Ecology and Evolution of the Grass-Endophyte Symbiosis
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Ecology and Evolution of the Grass-Endophyte Symbiosis
Introductory Statistics with R Peter Dalgaard. Principles of Neural Science Eric R. What a Plant Knows Daniel Chamovitz. The Big Picture Sean Carroll. The Way of the Cell Franklin M. How the Mind Works Steven Pinker. Anatomy of Exercise for Women Lisa Purcell. Horse Anatomy Peter C. Introducing Mind and Brain Angus Gellatly. Why We Run Bernd Heinrich. Animal Locomotion Sheila Patek. Functional Morphology Johannes W. At intermediate level of host genetic variability, we predict that endophyte-infected plants would have higher fitness than noninfected ones due to the mutualism Fig.
Thus, in this zone, plant fitness regardless the infection status and mutualism effectiveness both increase with genetic distance between parents. The vertical transmission efficiency would also be sensitive to the compatibility and host level of heterosis; however, it would be less sensitive compared to relative fitness to the compatibility Fig. But it is also possible to predict a reduction in the mutualism effectiveness with high transmission efficiency.
This could be due to the increase in plant fitness associated with heterosis i. However, although compatibility has started to fall, transmission efficiency remains high. In this specific zone, a vertically transmitted microorganism like the endophyte could behave as a free-rider, because the fitness of the host is highest in self-incompatible species Denison et al. Finally, at high levels of host genetic variability, endophyte-infected plants would present equal or lower fitness than noninfected ones for two reasons: Out-breeding depressed plants and inter-specific hybrids have diminished biomass and seed production Jauhar ; Ellstrand and Schierenbeck Essentially, the very low genetic specificity of inter-specific hybrids would prevent the expression of the endophyte positive effects on plant fitness.
Our theoretical model allows for testable hypotheses on the genetic bases of the endophyte-grass symbiosis at population level. To understand the genetic controls of the interaction between Neotyphodium endophytes and host grasses, we need to separate the effects of the genetic variability as a whole, from those specific genes controlling the compatibility.
The positive relationship between genetic variability and host fitness can be accompanied by an enhanced probability of encountering incompatible genes between the host and the fungus.
Following these directions, experiments could be designed to test the different sources of genetic variability on the symbiosis performance. The screening of populations varying in the frequency of endophyte infection could be used as a way to find variability in the time-span of local coevolution between the host plant and the fungal endophyte.
Thus, we could manipulate the genetic background in host populations by performing reciprocal crosses to evaluate the mutualism effectiveness and the genetic specificity. The difference in the response of these two processes to genetic variability may be used to understand the existing discrepancies around the prevalence of this mutualism in nature. The model considers the compatibility and the effectiveness of mutualism as processes that are not independent but can respond differently to the maintenance of sexual reproduction in the host plants.
This is important in the light of the apparent lack of positive effects of endophytes in certain systems, focusing on factors that might reduce compatibility rather than mutualism effectiveness Faeth and Sullivan ; Saikkonen et al. Genetic specificity is expected to arise as a basic condition for the functioning of the mutualistic interaction; but it cannot be interpreted as an evolved adaptation when studying mutualism effectiveness Kiers et al. Previous studies have concluded that multiple genetic determinants are involved in the level of compatibility between the fungal endophyte and the host plant Chung et al.
Nonetheless, data are needed to support that endophytes would be adapted to benefit from the common sources of genetic variability without potential for conflict in genetic specificity.
Undoubtedly, the evolutionary stability and ubiquity of the endophyte-grass symbiosis should depend simultaneously on the capacity of endophytes to be effective, to tolerate rapid genetic changes in host plant populations, including the genetic changes in the same host plant after pollination, and to reproduce and spread efficiently through host seeds.
Although human interventions can aim at a specific target, unwanted secondary results are not rare, particularly when high-order interactions are neglected Thrall et al. The symbiosis would increase the initial frequency of resistant alleles and hence increasing the rate of host plant evolution toward herbicide resistance. Alternatively, this effect could be counterbalanced by reducing the herbicide selection pressure due to an enhanced survival in susceptible endophyte-infected plants.
These two pathways are likely to work simultaneously depending on the ecological scenario. The increase in genetic variability may also be acquired if the impact of endophytes in reducing mortality under herbicide selection also affects gene flow with related species. However, this could confer higher herbicide resistance reducing genetic specificity. Thus, the host would survive but the mutualism would become extinct. It was found that annual ryegrass populations that evolved resistant to diclofop-methyl in Australia were endophyte free, but other resistant populations from Argentina had high rates of endophyte infection Vila-Aiub et al.
