Abstract
Plant disease resistance (R) genes confer race-specific resistance to pathogens and are genetically defined on the basis of intra-specific functional polymorphism. Little is known about the evolutionary mechanisms that generate this polymorphism. Most R loci examined to date contain alternate alleles and/or linked homologs even in disease-susceptible plant genotypes. In contrast, the resistance to Pseudomonas syringae pathovar maculicola (RPM1) bacterial resistance gene is completely absent (rpm1-null) in 5/5 Arabidopsis thaliana accessions that lack RPM1 function. The rpm1-null locus contains a 98-bp segment of unknown origin in place of the RPM1 gene. We undertook comparative mapping of RPM1 and flanking genes in Brassica napus to determine the ancestral state of the RPM1 locus. We cloned two B. napus RPM1 homologs encoding hypothetical proteins with approximately 81% amino acid identity to Arabidopsis RPM1. Collinearity of genes flanking RPM1 is conserved between B. napus and Arabidopsis. Surprisingly, we found four additional B. napus loci in which the flanking marker synteny is maintained but RPM1 is absent. These B. napus rpm1-null loci have no detectable nucleotide similarity to the Arabidopsis rpm1-null allele. We conclude that RPM1 evolved before the divergence of the Brassicaceae and has been deleted independently in the Brassica and Arabidopsis lineages. These results suggest that functional polymorphism at R gene loci can arise from gene deletions.
MeSH Terms
Alleles
Amino Acid Sequence
Arabidopsis/genetics,microbiology
Arabidopsis Proteins
Base Sequence
Biological Evolution
Brassica/genetics,microbiology
Cloning, Molecular
Consensus Sequence
Genes, Plant
Genetic Linkage
Genotype
Immunity, Innate/genetics
Molecular Sequence Data
Plant Proteins/biosynthesis,chemistry,genetics
Polymorphism, Genetic
Pseudomonas/pathogenicity
Recombinant Proteins/biosynthesis,chemistry
Sequence Alignment
Sequence Homology, Amino Acid
Sequence Homology, Nucleic Acid
Chemicals
Arabidopsis Proteins
Plant Proteins
RPM1 protein, Arabidopsis
Recombinant Proteins
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Grant M R
Department of Biological Sciences, Wye College, Wye, Ashford, TN, USA.
McDowell J M
Sharpe A G
de Torres Zabala M
Lydiate D J
Dangl J L
References (28)
28 references, click to expand
-
The C/EBP family of transcription factors.
Immunobiology. 1995 Jul;193(2-4):171-85
PMID: 8530141
-
A disease resistance gene in Arabidopsis with specificity for two different pathogen avirulence genes.
Plant Cell. 1994 Jul;6(7):927-33
PMID: 8069104
-
Frequent nonreciprocal translocations in the amphidiploid genome of oilseed rape (Brassica napus).
Genome. 1995 Dec;38(6):1112-21
PMID: 18470235
-
Alleles of Pto and Fen occur in bacterial speck-susceptible and fenthion-insensitive tomato cultivars and encode active protein kinases.
Plant Cell. 1997 Jan;9(1):61-73
PMID: 9014365
-
A member of the tomato Pto gene family confers sensitivity to fenthion resulting in rapid cell death.
Plant Cell. 1994 Nov;6(11):1543-52
PMID: 7827490
-
Death Don't Have No Mercy: Cell Death Programs in Plant-Microbe Interactions.
Plant Cell. 1996 Oct;8(10):1793-1807
PMID: 12239362
-
Somatic excision of the Mu1 transposable element of maize.
Nucleic Acids Res. 1991 Feb 11;19(3):579-84
PMID: 1849263
-
Rapid reorganization of resistance gene homologues in cereal genomes.
Proc Natl Acad Sci U S A. 1998 Jan 6;95(1):370-5
PMID: 9419382
-
Identification and molecular mapping of a single Arabidopsis thaliana locus determining resistance to a phytopathogenic Pseudomonas syringae isolate.
Plant J. 1991 Nov;1(3):289-302
PMID: 21736648
-
The I2C family from the wilt disease resistance locus I2 belongs to the nucleotide binding, leucine-rich repeat superfamily of plant resistance genes.
Plant Cell. 1997 Apr;9(4):521-32
PMID: 9144960
-
Molecular genetics of plant disease resistance.
Science. 1995 May 5;268(5211):661-7
PMID: 7732374
-
Contrasting complexity of two rust resistance loci in flax.
Proc Natl Acad Sci U S A. 1995 May 9;92(10):4185-8
PMID: 11607543
-
Identification of a disease resistance locus in Arabidopsis that is functionally homologous to the RPG1 locus of soybean.
Plant J. 1993 Nov;4(5):813-20
PMID: 8275100
-
Novel disease resistance specificities result from sequence exchange between tandemly repeated genes at the Cf-4/9 locus of tomato.
Cell. 1997 Dec 12;91(6):821-32
PMID: 9413991
-
The avrRpm1 gene of Pseudomonas syringae pv. maculicola is required for virulence on Arabidopsis.
Mol Plant Microbe Interact. 1995 May-Jun;8(3):444-53
PMID: 7655064
-
Structure and evolution of the rp1 complex conferring rust resistance in maize.
Annu Rev Phytopathol. 1997;35:293-310
PMID: 15012525
-
Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance.
Science. 1995 Aug 11;269(5225):843-6
PMID: 7638602
-
The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1 receptors with N and L6.
Plant Cell. 1997 Jun;9(6):879-94
PMID: 9212464
-
Identification of the A and C genomes of amphidiploid Brassica napus (oilseed rape).
Genome. 1995 Dec;38(6):1122-31
PMID: 18470236
-
Conserved structure and function of the Arabidopsis flowering time gene CONSTANS in Brassica napus.
Plant Mol Biol. 1998 Jul;37(5):763-72
PMID: 9678571
-
Filler DNA is associated with spontaneous deletions in maize.
Proc Natl Acad Sci U S A. 1990 Nov;87(22):8731-5
PMID: 2247441
-
Comparative genome mapping in Brassica.
Genetics. 1996 Dec;144(4):1903-10
PMID: 8978073
-
Disease Lesion Mimicry Caused by Mutations in the Rust Resistance Gene rp1.
Plant Cell. 1996 Aug;8(8):1367-1376
PMID: 12239417
-
Inactivation of the flax rust resistance gene M associated with loss of a repeated unit within the leucine-rich repeat coding region.
Plant Cell. 1997 Apr;9(4):641-51
PMID: 9144966
-
Collinearity between a 30-centimorgan segment of Arabidopsis thaliana chromosome 4 and duplicated regions within the Brassica napus genome.
Genome. 1998 Feb;41(1):62-9
PMID: 9549059
-
Gene-for-gene complementarity in plant-pathogen interactions.
Annu Rev Genet. 1990;24:447-63
PMID: 2088175
-
The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor.
Cell. 1994 Sep 23;78(6):1101-15
PMID: 7923359
-
Structure and function of proteins controlling strain-specific pathogen resistance in plants.
Curr Opin Plant Biol. 1998 Aug;1(4):288-93
PMID: 10066601