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Molecular Breeding

, Volume 26, Issue 2, pp 357–370 | Cite as

Recombination is suppressed in an alien introgression in peanut harboring Rma, a dominant root-knot nematode resistance gene

  • Ervin D. Nagy
  • Ye Chu
  • Yufang Guo
  • Sameer Khanal
  • Shunxue Tang
  • Yan Li
  • Weibo B. Dong
  • Patricia Timper
  • Christopher Taylor
  • Peggy Ozias-Akins
  • C. Corley Holbrook
  • Vadim Beilinson
  • Niels C. Nielsen
  • H. Thomas Stalker
  • Steven J. Knapp
Article

Abstract

Rma, a dominant root-knot nematode resistance gene introduced into tetraploid peanut (Arachis hypogaea) from a synthetic allotetraploid donor (TxAG-6), has been widely deployed in modern cultivars. The genomic location and borders of the alien chromosome segment introgressed from TxAG-6 into NemaTAM (a BC7-derived introgression line) and other modern cultivars carrying Rma have not been genetically mapped, and resistance gene candidates (RGCs) have not been identified for Rma. Our study focused on densely populating the alien introgression with codominant DNA markers, identifying and mapping the borders of the alien introgression carried by NemaTAM, and identifying RGCs for Rma. Altogether, 2,847 simple sequence repeat (SSR) and 380 single strand conformational polymorphism (SSCP) markers were screened for linkage to Rma-247 of the SSCP markers targeted 202 nucleotide binding site (NBS) leucine-rich repeat (LRR) and other resistance (R) gene homologs (75 were identified by mining a peanut EST database). SSR, NBS-LRR, and Ser/Thr receptor-like protein loci within the alien introgression co-segregated with Rma in an F4 population (Gregory × Tifguard) and were tightly linked and spanned 3.4 cM in an F5 population (NemaTAM × GP-NC-WS-14). By comparative mapping in the A-genome progenitor of peanut (A. duranensis), Rma was discovered to have been introduced on an interstitial alien chromosome segment spanning one-third to one-half of chromosome 9A. Numerous codominant DNA markers were identified for finer mapping of Rma, shortening the alien introgression harboring Rma by marker-assisted selection, and introducing novel root-knot nematode R-genes into peanut by targeting syntenic segments on chromosomes 9A and 9B in wild diploid donors.

Keywords

Arachis Meloidogyne Marker-assisted selection Fabaceae Nucleotide binding site leucine-rich repeat Receptor-like kinase 

Notes

Acknowledgments

This research was supported by grants to S.J.K. from the United States Department of Agriculture Plant Genome Program (No. 2006-35604-17242) and S.J.K., P.O.A., H.T.S., C.C.H., and N.N. from the National Peanut Board, the Georgia Peanut Commodity Commission, the Georgia Seed Development Commission, and the Peanut Foundation.

Supplementary material

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Supplementary material 1 (PDF 354 kb)
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Supplementary material 3 (XLS 108 kb)
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Supplementary material 5 (PDF 24 kb)
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Supplementary material 6 (XLS 339 kb)

