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The arms race is ancient history in Arabidopsis, the wildflower

Key Points

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  • Progress in molecular genetic analyses of disease resistance in plants has been greatly influenced by research of plant associations with highly specialized biotrophic pathogens.

  • Natural variation in disease resistance is typically monogenic in both crops and wild species, most notably Arabidopsis thaliana.

  • Monogenic resistance usually involves concerted expression of multiple genes in a cascade of defence responses that couples receptor-like R genes with other defence-response genes that are functionally conserved or redundant among plant species.

  • Most R genes in plants encode receptor-like proteins, the largest structural class being characterized by a highly conserved nucleotide binding (NB) site and hyper-variable leucine rich repeat (LRR) domain.

  • Almost half of the 165 NB–LRR genes in Arabidopsis are located in one of thirteen clusters, the remaining genes residing in singlet or doublet loci. • The 'birth and death' model of R-gene evolution proposes that these genes have expanded within loci usually by unequal crossing-over between mispaired tandem copies, and have subsequently diverged as a result of further intragenic unequal crossing-over, point mutation, gene conversion and/or transposon insertion.

Abstract

Plant pathology was born after the nineteenth-century potato famine, and since then insightful genetic experiments have contributed to the great progress in our understanding of disease control. Our current view of plant resistance focuses on numerous polymorphic resistance loci, which contain genes known as R genes. The complete sequence of the Arabidopsis thaliana genome provides a framework for exploring the 'big bang' of R genes that occurred and how R genes evolved in plants from their associations with microorganisms, and for improving strategies for more sustainable deployment of disease resistance in crops.

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Figure 1: Phenotypes caused by downy mildew (Peronospora parasitica) in Arabidopsis.
Figure 2: Unrooted phylogenetic tree of nearly 150 NB–LRR genes in the Arabidopsis thaliana accession Columbia.
Figure 3: Map of NB–LRR gene clusters and of resistance genes in the Arabidopsis genome.
Figure 4: Physical structure of regions of Arabidopsis thaliana that contain clusters of NB–LRR genes.

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Acknowledgements

I am grateful for constructive reviews of the manuscript from four anonymous referees and helpful discussions from J. Dangl, J. Ellis, J. Jones, J. Burdon, M. Tör and D. Barbara. The author's work is supported largely by grants from the UK Biotechnology and Biological Sciences Research Council.

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Authors and Affiliations

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DATABASE LINKS

CF4

PTO

Xa21

CLAVATA1

ERECTA

APAF

RPM1

RPS2

RPS4

RPS5

RPP1

RPP5

RPP8

RPP13

avrRpt2

avrRps4

avrPphb

HRT

rpp8

RPP7

rpp13

RPP2

Cf4

Cf9

FURTHER INFORMATION

Phytophthera infestans

Resurgence of the Irish potato famine fungus

Functional and comparative genomics of R genes in plants at UC Davis

The Arabidopsis Information Resource

Nottingham Arabidopsis stock centre

AIMS: Arabidopsis Information Management System

Eric Holub's lab

Glossary

BIOTROPHIC

A type of parasite that derives its energy from the living cells of its host.

NECROTROPHIC

A type of parasite that derives its energy from dead cells that are part of a live host.

CLADE

An organismal lineage comprising an ancestor and all its descendants.

CULTIVAR

A cultivated variety (genetic strain) of a domesticated crop plant.

PATHOSYSTEM

An ecological subsystem defined by the phenomenon of parasitism. A plant pathosystem might include one or more host plant species along with the various parasites (insects, fungi, bacteria and so on) that use the hosts.

DICOTYLEDONS

Members of a subphylum of angiosperms that have two seed leaves (cotyledons) in the embryo.

STOMATA

Natural openings in the epidermis of a stem or leaf of a plant that are surrounded by specialized guard cells, and permit gas exchange with the air.

ACCESSION

A sample of a plant variety collected at a specific location and time.

MESOPHYLL

Leaf cells that lie beneath the outer epidermal cell layer.

PATHOVAR

Abbreviation for pathogen variety, a subspecific classification that indicates host origin and to some extent host specialization.

OOMYCETE

A phylum of filamentous eukaryotic microorganisms that, although fungal-like, are more closely related to yellow-green algae.

GENE CONVERSION

The non-reciprocal transfer of information between homologous genes as a consequence of heteroduplex formation, followed by repair of mismatches in the heteroduplexes.

PARALOGUE

Homologous genes that originated by gene duplication.

ORTHOLOGUE

Homologous genes that originated through speciation.

BALANCED POLYMORPHISM

Selective advantage of heterozygous individuals.

MICROEVOLUTION

Refers to small-scale changes that usually occur at the level of the species, and on short timescales.

FREQUENCY-DEPENDENT SELECTION

Describes the situation in which the selection pressure (in this case, imposed on the pathogen by different R genes alleles) varies with the proportion of individuals that carry a given allele or allelic combination in a population.

OUTCROSSING

(or outbreeding) Mating between unrelated individuals. Arabidopsis lyrata is self-incompatible and therefore breeds by crossing to other individuals in the species. By contrast, A. thaliana is self-compatible and therefore can self-pollinate.

ANGIOSPERMS

The phylum of flowering seed plants, including both dicotyledons and monocotyledons ( for example, grasses and cereals).

GYMNOSPERMS

Non-flowering seed plants (for example, pine).

MONOCOTYLEDONS

Angiosperms that have one seed leaf (cotyledon) in the embryo.

POLYPHYLETIC

Descended from different ancestors.

MACROEVOLUTION

Describes evolution that occurs at or above the level of species.

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Holub, E. The arms race is ancient history in Arabidopsis, the wildflower. Nat Rev Genet 2, 516–527 (2001). https://doi.org/10.1038/35080508

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