Evolution and genetic population structure of prickly lettuce (Lactuca serriola) and its RGC2 resistance gene cluster

Genetics

Volumn 178, Issue 3, 2008, Pages 1547-1558

  Kuang, Hanhui ^a,b,c   Van Eck, Herman J ^a,d   Sicard, Delphine ^b,e   Michelmore, Richard ^b   Nevo, Eviatar ^a  

^a UNIVERSITY OF HAIFA   (Israel)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c PLANT GENE EXPRESSION CENTER   (United States)

^d WAGENINGEN UNIVERSITY   (Netherlands)

^e UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ABIOTIC STRESS; ARTICLE; BIOTIC STRESS; CORRELATION ANALYSIS; GENETIC VARIABILITY; HAPLOTYPE; LETTUCE; MICROSATELLITE MARKER; NONHUMAN; PLANT GENE; POPULATION GENETIC STRUCTURE; PRIORITY JOURNAL; RGC2 GENE; ALLELE; AMPLIFIED FRAGMENT LENGTH POLYMORPHISM; EVOLUTION; GENE; GENETIC POLYMORPHISM; GENETICS; GENOME; GENOTYPE; IMMUNOLOGY; INNATE IMMUNITY; MOLECULAR GENETICS; MULTIGENE FAMILY; PLANT DISEASE; POPULATION DYNAMICS;

LACTUCA SERRIOLA;

ALLELES; AMPLIFIED FRAGMENT LENGTH POLYMORPHISM ANALYSIS; EVOLUTION; GENES, PLANT; GENOME, PLANT; GENOTYPE; IMMUNITY, NATURAL; LETTUCE; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PLANT DISEASES; POLYMORPHISM, GENETIC; POPULATION DYNAMICS; VARIATION (GENETICS);

EID: 45149106161     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.107.080796     Document Type: Article

References (54)

