Skip to main content
SpringerLink
Log in

Re-evaluation of the inheritance for root-knot nematode resistance in the Upland cotton germplasm line M-120 RNR revealed two epistatic QTLs conferring resistance

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

We report a second major QTL for root-knot nematode resistance in the highly resistant Upland cotton line M-120RNR and show epistasis between two resistant QTLs with different mechanisms conferring resistance.

Abstract

In an earlier study, we identified a major QTL on Chromosome 11 associated with resistance to root-knot nematode in the M-120 RNR Upland cotton line (Gossypium hirsutum L.) of the Auburn 623 RNR source. Herein, we re-evaluated the genetics of the resistance to root-knot nematode in the M-120 RNR × Pima S-6 population by linkage mapping using recently published SSR markers. The QTL analysis detected two regions significantly associated with the resistance phenotype. In addition to the QTL previously identified on Chromosome 11 (qMi-C11), a major QTL was identified on Chromosome 14 (qMi-C14). The resistance locus on qMi-C11 originated from the Clevewilt parent, while the qMi-C14 locus originated from the other resistant parent, Mexico Wild Jack Jones. The qMi-C14 locus had logarithms of odds score of 17 and accounted for 45 % of the total phenotype variation in egg production. It was also associated with galling index, but the percent variation explained was only 6 %, suggesting that the qMi-C11 locus had a much stronger effect on root gall suppression than egg production, while the qMi-C14 locus had a stronger effect on egg production than galling. The results also suggest that the transgressive segregation observed in the development of Auburn 623 RNR was due to the pyramiding of at least two main effect QTLs as well as an additive-by-additive epistatic effects between the two resistant loci. The SSRs markers tightly linked to the qMi-C11 and qMi-C14 loci will greatly facilitate the improvement of RKN resistance in cotton via marker-assisted breeding.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Blasingame D, Patel MV (2005) Cotton disease loss estimate committee report. In: Proceedings of Beltwide Cotton Conference, New Orleans. National Cotton Council of America, Memphis, pp 259–262

  • Blenda A, Scheffler J, Scheffler B, Palmer M, Lacape JM, Yu JZ, Jesudurai C, Jung S, Muthukumar S, Yellambalase P, Ficklin S, Staton M, Eshelman R, Ulloa M, Saha S, Burr B, Liu SL, Zhang TZ, Fang DQ, Pepper A, Kumpatla S, Jacobs J, Tomkins J, Cantrell R, Main D (2006) CMD: a cotton microsatellite database resource for Gossypium genomics. BMC Genome 7:132

    Article  Google Scholar 

  • Bridge J, Page SLR (1980) Estimation of root-knot nematode infestation levels on roots using a rating chart. Trop Pest Manag 26:296–298

    Article  Google Scholar 

  • Creech RG, Jenkins JN, Tang B, Lawrence GW, Mccarty JC (1995) Cotton resistance to root-knot nematode. 1. Penetration and reproduction. Crop Sci 35:365–368

    Article  Google Scholar 

  • Davis RF, Chee PW, Lubbers EL, May OL (2011) Registration of GA 120R1B3 germplasm line of cotton. J Plant Regist 5:384–387

    Article  Google Scholar 

  • Guo WZ, Cai CP, Wang CB, Han ZG, Song XL, Wang K, Niu XW, Wang C, Lu KY, Shi B, Zhang TZ (2007) A microsatellite-based, gene-rich linkage map reveals genome structure, function and evolution in Gossypium. Genetics 176:527–541

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Guo Y, Saha S, Yu JZ, Jenkins JN, Kohel RJ, Scheffler BE, Stelly David M (2008) BAC-derived SSR markers chromosome locations in cotton. Euphytica 161:361–370. doi:10.1007/s10681-007-9585-1

    Google Scholar 

  • Gutierrez OA, Jenkins JN, McCarty JC, Wubben MJ, Hayes RW, Callahan FE (2010) SSR markers closely associated with genes for resistance to root-knot nematode on chromosomes 11 and 14 of upland cotton. Theor Appl Genet 121:1323–1337

