Multiple horizontal mini-chromosome transfers drive genome evolution of clonal blast fungus lineages

Barragan, Ana Cristina, Latorre, Sergio M., Malmgren, Angus, Harant, Adeline, Win, Joe, Sugihara, Yu, Burbano, Hernán A., Kamoun, Sophien ORCID: https://orcid.org/0000-0002-0290-0315 and Langner, Thorsten (2024) Multiple horizontal mini-chromosome transfers drive genome evolution of clonal blast fungus lineages. Molecular Biology and Evolution, 41 (8). ISSN 0737-4038

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Abstract

Crop disease pandemics are often driven by asexually reproducing clonal lineages of plant pathogens that reproduce asexually. How these clonal pathogens continuously adapt to their hosts despite harboring limited genetic variation, and in absence of sexual recombination remains elusive. Here, we reveal multiple instances of horizontal chromosome transfer within pandemic clonal lineages of the blast fungus Magnaporthe (Syn. Pyricularia) oryzae. We identified a horizontally transferred 1.2Mb accessory mini-chromosome which is remarkably conserved between M. oryzae isolates from both the rice blast fungus lineage and the lineage infecting Indian goosegrass (Eleusine indica), a wild grass that often grows in the proximity of cultivated cereal crops. Furthermore, we show that this mini-chromosome was horizontally acquired by clonal rice blast isolates through at least nine distinct transfer events over the past three centuries. These findings establish horizontal mini-chromosome transfer as a mechanism facilitating genetic exchange among different host-associated blast fungus lineages. We propose that blast fungus populations infecting wild grasses act as genetic reservoirs that drive genome evolution of pandemic clonal lineages that afflict cereal crops.

Item Type: Article
Additional Information: Data Availability Statement: The authors confirm that all data underlying the findings are fully available without restriction. Files and code to perform the analyses described and to generate the plots presented are available as Supplementary Files, and in the git repositories: https://github.com/smlatorreo/mChr_Moryzae (Latorre 2024), https://github.com/CristinaBarragan/Barragan2024_mChr_Moryzae (Barragan 2024) and https://github.com/YuSugihara/Barragan_and_Latorre_et_al_2024 (Sugihara 2024). Sequencing reads were deposited in the European Nucleotide Archive (ENA) under study accession number PRJEB66235 (mini-chromosome sequences from Italian rice blast isolates) and PRJEB67435 (Br62- sequencing). In addition, the Br62 whole-genome assembly is available under GenBank accession number PRJEB66723. Funding Information: This project was supported by grants from the Gatsby Charitable Foundation, the UK Research and Innovation Biotechnology and Biological Sciences Research Council (UKRI-BBSRC) grants BBS/E/J/000PR9795, BBS/E/J/000P R979, BB/W002221/1, BB/W008300/1 and BB/R01356X/1 the European Research Council (ERC) advanced grant BLASTOFF 743165 (to SK) and ERC starting grant PANDEMIC 101077853 (to TL), the Royal Society grant RSWF\\R1\\191011 and a Philip Leverhulme Prize from The Leverhulme Trust (to HAB), the EPSRC Doctoral Training Partnerships (DTP), and a Walter Benjamin Postdoctoral Fellowship from the German Research Council (to ACB). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Uncontrolled Keywords: clonal blast fungus lineages,crop disease pandemics,genetic reservoirs,horizontal mini-chromosome transfer,wild hosts,ecology, evolution, behavior and systematics,molecular biology,genetics ,/dk/atira/pure/subjectarea/asjc/1100/1105
Faculty \ School: Faculty of Science > School of Biological Sciences
Faculty of Science > The Sainsbury Laboratory
UEA Research Groups: Faculty of Science > Research Groups > Plant Sciences
Related URLs:
Depositing User: LivePure Connector
Date Deposited: 23 Oct 2024 10:30
Last Modified: 17 Dec 2024 01:41
URI: https://ueaeprints.uea.ac.uk/id/eprint/97135
DOI: 10.1093/molbev/msae164

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