Theoretical and Applied Genetics

, Volume 127, Issue 4, pp 867–880 | Cite as

Genetic analysis of resistance to six virus diseases in a multiple virus-resistant maize inbred line

  • Jose Luis Zambrano
  • Mark W. Jones
  • Eric Brenner
  • David M. Francis
  • Adriana Tomas
  • Margaret G. Redinbaugh
Original Paper

Abstract

Key message

Novel and previously known resistance loci for six phylogenetically diverse viruses were tightly clustered on chromosomes 2, 3, 6 and 10 in the multiply virus-resistant maize inbred line, Oh1VI.

Abstract

Virus diseases in maize can cause severe yield reductions that threaten crop production and food supplies in some regions of the world. Genetic resistance to different viruses has been characterized in maize populations in diverse environments using different screening techniques, and resistance loci have been mapped to all maize chromosomes. The maize inbred line, Oh1VI, is resistant to at least ten viruses, including viruses in five different families. To determine the genes and inheritance mechanisms responsible for the multiple virus resistance in this line, F1 hybrids, F2 progeny and a recombinant inbred line (RIL) population derived from a cross of Oh1VI and the virus-susceptible inbred line Oh28 were evaluated. Progeny were screened for their responses to Maize dwarf mosaic virus, Sugarcane mosaic virus, Wheat streak mosaic virus, Maize chlorotic dwarf virus, Maize fine streak virus, and Maize mosaic virus. Depending on the virus, dominant, recessive, or additive gene effects were responsible for the resistance observed in F1 plants. One to three gene models explained the observed segregation of resistance in the F2 generation for all six viruses. Composite interval mapping in the RIL population identified 17 resistance QTLs associated with the six viruses. Of these, 15 were clustered in specific regions of chr. 2, 3, 6, and 10. It is unknown whether these QTL clusters contain single or multiple virus resistance genes, but the coupling phase linkage of genes conferring resistance to multiple virus diseases in this population could facilitate breeding efforts to develop multi-virus resistant crops.

Keywords

Recombinant Inbred Line Single Nucleotide Polymorphism Marker Recombinant Inbred Line Population Area Under Disease Progress Curve Resistance QTLs 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

RIL

Recombinant inbred line

F1

Filial 1

F2

Filial 2

CIM

Composite interval mapping

QTL

Quantitative trait loci

REML

Restricted maximum likelihood

AUDPC

Area under disease progress curve

LOD

Logarithm of the odds

Notes

Acknowledgments

We thank William Belote (Dupont, Stine-Haskell Research Center) for providing a P. maidis colony and to J. Todd (USDA-ARS) for maintaining the insect colonies. We also thank Geoff Parker (Ohio State University) for technical assistance with the SSR genotyping and Brayton Orchard (Ohio State University) for providing the Circos scripts for the QTL graph. JLZ thanks the Instituto Nacional Autónomo de Investigaciones Agropecuarias (INIAP), Ecuador for a fellowship to support his Ph.D. study. Salaries and research support were provided in part by State and Federal funds appropriated to the Ohio Agricultural Research and development Center, The Ohio State University.

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

122_2014_2263_MOESM1_ESM.xlsx (145 kb)
Supplementary material 1 (XLSX 144 kb)
122_2014_2263_MOESM2_ESM.pptx (97 kb)
Supplementary material 2 (PPTX 96 kb)

References

  1. Ali F, Yan J (2012) Disease resistance in maize and the role of molecular breeding in defending against global threats. J Integr Plant Biol 54:134–151PubMedCrossRefGoogle Scholar
  2. Balzarini M, Milligan S (2003) Best linear unbiased prediction (BLUP) for genotype performance. In: Kang MS (ed) Handbook of Formulas and Software for Plant Geneticists and Breeders. The Haworth Press Inc, New York, pp 181–191Google Scholar
  3. Bendahmane A, Kanyuka K, Baulcombe DC (1999) The Rx gene from potato controls separate virus resistance and cell death responses. Plant Cell 11:781–791PubMedCentralPubMedCrossRefGoogle Scholar
  4. Bonamico NC, Di Renzo MA, Ibañez MA, Borghi ML, Díaz DG, Salerno JC, Balzarini MG (2012) QTL analysis of resistance to Mal de Río Cuarto disease in maize using recombinant inbred lines. J Agric Sci 150:619CrossRefGoogle Scholar
  5. Cannon EKS, Birkett SM, Braun BL, Kodavali S, Jennewein DL, Yilmaz A, Antonescu V, Antonescu C, Harper LC, Gardiner JM, Schaeffer ML, Campbell DA, Andorf CA, Andorf C, Lisch D, Koch KE, McCarty DR, Quackenbush J, Grotewold E, Lushbough CM, Sen TZ, Lawrence CJ (2011) POPcorn: an online resource providing access to distributed and diverse maize project data. Int J Plant Genomics 2011:Article ID 923035Google Scholar
  6. Chisholm ST, Parra MA, Anderberg RJ, Carrington JC (2001) Arabidopsis RTM1 and RTM2 genes function in phloem to restrict long-distance movement of tobacco etch virus. Plant Physiol 127:1667–1675PubMedCentralPubMedCrossRefGoogle Scholar
  7. Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971PubMedCentralPubMedGoogle Scholar
  8. Clewer AG, Scarisbrick DH (2001) Practical statistics and experimental design for plant and crop science. Wiley, ChichesterGoogle Scholar
  9. Coaker GL (2003) Genetic and biochemical characterization of resistance to bacterial canker of tomato caused by Clavibacter michiganensis subsp. michiganensis. Ph.D. Dissertation, The Ohio State UniversityGoogle Scholar
  10. Cosson P, Schurdi-Levraud V, Le QH, Sicard O, Caballero M, Roux F, Le Gall O, Candresse T, Revers F (2012) The RTM resistance to potyviruses in Arabidopsis thaliana: natural variation of the RTM genes and evidence for the implication of additional genes. PLoS ONE 7:e39169PubMedCentralPubMedCrossRefGoogle Scholar
  11. De Souza IRP, Schuelter AR, Guimaraes CT, Schuster I, De Oliveira E, Redinbaugh M (2008) Mapping QTL contributing to SCMV resistance in tropical maize. Hereditas 145:167–173CrossRefGoogle Scholar
  12. Di Renzo MA, Bonamico NC, Diaz DG, Ibanez MA, Faricelli ME, Balzarini MG, Salerno JC (2004) Microsatellite markers linked to QTL for resistance to Mal de Rio Cuarto disease in Zea mays L. J Agric Sci 142:289–295CrossRefGoogle Scholar
  13. Diaz-Pendon J, Truniger V, Nieto C, Garcia-Mas J, Bendahmane A, Aranda M (2004) Advances in understanding recessive resistance to plant viruses. Mol Plant Pathol 5:223–233PubMedCrossRefGoogle Scholar
  14. Ding J, Li H, Wang Y, Zhao R, Zhang X, Chen J, Xia Z, Wu J (2012) Fine mapping of Rscmv2, a major gene for resistance to sugarcane mosaic virus in maize. Mol Breeding 30:1593–1600CrossRefGoogle Scholar
  15. Dintinger J, Verger D, Caiveau S, Risterucci AM, Gilles J, Chiroleu F, Courtois B, Reynaud B, Hamon P (2005) Genetic mapping of maize stripe disease resistance from the Mascarene source. Theor Appl Genet 111:347–359PubMedCrossRefGoogle Scholar
  16. Dussle CM, Melchinger AE, Kuntze L, Stork A, Luebberstedt T (2000) Molecular mapping and gene action of Scm1 and Scm2, two major QTL contributing to SCMV resistance in maize. Plant Breed 119:299–303CrossRefGoogle Scholar
  17. Friedman AR, Baker BJ (2007) The evolution of resistance genes in multi-protein plant resistance systems. Curr Opin Genet Dev 17:493–499PubMedCrossRefGoogle Scholar
  18. Gomez P, Rodriguez-Hernandez AM, Moury B, Aranda MA (2009) Genetic resistance for the sustainable control of plant virus diseases: breeding, mechanisms and durability. Eur J Plant Pathol 125:1–22CrossRefGoogle Scholar
  19. Gururani MA, Venkatesh J, Upadhyaya CP, Nookaraju A, Pandey SK, Park SW (2012) Plant disease resistance genes: current status and future directions. Physiol Mol Plant Pathol 78:51–65CrossRefGoogle Scholar
  20. Hull R (2002) Matthew’s Plant Virology. Academic Press, San DiegoGoogle Scholar
  21. Hunt RE, Nault LR, Gingery RE (1988) Evidence for infectivity of Maize chlorotic dwarf virus and for a helper component in its leafhopper transmission. Phytopathol 78:499–504CrossRefGoogle Scholar
  22. Ingvardsen CR, Xing Y, Frei UK, Luebberstedt T (2010) Genetic and physical fine mapping of Scmv2, a potyvirus resistance gene in maize. Theor Appl Genet 120:1621–1634PubMedCrossRefGoogle Scholar
  23. Jansen RC, Stam P (1994) High-resolution of quantitative traits into multiple loci via interval mapping. Genetics 136:1447–1455PubMedCentralPubMedGoogle Scholar
  24. Jones MW, Redinbaugh MG, Anderson RJ, Louie R (2004) Identification of quantitative trait loci controlling resistance to Maize chlorotic dwarf virus. Theor Appl Genet 110:48–57PubMedCrossRefGoogle Scholar
  25. Jones MW, Redinbaugh MG, Louie R (2007) The Mdm1 locus and maize resistance to Maize dwarf mosaic virus. Plant Dis 91:185–190CrossRefGoogle Scholar
  26. Jones E, Chu W, Ayele M, Ho J, Bruggeman E, Yourstone K, Rafalski A, Smith OS, McMullen MD, Bezawada C, Warren J, Babayev J, Basu S, Smith S (2009) Development of single nucleotide polymorphism (SNP) markers for use in commercial maize (Zea mays L.) germplasm. Mol Breed 24:165–176CrossRefGoogle Scholar
  27. Jones MW, Boyd EC, Redinbaugh MG (2011) Responses of maize (Zea mays L.) near isogenic lines carrying Wsm1, Wsm2 and Wsm3 to three viruses in the Potyviridae. Theor Appl Genet 123:729–740PubMedCrossRefGoogle Scholar
  28. Kang B, Yeam I, Jahn MM (2005) Genetics of plant virus resistance. Annu Rev Phytopathol 43:581–621PubMedCrossRefGoogle Scholar
  29. Kao CH, Zeng ZB (2002) Modeling epistasis of quantitative trait loci using Cockerham’s model. Genetics 160:1243–1261PubMedCentralPubMedGoogle Scholar
  30. Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175CrossRefGoogle Scholar
  31. Krzywinski MI, Schein JE, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA (2009) Circos: an information aesthetic for comparative genomics. Genome Res. doi: 10.1101/gr.092759.109 PubMedCentralPubMedGoogle Scholar
  32. Kyetere DT, Ming R, McMullen MD, Pratt RC, Brewbaker J, Musket T (1999) Genetic analysis of tolerance to maize streak virus in maize. Genome 42:20–26CrossRefGoogle Scholar
  33. Lanfermeijer FC, Dijkhuis J, Sturre MJG, de Haan P, Hille J (2003) Cloning and characterization of the durable tomato mosaic virus resistance gene Tm-2(2) from Lycopersicon esculentum. Plant Mol Biol 52:1037–1049PubMedCrossRefGoogle Scholar
  34. Lapierre H, Signoret PA (2004) Viruses and virus diseases of Poaceae (Gramineae). INRA ED, ParisGoogle Scholar
  35. Lazaro-Mixteco PE, Dinkova TD (2012) Identification of proteins from cap-binding complexes by mass spectrometry during maize (Zea mays L.) germination. J Mex Chem Soc 56:36–50Google Scholar
  36. Loesch PJ, Zuber MS (1967) An inheritance study of resistance to maize dwarf mosaic virus in corn (Zea Mays L). Agron J 59:423–426CrossRefGoogle Scholar
  37. Louie R (1986) Effects of genotype and inoculation protocols on resistance evaluation of maize to maize dwarf mosaic virus strains. Phytopathol 76:769–773CrossRefGoogle Scholar