    Article  CAS  PubMed  Google Scholar 

  • Han ZG, Guo WZ, Song XL, Zhang TZ (2004) Genetic mapping of EST-derived microsatellites from the diploid Gossypium arboreum in allotetraploid cotton. Mol Genet Genomics 272:308–327

    Article  CAS  PubMed  Google Scholar 

  • Han ZG, Wang CB, Song XL, Guo WZ, Gou JY, Li CH, Chen XY, Zhang TZ (2006) Characteristics, development and mapping of Gossypium hirsutum derived EST-SSRs in allotetraploid cotton. Theor Appl Genet 112:430–439

    Article  CAS  PubMed  Google Scholar 

  • Hussey RS, Baker KR (1973) A comparison of methods of collecting inocula of Meloidogyne spp., including a new technique. Plant Dis Rep 57:1025–1028

    Google Scholar 

  • Jenkins JN, Creech RG, Tang B, Lawrence GW, Mccarty JC (1995) Cotton resistance to root-knot nematode. 2. Post-penetration development. Crop Sci 35:369–373

    Article  Google Scholar 

  • Jenkins JN, McCarty JC, Wubben MJ, Hayes R, Gutierrez OA, Callahan F, Deng D (2012) SSR markers for marker assisted selection of root-knot nematode (Meloidogyne incognita) resistant plants in cotton (Gossypium hirsutum L.). Euphytica 183:49–54

    Article  CAS  Google Scholar 

  • Koenning SR, Wrather JA, Kirkpatrick TL, Walker NR, Starr JL, Mueller JD (2004) Plant-parasitic nematodes attacking cotton in the United States: old and emerging production challenges. Plant Dis 88:100–113

    Article  Google Scholar 

  • Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175

    Article  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincolnn SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  CAS  PubMed  Google Scholar 

  • McPherson MG, Jenkins JN, McCarty JC, Watson CE (1995) Combining ability analysis of root-knot nematode resistance in cotton. Crop Sci 35:373–375

    Article  Google Scholar 

  • McPherson MG, Jenkins JN, Watson CE, McCarty JC (2004) Inheritance of root-knot nematode resistance in M-315 RNR and M78-RNR cotton. J Cotton Sci 8:154–161

    Google Scholar 

  • Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis. A rapid method to detect markers in specific genomic regions by using segregating population. Proc Natl Acad Sci USA 88:6553–6558

    Article  Google Scholar 

  • Mota F, Alves G, Giband M, Gomes A, Sousa F, Mattos V, Barbosa V, Barroso P, Nicole M, Peixoto J (2012) New sources of resistance to Meloidogyne incognita race 3 in wild cotton accessions and histological characterization of the defence mechanisms. Plant Pathol. doi:10.1111/ppa.12022

    Google Scholar 

  • Nguyen TB, Giband M, Brottier P, Risterucci AM, Lacape JM (2004) Wide coverage of the tetraploid cotton genome using newly developed microsatellite markers. Theor Appl Genet 109:167–175

    Article  CAS  PubMed  Google Scholar 

  • Nicholas KB, Nicholas HB Jr (1997) GeneDoc: a tool for editing and annotating multiple sequence alignments. Distributed by the author (available at http://www.psc.edu/biomed/genedoc)

  • Niu C, Hinchliffe DJ, Cantrell RG, Wang CL, Roberts PA, Zhang JF (2007) Identification of molecular markers associated with root-knot nematode resistance in upland cotton. Crop Sci 47:951–960

    Article  CAS  Google Scholar 

  • Noe JP (1985) Analysis and interpretation of data from nematological experiments. In: Barker KR CC, Sasser JN (eds) An advanced treatise on Meloidogyne vol II, Methodology, North Carolina State University Graphics, Raleigh, pp 187–196

  • Ogallo JL, Goodell PB, Eckert J, Roberts PA (1997) Evaluation of NemX, a new cultivar of cotton with high resistance to Meloidogyne incognita. J Nematol 29:531–537