References

  1. Bertioli DJ, Leal-Bertioli SCM, Lion MB, Santos VL, Pappas G, Cannon SB, Guimaraes PM (2003) A large scale analysis of resistance gene homologues in Arachis. Mol Genet Genomics 270:34–45CrossRefPubMedGoogle Scholar
  2. Burow MD, Simpson CE, Paterson AH, Starr JL (1996) Identification of peanut (Arachis hypogaea L) RAPD markers diagnostic of root-knot nematode (Meloidogyne arenaria (Neal) Chitwood) resistance. Mol Breed 2:369–379CrossRefGoogle Scholar
  3. Burow MD, Simpson CE, Starr JL, Paterson AH (2001) Transmission genetics of chromatin from a synthetic amphidiploid to cultivated peanut (Arachis hypogaea L.): broadening the gene pool of a monophyletic polyploid species. Genetics 159:823–837PubMedGoogle Scholar
  4. Burow MD, Simpson CE, Faries MW, Starr JL, Paterson AH (2009) Molecular biogeographic study of recently described B- and A-genome Arachis species, also providing new insights into the origins of cultivated peanut. Genome 52:107–119CrossRefPubMedGoogle Scholar
  5. Canady MA, Ji Y, Chetelat RT (2006) Homeologous recombination in Solanum lycopersicoides introgression lines of cultivated tomato. Genetics 174:1775–1788CrossRefPubMedGoogle Scholar
  6. Chenna R, Sugawara H, Koike T, Lopez R, Gibson TJ, Higgins DG, Thompson JD (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31:3497–3500CrossRefPubMedGoogle Scholar
  7. Chetelat RT, Meglic V, Cisneros P (2000) A genetic map of tomato based on BC1 Lycopersicon esculentum x Solanum lycopersicoides reveals overall synteny but suppressed recombination between these homeologous genomes. Genetics 154:857–867PubMedGoogle Scholar
  8. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814CrossRefPubMedGoogle Scholar
  9. Choi R, Burow MD, Church G, Burow G, Paterson AH, Simpson CE, Starr JL (1999) Genetics and mechanism of resistance to Meloidogyne arenaria in peanut germplasm. J Nemat 31:283–290Google Scholar
  10. Chu Y, Holbrook CC, Timper P, Ozias-Akins P (2007) Development of a PCR-based molecular marker to select for nematode resistance in peanut. Crop Sci 47:841–847CrossRefGoogle Scholar
  11. Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833CrossRefPubMedGoogle Scholar
  12. Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure from small quantities of fresh leaf tissues. Phytochem Bull 19:11–15Google Scholar
  13. Ferguson ME, Bramel PJ, Chandra S (2004a) Gene diversity among botanical varieties in peanut (Arachis hypogaea L.). Crop Sci 44:1847–1854Google Scholar
  14. Ferguson ME, Burow MD, Schulze SR, Bramel PJ, Paterson AH, Kresovich S, Mitchell S (2004b) Microsatellite identification and characterization in peanut (A. hypogaea L.). Theor Appl Genet 108:1064–1070CrossRefPubMedGoogle Scholar
  15. Ferguson ME, Jarvis A, Stalker HT, Williams DE, Guarino L, Valls JFM, Pittman RN, Simpson CE, Bramel PJ (2005) Biogeography of wild Arachis (Leguminosae): distribution and environmental characterisation. Biodiv Conserv 14:1777–1798CrossRefGoogle Scholar
  16. Garcia GM, Stalker HT, Shroeder E, Kochert G (1996) Identification of RAPD, SCAR, and RFLP markers tightly linked to nematode resistance genes introgressed from Arachis cardenasii into Arachis hypogaea. Genome 39:836–845CrossRefPubMedGoogle Scholar
  17. Gimenes MA, Hoshino AA, Barbosa AVG, Palmieri DA, Lopes CR (2007) Characterization and transferability of microsatellite markers of the cultivated peanut (Arachis hypogaea). BMC Plant Biol 7Google Scholar
  18. Griffiths AJ, Wesseler S, Lewontin RC, Carroll SB (2008) Introduction to Genetic Analysis, 9th edn. W.H. Freeman, CAGoogle Scholar
  19. Guindon S, Lethiec F, Duroux P, Gascuel O (2005) PHYML Online: a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 33:W557–W559CrossRefPubMedGoogle Scholar
