Population Genomics of <i>Macrophomina</i> spp. Reveals Cryptic Host Specialization and Evidence for Meiotic Recombination

Knowledge of the factors structuring populations of pathogenic fungi is fundamental to disease management efforts and basic biology. However, this crucial information is missing for many important pathogens, including broad-host-range and drought-associated pathogens from the globally distributed <i>Macrophomina</i> genus. The objectives of this work were to evaluate the evidence for host specialization, geographic adaptation, and recombination using a global survey of <i>Macrophomina</i> isolates from diverse geographic, temporal, and host sources. We obtained high-quality short-read sequence data for 463 <i>Macrophomina</i> spp. isolates, representing four putative species, collected from 91 host plant species and soil in 23 countries. Analysis of bi-allelic, single-nucleotide polymorphisms revealed high diversity, admixture, and equal mating type ratios, suggesting ongoing recombination. Although most tested isolates asymptomatically colonized strawberry, only strawberry-derived isolates caused disease on this host. These isolates were all in a single lineage, suggesting that the ability to cause disease on strawberry is not widespread among <i>M. phaseolina</i>. Significant associations were also found between isolations from soybean plants and specific population clusters, suggesting that specialization for virulence or reproduction has also occurred for soybean. Geography × isolate genotype associations were weak, suggesting that <i>Macrophomina</i> spp. were frequently trafficked between regions. Reference-free whole-genome comparisons support current boundaries among four <i>Macrophomina</i> species, and new molecular markers were designed to specifically identify each species. Contrary to expectations, <i>M. phaseolina</i> should be considered a single species with both specialist and generalist populations in which meiosis can maintain genetic diversity. [Formula: see text] Copyright © 2025 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

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Journal
Molecular Plant-Microbe Interactions
Published
2025-01-01
DOI
https://doi.org/10.1094/mpmi-03-25-0032-r
Citations
2
Primary Topic
Plant Disease Management Techniques
Type
article
Field-Weighted Citation Impact
3.50
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article

Population Genomics of Macrophomina spp. Reveals Cryptic Host Specialization and Evidence for Meiotic Recombination

Glenn S. Cole, Eva H. Stukenbrock, José María Rosales Jaime, Gabriel O. Sacher et al.
2 citations
Molecular Plant-Microbe Interactions
Plant Disease Management Techniques
3.50
article

Population Genomics of Macrophomina spp. Reveals Cryptic Host Specialization and Evidence for Meiotic Recombination

Glenn S. Cole, Eva H. Stukenbrock, José María Rosales Jaime, Gabriel O. Sacher, Niloofar Vaghefi, Alexandre Reis Machado, Alemu Mengistu, J. Philipp Benz, Viviana Ortiz, C. Borrero, Dylan McFarlane, Martin I. Chilvers, Christine Jade Dilla-Ermita, Gustavo H. Goldman, Teresa E. Seijo, Apollo Gomez, Polly H. Goldman, Levente Kiss, José Ramos Muñoz, Kayla K. Pennerman, S.W. Mattner, Juan Carlos López‐Hernández, M. Gambardella, Steven J. Knapp, John C. Broome, Natália A. Peres, Kelly Ivors, Géssica Priscila Ramos, Horacio D. Lopez‐Nicora, Emile Gluck‐Thaler, Peter Montgomery Henry, M. Avilés, Frank N. Martin, Joseph M. Neal
article en
2 citations

Abstract

Knowledge of the factors structuring populations of pathogenic fungi is fundamental to disease management efforts and basic biology. However, this crucial information is missing for many important pathogens, including broad-host-range and drought-associated pathogens from the globally distributed <i>Macrophomina</i> genus. The objectives of this work were to evaluate the evidence for host specialization, geographic adaptation, and recombination using a global survey of <i>Macrophomina</i> isolates from diverse geographic, temporal, and host sources. We obtained high-quality short-read sequence data for 463 <i>Macrophomina</i> spp. isolates, representing four putative species, collected from 91 host plant species and soil in 23 countries. Analysis of bi-allelic, single-nucleotide polymorphisms revealed high diversity, admixture, and equal mating type ratios, suggesting ongoing recombination. Although most tested isolates asymptomatically colonized strawberry, only strawberry-derived isolates caused disease on this host. These isolates were all in a single lineage, suggesting that the ability to cause disease on strawberry is not widespread among <i>M. phaseolina</i>. Significant associations were also found between isolations from soybean plants and specific population clusters, suggesting that specialization for virulence or reproduction has also occurred for soybean. Geography × isolate genotype associations were weak, suggesting that <i>Macrophomina</i> spp. were frequently trafficked between regions. Reference-free whole-genome comparisons support current boundaries among four <i>Macrophomina</i> species, and new molecular markers were designed to specifically identify each species. Contrary to expectations, <i>M. phaseolina</i> should be considered a single species with both specialist and generalist populations in which meiosis can maintain genetic diversity. [Formula: see text] Copyright © 2025 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.

Molecular Plant-Microbe InteractionsVol. 38(6)
Pennsylvania State University (US), United States Department of Agriculture (US), University of Wisconsin–Madison (US), Pontificia Universidad Católica de Chile (CL), The University of Melbourne (AU), Universidade de São Paulo (BR), University of California, Santa Cruz (US), University of Southern Queensland (AU), La Trobe University (AU), Universidade Federal de Pernambuco (BR), Florida Gulf Coast University (US), Wisconsin Institutes for Discovery (US), Christian-Albrechts-Universität zu Kiel (DE), Michigan United (US), Driscoll Children's Hospital (US), Institute for Advanced Study (DE), Max Planck Institute for Evolutionary Biology (DE), Ecosystem Sciences (AU), The Ohio State University (US), Technical University of Munich (DE), Universidad de Sevilla (ES), University of California, Davis (US), Michigan State University (US)
Life in Land
Openalex Percentile: Top 8%
Plant Disease Management Techniques
3.50
DOIOpen Access PDFOpenAlex
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