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. 2001 May;158(1):423–438. doi: 10.1093/genetics/158.1.423

Recombination between paralogues at the Rp1 rust resistance locus in maize.

Q Sun 1, N C Collins 1, M Ayliffe 1, S M Smith 1, J Drake 1, T Pryor 1, S H Hulbert 1
PMCID: PMC1461629  PMID: 11333250

Abstract

Rp1 is a complex rust resistance locus of maize. The HRp1-D haplotype is composed of Rp1-D and eight paralogues, seven of which also code for predicted nucleotide binding site-leucine rich repeat (NBS-LRR) proteins similar to the Rp1-D gene. The paralogues are polymorphic (DNA identities 91-97%), especially in the C-terminal LRR domain. The remaining family member encodes a truncated protein that has no LRR domain. Seven of the nine family members, including the truncated gene, are transcribed. Sequence comparisons between paralogues provide evidence for past recombination events between paralogues and diversifying selection, particularly in the C-terminal half of the LRR domain. Variants selected for complete or partial loss of Rp1-D resistance can be explained by unequal crossing over that occurred mostly within coding regions. The Rp1-D gene is altered or lost in all variants, the recombination breakpoints occur throughout the genes, and most recombinant events (9/14 examined) involved the same untranscribed paralogue with the Rp1-D gene. One recombinant with a complete LRR from Rp1-D, but the amino-terminal portion from another homologue, conferred the Rp1-D specificity but with a reduced level of resistance.