  20. Guindon S, Delsuc F, Dufayard JF, Gascuel O (2009) Estimating maximum likelihood phylogenies with PhyML. Methods Mol Biol 537:113–137CrossRefPubMedGoogle Scholar
  21. Guo BZ, Chen XP, Dang P, Scully BT, Liang XQ, Holbrook CC, Yu JJ, Culbreath AK (2008) Peanut gene expression profiling in developing seeds at different reproduction stages during Aspergillus parasiticus infection. BMC Dev Biol 8:12CrossRefPubMedGoogle Scholar
  22. Halward TM, Stalker HT, Larue EA, Kochert G (1991) Genetic variation detectable with molecular markers among unadapted germplasm resources of cultivated peanut and related wild species. Genome 34:1013–1020Google Scholar
  23. Hayashi K, Yoshida H (2009) Refunctionalization of the ancient rice blast disease resistance gene Pit by the recruitment of a retrotransposon as a promoter. Plant J 57:413–425CrossRefPubMedGoogle Scholar
  24. He GH, Meng RH, Newman M, Gao GQ, Pittman RN, Prakash CS (2003) Microsatellites as DNA markers in cultivated peanut (Arachis hypogaea L.). BMC Plant Biol 3:3CrossRefPubMedGoogle Scholar
  25. He GH, Meng RH, Gao H, Guo BZ, Gao GQ, Newman M, Pittman RN, Prakash CS (2005) Simple sequence repeat markers for botanical varieties of cultivated peanut (Arachis hypogaea L.). Euphytica 142:131–136CrossRefGoogle Scholar
  26. Holbrook CC, Knauft DA, Dickson DW (1983) A technique for screening peanut for resistance to Meloidogyne arenaria. Plant Dis 67:957–958CrossRefGoogle Scholar
  27. Holbrook CC, Timper P, Culbreath AK, Kvien CK (2008a) Registration of ‘Tifguard’ peanut. J Plant Reg 2:92–94CrossRefGoogle Scholar
  28. Holbrook CC, Timper P, Dong WB, Kvien CK, Culbreath AK (2008b) Development of near-isogenic peanut lines with and without resistance to the peanut root-knot nematode. Crop Sci 48:194–198CrossRefGoogle Scholar
  29. Hopkins MS, Casa AM, Wang T, Mitchell SE, Dean RE, Kochert GD, Kresovich S (1999) Discovery and characterization of polymorphic simple sequence repeats (SSRs) in peanut. Crop Sci 39:1243–1247Google Scholar
  30. Isleib TG, Rice PW, Mozingo RW, Pattee HE (1999) Registration of ‘Gregory’ peanut. Crop Sci 39:1526Google Scholar
  31. Jarvis A, Ferguson ME, Williams DE, Guarino L, Jones PG, Stalker HT, Valls JFM, Pittman RN, Simpson CE, Bramel P (2003) Biogeography of wild Arachis: assessing conservation status and setting future priorities. Crop Sci 43:1100–1108Google Scholar
  32. Ji Y, Chetelat RT (2003) Homoeologous pairing and recombination in Solanum lycopersicoides monosomic addition and substitution lines of tomato. Theor Appl Genet 106:979–989PubMedGoogle Scholar
  33. Kochert G, Halward T, Branch WD, Simpson CE (1991) RFLP variability in peanut (Arachis hypogaea L.) cultivars and wild species. Theor Appl Genet 81:565–570CrossRefGoogle Scholar
  34. Korbie DJ, Mattick JS (2008) Touchdown PCR for increased specificity and sensitivity in PCR amplification. Nat Protoc 3:1452–1456CrossRefPubMedGoogle Scholar
  35. Krishna GK, Zhang JF, Burow M, Pittman RN, Delikostadinov SG, Lu YZ, Puppala N (2004) Genetic diversity analysis in Valencia peanut (Arachis hypogaea L.) using microsatellite markers. Cell Mol Biol Lett 9:685–697PubMedGoogle Scholar
  36. Lai Z, Nakazato T, Salmaso M, Burke JM, Tang S, Knapp SJ, Rieseberg LH (2005) Extensive chromosomal repatterning and the evolution of sterility barriers in hybrid sunflower species. Genetics 171:291–303CrossRefPubMedGoogle Scholar
  37. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948CrossRefPubMedGoogle Scholar
  38. Letunic I, Bork P (2007) Interactive Tree Of Life (iTOL): an online tool for phylogenetic tree display and annotation. Bioinformatics 23:127–128CrossRefPubMedGoogle Scholar
  39. Maizel JV Jr, Lenk RP (1981) Enhanced graphic matrix analysis of nucleic acid and protein sequences. Proc Natl Acad Sci USA 78:7665–7669CrossRefPubMedGoogle Scholar
  40. Meyers BC, Dickerman AW, Michelmore RW, Sivaramakrishnan S, Sobral BW, Young ND (1999) Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J 20:317CrossRefPubMedGoogle Scholar
  41. Meyers BC, Kozik A, Griego A, Kuang HH, Michelmore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15:809–834CrossRefPubMedGoogle Scholar
  42. Moretzsohn MC, Hopkins MS, Mitchell SE, Kresovich S, Valls JFM, Ferreira ME (2004) Genetic diversity of peanut (Arachis hypogaea L.) and its wild relatives based on the analysis of hypervariable regions of the genome. BMC Plant Biol 4:11CrossRefGoogle Scholar
  43. Moretzsohn MC, Leoi L, Proite K, Guimaraes PM, Leal-Bertioli SCM, Gimenes MA, Martins WS, Valls JFM, Grattapaglia D, Bertioli DJ (2005) A microsatellite-based, gene-rich linkage map for the AA genome of Arachis (Fabaceae). Theor Appl Genet 111:1060–1071CrossRefPubMedGoogle Scholar
  44. Moretzsohn MC, Barbosa AVG, Alves-Freitas DMT, Teixeira C, Leal-Bertioli SCM, Guimaraes PM, Pereira RW, Lopes CR, Cavallari MM, Valls JFM, Bertioli DJ, Gimenes MA (2009) A linkage map for the B-genome of Arachis (Fabaceae) and its synteny to the A-genome. BMC Plant Biol 9:40CrossRefPubMedGoogle Scholar
  45. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4326CrossRefPubMedGoogle Scholar
  46. Orita M, Iwahana H, Kanazawa H, Hayashi K, Sekiya T (1989) Detection of polymorphisms of human DNA by gel-electrophoresis as single strand conformation polymorphisms. Proc Natl Acad Sci USA 86:2766–2770CrossRefPubMedGoogle Scholar
  47. Pan QL, Wendel J, Fluhr R (2000) Divergent evolution of plant NBS-LRR resistance gene homologues in dicot and cereal genomes. J Mol Evol 50:203–213PubMedGoogle Scholar
  48. Park SJ, Kang CH, Chae JC, Rhee SK (2008) Metagenome microarray for screening of fosmid clones containing specific genes. FEMS Microbiol Lett 284:28–34CrossRefPubMedGoogle Scholar
  49. Pertuze RA, Ji Y, Chetelat RT (2003) Transmission and recombination of homeologous Solanum sitiens chromosomes in tomato. Theor Appl Genet 107:1391–1401CrossRefPubMedGoogle Scholar
  50. Quigley GJ, Gehrke L, Roth DA, Auron PE (1984) Computer-aided nucleic acid secondary structure modeling incorporating enzymatic digestion data. Nucleic Acids Res 12:347–366CrossRefPubMedGoogle Scholar
  51. Radwan O, Gandhi S, Heesacker A, Whitaker B, Taylor C, Plocik A, Kesseli R, Kozik A, Michelmore RW, Knapp SJ (2008) Genetic diversity and genomic distribution of homologs encoding NBS-LRR disease resistance proteins in sunflower. Mol Gen Genomics 2:111–125CrossRefGoogle Scholar
  52. Ramos ML, Fleming G, Chu Y, Akiyama M, Gallo M, Ozias-Akins P (2006) Chromosomal and phylogenetic context for conglutin genes in Arachis based on genomic sequence. Mol Genet Gen 275:578–592Google Scholar
  53. Salamov AA, Solovyev VV (2000) Ab initio gene finding in Drosophila genomic DNA. Genome Res 10:516–522CrossRefPubMedGoogle Scholar
  54. Sanguinetti CJ, Neto ED, Simpson AJG (1994) Rapid silver staining and recovery of PCR products separated on polyacrylamide gels. Biotechniques 17:914PubMedGoogle Scholar
  55. Sasser JN (1977) Worldwide dissemination and importance of root-knot nematodes, Meloidogyne spp. J Nemat 9:26–29Google Scholar
  56. Schnable PS, Hsia AP, Nikolau BJ (1998) Genetic recombination in plants. Curr Opin Plant Biol 1:123–129CrossRefPubMedGoogle Scholar
  57. Seijo JG, Lavia GI, Fernandez A, Krapovickas A, Ducasse D, Moscone EA (2004) Physical mapping of the 5S and 18S–25S rRNA genes by fish as evidence that Arachis duranensis and A. ipaensis are the wild diploid progenitors of A. hypogaea (Leguminosae). Am J Bot 91:1294–1303CrossRefGoogle Scholar
