Recombination between diverged clusters of the tomato Cf-9 plant disease resistance gene family.

The tomato Cf-4 and Cf-9 genes are the founder members of a large gene family of homologues of Cladosporium fulvum resistance gene Cf-9 (Hcr9 genes), several of which confer resistance against C. fulvum through recognition of different pathogen-encoded avirulence determinants. Three loci of tandemly repeated Hcr9 genes-Southern Cross (SC), Milky Way (MW), and Northern Lights (NL)-are located on the short arm of tomato chromosome 1. Comparisons between 2 SC-Hcr9s, 11 from MW, and 5 from NL implicated sequence exchange between gene family members in their evolution. The extent to which novel variants can be generated by recombination depends on the degree of sequence polymorphism available within the gene family. Here we show that physical separation of Hcr9 genes can be associated with elevated sequence divergence. Two diverged subclasses of Hcr9s could be defined. These are physically separated from each other, with members of one class exclusively residing at Northern Lights. One exceptional Hcr9 at Northern Lights carried sequence features specific for Hcr9s at other loci, suggesting a recent transfer of this gene by an interlocus recombination event. As members of diverged subclasses are brought into physical vicinity within a tandem repeat, a larger spectrum of sequence variants can potentially be generated by subsequent interhomologue sequence exchange.

[1]  J. D. Jones,et al.  Homologues of the Cf-9 disease resistance gene (Hcr9s) are present at multiple loci on the short arm of tomato chromosome 1. , 1999, Molecular plant-microbe interactions : MPMI.

[2]  S. Goff,et al.  Intragenic Recombination and Diversifying Selection Contribute to the Evolution of Downy Mildew Resistance at the RPP8 Locus of Arabidopsis , 1998, Plant Cell.

[3]  P. Rohani,et al.  Receptor-like Genes in the Major Resistance Locus of Lettuce Are Subject to Divergent Selection , 1998, Plant Cell.

[4]  R. Michelmore,et al.  The Major Resistance Gene Cluster in Lettuce Is Highly Duplicated and Spans Several Megabases , 1998, Plant Cell.

[5]  David A. Jones,et al.  The Tomato Cf-5 Disease Resistance Gene and Six Homologs Show Pronounced Allelic Variation in Leucine-Rich Repeat Copy Number , 1998, Plant Cell.

[6]  Jonathan D. G. Jones,et al.  Three Genes of the Arabidopsis RPP1 Complex Resistance Locus Recognize Distinct Peronospora parasitica Avirulence Determinants , 1998, Plant Cell.

[7]  J. D. Jones,et al.  Genetic and molecular analysis of tomato Cf genes for resistance to Cladosporium fulvum. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[8]  F. Takken,et al.  Identification and Ds-tagged isolation of a new gene at the Cf-4 locus of tomato involved in disease resistance to Cladosporium fulvum race 5. , 1998, The Plant journal : for cell and molecular biology.

[9]  Shiping Zhang,et al.  Xa21D Encodes a Receptor-like Molecule with a Leucine-Rich Repeat Domain That Determines Race-Specific Recognition and Is Subject to Adaptive Evolution , 1998, Plant Cell.

[10]  Jonathan D. G. Jones,et al.  The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals , 1998, Current Biology.

[11]  W. Stemmer,et al.  DNA shuffling of a family of genes from diverse species accelerates directed evolution , 1998, Nature.

[12]  M. Yano,et al.  Rapid reorganization of resistance gene homologues in cereal genomes. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Jonathan D. G. Jones,et al.  Novel Disease Resistance Specificities Result from Sequence Exchange between Tandemly Repeated Genes at the Cf-4/9 Locus of Tomato , 1997, Cell.

[14]  J. D. Jones,et al.  Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. , 1997, The Plant cell.

[15]  G. Wang,et al.  Evolution of the rice Xa21 disease resistance gene family. , 1997, The Plant cell.

[16]  E. A. van der Biezen,et al.  The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the toll and interleukin-1 receptors with N and L6. , 1997, The Plant cell.

[17]  E. Finnegan,et al.  Inactivation of the flax rust resistance gene M associated with loss of a repeated unit within the leucine-rich repeat coding region. , 1997, The Plant cell.

[18]  Jonathan D. G. Jones,et al.  The Role of Leucine-Rich Repeat Proteins in Plant Defences , 1997 .

[19]  S. Hulbert.  Structure and evolution of the rp1 complex conferring rust resistance in maize. , 1997, Annual review of phytopathology.

[20]  J. Luck,et al.  Advances in the molecular genetic analysis of the flax-flax rust interaction. , 1997, Annual review of phytopathology.

[21]  Daniel T. Lavelle,et al.  Tomato Prf Is a Member of the Leucine-Rich Repeat Class of Plant Disease Resistance Genes and Lies Embedded within the Pto Kinase Gene Cluster , 1996, Cell.

[22]  R Staden,et al.  The staden sequence analysis package , 1996, Molecular biotechnology.

[23]  Jonathan D. G. Jones,et al.  The Tomato Cf-2 Disease Resistance Locus Comprises Two Functional Genes Encoding Leucine-Rich Repeat Proteins , 1996, Cell.

[24]  J. D. Jones,et al.  Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. , 1994, Science.

[25]  J. Deisenhofer,et al.  The leucine-rich repeat: a versatile binding motif. , 1994, Trends in biochemical sciences.

[26]  John M. Hancock,et al.  Detection and quantification of concerted evolution and molecular drive. , 1993, Methods in enzymology.