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pb34ov.qxd 06/20/2000 08:27 Page 273 273 Biotic interactions Genomics and coevolution Editorial overview Thomas Mitchell-Olds* and Joy Bergelson† Addresses *Department of Genetics and Evolution, Max Planck Institute of Chemical Ecology; Carl-Zeiss-Promenade 10, 07745 Jena, Germany; e-mail: [email protected] † Department of Ecology and Evolutionary Biology, University of Chicago, 1101 East 57th St, Chicago, Illinois 60637, USA Current Opinion in Plant Biology 2000, 3:273-277 1369-5266/00/$ - see front matter © 2000 Elsevier Science Ltd. All rights reserved. Abbreviations avr avirulence LRR leucine-rich repeat NBS nucleotide-binding site R resistance Introduction Biotic interactions such as symbiosis, herbivory, and disease have important impacts on plant ecology and evolution. The evolution of virulence and pesticide resistance by pathogens and insects provides continuing challenges in agriculture. Research using genomics and related technologies continues to improve our knowledge of the functional basis of plant defense. Nevertheless, public skepticism regarding biotechnology demands that we improve our understanding of naturally occurring genetic variation for yield, resistance, and fitness traits in agricultural and natural plant populations. Collaborations involving ecologists, evolutionary biologists, and molecular geneticists will be essential for understanding and manipulating biotic interactions among plants, pathogens, and insects. This issue reviews recent advances in understanding population and functional aspects of plant defense. Our editorial overview also highlights several topics that are not considered in the accompanying reviews. host and herbivore species can significantly impact each others’ evolution, even when interactions between them are diffuse. For example, Juenger and Bergelson [4] found that strong linear and nonlinear diffuse selection were imposed on scarlet gilia by three types of herbivores (i.e. seed flies, caterpillars and mammalian grazers). The distinction between pairwise and diffuse coevolution becomes more complex when genes involved in ‘gene-for-gene’ interactions are considered. Gene-forgene interactions are typified by plant resistance (R)-genes and microbial pathogens, but also are involved in rare examples of plant–insect interactions (e.g. wheat–hessian fly [5]). Gene-for-gene models assume [6] that single plant resistance genes interact specifically with single pathogen avirulence genes. It is now clear that a strict gene-for-gene model of coevolutionary interactions between one R-gene and one avirulence (avr)-gene is overly simplistic; a single avr-locus may recognize multiple R-genes, single R-genes can control resistance to several pest species, and tight genomic clustering of R-genes might influence the evolutionary dynamics of resistance [7,8] (see reviews by Ellis, Dodds and Pryor, pp 278–284; Young, pp 285–290; and White, Yang and Johnson, pp 291–298). More realistic models of plant–pathogen coevolution must incorporate a genomic perspective of R-gene dynamics, in which a number of R-genes can evolve resistance to a pathogen that has overcome a plant’s defenses. Under this ‘gene-forgenome’ hypothesis, it is the genome-wide dynamics of R-genes that modulate the resistance response, not simply allelic change at individual resistance genes. Resistance genes Coevolution Ehrlich and Raven [1] proposed that antagonistic chemical interactions between plants and herbivores have caused stepwise chemical coevolution between species, leading to the adaptive radiation of host plants and herbivorous insects. These historical interactions may be responsible for current patterns, in which related plant species have similar secondary chemistry, and closely related insect taxa choose similar host species. Recently, the concept of coevolution has been refined to distinguish between pairwise and diffuse coevolution [2]. Pairwise coevolution refers to a reciprocal stepwise ‘arms race’ between a host plant and an insect or pathogen species. Diffuse coevolution is more common, denoting interactions in which related pest species attack a range of plants that share similar chemical defenses. Although strictly pairwise coevolution may be rare [3], groups of related Recent studies of resistance genes have shown that NBS-LRR (nucleotide-binding site leucine-rich repeat) genes control the host plant recognition of many pathogen and pest species. Functional and evolutionary aspects of these resistance genes are discussed in several reviews in this issue (by Ellis, Dodds and Pryor; by Young; and by Stahl and Bishop, pp 299–304) and by Pan et al. [9]. One common observation is that R-gene loci within a cluster reveal evidence of diversifying selection. This pattern of selection is often interpreted as evidence of a rapid evolutionary change, such as that which occurs during an arms race [10–13]. Surprisingly, little evidence of diversifying selection has been found for