Effector loss and gain drives host range at a fitness cost

Epidemic preparedness depends on tracking microbial evolution that drives shifts in ecological behaviors such as disease emergence. However, the genetic constraints mediating microbial emergence for generalist and specialist behaviors remain poorly described. Here, we addressed this question by combining comparative and functional genomics with phylogeny-based evolutionary analyses of the cereal pathogen Xanthomonas translucens. We show that a generalist X. translucens subgroup arose from a specialist ancestor, and the loss of a single effector gene, xopAL1, contributed to the generalist host expansion by promoting host jump from barley to wheat. Deleting barley-specialist X. translucens xopAL1 recapitulated the host jump to wheat and demonstrates risk across each globally distributed genetic lineage. However, this niche expansion via XopAL1 loss incurs a significant fitness cost to colonize barley. Moreover, the specialist lineage gained an additional effector gene, xopAJ, which enhanced virulence on barley while restricting oat infection, thereby reinforcing niche specialization. We further conducted transcriptomic analysis of wheat and determined that XopAL1 triggers a defense response that involves the reduction of photosynthetic processes. Our work provides an experimentally validated evolutionary framework to understand mechanisms of intergenera host jump. Overall, we demonstrate that single events of gene loss and gain shape ecological behaviors by creating a dynamic trade-off between niche breadth and specialization.

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Publication Details

Journal
PLoS Pathogens
Published
2026-08-03
DOI
https://doi.org/10.1371/journal.ppat.1014145
Primary Topic
Plant Pathogenic Bacteria Studies
Type
article
Field-Weighted Citation Impact
0.00

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article

Effector loss and gain drives host range at a fitness cost

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PLoS Pathogens
Plant Pathogenic Bacteria Studies
article

Effector loss and gain drives host range at a fitness cost

Muhammad Uzair, Jelmer W. Poelstra, Jules Butchacas, H. D. Lopez-Nicora, Verónica Román-Reyna, Jonathan M. Jacobs, Tracy E. Hawk, Emmanuelle Lauber, Laurent D. Noël, Rebecca D. Curland, Nathaniel Heiden, Marcus V. Merfa, Lillian Ebeling-Koning, Hannah Toth, E. J. Rodgers, Laurie Marsan, Zachary Konkel, Jason C. Slot, Ruth Dill-Macky, Godwin E. Oduokpaha, Zhaohui Liu, Temitope F. Oladele
article en

Abstract

Epidemic preparedness depends on tracking microbial evolution that drives shifts in ecological behaviors such as disease emergence. However, the genetic constraints mediating microbial emergence for generalist and specialist behaviors remain poorly described. Here, we addressed this question by combining comparative and functional genomics with phylogeny-based evolutionary analyses of the cereal pathogen Xanthomonas translucens. We show that a generalist X. translucens subgroup arose from a specialist ancestor, and the loss of a single effector gene, xopAL1, contributed to the generalist host expansion by promoting host jump from barley to wheat. Deleting barley-specialist X. translucens xopAL1 recapitulated the host jump to wheat and demonstrates risk across each globally distributed genetic lineage. However, this niche expansion via XopAL1 loss incurs a significant fitness cost to colonize barley. Moreover, the specialist lineage gained an additional effector gene, xopAJ, which enhanced virulence on barley while restricting oat infection, thereby reinforcing niche specialization. We further conducted transcriptomic analysis of wheat and determined that XopAL1 triggers a defense response that involves the reduction of photosynthetic processes. Our work provides an experimentally validated evolutionary framework to understand mechanisms of intergenera host jump. Overall, we demonstrate that single events of gene loss and gain shape ecological behaviors by creating a dynamic trade-off between niche breadth and specialization.

PLoS PathogensVol. 22(8)
Centre National de la Recherche Scientifique (FR), University of Minnesota (US), Université Fédérale de Toulouse Midi-Pyrénées (FR), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR), The Ohio State University (US), North Dakota State University (US), University of Tennessee at Knoxville (US)
Ohio State University, American Malting Barley Association, Université de Toulouse, Centre National de la Recherche Scientifique, Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement, National Institute of Food and Agriculture
Good health and well-being
Openalex Percentile: Top 11%
Plant Pathogenic Bacteria Studies
DOIOpen Access PDFOpenAlex
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