Trends in Genetics
ReviewMolecular evolution of plant immune system genes
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
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