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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)

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Abstract

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Transgene-based analysis of the MIC-3 gene provides the first report of a cotton gene having a direct role in mediating cotton resistance to root-knot nematode.

Abstract

Major quantitative trait loci have been mapped to Upland cotton (Gossypium hirsutum L.) chromosomes 11 and 14 that govern the highly resistant phenotype in response to infection by root-knot nematode (RKN; Meloidogyne incognita); however, nearly nothing is known regarding the underlying molecular determinants of this RKN-resistant phenotype. Multiple lines of circumstantial evidence have strongly suggested that the MIC (Meloidogyne Induced Cotton) gene family plays an integral role in mediating cotton resistance to RKN. In this report, we demonstrate that overexpression of MIC-3 in the RKN-susceptible genetic background Coker 312 reduces RKN egg production by ca. 60–75 % compared to non-transgenic controls and transgene-null sibling lines. MIC-3 transcript and protein overexpression were confirmed in root tissues of multiple independent transgenic lines with each line showing a similar level of increased resistance to RKN. In contrast to RKN fecundity, transgenic lines showed RKN-induced root galling similar to the susceptible controls. In addition, we determined that this effect of MIC-3 overexpression was specific to RKN as no effect was observed on reniform nematode (Rotylenchulus reniformis) reproduction. Transgenic lines did not show obvious alterations in growth, morphology, flowering, or fiber quality traits. Gene expression analyses showed that MIC-3 transcript levels in uninfected transgenic roots exceeded levels observed in RKN-infected roots of naturally resistant plants and that overexpression did not alter the regulation of native MIC genes in the genome. These results are the first report describing a direct role for a specific gene family in mediating cotton resistance to a plant-parasitic nematode.

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Acknowledgments

The authors would like to thank Dr. Russ Hayes (USDA-ARS) for his assistance in performing the statistical analyses of the nematode infection experiments. The authors also thank Drs. Patricia Timper and Jack McCarty Jr. (USDA-ARS) for their critical review of the manuscript and helpful comments.

Conflict of interest

The authors declare no conflict of interests.

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Authors and Affiliations

  1. Genetics and Precision Agriculture Research Unit, Crop Science Research Laboratory, USDA-ARS, 810 Highway 12 East, Mississippi State, MS, 39762, USA

    Martin J. Wubben, Franklin E. Callahan & Johnie N. Jenkins

  2. Cropping Systems Research Laboratory, USDA-ARS, Lubbock, TX, USA

    Jeff Velten & John J. Burke

Authors
  1. Martin J. Wubben
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  2. Franklin E. Callahan
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  3. Jeff Velten
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  4. John J. Burke
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  5. Johnie N. Jenkins
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Corresponding author

Correspondence to Martin J. Wubben.

Additional information

Communicated by Brian Diers.

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.

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Wubben, M.J., Callahan, F.E., Velten, J. et al. 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 (2015). https://doi.org/10.1007/s00122-014-2421-9

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  • DOI: https://doi.org/10.1007/s00122-014-2421-9

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