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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
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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.
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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].
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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.
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