Multiple origins or widespread gene flow in agricultural fields? Regional population genomics of herbicide resistance in Bromus tectorum

Authors: RIBERIO, VICTOR - Oregon State University; Gallagher, Joseph; MALLORY-SMITH, CAROL - Oregon State University; BARROSO, JUDIT - Oregon State University; BRUNHARO, CAIO - Pennsylvania State University

Submitted to: Molecular Ecology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/28/2025
Publication Date: 5/8/2025
Citation: Riberio, V.H., Gallagher, J.P., Mallory-Smith, C., Barroso, J., Brunharo, C.A. 2025. Multiple origins or widespread gene flow in agricultural fields? Regional population genomics of herbicide resistance in Bromus tectorum. Molecular Ecology. 34(11). Article e17791. https://doi.org/10.1111/mec.17791.
DOI: https://doi.org/10.1111/mec.17791

Interpretive Summary: Bromus tectorum is a global weed that has successfully colonized a variety of habitats. In the United States Pacific Northwest, B. tectorum is a problematic weed in grass seed and dryland wheat production systems and has developed herbicide resistance to ALS inhibitor herbicides. Here, we asked how this herbicide resistance arose in populations collected from northeastern Oregon. We detected several target site mutations known to cause herbicide resistance in the ALS gene in these populations. However, these target site mutations were not associated with the genetic structure of populations within the region. This suggests these mutations were evolving independently in each of these populations. These populations also display long distance gene flow among populations, which may serve as another avenue for herbicide resistance to spread. This serves as an example of how herbicide resistance might repeatedly evolve in weed species.

Technical Abstract: The repeated evolution of herbicide resistance in agriculture provides an unprecedented opportunity to understand how organisms rapidly respond to strong anthropogenic-driven selection pressure. We recently identified agricultural populations of the grass species Bromus tectorum L. with resistance to multiple herbicides. To understand the evolutionary origins and spread of resistance, we investigated the resistance mechanisms to acetolactate synthase (ALS) inhibitors and photosystem II inhibitors, two widely used herbicide modes of action, in 49 B. tectorum populations. We assessed the genetic diversity, structure and relatedness in a subset of 21 populations. Resistance to ALS inhibitors was associated with multiple nonsynonymous mutations in ALS, the target site gene, despite the relatively small geographic region where populations originated, suggesting ALS inhibitor resistance evolution occurred multiple times in the region. We also found evidence that mechanisms not related to the target site evolved and were common in the populations studied. Resistance to photosystem II inhibitors was confirmed in two populations and was conferred by nonsynonymous mutations in the plastid gene psbA. Population genomics analyses suggested that ALS resistance in most populations, at the nucleotide level, spread via gene flow, except for one population where we found evidence that Pro-197-His mutations may have evolved in three separate events. Our results suggest that both gene flow via pollen and/or seed dispersal and multiple local evolutionary events were involved in the spread of herbicide-resistant B. tectorum. Our results provide an empirical example of the rapid repeated evolution of a trait under strong anthropogenic selection and elucidate the evolutionary origins of herbicide resistance in a plant species of agricultural importance.