletic grade. A formal phylogenetic classification is proposed herein and includes two phyla, six subphyla, four classes and 16 orders. On the basis of these results, the phyla Mucoromycota and Zoopagomycota are circumscribed. Zoopagomycota comprises Entomophtoromycotina, Kickxellomycotina and Zoopagomycotina; it constitutes the earliest diverging lineage of zygomycetes and contains species that are primarily parasites and pathogens of small animals (e.g. amoeba, insects, etc.) and other fungi, i.e. mycoparasites. Mucoromycota comprises Glomeromycotina, Mortierellomycotina, and Mucoromycotina and is sister to Dikarya. It is the more derived clade of zygomycetes and mainly consists of mycorrhizal fungi, root endophytes, and decomposers of plant material. Evolution of trophic modes, morphology, and analysis of genome-scale data are discussed.

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“…(Halary et al, 2011), suggesting that sexual reproduction in AMF could be possible. A putative multi-allelic mating-type locus, containing genes with structural and evolutionary similarity with mating-type loci of other taxa, was found in the genomes of five isolates of R. irregulare (Ropars et al, 2016). Additional studies should be carried out in order to investigate whether anastomosis between different AMF genotypes may prelude parasexual cycle or sexual recombination, and thus affect their reproductive success.…”

Section: Asymbiotic Myceliummentioning

confidence: 99%

Compatibility and incompatibility in hyphal anastomosis of arbuscular mycorrhizal fungi

Novais

Pepe

Siqueira

et al. 2017

Sci. agric. (Piracicaba, Braz.)

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Arbuscular mycorrhizal fungi (AMF), which live in symbiosis with 80 % of plants, are not able to grow when separated from their hosts. Spore germination is not host-regulated and germling growth is shortly arrested in the absence of host roots. Germling survival chances may be increased by hyphal fusions (anastomoses), which allow access to nutrients flowing in the extraradical mycelium (ERM). Perfect anastomoses, occurring with high frequency among germlings and the ERM of the same isolate, show protoplasm continuity and disappearance of hyphal walls. A low frequency of perfect fusions has been detected among co-specific genetically different isolates, although fungal nuclei have been consistently detected in all perfect fusions, suggesting active nuclear migration. When plants of different taxa establish symbioses with the same AMF species, anastomoses between ERM spreading from single root systems establish a common mycelium, which is an essential element to plant nutrition and communication. The interaction among mycelia produced by different isolates may also lead to pre-fusion incompatibility which hinders anastomosis formation, or to incompatibility after fusion, which separates the hyphal compartments. Results reported here, obtained by analyses of hyphal compatibility/ incompatibility in AMF, suggest that anastomosis formation and establishment of protoplasm flow, fundamental to the maintenance of mycelial physiological and genetic continuity, may affect the fitness of these ecologically important biotrophic fungi.

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Evidence for the sexual origin of heterokaryosis in arbuscular mycorrhizal fungi

Cited by 156 publications

References 65 publications

Evidence of non-tandemly repeated rDNAs and their intragenomic heterogeneity in Rhizophagus irregularis

Evidence of non-tandemly repeated rDNAs and their intragenomic heterogeneity in Rhizophagus irregularis

A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data

Compatibility and incompatibility in hyphal anastomosis of arbuscular mycorrhizal fungi

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