1. BAKKER, E. G., C. TOOMAJIAN, M. KREITMAN and J. BERGELSON, 2006 A genome-wide survey of R gene polymorphisms in Arabidopsis. Plant Cell 18: 1803-1818.
2. BEHARAV, A., D. LEWINSOHN, A. LEBEDA and E. NEVO, 2006 New wild Lactuca genetic resources with resistance against Bremia lactucae. Genet. Resour. Crop Evol. 53: 467-474.
3. BLACK, W., and M. E. GALLEGLY, 1957 Screening of Solanum species for resistance to physiologic races of Phytophthora infestans. Amer. Potato J. 34: 273-281.
4. BOREVITZ, J. O., S. P. HAZEN, T. P. MICHAEL, G. P. MORRIS, I. R. BAXTER et al., 2007 Genome-wide patterns of single-feature polymorphism in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 104: 12057-12062.
5. BOYKO, A., P. KATHIRIA, F. J. ZEMP, Y. YAO, I. POGRIBNY et al., 2007 Transgenerational changes in the genome stability and methylation in pathogen-infected plants (virus-induced plant genome instability). Nucleic Acids Res. 35: 1714-1725.
6. CAICEDO, A. L., and B. A. SCHAAL, 2004 Heterogeneous evolutionary processes affect R gene diversity in natural populations of Solanum pimpinellifolium. Proc. Natl. Acad. Sci. USA 101: 17444-17449.
7. CAICEDO, A. L., B. A. SCHAAL and B. N. KUNKEL, 1999 Diversity and molecular evolution of the RPS2 resistance gene in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 96: 302-306.
8. CLARK, R. M., G. SCHWEIKERT, C. TOOMAJIAN, S. OSSOWSKI, G. ZELLER et al., 2007 Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science 317: 338-342.
9. CRUTE, I. R., 1992 The role of resistance breeding in the integrated control of downy mildew (Bremia lactucae) in protected lettuce. Euphytica 63: 95-102.
10. ELLIS, J. G., G. J. LAWRENCE, J. E. LUCK and P. N. DODDS, 1999 Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell 11: 495-506.
11. FARRARA, B., T. W. ILOTT and R. W. MICHELMORE, 1987 Genetic analysis of factors for resistance to downy mildew (Bremia lactucae) in species of lettuce (Lactuca sativa and L. serriola). Plant Pathol. 36: 499-514.
12. FU, Y. X., 1997 Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915-925.
13. FU, Y. X., and W. H. LI, 1993 Statistical tests of neutrality of mutations. Genetics 133: 693-709.
14. HILL, M., H. WITSENBOER, M. ZABEAU, P. VOS, R. KESSELI et al., 1996 PCR-based fingerprinting using AFLPs as a tool for studying genetic relationships in Lactuca spp. Theor. Appl. Genet. 93: 1202-1210.
15. HUDSON, R. R., and N. L. KAPLAN, 1985 Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111: 147-164.
16. KASHI, Y., and D. G. KING, 2006 Simple sequence repeats as advantageous mutators in evolution. Trends Genet. 22: 253-259.
17. KESSELI, R., O. OCHOA and R. MICHELMORE, 1991 Variation at RFLP loci. in Lactuca spp. and origin of cultivated lettuce Lactuca sativa. Genome 34: 430-436.
18. KESSELI, R. V., I. PARAN and R. W. MICHELMORE, 1994 Analysis of a detailed genetic linkage map of Lactuca sativa (Lettuce) constructed from RFLP and RAPD markers. Genetics 136: 1435-1446.
19. KUANG, H., S.-S. WOO, B. C. MEYERS, E. NEVO and R. W. MICHELMORE, 2004 Multiple genetic processes result in heterogeneous rates of evolution within the major cluster disease resistance genes in lettuce. Plant Cell 16: 2870-2894.
20. KUANG, H., O. E. OCHOA, E. NEVO and R. W. MICHELMORE, 2006 The disease resistance gene Dm3 is infrequent in natural populations of Lactuca serriola due to deletions and frequent gene conversions at the RGC2 locus. Plant J. 47: 38-48.
21. LEBEDA, A., and I. PETRŽELOVA, 2004a Variation and distribution of virulence phenotypes of Bremia lactucae in natural populations of Lactuca serriola. Plant Pathol. 53: 316-324.
22. LEBEDA, A., and I. PETRŽELOVA, 2004b Occurrence of race-specific resistance to Bremia lactucae in Lactuca serriola germplasm originating from four European countries, pp. 113-116 in Genetic Variation for Plant Breeding, edited by J. VOLLMANN, H. GRAUSGRUBER and P. RUCKENBAUER. BOKU-University of Natural Resources and Applied Life Sciences, Vienna.
23. LEBEDA, A., I. DOLEZALOVA, E. KRISTKOVA and B. MIESLEROVA, 2001 Biodiversity and ecogeography of wild Lactuca spp. in some European countries. Genet. Resour. Crop Evol. 48: 153-164.
24. LEBEDA, A., D. A. C. PINK and D. ASTLEY,2002 Aspects of the interactions between wild Lactuca spp. and related genera and lettuce downymildew(Bremialactucae), pp.85-117 in Advances in Downy Mildew Research, edited by P. T. N. SPENCER-PHILLIPS, U. GISI and A. LEBEDA. Kluwer Academic Publishers, Dordrecht, The Netherlands.
25. LEBEDA, A., I. DOLEŽALOVA, V. FERA KOVA and D. ASTLEY, 2004 Geographical distribution of wild Lactuca species (Asteraceae, Lactuceae). Botanical Review 70: 328-356.