  38. Louie R (1995) Vascular puncture of maize kernels for the mechanical transmission of maize white line mosaic virus and other viruses of maize. Phytopathol 85:139–143CrossRefGoogle Scholar
  39. Louie R, Anderson RJ (1993) Evaluation of maize chlorotic dwarf virus resistance in maize with multiple inoculations by Graminella nigrifrons (Homoptera: Cicadellidae). J Econ Entomol 86:1579–1583Google Scholar
  40. Louie R, Knoke JK, Reichard DL (1983) Transmission of maize dwarf mosaic virus with solid-stream inoculum. Plant Dis 67:1328–1331CrossRefGoogle Scholar
  41. Louie R, Abt JJ, Anderson RJ, Redinbaugh MG, Gordon DT (2000) Maize necrotic streak virus, a new maize virus with similarity to species of the family Tombusviridae. Plant Dis 84:1133–1139CrossRefGoogle Scholar
  42. Louie R, Redinbaugh MG, Anderson RJ, Jones MW (2002) Registration of maize germplasm Oh1VI. Crop Sci 42:991–991CrossRefGoogle Scholar
  43. Lozano R, Ponce O, Ramirez M, Mostajo N, Orjeda G (2012) Genome-wide identification and mapping of NBS-encoding resistance genes in Solanum tuberosum group phureja. PLoS ONE 7:e34775PubMedCentralPubMedCrossRefGoogle Scholar
  44. Lubberstedt T, Ingvardsen C, Melchinger AE, Xing Y, Salomon R, Redinbaugh MG (2006) Two chromosome segments confer multiple potyvirus resistance in maize. Plant Breed 125:352–356CrossRefGoogle Scholar
  45. McMullen MD, Louie R (1989) The linkage of molecular markers to a gene controlling the symptom response in maize to Maize dwarf mosaic virus. Mol Plant Microbe Interact 2:309–314CrossRefGoogle Scholar
  46. McMullen MD, Louie R (1991) Identification of a gene for resistance to wheat streak mosaic virus in maize. Phytopathol 81:624–627CrossRefGoogle Scholar
  47. McMullen MD, Louie R, Simcox KD, Jones MW (1994) Three genetic loci control resistance to wheat streak mosaic virus in the maize inbred Pa405. Mol Plant Microbe Interact 7:708–712CrossRefGoogle Scholar
  48. Ming R, Brewbaker JL, Pratt RC, Musket TA, McMullen MD (1997) Molecular mapping of a major gene conferring resistance to maize mosaic virus. Theor Appl Genet 95:271–275CrossRefGoogle Scholar
  49. Nault LR, Knoke JK (1981) Maize vectors. In: Knoke JK, Gordon DT, Scott GE (eds) Virus and virus-like diseases of maize in the United States. Southern Cooperative Series Bulletin, Wooster, pp 77–84Google Scholar
  50. Redinbaugh MG, Pratt RC (2009) Virus resistance. In: Bennetzen JL, Hake SC (eds) Handbook of maize: its biology. Springer, New York, pp 251–268CrossRefGoogle Scholar
  51. Redinbaugh MG, Houghton W, Salomon R, Creamer R, Hogenhout SA, Gordon DT, Ackerman J, Meulia T, Seifers DL, Abt JJ, Styer WE, Anderson RJ (2002) Maize fine streak virus, a new leafhopper-transmitted rhabdovirus. Phytopathol 92:1167–1174CrossRefGoogle Scholar
  52. Schnable PS, Ware D, Fulton RS et al (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326:1112–1115PubMedCrossRefGoogle Scholar
  53. Slykhuis JT (1955) Aceria tulipae Keifer (Acarina: Eriophyidae) in relation to spread of wheat streak mosaic virus. Phytopathol 45:116–128Google Scholar
  54. Stewart LR, Haque MA, Jones MW, Redinbaugh MG (2013) Response of maize (Zea mays L.) lines carrying Wsm1, Wsm2, and Wsm3 to the potyviruses Johnsongrass mosaic virus and Sorghum mosaic virus. Molecular Breed 31:289–297Google Scholar
  55. Tao YF, Jiang L, Liu QQ, Zhang Y, Zhang R, Ingvardsen CR, Frei UK, Wang BB, Lai JS, Lubberstedt T, Xu ML (2013) Combined linkage and association mapping reveals candidates for Scmv1, a major locus involved in resistance to sugarcane mosaic virus (SCMV) in maize. BMC Plant Biol 13:162PubMedCrossRefGoogle Scholar
