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Enemy release after introduction of disease-resistant genotypes into plant-pathogen systems.

ABSTRACT: Predicting the magnitude of enemy release in host-pathogen systems after introduction of novel disease resistance genes has become a central problem in ecology. Here, we develop a general quantitative framework for predicting changes in realized niche size and intrinsic population growth rate after introgression of disease resistance genes into wild host populations. We then apply this framework to a model host-pathogen system targeted by genetically modified and conventionally bred disease-resistant host lines (Trifolium repens lines expressing resistance to Clover yellow vein potyvirus) and show that, under a range of ecologically realistic conditions, the introduction of novel pathogen resistance genes into host populations can pose a quantifiable risk to associated nontarget native plant communities. In the host-pathogen system studied, we predict that pathogen release could result in an increase in the intrinsic rate of population growth of up to 15% and the expansion of host populations into some marginal environments. This approach has general applicability to the ecological risk assessment of all novel disease-resistant plant genotypes that target coevolutionary host-pathogen systems for improvement of agricultural productivity.

SUBMITTER: Godfree RC

PROVIDER: S-EPMC1815254 | biostudies-literature | 2007 Feb

REPOSITORIES: biostudies-literature

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Enemy release after introduction of disease-resistant genotypes into plant-pathogen systems.

Godfree Robert C RC Thrall Peter H PH Young Andrew G AG

Proceedings of the National Academy of Sciences of the United States of America 20070213 8

Predicting the magnitude of enemy release in host-pathogen systems after introduction of novel disease resistance genes has become a central problem in ecology. Here, we develop a general quantitative framework for predicting changes in realized niche size and intrinsic population growth rate after introgression of disease resistance genes into wild host populations. We then apply this framework to a model host-pathogen system targeted by genetically modified and conventionally bred disease-resi ...[more]

PMID: 17299054

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Project description:The enemy release hypothesis is often cited as a potential explanation for the success of introduced plants; yet, empirical evidence for enemy release is mixed. We aimed to quantify changes in herbivory and defense in introduced plants while controlling for three factors that might have confounded past studies: using a wide native range for comparison with the introduced range, measuring defense traits without determining whether they affect herbivore preferences, and not considering the effect of time since introduction. The first hypothesis we tested was that introduced plants will have evolved lower levels of plant defense compared to their source population. We grew South African (source) and Australian (introduced) beach daisies (Arctotheca populifolia) in a common-environment glasshouse experiment and measured seven defense traits. Introduced plants had more ash, alkaloids, and leaf hairs than source plants, but were also less tough, with a lower C:N ratio and less phenolics. Overall, we found no difference in defense between source and introduced plants. To determine whether the feeding habits of herbivores align with changes in defense traits, we conducted preference feeding trials using five different herbivore species. Herbivores showed no overall preference for leaves from either group. The second hypothesis we tested was that herbivory on introduced plant species will increase through time after introduction to a new range. We recorded leaf damage on herbarium specimens of seven species introduced to eastern Australia and three native control species. We found no change in the overall level of herbivory experienced by introduced plants since arriving in Australia.ConclusionIn the field of invasion ecology, we need to rethink the paradigm that species introduced to a new range undergo simple decreases in defenses against herbivores. Instead, plants are likely to employ a range of defense traits that evolve in both coordinated and opposing ways in response to a plethora of different biotic and abiotic selective pressures.

Project description:Within the landscape of globally distributed pathogens, populations differentiate via both adaptive and nonadaptive forces. Individual populations are likely to show unique trends of genetic diversity, host-pathogen interaction, and ecological adaptation. In plant pathogens, allopatric divergence may occur particularly rapidly within simplified agricultural monoculture landscapes. As such, the study of plant pathogen populations in monocultures can highlight the distinct evolutionary mechanisms that lead to local genetic differentiation. Xylella fastidiosa is a plant pathogen known to infect and damage multiple monocultures worldwide. One subspecies, Xylella fastidiosa subsp. fastidiosa, was first introduced to the United States ∼150 years ago, where it was found to infect and cause disease in grapevines (Pierce's disease of grapevines, or PD). Here, we studied PD-causing subsp. fastidiosa populations, with an emphasis on those found in the United States. Our study shows that following their establishment in the United States, PD-causing strains likely split into populations on the East and West Coasts. This diversification has occurred via both changes in gene content (gene gain/loss events) and variations in nucleotide sequence (mutation and recombination). In addition, we reinforce the notion that PD-causing populations within the United States acted as the source for subsequent subsp. fastidiosa outbreaks in Europe and Asia.IMPORTANCE Compared to natural environments, the reduced diversity of monoculture agricultural landscapes can lead bacterial plant pathogens to quickly adapt to local biological and ecological conditions. Because of this, accidental introductions of microbial pathogens into naive regions represents a significant economic and environmental threat. Xylella fastidiosa is a plant pathogen with an expanding host and geographic range due to multiple intra- and intercontinental introductions. X. fastidiosa subsp. fastidiosa infects and causes disease in grapevines (Pierce's disease of grapevines [PD]). This study focused on PD-causing X. fastidiosa populations, particularly those found in the United States but also invasions into Taiwan and Spain. The analysis shows that PD-causing X. fastidiosa has diversified via multiple cooccurring evolutionary forces acting at an intra- and interpopulation level. This analysis enables a better understanding of the mechanisms leading to the local adaptation of X. fastidiosa and how a plant pathogen diverges allopatrically after multiple and sequential introduction events.

Dataset Information

Enemy release after introduction of disease-resistant genotypes into plant-pathogen systems.

Publications

Enemy release after introduction of disease-resistant genotypes into plant-pathogen systems.

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