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Selected References

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  1. Anderson P. A., Lawrence G. J., Morrish B. C., Ayliffe M. A., Finnegan E. J., Ellis J. G. 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):641–651. doi: 10.1105/tpc.9.4.641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Baker B., Zambryski P., Staskawicz B., Dinesh-Kumar S. P. Signaling in plant-microbe interactions. Science. 1997 May 2;276(5313):726–733. doi: 10.1126/science.276.5313.726. [DOI] [PubMed] [Google Scholar]
  3. Botella M. A., Parker J. E., Frost L. N., Bittner-Eddy P. D., Beynon J. L., Daniels M. J., Holub E. B., Jones J. D. Three genes of the Arabidopsis RPP1 complex resistance locus recognize distinct Peronospora parasitica avirulence determinants. Plant Cell. 1998 Nov;10(11):1847–1860. doi: 10.1105/tpc.10.11.1847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Collins N., Drake J., Ayliffe M., Sun Q., Ellis J., Hulbert S., Pryor T. Molecular characterization of the maize Rp1-D rust resistance haplotype and its mutants. Plant Cell. 1999 Jul;11(7):1365–1376. doi: 10.1105/tpc.11.7.1365. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Crute I. R., Pink DAC. Genetics and Utilization of Pathogen Resistance in Plants. Plant Cell. 1996 Oct;8(10):1747–1755. doi: 10.1105/tpc.8.10.1747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dixon M. S., Hatzixanthis K., Jones D. A., Harrison K., Jones J. D. The tomato Cf-5 disease resistance gene and six homologs show pronounced allelic variation in leucine-rich repeat copy number. Plant Cell. 1998 Nov;10(11):1915–1925. doi: 10.1105/tpc.10.11.1915. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dixon M. S., Jones D. A., Keddie J. S., Thomas C. M., Harrison K., Jones J. D. The tomato Cf-2 disease resistance locus comprises two functional genes encoding leucine-rich repeat proteins. Cell. 1996 Feb 9;84(3):451–459. doi: 10.1016/s0092-8674(00)81290-8. [DOI] [PubMed] [Google Scholar]
  8. Dooner H. K., Martínez-Férez I. M. Recombination occurs uniformly within the bronze gene, a meiotic recombination hotspot in the maize genome. Plant Cell. 1997 Sep;9(9):1633–1646. doi: 10.1105/tpc.9.9.1633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ellis J. G., Lawrence G. J., Luck J. E., Dodds P. N. Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell. 1999 Mar;11(3):495–506. doi: 10.1105/tpc.11.3.495. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ellis J., Dodds P., Pryor T. The generation of plant disease resistance gene specificities. Trends Plant Sci. 2000 Sep;5(9):373–379. doi: 10.1016/s1360-1385(00)01694-0. [DOI] [PubMed] [Google Scholar]
  11. Ellis J., Jones D. Structure and function of proteins controlling strain-specific pathogen resistance in plants. Curr Opin Plant Biol. 1998 Aug;1(4):288–293. doi: 10.1016/1369-5266(88)80048-7. [DOI] [PubMed] [Google Scholar]
  12. Ellis J., Lawrence G., Ayliffe M., Anderson P., Collins N., Finnegan J., Frost D., Luck J., Pryor T. Advances in the molecular genetic analysis of the flax-flax rust interaction. Annu Rev Phytopathol. 1997;35:271–291. doi: 10.1146/annurev.phyto.35.1.271. [DOI] [PubMed] [Google Scholar]
  13. Endo T., Ikeo K., Gojobori T. Large-scale search for genes on which positive selection may operate. Mol Biol Evol. 1996 May;13(5):685–690. doi: 10.1093/oxfordjournals.molbev.a025629. [DOI] [PubMed] [Google Scholar]
  14. Grant M. R., Godiard L., Straube E., Ashfield T., Lewald J., Sattler A., Innes R. W., Dangl J. L. Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science. 1995 Aug 11;269(5225):843–846. doi: 10.1126/science.7638602. [DOI] [PubMed] [Google Scholar]
  15. Hu G., Hulbert S. Evidence for the involvement of gene conversion in meiotic instability of the Rp1 rust resistance genes of maize. Genome. 1994 Oct;37(5):742–746. doi: 10.1139/g94-105. [DOI] [PubMed] [Google Scholar]
  16. Hu G., Richter T. E., Hulbert S. H., Pryor T. Disease Lesion Mimicry Caused by Mutations in the Rust Resistance Gene rp1. Plant Cell. 1996 Aug;8(8):1367–1376. doi: 10.1105/tpc.8.8.1367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hughes A. L., Nei M. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature. 1988 Sep 8;335(6186):167–170. doi: 10.1038/335167a0. [DOI] [PubMed] [Google Scholar]
  18. Hulbert S. H. Structure and evolution of the rp1 complex conferring rust resistance in maize. Annu Rev Phytopathol. 1997;35:293–310. doi: 10.1146/annurev.phyto.35.1.293. [DOI] [PubMed] [Google Scholar]
  19. Hwang C. F., Bhakta A. V., Truesdell G. M., Pudlo W. M., Williamson V. M. Evidence for a role of the N terminus and leucine-rich repeat region of the Mi gene product in regulation of localized cell death. Plant Cell. 2000 Aug;12(8):1319–1329. doi: 10.1105/tpc.12.8.1319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kobe B., Deisenhofer J. A structural basis of the interactions between leucine-rich repeats and protein ligands. Nature. 1995 Mar 9;374(6518):183–186. doi: 10.1038/374183a0. [DOI] [PubMed] [Google Scholar]
  21. Lawrence G. J., Finnegan E. J., Ayliffe M. A., Ellis J. G. The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and the tobacco viral resistance gene N. Plant Cell. 1995 Aug;7(8):1195–1206. doi: 10.1105/tpc.7.8.1195. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Luck J. E., Lawrence G. J., Dodds P. N., Shepherd K. W., Ellis J. G. Regions outside of the leucine-rich repeats of flax rust resistance proteins play a role in specificity determination. Plant Cell. 2000 Aug;12(8):1367–1377. doi: 10.1105/tpc.12.8.1367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Martin G. B., Brommonschenkel S. H., Chunwongse J., Frary A., Ganal M. W., Spivey R., Wu T., Earle E. D., Tanksley S. D. Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science. 1993 Nov 26;262(5138):1432–1436. doi: 10.1126/science.7902614. [DOI] [PubMed] [Google Scholar]
  24. McDowell J. M., Dhandaydham M., Long T. A., Aarts M. G., Goff S., Holub E. B., Dangl J. L. Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis. Plant Cell. 1998 Nov;10(11):1861–1874. doi: 10.1105/tpc.10.11.1861. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Michelmore R. W., Meyers B. C. Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 1998 Nov;8(11):1113–1130. doi: 10.1101/gr.8.11.1113. [DOI] [PubMed] [Google Scholar]
  26. Mindrinos M., Katagiri F., Yu G. L., Ausubel F. M. The A. thaliana disease resistance gene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell. 1994 Sep 23;78(6):1089–1099. doi: 10.1016/0092-8674(94)90282-8. [DOI] [PubMed] [Google Scholar]
  27. Parker J. E., Coleman M. J., Szabò V., Frost L. N., Schmidt R., van der Biezen E. A., Moores T., Dean C., Daniels M. J., Jones J. D. 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):879–894. doi: 10.1105/tpc.9.6.879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Parniske M., Hammond-Kosack K. E., Golstein C., Thomas C. M., Jones D. A., Harrison K., Wulff B. B., Jones J. D. 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):821–832. doi: 10.1016/s0092-8674(00)80470-5. [DOI] [PubMed] [Google Scholar]
  29. Richter T. E., Pryor T. J., Bennetzen J. L., Hulbert S. H. New rust resistance specificities associated with recombination in the Rp1 complex in maize. Genetics. 1995 Sep;141(1):373–381. doi: 10.1093/genetics/141.1.373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Salmeron J. M., Oldroyd G. E., Rommens C. M., Scofield S. R., Kim H. S., Lavelle D. T., Dahlbeck D., Staskawicz B. J. 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. Cell. 1996 Jul 12;86(1):123–133. doi: 10.1016/s0092-8674(00)80083-5. [DOI] [PubMed] [Google Scholar]
  31. Schnable P. S., Hsia A. P., Nikolau B. J. Genetic recombination in plants. Curr Opin Plant Biol. 1998 Apr;1(2):123–129. doi: 10.1016/s1369-5266(98)80013-7. [DOI] [PubMed] [Google Scholar]
  32. Schwarz-Sommer Z., Leclercq L., Göbel E., Saedler H. Cin4, an insert altering the structure of the A1 gene in Zea mays, exhibits properties of nonviral retrotransposons. EMBO J. 1987 Dec 20;6(13):3873–3880. doi: 10.1002/j.1460-2075.1987.tb02727.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Shepherd K. W., Mayo G. M. Genes conferring specific plant disease resistance. Science. 1972 Jan 28;175(4020):375–380. doi: 10.1126/science.175.4020.375. [DOI] [PubMed] [Google Scholar]
  34. Simons G., Groenendijk J., Wijbrandi J., Reijans M., Groenen J., Diergaarde P., Van der Lee T., Bleeker M., Onstenk J., de Both M. Dissection of the fusarium I2 gene cluster in tomato reveals six homologs and one active gene copy. Plant Cell. 1998 Jun;10(6):1055–1068. doi: 10.1105/tpc.10.6.1055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Smith G. P. Evolution of repeated DNA sequences by unequal crossover. Science. 1976 Feb 13;191(4227):528–535. doi: 10.1126/science.1251186. [DOI] [PubMed] [Google Scholar]
  36. Song W. Y., Pi L. Y., Wang G. L., Gardner J., Holsten T., Ronald P. C. Evolution of the rice Xa21 disease resistance gene family. Plant Cell. 1997 Aug;9(8):1279–1287. doi: 10.1105/tpc.9.8.1279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sudupak M. A., Bennetzen J. L., Hulbert S. H. Unequal exchange and meiotic instability of disease-resistance genes in the Rp1 region of maize. Genetics. 1993 Jan;133(1):119–125. doi: 10.1093/genetics/133.1.119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Thomas C. M., Jones D. A., Parniske M., Harrison K., Balint-Kurti P. J., Hatzixanthis K., Jones J. D. Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell. 1997 Dec;9(12):2209–2224. doi: 10.1105/tpc.9.12.2209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Wang G. L., Ruan D. L., Song W. Y., Sideris S., Chen L., Pi L. Y., Zhang S., Zhang Z., Fauquet C., Gaut B. S. Xa21D encodes a receptor-like molecule with a leucine-rich repeat domain that determines race-specific recognition and is subject to adaptive evolution. Plant Cell. 1998 May;10(5):765–779. doi: 10.1105/tpc.10.5.765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Whitham S., Dinesh-Kumar S. P., Choi D., Hehl R., Corr C., Baker B. The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell. 1994 Sep 23;78(6):1101–1115. doi: 10.1016/0092-8674(94)90283-6. [DOI] [PubMed] [Google Scholar]
  41. Zhang J., Kumar S., Nei M. Small-sample tests of episodic adaptive evolution: a case study of primate lysozymes. Mol Biol Evol. 1997 Dec;14(12):1335–1338. doi: 10.1093/oxfordjournals.molbev.a025743. [DOI] [PubMed] [Google Scholar]

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