  58. Seijo G, Lavia GI, Fernandez A, Krapovickas A, Ducasse DA, Bertioli DJ, Moscone EA (2007) Genomic relationships between the cultivated peanut (Arachis hypogaea, Leguminosae) and its close relatives revealed by double GISH. Am J Bot 94:1963–1971CrossRefGoogle Scholar
  59. Shen Y, Ronald P (2002) Molecular determinants of disease and resistance in interactions of Xanthomonas oryzae pv. oryzae and rice. Microbes Infect 4:1361–1367CrossRefPubMedGoogle Scholar
  60. Simpson CE, Starr JL (2001) Registration of ‘COAN’ peanut. Crop Sci 41:918Google Scholar
  61. Simpson CE, Nelson SC, Starr JL, Woodard KE, Smith OD (1993) Registration of TxAG-6 and TxAG-7 peanut germplasm lines. Crop Sci 33:1418Google Scholar
  62. Simpson CE, Starr JL, Church GT, Burow MD, Paterson AH (2003) Registration of ‘NemaTAM’ peanut. Crop Sci 43:1561Google Scholar
  63. Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Holsten T, Gardner J, Wang B, Zhai WX, Zhu LH, Fauquet C, Ronald P (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804–1806CrossRefPubMedGoogle Scholar
  64. Song WY, Pi LY, Wang GL, Gardner J, Holsten T, Ronald PC (1997) Evolution of the rice Xa21 disease resistance gene family. Plant Cell 9:1279–1287CrossRefPubMedGoogle Scholar
  65. Stalker HT, Beute MK, Shew BB, Barker KR (2002) Registration of two root-knot nematode-resistant peanut germplasm lines. Crop Sci 42:314–316PubMedGoogle Scholar
  66. Stam P (1993) Construction of integrated genetic linkage maps by means of a new computer package: JoinMap. Plant J 3:739–744CrossRefGoogle Scholar
  67. Staskawicz BJ (2001) Genetics of plant-pathogen interactions specifying plant disease resistance. Plant Physiol 125:73–76CrossRefPubMedGoogle Scholar
  68. van Berloo R (2008) GGT 2.0: versatile software for visualization and analysis of genetic data. J Hered 99:232–236CrossRefPubMedGoogle Scholar
  69. Wang GL, Ruan DL, Song WY, Sideris S, Chen LL, Pi LY, Zhang SP, Zhang Z, Fauquet C, Gaut BS, Whalen MC, Ronald PC (1998) 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 10:765–779CrossRefPubMedGoogle Scholar
  70. Wang GL, Wu C, Zeng L, He C, Baraoidan M, da Silva F, Williams CE, Ronald PC, Leung H (2004) Isolation and characterization of rice mutants compromised in Xa21-mediated resistance to X. oryzae pv. oryzae. Theor Appl Genet 108:379–384CrossRefPubMedGoogle Scholar
  71. Wang YS, Pi LY, Chen X, Chakrabarty PK, Jiang J, De Leon AL, Liu GZ, Li L, Benny U, Oard J, Ronald PC, Song WY (2006) Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance. Plant Cell 18:3635–3646CrossRefPubMedGoogle Scholar
  72. Yuksel B, Estill JC, Schulze SR, Paterson AH (2005) Organization and evolution of resistance gene analogs in peanut. Mol Genet Genomics 274:248–263CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Ervin D. Nagy
    • 1
  • Ye Chu
    • 2
  • Yufang Guo
    • 1
  • Sameer Khanal
    • 1
  • Shunxue Tang
    • 1
  • Yan Li
    • 1
  • Weibo B. Dong
    • 3
  • Patricia Timper
    • 4
  • Christopher Taylor
    • 1
  • Peggy Ozias-Akins
    • 2
  • C. Corley Holbrook
    • 4
  • Vadim Beilinson
    • 5
  • Niels C. Nielsen
    • 5
  • H. Thomas Stalker
    • 5
  • Steven J. Knapp
    • 1
  1. 1.Institute of Plant Breeding, Genetics, and GenomicsUniversity of GeorgiaAthensUSA
  2. 2.Department of HorticultureUniversity of GeorgiaTiftonUSA
  3. 3.Department of Plant PathologyUniversity of GeorgiaTiftonUSA
  4. 4.U.S. Department of AgricultureAgricultural Research ServiceTiftonUSA
  5. 5.Department of Crop ScienceNorth Carolina State UniversityRaleighUSA

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