R-genes that lie outside of R-gene clusters. For example, rather than revealing a dynamic arms race between host and pathogen, a molecular evolutionary analysis of Rpm1 [14] found that alleles at this locus have been maintained for pb34ov.qxd 06/20/2000 274 08:27 Page 274 Biotic interactions nearly 10 million years. Similar results have now been obtained for Rps5 (D Tian, J Bergelson, unpublished data) and Rps2 (R Mauricio, J Bergelson, unpublished data) in Arabidopsis, loci that are not found in R-gene clusters. Although these three examples of evolutionary stasis at R-gene loci appear to contradict the conclusions drawn from studies of R-gene clusters, it is important to realize that diversifying selection among R-gene loci is compatible with both the existence of an arms-race and with the maintenance of an ancient polymorphism. It will take a molecular population genetic study of R-genes located within clusters to determine whether these R-genes experience different evolutionary dynamics to those that are found in isolation. As some nucleotide polymorphisms may be several million years old [14,15], they may have been widely dispersed during Pleistocene migrations [16]. During historical migrations resistance alleles have experienced many ecological environments and may have interacted with a broader range of pathogens and avirulence genes than is known from laboratory studies. Analyses combining genomics and molecular ecology may elucidate the functional and historical influences of resistance mechanisms on molecular evolution. Likewise, molecular understanding should provide the basis for ecological and evolutionary studies of many plant–pest and plant–symbiont systems (see review by M Parniske, pp 320–328). Although NBS-LRR genes play a central role in disease resistance, toxins and chemical defenses are also important in plant–pathogen interactions [17,18]. For example, the Arabidopsis pad3 mutant is deficient in its production of camalexin, an indole-type phytoalexin. As a consequence, these plants are more susceptible to the fungal pathogen Alternaria brassicicola, but their resistance to Pseudomonas syringae, Peronospora parasitica, and Erysiphe orontii are unchanged [19]. Map-based cloning showed that PAD3 encodes a cytochrome P450 monooxygenase with similarity to other enzymes involved in indole-derived secondary metabolism [20]. Genomic approaches will continue to expand our understanding of plant defense genes that have been difficult to identify using biochemical methods. In the fungal pathogen Cochliobolus carbonum, the Tox2 locus produces HC toxin (cyclo[D-Pro-L-Ala-D-Ala-L-Aeo], where Aeo stands for 2-amino-9,10-epoxi-8-oxodecanoic acid), which inhibits histone diacetylases in many organisms. Most monocots produce a detoxification enzyme, HC-toxin reductase, encoded by one or a few Hm loci. In sorghum, rice, and other close relatives of maize, functional Hm loci cause durable nonhost resistance to this pathogen [21]. Some maize genotypes, however, lack functional Hm loci, causing susceptibility to southern corn leaf blight disease. In susceptible plants, Hm1 has been disrupted by a transposon insertion, leading to a gene-for-gene interaction between the Tox2 locus in the pathogen and the Hm1 host gene. Potentially durable nonhost resistance is widespread in nature and of great value in agriculture (see review by MC Heath, pp 315–319). Understanding the functional and evolutionary basis of such interactions is an important research goal. Macroevolution Molecular methods for inferring phylogenetic relationships provide powerful tools for studying macroevolutionary patterns of plant–insect interactions. DNA sequences are available from species whose divergence dates are known from the fossil record, hence rates of evolutionary change can be calibrated. Using such a molecular clock, one can estimate ages of adaptive radiations and changes in host plants. When phylogenetic trees are known from lineages of plant hosts and insect herbivores, researchers can infer the importance of host switching, co-speciation (i.e. simultaneous speciation of insects and their hosts), etc. With more than 350,000 species, beetles are the most diverse eukaryotic group. Curculionid and Chrysomelid beetles form a single clade that includes more than 135,000 species. Before the origin of flowering plants, the Jurassic ancestors of these beetles fed on conifers and cycads. Indeed, lineages of phytophagous beetles and their coniferous Araucaria host plants may have been continuously associated in a single location, now Argentina, for more than 200 million years. By estimating a phylogeny of the Curculionid and Chrysomelid beetles, Farrell [22] inferred that angiosperm feeding originated five times from ancestral conifer/cycad feeders. He also inferred that adaptive radiations (i.e. bursts of insect speciation on rapidly diversifying angiosperms) led to significantly greater beetle diversity on flowering plants than on the ancestral coniferous and cycad hosts. Thus, the vast diversity of beetle species is attributable to the adaptive radiations of these herbivorous insects on flowering plants, which has increased the diversity of Curculionid and Chrysomelid beetles by about 100,000 species. Detailed phylogenetic studies of host-switching, possible coevolution, and speciation have been conducted in several groups of herbivorous beetles and their host plants [23–25]. Ehrlich and Raven [1] have proposed that evolutionary shifts to new host species may be influenced by the similar chemistry of alternative host plants. Alternatively, parallel speciation or geographical proximity might also govern associations between related species of plants and insects. To test these alternative hypotheses, Becerra and Venable [26,27] examined the relative importance of plant terpenoid chemistry, phylogenetic relationships, and host biogeography in Blepharida beetles and their Bursera host plants in Mexico. Host-plant chemistry was more important than host-plant phylogeny or geographical range in influencing the evolution of this plant–insect interaction. Evolving species of Bursera hosts show independent convergent evolution of similar terpenoid chemistry, and insect-host switching is primarily determined by plant chemistry. pb34ov.qxd 06/20/2000 08:27 Page 275 Editorial overview Mitchell-Olds and Bergelson Another interesting application of a phylogenetic approach involves a study of mutualisms. An obligate mutualistic relationship exists between yucca plants and yucca moths, benefiting both partners. Adult yucca moths are the only pollinators of yucca flowers, hence they are essential for the reproduction of yucca plants. However, female moths lay their eggs within the yucca ovary, where developing larvae feed upon yucca seeds. Moth larvae must feed on yucca plants for survival and they reduce host-plant fitness by seed predation. Ecologists have been intrigued by the evolutionary stability of such obligate mutualistic interactions. In particular, theoretical predictions suggest that mutualisms might be evolutionarily unstable if ‘cheater’ moth genotypes arose that eat seeds without providing the pollination service [28]. Indeed, several nonpollinating yucca moth species are known. Recently, Pellmyr and Leebens-Mack [29] inferred a molecular phylogeny of yucca moth species, employing known molecular evolutionary rates to estimate the age of this mutualistic interaction. According to their phylogeny, moth lineages colonized yucca plants about 40 million years ago, and yucca pollination arose about 35 million years ago. Consequently, this complex mutualistic relationship has persisted for many millions of years. During the last one to three million years, cheater behavior has evolved independently at least twice, and has persisted for long evolutionary periods. Coexisting pollinators and cheaters are not closely related, supporting predictions that cheating is evolutionarily unstable within a single species [28]. 275 insect partners show genetically differentiated populations, with an imperfect correspondence of genotypes between Greya and the host plants. Genetic differentiation among plant populations shapes the patterns of host usage by Greya: the insects prefer plant genotypes from their local populations. Finally, the contribution of Greya to host pollination depends on the abundance of other pollinator species, which is geographically heterogeneous. Consequently, this Greya–plant interaction may vary among locations from mutualism (i.e. Greya pollination has an important role) to antagonism (i.e. seed predation outweighs pollination). Parker and Spoerke [33] sampled nitrogen-fixing Bradyrhizobium symbionts and their annual legume host, A. bracteata, from natural populations across a 1000 km area. They observed a positive correlation between the genetic divergence of the A. bracteata hosts and their symbionts: genetically similar plants had genetically similar bacteria, and vice versa. In this system, bacteria are acquired from adjacent soil rather than being transmitted from maternal to progeny plants. Despite this yearly mixing of host and symbiont, genetically similar plants from 1000 km apart had identical bacterial symbionts. Different genotypes of A. bracteata selectively acquire particular bacterial genotypes from the surrounding soil. In this system, certain plant–bacterial combinations may have a long history of coevolutionary interaction, with a relatively low rate of partner switching. Thus, unlike the Greya system described above, there appears to be sufficient migration to ensure that the local population structure does not drive the coevolutionary dynamics between A. bracteata and its Bradyrhizobium. Geographic variation Although species of plants, insects, and pathogens may have broad geographical ranges, restricted patterns of migration and gene flow may cause local interactions between plant and pest species to be geographically restricted. These geographical patterns may cause unique