Ribeiro Victor H V, Gallagher Joseph, Mallory-Smith Carol, Barroso Judit, Brunharo Caio A C G
Department of Crop and Soil Science, Oregon State University, Corvallis, Oregon, USA.
Research Molecular Biologist, Forage Seed and Cereal Research Unit, United States Department of Agriculture, Corvallis, Oregon, USA.
Mol Ecol. 2025 Jun;34(11):e17791. doi: 10.1111/mec.17791. Epub 2025 May 8.
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.
农业中除草剂抗性的反复进化为了解生物体如何快速响应强大的人为驱动选择压力提供了前所未有的机会。我们最近鉴定出了对多种除草剂具有抗性的禾本科植物野燕麦（Bromus tectorum L.）的农业种群。为了了解抗性的进化起源和传播，我们研究了49个野燕麦种群对乙酰乳酸合成酶（ALS）抑制剂和光系统II抑制剂这两种广泛使用的除草剂作用模式的抗性机制。我们评估了21个种群子集的遗传多样性、结构和相关性。尽管种群起源的地理区域相对较小，但对ALS抑制剂的抗性与靶标位点基因ALS中的多个非同义突变相关，这表明该区域多次发生了ALS抑制剂抗性进化。我们还发现有证据表明，与靶标位点无关的机制也在进化且在所研究的种群中很常见。在两个种群中证实了对光系统II抑制剂的抗性，其由质体基因psbA中的非同义突变赋予。种群基因组学分析表明，在核苷酸水平上，大多数种群中的ALS抗性是通过基因流传播的，除了一个种群，我们发现有证据表明Pro-197-His突变可能在三个独立事件中发生了进化。我们的结果表明，通过花粉和/或种子传播的基因流以及多个局部进化事件都参与了抗除草剂野燕麦的传播。我们的结果提供了一个在强大的人为选择下性状快速反复进化的实证例子，并阐明了一种具有农业重要性的植物物种中除草剂抗性的进化起源。