Annual ryegrass resistant populations from Italy were related to both, gene introgressions from related Festuca species and spontaneous mutations Dinelli et al. Therefore, if resistance was acquired through gene flow from other species, our model would predict symbiosis extinction; this may explain why some resistant populations retain high endophyte infection levels i.
In the context of climate global change, sustainable management of natural and agricultural systems requires knowledge of the adaptive mechanisms and evolutionary trajectories of plants and associated organisms Thrall et al. As has been shown throughout the article, the interaction between leaf Neotyphodium fungal endophyte and cool-season grasses often challenges both the theoretical and the experimental evidence. The permanent and potential negative effects of gene flow on the compatibility were invoked to predict the unlikely development of Neotyphodium endophyte associations with annual plants Saikkonen et al.
However, Lolium multiflorum and Lolium rigidum are annual ryegrasses grasses with high levels of endophyte infection and genetic heterogeneity in diverse ecosystems worldwide Balfourier et al. Thus, it is possible to expect lower levels of specificity for annual or allogamous than for perennial or autogamous host plant species. We are aware of the speculative character of our model; nonetheless it is proposed as a provisory stepping stone to inform urgently needed well-designed experiments to address the evolutionary and agronomic questions associated with this fascinating system. The symbiosis between Neotyphodium endophyte fungi and cool-season grasses is a useful model system in ecology and evolution, and it is a challenge for the management of agricultural systems.
Here, we present a general framework to interpret the underlying mechanisms and processes that regulate evolutionary stability of hereditary symbioses, taking into account that the interaction of endophytes has usually evolved in naturally allogamous host species for which hybridization is the rule. Based only on life history traits of both partners, our model applies equally to vertically transmitted endophytes housed in allogamous plant species, leaving without sense the controversy concerning the use of the term mutualism for wild or agronomic grasses.
We incorporate a theoretical relationship between heterosis and plant fitness, and we offer perspectives for the mutualism effectiveness, the compatibility between both partners, and the efficiency of endophyte vertical transmission with respect to genetic distance among host parent plants. Theory and a few empirical studies support our predictions, but there are still more questions than answers.
Gregory P. Cheplick and Stanley Faeth
From this evolutionary perspective, the endophyte-grass symbiosis can be considered as an integrated entity able to face the environmental heterogeneity in space and time. Finally, we predict that natural selection and coevolution favor generalist rather than specialist endophytes. High plasticity to environmental and genetic changes in host populations together with the high adaptation to the apoplastic medium of the host plants Easton ; Christensen et al.
We are especially grateful to M. Three anonymous reviewers provided insightful comments that helped to improve the content and organization of the manuscript. Since endophytes are exclusively vertically transmitted and they can be lost in different stages of the host life cycle Fig. The specificity between the host plant and the fungal endophyte i. While genetic specificity and mutualism effectiveness are not completely independent, they could be not collinear Kiers et al. National Center for Biotechnology Information , U.
Journal List Evol Appl v. Published online Aug Received Jul 2; Accepted Jul 9. This article has been cited by other articles in PMC. Introduction Evolutionary perspectives have contributed to agriculture, for example, by providing elements to understand crop adaptation to low-input production systems and trade-offs between different plant traits Sadras and Denison Evolutionary perspective for understanding the symbiosis between Neotyphodium endophytes and cool-season grasses Life history traits of both partners and sources of genetic variability Many mutualistic interactions are thought to derive from antagonistic relationships where coevolution has extended the ecological niche of both partners Douglas ; Herre et al.
Open in a separate window. A model of the Neotyphodium endophyte-grass symbiosis as integrated entity Our model, presented in Fig.
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- Introduction.
Hybridization as fitness stimulus for evolution. Future challenges Our theoretical model allows for testable hypotheses on the genetic bases of the endophyte-grass symbiosis at population level. Conclusions The symbiosis between Neotyphodium endophyte fungi and cool-season grasses is a useful model system in ecology and evolution, and it is a challenge for the management of agricultural systems. Acknowledgments We are especially grateful to M. Glossary Endophyte transmission efficiency: Vertically transmitted fungal endophytes: Armbruster P, Reed DH.
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A fungus among us: