Generation of unequal nuclear genotype proportions in <i>Rhizophagus irregularis</i> progeny causes allelic imbalance in gene transcription

Robbins, Chanz; Corella, Joaquim Cruz; Aletti, Consolée; Seiler, Réjane; Mateus, Ivan D.; Lee, Soon‐Jae; Masclaux, Frédéric G.; Sanders, Ian R.

doi:10.1111/nph.17530

Cited by 12 publications

(16 citation statements)

References 68 publications

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“…Because the traits that we examined affect fungal and plant performance, this work has immediate implications for understanding the links between AMF nuclear status and mycorrhizal ecology. As such, these findings lay a foundation for future work that examines functional differences between AMF homokaryons and dikaryons in plantae and within AMF populations, including gene expression ( Robbins et al, 2021 ). Lastly, the findings of this study have direct implications in efforts to produce efficient mycorrhizal fungal inocula.…”

Section: Discussionmentioning

confidence: 87%

Homo- and Dikaryons of the Arbuscular Mycorrhizal Fungus Rhizophagus irregularis Differ in Life History Strategy

et al. 2021

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Arbuscular mycorrhizal fungi (AMF) are obligate plant symbionts that have the potential to improve crop yield. These multinucleate organisms are either “homokaryotic” or “dikaryotic”. In AMF dikaryons, thousands of nuclei originating from two parental strains coexist in the same cytoplasm. In other fungi, homokaryotic and dikaryotic strains show distinct life history traits (LHTs), such as variation in growth rates and fitness. However, how such traits compare between dikaryons and homokaryons of AMF is unknown. To address this, we measured 20 LHT of four dikaryons and five homokaryons of the model fungus Rhizophagus irregularis across root organ cultures of three host plants (carrot, chicory, and tobacco). Our analyses show that dikaryons have clearly distinct life history strategies (LHSs) compared to homokaryons. In particular, spores of homokaryons germinate faster and to a higher proportion than dikaryons, whereas dikaryons grow significantly faster and create a more complex hyphal network irrespective of host plant species. Our study links AMF nuclear status with key LHT with possible implications for mycorrhizal symbiotic functioning.

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Section: Discussionmentioning

confidence: 87%

Homo- and Dikaryons of the Arbuscular Mycorrhizal Fungus Rhizophagus irregularis Differ in Life History Strategy

et al. 2021

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“…Theoretically, if a nuclear genotype has decreased fitness, it could still be sustained within the mycelium at lower counts. If transcription is proportional to the quantity of nuclear genotype ( Robbins et al, 2021 ), then those less abundant nuclei could have less or no influence on the phenotype, until the environment changes in their favour ( Zhang et al, 2019 ).…”

Section: Nuclear Genotype Heterogeneity and Dynamicsmentioning

confidence: 99%

“…Regardless, it would be expected, in the absence of division of labour, that spore genotypes reflect NGH of the heterokaryon. However, nuclear transmission from heterokaryon to spores can be biassed toward a single nuclear genotype ( Meunier et al, 2018 ; Robbins et al, 2021 ). This implies that nuclear competition extends to sporulation and can lead to decreased fitness of germlings.…”

Section: The Role Of Nuclear Genotype Heterogeneity In Competition Co...mentioning

confidence: 99%

A Nuclei-Based Conceptual Model of (Eco)evolutionary Dynamics in Fungal Heterokaryons

Lakovic

Rillig

2022

Front. Microbiol.

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Filamentous fungi are characterised by specific features, such as multinuclearity, coexistence of genetically different nuclei and nuclear movement across the mycelial network. These attributes make them an interesting, yet rather underappreciated, system for studying (eco)evolutionary dynamics. This is especially noticeable among theoretical studies, where rather few consider nuclei and their role in (eco)evolutionary dynamics. To encourage such theoretical approaches, we here provide an overview of existing research on nuclear genotype heterogeneity (NGH) and its sources, such as mutations and vegetative non-self-fusion. We then discuss the resulting intra-mycelial nuclear dynamics and the potential consequences for fitness and adaptation. Finally, we formulate a nuclei-based conceptual framework, which considers three levels of selection: a single nucleus, a subpopulation of nuclei and the mycelium. We compare this framework to other concepts, for example those that consider only the mycelium as the level of selection, and outline the benefits of our approach for studying (eco)evolutionary dynamics. Our concept should serve as a baseline for modelling approaches, such as individual-based simulations, which will contribute greatly to our understanding of multilevel selection and (eco)evolutionary dynamics in filamentous fungi.

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“…A genetic bottleneck, where only 1 or 2 nuclei co-occur has never been detected in AMF. Despite the last feature, two studies that evaluated nuclear imbalance in dikaryon isolates show that nuclei ratio among single-spore lines are conserved despite multiple culturing for years [57] or are stable when exposed to different host plants [26]. These studies suggest that a nuclei regulation mechanism should exist and could be responsible of the stability of the nucleotypes in the dikaryons.…”

Section: Plos Onementioning

confidence: 99%

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

et al. 2022

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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.

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Generation of unequal nuclear genotype proportions in Rhizophagus irregularis progeny causes allelic imbalance in gene transcription

Abstract: Generation of disproportionate nuclear genotype proportions in Rhizophagus irregularis progeny causes allelic imbalance in gene transcription

Cited by 12 publications

References 68 publications

Homo- and Dikaryons of the Arbuscular Mycorrhizal Fungus Rhizophagus irregularis Differ in Life History Strategy

Homo- and Dikaryons of the Arbuscular Mycorrhizal Fungus Rhizophagus irregularis Differ in Life History Strategy

A Nuclei-Based Conceptual Model of (Eco)evolutionary Dynamics in Fungal Heterokaryons

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

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