The disease resistance gene Dm3 is infrequent in natural populations of Lactuca serriola due to deletions and frequent gene conversions at the RGC2 locus.

Resistance genes can exhibit heterogeneous patterns of variation. However, there are few data on their frequency and variation in natural populations. We analysed the frequency and variation of the resistance gene Dm3, which confers resistance to Bremia lactucae (downy mildew) in 1033 accessions of Lactuca serriola (prickly lettuce) from 49 natural populations. Inoculations with an isolate of Bremia lactucae carrying avirulence gene Avr3 indicated that the frequency of Dm3 in natural populations of L. serriola was very low. Molecular analysis demonstrated that Dm3 was present in only one of the 1033 wild accessions analysed. The sequence of the 5' region of Dm3 was either highly conserved among accessions, or absent. In contrast, frequent chimeras were detected in the 3' leucine-rich repeat-encoding region. Therefore low frequency of the Dm3 specificity in natural populations was due to either the recent evolution of Dm3 specificity, or deletions of the whole gene as well as variation in 3' region caused by frequent gene conversions. This is the most extensive analysis of the prevalence of a known disease resistance gene to date, and indicates that the total number of resistance genes in a species may be very high. This has implications for the scales of germplasm conservation and exploitation of sources of resistance.

[1]  E. Nevo,et al.  New Wild Lactuca Genetic Resources with Resistance Against Bremia lactucae , 2006, Genetic Resources and Crop Evolution.

[2]  Blake C Meyers,et al.  Multiple Genetic Processes Result in Heterogeneous Rates of Evolution within the Major Cluster Disease Resistance Genes in Lettucew⃞ , 2004, The Plant Cell Online.

[3]  A. Lebeda,et al.  Variation and distribution of virulence phenotypes of Bremia lactucae in natural populations of Lactuca serriola , 2004 .

[4]  R. Innes Guarding the Goods. New Insights into the Central Alarm System of Plants1 , 2004, Plant Physiology.

[5]  R. Michelmore,et al.  The Maintenance of Extreme Amino Acid Diversity at the Disease Resistance Gene, RPP13, in Arabidopsis thaliana , 2004, Genetics.

[6]  R. Groenwold,et al.  New sources of major gene resistance in Lactuca to Bremia lactucae , 1991, Euphytica.

[7]  S. Tanksley,et al.  Genetics of actin-related sequences in tomato , 1986, Theoretical and Applied Genetics.

[8]  A. Lebeda,et al.  Evolution and distribution of virulence in the German population of Bremia lactucae , 2003 .

[9]  Eli Stahl,et al.  Signature of balancing selection in Arabidopsis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[10]  Blake C Meyers,et al.  Dm3 is one member of a large constitutively expressed family of nucleotide binding site-leucine-rich repeat encoding genes. , 2002, Molecular plant-microbe interactions : MPMI.

[11]  A. Lebeda Occurrence and Variation in Virulence of Bremia Lactucae in Natural Populations of Lactuca Serriola , 2002 .

[12]  P. Dodds,et al.  Contrasting modes of evolution acting on the complex N locus for rust resistance in flax. , 2001, The Plant journal : for cell and molecular biology.

[13]  P. D. de Wit,et al.  Intragenic recombination generated two distinct Cf genes that mediate AVR9 recognition in the natural population of Lycopersicon pimpinellifolium , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Jonathan D. G. Jones,et al.  Plant pathogens and integrated defence responses to infection , 2001, Nature.

[15]  R. Michelmore,et al.  Recombination and spontaneous mutation at the major cluster of resistance genes in lettuce (Lactuca sativa). , 2001, Genetics.

[16]  D. Klessig,et al.  Members of the Arabidopsis HRT/RPP8 Family of Resistance Genes Confer Resistance to Both Viral and Oomycete Pathogens , 2000, Plant Cell.

[17]  E. A. van der Biezen,et al.  Pronounced Intraspecific Haplotype Divergence at the RPP5 Complex Disease Resistance Locus of Arabidopsis , 1999, Plant Cell.

[18]  E. Nevo,et al.  Molecular diversity at the major cluster of disease resistance genes in cultivated and wild Lactuca spp. , 1999, Theoretical and Applied Genetics.

[19]  B. Kunkel,et al.  Diversity and molecular evolution of the RPS2 resistance gene in Arabidopsis thaliana. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[20]  B C Meyers,et al.  Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. , 1998, Genome research.

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

[22]  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.

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

[24]  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.

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

[26]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[27]  I. Crute The role of resistance breeding in the integrated control of downy mildew (Bremia lactucae) in protected lettuce , 1992 .

[28]  R. Michelmore,et al.  Variation at RFLP loci in Lactuca spp. and origin of cultivated lettuce (L. sativa) , 1991 .

[29]  A. Lupas,et al.  Predicting coiled coils from protein sequences , 1991, Science.

[30]  S. Sawyer Statistical tests for detecting gene conversion. , 1989, Molecular biology and evolution.

[31]  R. Michelmore,et al.  Genetic analysis of factors for resistance to downy mildew (Bremia lactucae) in species of lettuce (Lactuca sativa and L. serriola) , 1987 .

[32]  I. Crute,et al.  Variation for specific virulence in the Finnish Bremia lactucae population , 1981 .

[33]  G. Dixon,et al.  Frequency and geographical distribution of specific virulence factors in Bremia lactucae populations in England from 1973 to 1975 , 1978 .

[34]  R. N. Carter,et al.  Prickly Lettuce (Lactuca serriola L.) in Britain , 1977 .

[35]  I. Crute,et al.  The genetic relationship between races of Bremiae lactucae and cultivars of Lactuca sativa , 1976 .