26. LI, Y.-C., A. B. KOROL, T. FAHIMA and E. NEVO, 2004 Microsatellites within genes: Structure, function, and evolution. Mol. Biol. Evol. 21: 991-1007.
27. LINDQVIST, K., 1960 On the origin of cultivated lettuce. Hereditas 46: 319-350.
28. LUCHT, J. M., B. MAUCH-MANI, H.-Y. STEINER, J.-P. METRAUX, J. RYALS et al., 2002 Pathogen stress increases somatic recombination frequency in Arabidopsis. Nature Genet. 30: 311-314.
29. MAURICIO, R., E. A. STAHL, T. KORVES, D. TIAN, M. KREITMAN et al., 2003 Natural selection for polymorphism in the disease resistance gene RPS2 of Arabidopsis thaliana. Genetics 163: 735-746.
30. MEYERS, B. C., D. B. CHIN, K. A. SHEN, S. SIVARAMAKRISHNAN, D. O. LAVELLE et al., 1998 The major resistance gene cluster in lettuce is highly duplicated and spans several megabases. Plant Cell 10: 1817-1832.
31. MOLINIER, J., G. RIES, C. ZIPFEL and B. HOHN, 2006 Transgenerational memory of stress in plants. Nature 442: 1046-1049.
32. NEI, M., 1973 Analysis of gene diversity in subdivided populations. Proc. Natl. Acad. Sci. USA 70: 3321-3323.
33. NEI, M., 1978 Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89: 583-590.
34. NEVO, E., 1998 Genetic diversity in wild cereals: Regional and local studies and their bearing on conservation ex-situ and in-situ. Genet. Resour. Crop Evol. 45: 355-370.
35. NEVO, E., 2001 Evolution of genome-phenome diversity under environmental stress. Proc. Natl. Acad. Sci. USA 98: 6233-6240.
36. PETRŽELOVA, I., and A. LEBEDA, 2004 Occurrence of Bremia lactucae in natural populations of Lactuca serriola. J. Phytopathol. 152: 391-398.
37. PRINCE, S. D., and R. N. CARTER, 1977 Prickly lettuce (Lactuca serriola L.) in Britain. Watsonia 11: 331-338.
38. ROSE, L. E., P. D. BITTNER-EDDY, C. H. LANGLEY, E. B. HOLUB, R. W. MICHELMORE et al., 2004 The maintenance of extreme amino acid diversity at the disease resistance gene, RPP13, in Arabidopsis thaliana. Genetics 166: 1517-1527.
39. ROSE, L. E., R. W. MICHELMORE and C. H. LANGLEY, 2007 Natural variation in the Pto disease resistance gene within species of wild tomato (Lycopersicon) II. Population genetics of Pto. Genetics 175: 1307-1319.
40. ROUPPE VAN DER VOORT, J. N., P. VAN ZANDVOORT, H. J. VAN ECK, R. T. FOLKERTSMA, R. C. HUTTEN et al., 1997 Use of allele specificity of comigrating AFLP markers to align genetic maps from different potato genotypes. Mol. Gen. Genet. 255: 438-447.
41. ROZAS, J., and R. ROZAS, 1999 DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15: 174-175.
42. SHEN, J., H. ARAKI, L. CHEN, J.-Q. CHEN and D. TIAN, 2006 Unique evolutionary mechanism in R-genes under the presence/absence polymorphism in Arabidopsis thaliana. Genetics 172: 1243-1250.
43. SHEN, K. A., D. B. CHIN, R. ARROYO- GARCIA, O. E. OCHOA, D. O. LAVELLE et al., 2002 Dm3 is onemember of a large constitutively expressed family of nucleotide binding site-leucine-rich repeat encoding genes. Mol. Plant-Microbe Interact. 15: 251-261.
44. SICARD, D., S. S. WOO, R. ARROYO-G ARCIA, O. OCHOA, D. NGUYEN et al., 1999 Molecular diversity at the major cluster of disease resistance genes in cultivated and wild Lactuca spp. Theor. Appl. Genet. 99: 405-418.
45. SIMIER, M., J. THIOULOUSE and J.-M. OLIVIER, 1998 ADE-4 software: A tool for multivariate analysis and graphical display. Oceanis 24: 393-416.
46. STAHL, E. A., G. DWYER, R. MAURICIO, M. KREITMAN and J. BERGELSON, 1999 Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 400: 667-671.
47. TAJIMA, F., 1989 Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.
48. THOMPSON, J. D., T. J. GIBSON, F. PLEWNIAK, F. JEANMOUGIN and D. G. HIGGINS, 1997 The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25: 4876-4882.
49. TIAN, D., H. ARAKI, E. STAHL, J. BERGELSON and M. KREITMAN, 2002 Signature of balancing selection in Arabidopsis. Proc. Natl. Acad. Sci. USA 99: 11525-11530.
50. TIAN, D., M. B. TRAW, J. Q. CHEN, M. KREITMAN and J. BERGELSON, 2003 Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423: 74-77.
51. VOS, P., R. HOGERS, M. BLEEKER, M. REIJANS, T. VAN DE LEE et al., 1995 AFLP: a new technique for DNA fingerprinting. Nucleic Acids Res. 23: 4407-4414.
52. WROBLEWSKI, T., U. PISKUREWICZ, A. TOMCZAK, O. OCHOA and R. W. MICHELMORE, 2007 Silencing of the major family of NBS-LRR-encoding genes in lettuce results in the loss of multiple resistance specificities. Plant J. 51: 803-818.
53. YEH, F. C., and T. J. B. BOYLE, 1997 Population genetic analysis of codominant and dominant markers and quantitative traits. Belg. J. Bot. 129: 157.
54. ZOHARY, D., 1991 The wild genetic-resources of cultivated lettuce (Lactuca sativa L). Euphytica 53: 31-35.