  56. Todd JC, Hoy C, Hogenhout SA, Ammar E, Redinbaugh MG (2010) Plant host range and leafhopper transmission of Maize fine streak virus. Phytopathol 100:1138–1145CrossRefGoogle Scholar
  57. Truniger V, Nieto C, Gonzalez-Ibeas D, Aranda M (2008) Mechanism of plant eIF4E-mediated resistance against a carmovirus (Tombusviridae): cap-independent translation of a viral RNA controlled in cis by an (a)virulence determinant. Plant J 56:716–727PubMedCrossRefGoogle Scholar
  58. Uyemoto JK, Bockelman DL, Claflin LE (1980) Severe outbreak of corn lethal necrosis disease in Kansas. Plant Dis 64:99–100CrossRefGoogle Scholar
  59. van Ooijen JW, Voorrips RE (2001) JoinMap version 3.0, software for the calculation of genetic linkage maps. Plant Research Int, The NetherlandsGoogle Scholar
  60. van Ooijen JW, Boer MP, Jansen RC, Maliepaard C (2002) MapQTL 4.0, Software for the calculation of QTL positions on genetic maps. Plant Research Int, The NetherlandsGoogle Scholar
  61. Vasquez J, Mora E (2007) Incidence of and yield loss caused by Maize rayado fino virus in maize cultivars in Ecuador. Euphytica 153:339–342CrossRefGoogle Scholar
  62. Wang G, Chen Y, Zhao J, Li L, Korban SS, Wang F, Li J, Dai J, Xu M (2007) Mapping of defense response gene homologs and their association with resistance loci in maize. J Integr Plant Biol 49:1580–1598CrossRefGoogle Scholar
  63. Wangai AW, Redinbaugh MG, Kinyua ZM, Miano DW, Leley PK, Kasina M, Mahuku G, Scheets K, Jeffers D (2012) First report of Maize chlorotic mottle virus and Maize lethal necrosis in Kenya. Plant Dis 96:1582–1582CrossRefGoogle Scholar
  64. Welz HG, Schechert A, Pernet A, Pixley KV, Geiger HH (1998) A gene for resistance to the maize streak virus in the African CIMMYT maize inbred line CML202. Mol Breed 4:147–154CrossRefGoogle Scholar
  65. Wisser RJ, Nelson RJ, Balint-Kurti P (2006) The genetic architecture of disease resistance in maize: a synthesis of published studies. Phytopathol 96:120–129CrossRefGoogle Scholar
  66. Wu J, Ding J, Du Y, Xu Y, Zhang X (2007) Genetic analysis and molecular mapping of two dominant complementary genes determining resistance to Sugarcane mosaic virus in maize. Euphytica 156:355–364CrossRefGoogle Scholar
  67. Xia XC, Melchinger AE, Kuntze L, Lubberstedt T (1999) Quantitative trait loci mapping of resistance to Sugarcane mosaic virus in maize. Phytopathol 89:660–667CrossRefGoogle Scholar
  68. Xiao W, Zhao J, Fan S, Li L, Dai J, Xu M (2007) Mapping of genome-wide resistance gene analogs (RGAs) in maize (Zea mays L.). Theor Appl Genet 115:501–508PubMedCrossRefGoogle Scholar
  69. Zambrano JL, Francis MD, Redinbaugh MG (2013) Identification of resistance to Maize rayado fino virus in maize inbred lines. Plant Dis 97:1418–1423CrossRefGoogle Scholar
  70. Zhang SH, Li XH, Wang ZH, George ML, Jeffers D, Wang FG, Liu XD, Li MS, Yuan LX (2003) QTL mapping for resistance to SCMV in Chinese maize germplasm. Maydica 48:307–312Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg (outside the USA) 2014

Authors and Affiliations

  • Jose Luis Zambrano
    • 1
    • 2
  • Mark W. Jones
    • 3
  • Eric Brenner
    • 3
  • David M. Francis
    • 1
  • Adriana Tomas
    • 4
  • Margaret G. Redinbaugh
    • 3
  1. 1.Department of Horticulture and Crop ScienceThe Ohio State University-Ohio Agriculture Research and Development Center (OSU-OARDC)WoosterUSA
  2. 2.Instituto Nacional Autónomo de Investigaciones Agropecuarias (INIAP)Programa Nacional del MaízQuitoEcuador
  3. 3.USDA, Agricultural Research Service, Corn, Soybean and Wheat Quality Research Unit, and Department of Plant PathologyOSU-OARDCWoosterUSA
  4. 4.Genetic DiscoveryDuPont Agricultural BiotechnologyWilmingtonUSA

Personalised recommendations