Abstract
Key message
Genetic analysis of MIC-3 transgene with RKN resistance QTLs provides insight into the resistance regulatory mechanism and provides a framework for testing additional hypotheses.
Abstract
Resistance to root-knot nematode (RKN) (Meloidogyne incognita) in Upland cotton (Gossypium hirsutum) is mediated by two major quantitative trait loci (QTL) located on chromosomes 11 and 14. The MIC-3 (Meloidogyne Induced Cotton3) protein accumulates specifically within the immature galls of RKN-resistant plants that possess these QTLs. Recently, we showed that MIC-3 overexpression in an RKN-susceptible cotton genotype suppressed RKN egg production but not RKN-induced root galling. In this study, the MIC-3 overexpression construct T-DNA in the single-copy transgenic line ‘14-7-1’ was converted into a codominant molecular marker that allowed the marker assisted selection of F2:3 cotton lines, derived from a cross between 14-7-1 and M-240 RNR, having all possible combinations of the chromosomes 11 and 14 QTLs with and without the MIC-3 overexpression construct. Root-knot nematode reproduction (eggs g−1 root) and severity of RKN-induced root galling were assessed in these lines. We discovered that the addition of MIC-3 overexpression suppressed RKN reproduction in lines lacking both resistance QTLs and in lines having only the chromosome 14 QTL, suggesting an additive effect of the MIC-3 construct with this QTL. In contrast, MIC-3 overexpression did not improve resistance in lines having the single chromosome 11 QTL or in lines having both resistance QTLs, suggesting an epistatic interaction between the chromosome 11 QTL and the MIC-3 construct. Overexpression of MIC-3 did not affect the severity of RKN-induced root galling regardless of QTL genotype. These data provide new insights into the relative order of action of the chromosomes 11 and 14 QTLs and their potential roles in regulating MIC-3 expression as part of the RKN resistance response.
Similar content being viewed by others
References
Buriev ZT, Saha S, Abdurakhmonov IY, Jenkins JN, Abdukarimov A, Scheffler BE, Stelly DM (2010) Clustering, haplotype diversity and locations of MIC-3: a unique root-specific defense-related gene family in Upland cotton (Gossypium hirsutum L.). Theor Appl Genet 120:587–606
Callahan FE, Jenkins JN, Creech RG, Lawrence GW (1997) Changes in cotton root proteins correlated with resistance to root knot nematode development. J Cotton Sci 1:38–47
Callahan FE, Zhang X-D, Ma D-P, Jenkins JN, Hayes RW, Tucker ML (2004) Comparison of MIC-3 protein accumulation in response to root-knot nematode infection in cotton lines displaying a range of resistance levels. J Cotton Sci 8:186–190
Gutierrez OA, Stelly DM, Saha S, Jenkins JN, McCarty JC Jr, Raska DA, Scheffler BE (2009) Integrative placement and orientation of non-redundant SSR loci in cotton linkage groups by deficiency analysis. Mol Breed 23:693–707
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
He Y, Kumar P, Shen X, Davis RF, Becelaere GV, May OL, Nichols RL, Chee PW (2014) 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
Hussey RS, Barker KR (1973) A comparison of methods of collecting inocula of Meloidogyne spp. Including a new technique. Plant Dis Report 57:1025–1028
Jenkins JN, Creech RG, Tang B, Lawrence GW, McCarty JC (1995) Cotton resistance to root-knot nematode: II. Post-penetration development. Crop Sci 35:369–373
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
Lawrence KS et al (2015) Cotton disease loss estimate committee report, 2014. In: 2015 Beltwide cotton conferences, San Antonio, pp 188–190
McPherson MG, Jenkins JN, Watson CE, McCarty JC Jr (2004) Inheritance of root-knot nematode resistance in M-315 RNR and M78-RNR cotton. J Cotton Sci 8:154–161
Mitchum MG, Hussey RS, Baum TJ, Wang X, Elling AA, Wubben MJ, Davis EL (2013) Nematode effector proteins: an emerging paradigm of parasitism. New Phytol. doi:10.1111/nph.12323
Shen X, Becelaere GV, Kumar P, Davis RF, May OL, Chee P (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
Shepherd RL (1983) Indices of resistance to root-knot nematodes for primitive race stocks of upland cotton. Agricultural reviews and manuals. ARM-S—United States, Dept. of Agriculture. Agricultural Research Service, Southern Region. Agric Rev Man ARM-S US Dep Agric Agric Res Serv Res South Reg (33)
Shepherd RL, McCarty JC Jr, Jenkins JN, Parrott WL (1996) Registration of nine cotton germplasm lines resistant to root-knot nematode. Crop Sci 36:820
Wendel JF, Brubaker C, Alvarez I, Cronn R, Stewart JM (2009) Evolution and natural history of the cotton genus. In: Paterson AH (ed) Genetics and genomics of cotton. Springer, New York, pp 3–22
Wubben MJ, Callahan FE, Hayes RW, Jenkins JN (2008) Molecular characterization and temporal expression analyses indicate that the MIC (Meloidogyne Induced Cotton) gene family represents a novel group of root-specific defense-related genes in upland cotton (Gossypium hirsutum L.). Planta 228:111–123
Wubben MJ, Callahan FE, Velten J, Burke JJ, Jenkins JN (2015) Overexpression of MIC-3 indicates a direct role for the MIC gene family in mediating Upland cotton (Gossypium hirsutum) resistance to root-knot nematode (Meloidogyne incognita). Theor Appl Genet 128:199–209
Ynturi P, Jenkins JN, McCarty JC Jr, 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
Zhang X-D, Callahan FE, Jenkins JN, Ma D-P, Karaca M, Saha S, Creech RG (2002) A novel root-specific gene, MIC-3, with increased expression in nematode-resistant cotton (Gossypium hirsutum L.) after root-knot nematode infection. Biochem Biophys Acta 1576:214–218
Zhang T, Hu Y, Jiang W, Fang L, Guan X, Chen J, Zhang J, Saski CA, Scheffler BE, Stelly DM, Hulse-Kemp AM, Wan Q, Liu B, Liu C, Wang S, Pan M, Wang Y, Wang D, Ye W, Chang L, Zhang W, Song Q, Kirkbride RC, Chen X, Dennis E, Llewellyn DJ, Peterson DG, Thaxton P, Jones DC, Wang Q, Xu X, Zhang H, Wu H, Zhou L, Mei G, Chen S, Tian Y, Xiang D, Li X, Ding J, Zuo Q, Tao L, Liu Y, Li J, Lin Y, Hui Y, Cao Z, Cai C, Zhu X, Jiang Z, Zhou B, Guo W, Li R, Chen ZJ (2015) Sequencing of allotetraploid cotton (Gossypium hirsutum L. acc. TM-1) provides a resource for fiber improvement. Nat Biotechnol 33:531–540
Acknowledgments
The authors thank Drs. John Brooks and Mike McLaughlin (USDA-ARS) for their critical review of the manuscript and helpful suggestions.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflicts of interest.
Additional information
Communicated by Y. Xue.
Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the United States Department of Agriculture.
Rights and permissions
About this article
Cite this article
Wubben, M.J., Callahan, F.E., Jenkins, J.N. et al. Coupling of MIC-3 overexpression with the chromosomes 11 and 14 root-knot nematode (RKN) (Meloidogyne incognita) resistance QTLs provides insights into the regulation of the RKN resistance response in Upland cotton (Gossypium hirsutum). Theor Appl Genet 129, 1759–1767 (2016). https://doi.org/10.1007/s00122-016-2737-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-016-2737-8