Abstract
Wheat, one of the most important food crops, is threatened by a blast disease pandemic. Here, we show that a clonal lineage of the wheat blast fungus recently spread to Asia and Africa following two independent introductions from South America. Through a combination of genome analyses and laboratory experiments, we show that the decade-old blast pandemic lineage can be controlled by the Rmg8 disease resistance gene and is sensitive to strobilurin fungicides. However, we also highlight the potential of the pandemic clone to evolve fungicide-insensitive variants and sexually recombine with African lineages. This underscores the urgent need for genomic surveillance to track and mitigate the spread of wheat blast outside of South America and to guide preemptive wheat breeding for blast resistance.
Original language | English |
---|---|
Article number | e3002052 |
Journal | PLoS Biology |
Volume | 21 |
Issue number | 4 |
DOIs | |
Publication status | Published - 11 Apr 2023 |
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In: PLoS Biology, Vol. 21, No. 4, e3002052, 11.04.2023.
Research output: Contribution to journal › Article › peer-review
TY - JOUR
T1 - Genomic surveillance uncovers a pandemic clonal lineage of the wheat blast fungus
AU - Latorre, Sergio M.
AU - Were, Vincent M.
AU - Foster, Andrew J.
AU - Langner, Thorsten
AU - Malmgren, Angus
AU - Harant, Adeline
AU - Asuke, Soichiro
AU - Reyes-Avila, Sarai
AU - Gupta, Dipali Rani
AU - Jensen, Cassandra
AU - Ma, Weibin
AU - Mahmud, Nur Uddin
AU - Mehebub, Md Shåbab
AU - Mulenga, Rabson M.
AU - Muzahid, Abu Naim Md
AU - Paul, Sanjoy Kumar
AU - Rabby, S. M.Fajle
AU - Al Mahbub Rahat, Abdullah
AU - Ryder, Lauren
AU - Shrestha, Ram-Krishna
AU - Sichilima, Suwilanji
AU - Soanes, Darren M.
AU - Singh, Pawan Kumar
AU - Bentley, Alison R.
AU - Saunders, Diane G. O.
AU - Tosa, Yukio
AU - Croll, Daniel
AU - Lamour, Kurt H.
AU - Islam, Tofazzal
AU - Tembo, Batiseba
AU - Win, Joe
AU - Talbot, Nicholas J.
AU - Burbano, Hernán A.
AU - Kamoun, Sophien
N1 - Data Availability Statement: Genotyping and whole-genome sequencing data included in this article were released without restrictions as soon as they were produced through the OpenWheatBlast Community (https://zenodo.org/communities/openwheatblast). OpenWheatBlast collects research output datasets on wheat blast and encourages scientists to analyze and share them before formal publication. We list below the preprints that were shared through the OpenWheatBlast community and whose data were analyzed in this publication: - J. P. Ascari, et al. 2021. Multiplex amplicon sequencing dataset for genotyping the wheat blast fungus from the Minas Gerais state of Brazil. https://doi.org/10.5281/zenodo.4737375 - D. Croll. 2021. Whole-genome analyses of 286 Magnaporthe oryzae genomes suggest that an independent introduction of a global pandemic lineage is at the origin of the Zambia wheat blast outbreak. https://doi.org/10.5281/zenodo.4655959 - C. Jensen, et al. 2019. Rmg8 confers resistance to the Bangladeshi lineage of the wheat blast fungus. https://doi.org/10.5281/zenodo.2574196 - S. M. Latorre, et al. 2022. A curated set of mating-type assignment for the blast fungus (Magnaporthales). https://doi.org/10.5281/zenodo.6369833 - S. M. Latorre & H. A. Burbano. 2021. The emergence of wheat blast in Zambia and Bangladesh was caused by the same genetic lineage of Magnaporthe oryzae. https://doi.org/10.5281/zenodo.4619405 - B. Tembo, et al. 2021. Whole genome shotgun sequences of Magnaporthe oryzae wheat blast isolates from Zambia. https://doi.org/10.5281/zenodo.4637175 - B. Tembo, et al. 2021. Multiplex amplicon sequencing dataset for genotyping pandemic populations of the wheat blast fungus. https://doi.org/10.5281/zenodo.4605959 - V. Were, et al. 2021. Genome sequences of sixty Magnaporthe oryzae isolates from multiple host plant species. https://doi.org/10.5281/zenodo.4627043 - J. Win, et al. 2021. A pandemic clonal lineage of the wheat blast fungus. https://doi.org/10.5281/zenodo.4618522 The datasets and scripts generated during and/or analyzed during the current study are available in the Github repository: https://github.com/Burbano-Lab/wheat-clonal-linage under the DOI: https://doi.org/10.5281/zenodo.7590238. Funding information: This study was supported by the UK Biological Sciences Research Council (BBSRC) grants BBS/E/J/000PR9795 to SK and NJT, BBS/E/J/000PR9796 to NJT, BBS/E/J/000PR9798 to SK and NJT, BB/P023339/1 to NJT, BB/W008157/1 to SK, BB/W008300/1 to HAB, BB/R01356X/1 equipment grant to University College London, the Gatsby Charitable Foundation (https://www.gatsby.org.uk/) to SK and NJT, The Krishi Gobeshona Foundation (KGF) of Bangladesh grants KGF TF50-C/17 and TF 92-FNS/21 to TI, The Leverhulme Trust (Philip Leverhulme Prize) to HAB, Royal Society RSWF\R1\191011 to HAB, and European Research Council BLASTOFF grant 743165 to SK. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Copyright: © 2023 Latorre et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
PY - 2023/4/11
Y1 - 2023/4/11
N2 - Wheat, one of the most important food crops, is threatened by a blast disease pandemic. Here, we show that a clonal lineage of the wheat blast fungus recently spread to Asia and Africa following two independent introductions from South America. Through a combination of genome analyses and laboratory experiments, we show that the decade-old blast pandemic lineage can be controlled by the Rmg8 disease resistance gene and is sensitive to strobilurin fungicides. However, we also highlight the potential of the pandemic clone to evolve fungicide-insensitive variants and sexually recombine with African lineages. This underscores the urgent need for genomic surveillance to track and mitigate the spread of wheat blast outside of South America and to guide preemptive wheat breeding for blast resistance.
AB - Wheat, one of the most important food crops, is threatened by a blast disease pandemic. Here, we show that a clonal lineage of the wheat blast fungus recently spread to Asia and Africa following two independent introductions from South America. Through a combination of genome analyses and laboratory experiments, we show that the decade-old blast pandemic lineage can be controlled by the Rmg8 disease resistance gene and is sensitive to strobilurin fungicides. However, we also highlight the potential of the pandemic clone to evolve fungicide-insensitive variants and sexually recombine with African lineages. This underscores the urgent need for genomic surveillance to track and mitigate the spread of wheat blast outside of South America and to guide preemptive wheat breeding for blast resistance.
UR - http://www.scopus.com/inward/record.url?scp=85152244424&partnerID=8YFLogxK
U2 - 10.1371/journal.pbio.3002052
DO - 10.1371/journal.pbio.3002052
M3 - Article
C2 - 37040332
AN - SCOPUS:85152244424
SN - 1544-9173
VL - 21
JO - PLoS Biology
JF - PLoS Biology
IS - 4
M1 - e3002052
ER -