    CAS  PubMed Central  PubMed  Google Scholar 

  • Reddy OUK, Pepper AE, Ibrokhim A, Saha S, Jenkins JN, Brooks T, Bolek Y, El-Zik KM (2001) New dinucleotide and trinucleotide microsatellite marker resources for cotton genome research. J Cotton Sci 5:103–113

    Google Scholar 

  • Robinson AF, Bowman DT, Cook CG, Jenkins JN, Jones JE, May LO, Oakley SR, Oliver MJ, Roberts PA, Robinson M, Smith CW, Starr JL, Stewart JM (2001) Nematode Resistance. In: Kirkpatrick TL, Rothrock CS (eds) Compendium of cotton diseases. The American Phytopathological Society, St. Paul, pp 68–72

    Google Scholar 

  • Rong J, Abbey C, Bowers JE, Brubaker CL, Chang C, Chee PW, Delmonte TA, Ding X, Garza JJ, Marler BS, Park CH, Pierce GJ, Rainey KM, Rastogi VK, Schulze SR, Trolinder NL, Wendel JF, Wilkins TA, Williams-Coplin TD, Wing RA, Wright RJ, Zhao X, Zhu L, Paterson AH (2004) A 3347-locus genetic recombination map of sequence-tagged sites reveals features of genome organization, transmission and evolution of cotton (Gossypium). Genetics 166:389–417

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shen XL, Van Becelaere G, Kumar P, Davis RF, May OL, Chee PW (2006) QTL mapping for resistance to root-knot nematodes in the M-120 RNR upland cotton line (Gossypium hirsutum L.) of the Auburn 623 RNR source. Theor Appl Genet 113:1539–1549

    Article  CAS  PubMed  Google Scholar 

  • Shen XL, He YJ, Lubbers EL, Davis RF, Nichols RL, Chee PW (2010) Fine mapping QMi-C11 a major QTL controlling root-knot nematodes resistance in upland cotton. Theor Appl Genet 121:1623–1631

    Article  PubMed  Google Scholar 

  • Shepherd RL (1974a) Registration of Auburn 623 RNR cotton germplasm. Crop Sci 14:911

    Article  Google Scholar 

  • Shepherd RL (1974b) Transgressive segregation for root-knot nematode resistance in cotton. Crop Sci 14:872–875

    Article  Google Scholar 

  • Shepherd RL (1979) A quantitative technique for evaluating cotton for root-knot nematode resistance. Phytopathology 69:427–430

    Article  Google Scholar 

  • Shepherd RL, McCarty JC, Jenkins JN (1996) Registration of nine cotton germplasm lines resistance to root-knot nematode. Crop Sci 36:820

    Article  Google Scholar 

  • Starr JL, Carneiro RG, Ruano O (2005) Nematode parasites of cotton and other tropical fiber crops. In: Luc M, Sikora RA, Bridge J (eds) Plant parasitic nematodes in subtropical and tropical agriculture, 2nd edn. Wallingford, UK, pp 733–750

  • Starr JL, Koenning SR, Eirkpatrick TL, Robinson AF, Roberts PA, Nichols RL (2007) The future of nematode management in cotton. J Nematol 39:283–294

    CAS  PubMed Central  PubMed  Google Scholar 

  • Taliercio E, Allen RD, Essenberg M, Klueva N, Nguyen H, Patil MA, Payton P, Millena ACM, Phillips AL, Pierce ML, Scheffler B, Turley R, Wang J, Zhang DS, Scheffler J (2006) Analysis of ESTs from multiple Gossypium hirsutum tissues and identification of SSRs. Genome 49:306–319

    Article  CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: Xexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882

    Article  Google Scholar 

  • Wang S, Basten C, Zeng Z (2005) Windows QTL cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh

  • Wang CL, Ulloa M, Roberts PA (2008) A transgressive segregation factor (RKN2) in Gossypium barbadense for nematode resistance clusters with gene rkn1 in G. hirsutum. Mol Genet Genomics 279:41–52

