Trends in Genetics
Volume 22, Issue 12, December 2006, Pages 662-670
Journal home page for Trends in Genetics

Review
Molecular evolution of plant immune system genes

https://doi.org/10.1016/j.tig.2006.09.011Get rights and content

Molecular population genetic studies are providing new perspectives on the evolution of genes that confer resistance to pathogens and herbivores. Here, we compare the evolutionary history of different components of the defense response (detection, signaling and response) and of genes with parallel function in plants and Drosophila. A review of the literature indicates that the dominant form of selection acting on defense genes (balancing, positive and purifying) differs among components of defense. Sampling of particular classes of genes and genes from non-model organisms, however, remains limited. Future studies combining molecular evolutionary analyses with ecological genetic and functional analyses should better reveal how natural selection has shaped defense gene evolution.

Introduction

Herbivores and pathogens can have strong effects on plant fitness, regulate plant population sizes, and cause considerable economic damage in managed ecosystems [1]. Understanding the evolution of defense-related traits, including a diverse array of morphological structures, physiological responses, secondary metabolites, RNAs and proteins, provides insight into the role of herbivore- and pathogen-imposed selection on plants. This information could help to guide the development of durably resistant crop varieties and more sustainable pest management strategies.

Our knowledge of the evolution of plant defense traits comes primarily from ecological genetic investigations, which examine the process of natural selection and the genetic architecture of traits in contemporary populations. Whereas ecological genetic approaches provide insight into short-term evolution, molecular population genetics (see Glossary) provides a means for examining the long-term evolution of genes that contribute to defense and other ecologically important traits 2, 3 (Box 1). Although these approaches are most often taken in isolation from one another, recent work has highlighted the potential for integrating molecular and field studies to understand the role of natural selection in defense gene evolution.

Here we review recent studies that have characterized the evolutionary history of plant defense genes. Because the interpretation of molecular evolutionary analyses is strengthened by knowledge of gene function, most studies have focused on components of defense that are genetically best characterized. In particular, analyses have focused on genes involved in pathogen detection and the initiation of a defense response, and genes encoding protein-based defenses that are part of that response, primarily from Arabidopsis thaliana and close relatives of maize (Box 2). In an effort to identify broad patterns in immune system evolution, we take a comparative approach to reviewing past studies. In particular, we compare the evolution of defense-related genes that differ in putative function, and also compare the evolutionary histories of plant defense genes with genes having parallel functions in Drosophila.

Section snippets

Detection genes

The vast majority of plant proteins involved in detection are encoded by NBS-LRR (nucleotide binding site-leucine rich repeat) resistance genes (R-genes), most of which are members of large multigene families [4]. Analyses of the rate at which nonsynonymous and synonymous mutations accumulate (dN/dS; Box 3) in R-gene family members have revealed evidence for positive selection having driven their divergence in all taxa for which tests have been conducted, including A. thaliana [5], Lactuca

Intracellular signaling genes

In both plants and insects, pathogen detection leads to the initiation of a signal cascade that culminates in a defense response (Box 2). Several plant genes involved in these cascades have been identified [33], but none has been subject to molecular evolutionary analysis. Interestingly, some insect defense signaling genes show strong evidence of having evolved in response to positive selection. For example, elevated levels of amino acid fixation relative to polymorphism in the D. simulans

Genes encoding proteins that inhibit pathogen and herbivore growth

The other major class of plant defense genes that have been subject to molecular evolutionary analyses are those encoding proteins that can directly inhibit enemy growth and fitness. To date, inter-specific divergence of chitinases in Arabis [37] and Poaceae taxa [38], β-1,3-endoglucanases in Glycine and a set of other dicots [39], and polygalacturonase inhibitor proteins (PGIPs) among legumes [40] and other dicots [41] have been investigated. These analyses have used codon-specific tests of

Other defense-related genes

Although little studied by molecular population geneticists, many defenses are products of biochemical pathways – secondary metabolites – that are either preformed or induced following infection or attack. One exception involves glucosinolate biosynthesis and hydrolysis genes in the Brassicaceae. A major quantitative trait locus (QTL) for glucosinolate production lies within the GS-Elong region, which contains MAM1, MAM2 and MAM-L [55]. Nucleotide polymorphism in one biosynthesis-related gene,

Conclusions and future prospects

Recent molecular evolutionary analyses have been used to characterize the evolutionary processes that shape nucleotide variation in genes involved in protecting plants against herbivores and pathogens. These analyses reveal apparently diverse selective histories including rapidly evolving protein-based defenses (e.g. chitinases), ancient polymorphisms maintained by selection (e.g. RPS2) and genes in which only purifying selection has operated. Although the number of molecular population genetic

Acknowledgements

We thank L.E. Rose, B.S. Gaut, B. Lazzaro and three anonymous reviewers for comments and suggestions that greatly improved this review. We also acknowledge the US National Science Foundation (DEB 0235027 to P.T.) for financial support.

