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Adaptive and maladaptive expression plasticity underlying herbicide resistance in an agricultural weed.

ABSTRACT: Plastic phenotypic responses to environmental change are common, yet we lack a clear understanding of the fitness consequences of these plastic responses. Here, we use the evolution of herbicide resistance in the common morning glory (Ipomoea purpurea) as a model for understanding the relative importance of adaptive and maladaptive gene expression responses to herbicide. Specifically, we compare leaf gene expression changes caused by herbicide to the expression changes that evolve in response to artificial selection for herbicide resistance. We identify a number of genes that show plastic and evolved responses to herbicide and find that for the majority of genes with both plastic and evolved responses, plastic responses appear to be adaptive. We also find that selection for herbicide response increases gene expression plasticity. Overall, these results show the importance of adaptive plasticity for herbicide resistance in a common weed and that expression changes in response to strong environmental change can be adaptive.

SUBMITTER: Josephs EB

PROVIDER: S-EPMC8327940 | biostudies-literature | 2021 Aug

REPOSITORIES: biostudies-literature

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Adaptive and maladaptive expression plasticity underlying herbicide resistance in an agricultural weed.

Josephs Emily B EB Van Etten Megan L ML Harkess Alex A Platts Adrian A Baucom Regina S RS

Evolution letters 20210614 4

Plastic phenotypic responses to environmental change are common, yet we lack a clear understanding of the fitness consequences of these plastic responses. Here, we use the evolution of herbicide resistance in the common morning glory (<i>Ipomoea purpurea</i>) as a model for understanding the relative importance of adaptive and maladaptive gene expression responses to herbicide. Specifically, we compare leaf gene expression changes caused by herbicide to the expression changes that evolve in resp ...[more]

PMID: 34367667

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Project description:BACKGROUND AND AIMS: Selective pressures exerted by agriculture on populations of arable weeds foster the evolution of adaptive traits. Germination and emergence dynamics and herbicide resistance are key adaptive traits. Herbicide resistance alleles can have pleiotropic effects on a weed's life cycle. This study investigated the pleiotropic effects of three acetyl-coenzyme A carboxylase (ACCase) alleles endowing herbicide resistance on the seed-to-plant part of the life cycle of the grass weed Alopecurus myosuroides. METHODS: In each of two series of experiments, A. myosuroides populations with homogenized genetic backgrounds and segregating for Leu1781, Asn2041 or Gly2078 ACCase mutations which arose independently were used to compare germination dynamics, survival in the soil and seedling pre-emergence growth among seeds containing wild-type, heterozygous and homozygous mutant ACCase embryos. KEY RESULTS: Asn2041 ACCase caused no significant effects. Gly2078 ACCase major effects were a co-dominant acceleration in seed germination (1·25- and 1·10-fold decrease in the time to reach 50 % germination (T50) for homozygous and heterozygous mutant embryos, respectively). Segregation distortion against homozygous mutant embryos or a co-dominant increase in fatal germination was observed in one series of experiments. Leu1781 ACCase major effects were a co-dominant delay in seed germination (1·41- and 1·22-fold increase in T50 for homozygous and heterozygous mutant embryos, respectively) associated with a substantial co-dominant decrease in fatal germination. CONCLUSIONS: Under current agricultural systems, plants carrying Leu1781 or Gly2078 ACCase have a fitness advantage conferred by herbicide resistance that is enhanced or counterbalanced, respectively, by direct pleiotropic effects on the plant phenology. Pleiotropic effects associated with mutations endowing herbicide resistance undoubtedly play a significant role in the evolutionary dynamics of herbicide resistance in weed populations. Mutant ACCase alleles should also prove useful to investigate the role played by seed storage lipids in the control of seed dormancy and germination.

Project description:Adaptive phenotypic plasticity may improve the response of individuals when faced with new environmental conditions. Typically, empirical evidence for plasticity is based on phenotypic reaction norms obtained in reciprocal transplant experiments. In such experiments, individuals from their native environment are transplanted into a different environment, and a number of trait values, potentially implicated in individuals' response to the new environment, are measured. However, the interpretations of reaction norms may differ depending on the nature of the assessed traits, which may not be known beforehand. For example, for traits that contribute to local adaptation, adaptive plasticity implies nonzero slopes of reaction norms. By contrast, for traits that are correlated to fitness, high tolerance to different environments (possibly due to adaptive plasticity in traits that contribute to adaptation) may, instead, result in flat reaction norms. Here we investigate reaction norms for adaptive versus fitness-correlated traits and how they may affect the conclusions regarding the contribution of plasticity. To this end, we first simulate range expansion along an environmental gradient where plasticity evolves to different values locally and then perform reciprocal transplant experiments in silico. We show that reaction norms alone cannot inform us whether the assessed trait exhibits locally adaptive, maladaptive, neutral, or no plasticity, without any additional knowledge of the traits assessed and species' biology. We use the insights from the model to analyse and interpret empirical data from reciprocal transplant experiments involving the marine isopod Idotea balthica sampled from two geographical locations with different salinities, concluding that the low-salinity population likely has reduced adaptive plasticity relative to the high-salinity population. Overall, we conclude that, when interpreting results from reciprocal transplant experiments, it is necessary to consider whether traits assessed are locally adaptive with respect to the environmental variable accounted for in the experiments or correlated to fitness.

Dataset Information

Adaptive and maladaptive expression plasticity underlying herbicide resistance in an agricultural weed.

Publications

Adaptive and maladaptive expression plasticity underlying herbicide resistance in an agricultural weed.

Similar Datasets

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