ecological and evolutionary dynamics at different locations [30,31], with outcomes very different from those predicted for large, homogeneous populations. To model coevolutionary interactions in natural populations, Thompson [3,32] proposed the ‘geographic mosaic’ hypothesis. This hypothesis entails three components: first, a selection mosaic among populations favoring different evolutionary interactions in different locations; second, reciprocal selection occurring in a subset of locations or coevolutionary hotspots; and third, gene flow among populations causing continual geographic mixing of coevolving traits. Consequently, the geographic mosaic hypothesis offers three ecological predictions: first, populations will differ for coevolving traits; second, interacting species will be well matched in some locations and mismatched (maladapted) in others; and third, coevolved traits will be uncommon at the species level. For plant–insect interactions, conformation to the geographic mosaic hypothesis is best documented for Lithophragma and Huechera host plants, which are pollinated and parasitized by Greya moths (reviewed in [32]). Both plant and Functional genomics Expression profiling quantifies levels of gene expression for hundreds or thousands of genes simultaneously, and provides important tools for investigating development, gene regulation, and many questions in evolutionary biology. Reymond et al. [34] studied expression levels of 150 genes in wild-type and mutant Arabidopsis leaves exposed to dehydration, mechanical wounding, or herbivory by Pieris cabbage butterflies. The genes were chosen on the basis of their known functionality in wound responses, disease resistance, or as constitutive controls. About 30% of these genes showed greater than twofold changes in gene expression in response to at least one of the three treatments. A number of wound- and insectinducible genes were also induced by water stress. Responses to wounding versus insect feeding were similar but not identical: several genes showed differential responses to these treatments. The coi1 mutant, which has a deficiency in its jasmonate response pathway, allowed identification of two categories of wound-inducible genes, that is, either dependent or independent of coi1. The imperfect correspondence between wound-, jasmonate-, and herbivory-induced genes complicates attempts to completely mimic responses to herbivory by application of jasmonates [35–37], which have extensive pleiotropic effects on growth and metabolism [38]. pb34ov.qxd 06/20/2000 276 08:27 Page 276 Biotic interactions We can anticipate additional studies in the near future that will examine cross-talk between responses to biotic and abiotic stress. These multivariate characterizations of gene expression in response to herbivory and disease will lead to a major challenge: elucidating the functional importance of thousands of differentially expressed genes. Natural selection can ‘fine-tune’ the expression and function of genes with very small effects on fitness. Although fitness differences of less than 0.1% are important for adaptation, such evolutionarily important effects are below the limit of resolution for experiments in functional genomics. Many gene knockouts without detectable phenotypic effects may belong to this category. Other reviews in this issue Studies in natural ecosystems have found that levels of susceptibility to insects and pathogens are genetically polymorphic in many plant species. To explain this genetic variation for ecologically important traits, researchers hypothesize that resistance may be costly, and genetic polymorphisms represent trade-offs between investing in growth or defense. Recent studies on costs of resistance are reviewed by Purrington (pp 305–308). Plant defenses occur within an ecological context that includes insect parasitoids and predators that attack herbivore species. These tri-trophic interactions in natural and agricultural populations are discussed by Agrawal (pp 329–335). In plant signal transduction, trade-offs may exist between pathogen and herbivore resistance (Felton and Korth, pp 309–314). There is increasing evidence that a clear dichotomy between herbivore- and pathogen-specific defense pathways may not exist. Herbivore–pathogen interactions also occur at the level of insect transmission of plant viruses (discussed by Power, pp 336–340). Throughout this issue, the importance of multidisciplinary approaches at the molecular, evolutionary, and ecological level is clear. Acknowledgements TMO was supported by the Max-Planck-Gesellschaft, the US National Science Foundation (NSF) (DEB-9527725), Bundesministerium für Bildung und Forschung, and the European Union. JB was supported by a NSF Presidential Award, a Packard Fellowship and the National Institute of Health. We thank M Clauss, D Kliebenstein, and J Kroymann for comments on the manuscript, and S Dix for expert secretarial assistance. References 1. 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