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Resolving the haplotypes of arbuscular mycorrhizal fungi highlights the role of two nuclear populations in host interactions

View ORCID ProfileJana Sperschneider, View ORCID ProfileGokalp Yildirir, Yanina Rizzi, View ORCID ProfileMathu Malar C, Essam Sorwar, View ORCID ProfileEric CH Chen, View ORCID ProfileWataru Iwasaki, View ORCID ProfileElizabeth K. Brauer, Whynn Bosnich, View ORCID ProfileCaroline Gutjahr, View ORCID ProfileNicolas Corradi
doi: https://doi.org/10.1101/2023.01.15.524138
Jana Sperschneider
1Black Mountain Science and Innovation Park, CSIRO Agriculture and Food, Canberra, Australia
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Gokalp Yildirir
2Department of Biology, University of Ottawa, ON, Ottawa, K1N 6N5, Canada
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Yanina Rizzi
3Plant Genetics, TUM School of Life Sciences, Technical University of Munich (TUM), Emil Ramann Str. 4, 85354 Freising, Germany
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Mathu Malar C
2Department of Biology, University of Ottawa, ON, Ottawa, K1N 6N5, Canada
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Essam Sorwar
2Department of Biology, University of Ottawa, ON, Ottawa, K1N 6N5, Canada
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Eric CH Chen
4The University of Tokyo, Department of Integrated Biosciences, Graduate School of Frontier Sciences, Agriculture and Agri-Food Canada, Ottawa, ON, Canada
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Wataru Iwasaki
4The University of Tokyo, Department of Integrated Biosciences, Graduate School of Frontier Sciences, Agriculture and Agri-Food Canada, Ottawa, ON, Canada
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Elizabeth K. Brauer
2Department of Biology, University of Ottawa, ON, Ottawa, K1N 6N5, Canada
5Ottawa Research and Development Centre, Agriculture and Agri-Food Canada, Ottawa, ON, Canada
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Whynn Bosnich
5Ottawa Research and Development Centre, Agriculture and Agri-Food Canada, Ottawa, ON, Canada
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Caroline Gutjahr
3Plant Genetics, TUM School of Life Sciences, Technical University of Munich (TUM), Emil Ramann Str. 4, 85354 Freising, Germany
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Nicolas Corradi
2Department of Biology, University of Ottawa, ON, Ottawa, K1N 6N5, Canada
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  • ORCID record for Nicolas Corradi
  • For correspondence: ncorradi@uottawa.ca
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Abstract

Arbuscular mycorrhizal fungi (AMF) are prominent root symbionts with a multinucleate cytoplasm that can carry thousands of nuclei deriving from two parental strains and varying in relative abundance in a large syncytium. Here, we set out to improve our understanding of such remarkable genetics by resolving the nuclear genomes of all publicly available AMF heterokaryons using PacBio HiFi and Hi-C sequencing. We find that all AMF heterokaryons carry two sets of homologous chromosomes, where genes associated with plant colonization reside in gene-sparse, repeat-rich compartments. The co-existing nuclear genomes are phylogenetically related but differ significantly in content and epigenetics, resulting in nucleus-specific regulatory programs during mycorrhizal interactions. AMF heterokaryons carry signatures of past genetic exchange indicative of sexual reproduction, followed by clonal haplotype evolution. This work uncovers the contribution and origin of nuclear genomes present in AMF heterokaryons and opens avenues for improvement and environmental application of these strains.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • - RNA-seq data and analyses from two additional plants (whole plants) - Analyses of intra-haplotype diversity - Two authors were added

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted February 17, 2023.
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Resolving the haplotypes of arbuscular mycorrhizal fungi highlights the role of two nuclear populations in host interactions
Jana Sperschneider, Gokalp Yildirir, Yanina Rizzi, Mathu Malar C, Essam Sorwar, Eric CH Chen, Wataru Iwasaki, Elizabeth K. Brauer, Whynn Bosnich, Caroline Gutjahr, Nicolas Corradi
bioRxiv 2023.01.15.524138; doi: https://doi.org/10.1101/2023.01.15.524138
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Resolving the haplotypes of arbuscular mycorrhizal fungi highlights the role of two nuclear populations in host interactions
Jana Sperschneider, Gokalp Yildirir, Yanina Rizzi, Mathu Malar C, Essam Sorwar, Eric CH Chen, Wataru Iwasaki, Elizabeth K. Brauer, Whynn Bosnich, Caroline Gutjahr, Nicolas Corradi
bioRxiv 2023.01.15.524138; doi: https://doi.org/10.1101/2023.01.15.524138

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