Glossary

Balancing selection
A form of natural selection that maintains genetic variation at an individual locus. Unlike positive selection, balancing selection increases levels of nucleotide variation at linked sites. A variety of mechanisms can result in elevated levels of polymorphism including over-dominance (heterozygote advantage), frequency-dependent selection, and temporally or spatially variable selection.
Ecological genetics
A branch of evolutionary biology focused on understanding the process of

References (84)

  • J. Bergelson

    Evolutionary dynamics of plant R-genes

    Science

    (2001)
  • B.C. Meyers

    Receptor-like genes in the major resistance locus of lettuce are subject to divergent selection

    Plant Cell

    (1998)
  • P.N. Dodds

    Genetic analysis and evolution of plant disease resistance genes

  • G.-L. Wang

    Xa21D encodes a receptor-like molecule with a leucine rich repeat domain that determines race-specific recognition and is subject to adaptive evolution

    Plant Cell

    (1998)
  • B.C. Couch

    Pervasive purifying selection characterizes the evolution of I2 homologues

    Mol. Plant Microbe Interact.

    (2006)
  • M. Mondragon-Palomino

    Patterns of positive selection in the complete NBS-LRR gene family of Arabidopsis thaliana

    Genome Res.

    (2002)
  • E.A. Stahl

    Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis

    Nature

    (1999)
  • A.L. Caicedo

    Diversity and molecular evolution of the Rps2 resistance gene in Arabidopsis thaliana

    Proc. Natl. Acad. Sci. U. S. A.

    (1999)
  • R. Mauricio

    Natural selection for polymorphism in the disease resistance gene Rps2 of Arabidopsis

    Genetics

    (2003)
  • D. Tian

    Signature of balancing selection in Arabidopsis

    Proc. Natl. Acad. Sci. U. S. A.

    (2002)
  • J. Shen

    Unique evolutionary mechanism in R-genes under the presence/absence polymorphism in Arabidopsis thaliana

    Genetics

    (2006)
  • L.E. Rose

    The maintenance of extreme amino acid diversity at the disease resistance gene, RPP13, in Arabidopsis thaliana

    Genetics

    (2004)
  • A.L. Caicedo et al.

    Heterogeneous evolutionary processes affect R gene diversity in natural populations of Solanum pimpinellifolium

    Proc. Natl. Acad. Sci. U. S. A.

    (2004)
  • D. Tian

    Pleiotropic cost of R-gene mediated resistance in Arabidopsis thaliana

    Nature

    (2003)
  • P.N. Dodds

    Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes

    Proc. Natl. Acad. Sci. U. S. A.

    (2006)
  • E. Richly

    Mode of amplification and reorganization of resistance genes during recent Arabidopsis thaliana evolution

    Mol. Biol. Evol.

    (2002)
  • M. Mondragon-Palomino et al.

    Gene conversion and the evolution of three leucine-rich repeat gene families in Arabidopsis thaliana

    Mol. Biol. Evol.

    (2005)
  • J.B.S. Haldane

    Disease and evolution

    Ric. Sci. Suppl. A.

    (1949)
  • M. Salathe

    Neutral drift and polymorphism in gene-for-gene systems

    Ecol. Lett.

    (2005)
  • P.H. Thrall et al.

    Evolution of gene-for-gene systems in metapopulations: the effect of spatial scale of host and pathogen dispersal

    Plant Pathol.

    (2002)
  • V. Leclerc et al.

    The immune response of Drosophila melanogaster

    Immunol. Rev.

    (2004)
  • F.M. Jiggins et al.

    The evolution of parasite recognition genes in the innate immune system: purifying selection on Drosophila melanogaster peptidoglycan recognition proteins

    J. Mol. Evol.

    (2003)
  • T.A. Schlenke et al.

    Natural selection drives Drosophila immune system evolution

    Genetics

    (2003)
  • T.A. Schlenke et al.

    Linkage disequilibrium and recent selection at three immunity receptor loci in Drosophila simulans

    Genetics

    (2005)
  • Z. Nimchuk

    Recognition and response in the plant immune system

    Annu. Rev. Genet.

    (2003)
  • D.J. Begun et al.

    Adaptive evolution of relish, a Drosophila NF-κB/IκB protein

    Genetics

    (2000)
  • M.S. Bulmer et al.

    Variation in positive selection in termite GNBPs and Relish

    Mol. Biol. Evol.

    (2006)
  • M.B. Mudgett

    New insights to the function of phytopathogenic bacterial type III effectors in plants

    Annu. Rev. Plant Biol.

    (2005)
  • J.G. Bishop

    Rapid evolution in plant chitinases: molecular targets of selection in plant-pathogen coevolution

    Proc. Natl. Acad. Sci. U. S. A.

    (2000)
  • P. Tiffin

    Comparative evolutionary histories of chitinase genes in the genus Zea and the family Poaceae

    Genetics

    (2004)
  • J.G. Bishop

    Selection on glycine β-1,3-endoglucanase genes differentially inhibited by a Phytophthora glucanase inhibitor protein

    Genetics

    (2005)
  • J.G. Bishop

    Directed mutagenesis confirms the functional importance of positively selected sites in polygalacturonase inhibitor protein

    Mol. Biol. Evol.

    (2005)
  • Cited by (104)

    • Antioxidant peptides from plants: a review

      2024, Phytochemistry Reviews
    View all citing articles on Scopus
    View full text