    Article  CAS  PubMed  Google Scholar 

  • Wang CL, Ulloa M, Mullens TR, Yu JZ, Roberts PA (2012) QTL analysis for transgressive resistance to root-knot nematode in interspecific cotton (Gossypium spp.) progeny derived from susceptible parents. PLoS One 7(4):e34874. doi:10.1371/journal.pone.0034874

  • Wu X, Blake S, Sleper DA, Shannon JG, Cregan P, Nguyen HT (2009) QTL, additive and epistatic effects for SCN resistance in PI 437654. Theor Appl Genet 118:1093–1105

    Article  CAS  PubMed  Google Scholar 

  • Xiao J, Wu K, Fang DD, Stelly DM, Yu J, Cantrell R (2009) New SSR markers for use in cotton (Gossypium spp.) improvement. J Cotton Sci 13:75–157

    CAS  Google Scholar 

  • Yang J, Hu C, Hu H, Yu R, Xia Z, Ye X, Zhu J (2008) QTLNetwork: mapping and visualizing genetic architecture of complex traits in experimental populations. Bioinformatics 24:721–723

    Article  PubMed  Google Scholar 

  • Ynturi P, Jenkins JN, McCarty JC, Gutierrez OA, Saha S (2006) Association of root-knot nematode resistance genes with simple sequence repeat markers on two chromosomes in cotton. Crop Sci 46:2670–2674

    Article  CAS  Google Scholar 

  • Zhang J, Guo WZ, Zhang TZ (2002) Molecular linkage map of allotetraploid cotton (Gossypium hirsutum L. × Gossypium barbadense L.) with a haploid population. Theor Appl Genet 105:1166–1174

    Article  CAS  PubMed  Google Scholar 

  • Zhou E, Star JL, Smith CW (1999) Inheritance of resistance to Meloidogyne incognita in the cotton cultivar Acala NemX. J Nematol 31:584–585

    Google Scholar 

Download references

Acknowledgments

We thank the Zhang lab for SSR primer sequences; Jennifer McCurdy and Rippy Singh for technical assistance; Ed Lubbers for valuable comments; and gratefully acknowledge the financial support from the Georgia Cotton Commission and Cotton Incorporated.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

The experiments comply with the current laws of the country in which they were performed.

Author information

Author notes

  1. Xinlian Shen

    Present address: Biotechnology Institute, Jiangsu Academy of Agricultural Sciences, Nanjing, 210014, China

  2. Guillermo Van Becelaere

    Present address: Monsanto Company, Ruta 8, Km 214, 2718, Fontezuela (B), Argentina

Authors and Affiliations

  1. Cotton Molecular Breeding Laboratory, University of Georgia, Tifton, GA, 31793, USA

    Yajun He, Pawan Kumar, Xinlian Shen, Guillermo Van Becelaere & Peng W. Chee

  2. Crop Protection and Management Research Unit, USDA-ARS, Tifton, GA, 31793, USA

    Richard F. Davis

  3. GA Research Station, Delta and Pine Land Company, 381 Williams Gibbs Rd, Tifton, GA, 31793, USA

    O. Lloyd May

  4. Cotton Incorporated, 6399 Weston Parkway, Cary, NC, 27513, USA

    Robert L. Nichols

Authors
  1. Yajun He
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pawan Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xinlian Shen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Richard F. Davis
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Guillermo Van Becelaere
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. O. Lloyd May
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Robert L. Nichols
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Peng W. Chee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Peng W. Chee.

Additional information

Communicated by M. Gore.

Y. He and P. Kumar contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

He, Y., Kumar, P., Shen, X. et al. Re-evaluation of the inheritance for root-knot nematode resistance in the Upland cotton germplasm line M-120 RNR revealed two epistatic QTLs conferring resistance. Theor Appl Genet 127, 1343–1351 (2014). https://doi.org/10.1007/s00122-014-2302-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-014-2302-2

Keywords

Search

Navigation