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Identification and confirmation of greenbug resistance loci in an advanced mapping population of sorghum

Published online by Cambridge University Press:  10 November 2017

SOMASHEKHAR PUNNURI  and
YINGHUA HUANG
SOMASHEKHAR PUNNURI
Affiliation:
Department of Plant Biology, Ecology and Evolution, Oklahoma State University, Stillwater, OK 74078, USA
YINGHUA HUANG*
Affiliation:
Department of Plant Biology, Ecology and Evolution, Oklahoma State University, Stillwater, OK 74078, USA USDA-ARS Plant Science Research Laboratory, 1301 N. Western Road, Stillwater, OK 74075, USA
*
*To whom all correspondence should be addressed. Email: yinghua.huang@ars.usda.gov
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Summary

Greenbug infestations to sorghum can cause severe and above economic threshold damage in the Great Plains of the United States. The current study was conducted to identify quantitative trait loci (QTLs) and potential candidate genes residing within the QTL region responsible for greenbug resistance in an advanced mapping population. Inter-crossed populations are useful in detecting QTLs tightly linked to genetic markers with high resolution. In the current study, QTLs responsible for greenbug resistance in sorghum were mapped using an inter-cross population derived from two parents, BTx623 (greenbug-susceptible line) and PI 607900 (greenbug-resistant line). Molecular markers for 115 loci were used to construct a linkage map which eventually facilitated tagging portions of the sorghum genome regions responsible for greenbug resistance. The molecular genetic map covered all the chromosomes of sorghum with a total genome length of 963·0 cM. The advanced mapping population revealed and confirmed the location of greenbug resistance loci, which explained a high phenotypic variation from 72·9 to 80·9% of greenbug resistance. The loci for greenbug resistance were mapped to the region flanked by markers Starssbnm 93 and Starssbnm 102 on chromosome 9 with an increased allelic effect from the resistant parent. The locations of these loci were compared with a previous study on QTL analysis using an F2 mapping population. The results from the present study were in agreement with the findings in the F2 QTL analysis and identified QTLs had a better confidence interval. The markers/QTLs identified from the current study can be effectively utilized in marker-assisted selection and map-based cloning experiments.

Type
Crops and Soils Research Papers
Information
The Journal of Agricultural Science , Volume 155 , Issue 10 , December 2017 , pp. 1610 - 1622
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Copyright
Copyright © Cambridge University Press 2017 

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Footnotes

†

Present address: 1005 State University Dr., Agricultural Research Station, Fort Valley State University, Fort Valley, GA 31030, USA.

References

REFERENCES

Agrama, H. A., Wilde, G. E., Reese, J. C., Campbell, L. R. & Tuinstra, M. R. (2002). Genetic mapping of QTLs associated with greenbug resistance and tolerance in Sorghum bicolor . Theoretical and Applied Genetics 104, 1371–1378.Google Scholar
Andrews, D. J., Bramel-Cox, P. J. & Wilde, G. E. (1993). New sources of resistance to greenbug, biotype I, in sorghum. Crop Science 33, 198–199.CrossRefGoogle Scholar
Burd, J. D. & Porter, D. R. (2006). Biotypic diversity in greenbug (Hemiptera: Aphididae): characterizing new virulence and host associations. Journal of Economic Entomology 99, 959–965.Google Scholar
Cai, W. & Morishima, H. (2002). QTL clusters reflect character associations in wild and cultivated rice. Theoretical and Applied Genetics 104, 1217–1228.Google Scholar
Cone, K. C. & Coe, E. H. (2009). Genetic mapping and maps. In Handbook of Maize (Eds Bennetzen, J. L. & Hake, S.), pp. 507–522. New York: Springer.CrossRefGoogle Scholar
Churchill, G. A. & Doerge, R. W. (1994). Empirical threshold values for quantitative trait mapping. Genetics 138, 963–971.Google Scholar
Darvasi, A. (1998). Experimental strategies for the genetic dissection of complex traits in animal models. Nature Genetics 18, 19–24.Google Scholar
Darvasi, A. & Soller, M. (1994). Optimum spacing of genetic markers for determining linkage between marker loci and quantitative trait loci. Theoretical and Applied Genetics 89, 351–357.Google Scholar
Darvasi, A. & Soller, M. (1995). Advanced intercross lines, an experimental population for fine genetic mapping. Genetics 141, 1199–1207.Google Scholar
Darvasi, A., Weinreb, A., Minke, V., Weller, J. I. & Soller, M. (1993). Detecting marker-QTL linkage and estimating QTL gene effect and map location using a saturated genetic map. Genetics 134, 943–951.Google Scholar
Dogimont, C., Bendahmane, A., Chovelon, V. & Boissot, N. (2010). Host plant resistance to aphids in cultivated crops: genetic and molecular bases, and interactions with aphid populations. Comptes Rendus Biologies 333, 566–573.Google Scholar
Falke, K. C., Melchinger, A. E., Flachenecker, C., Kusterer, B. & Frisch, M. (2006). Comparison of linkage maps from F2 and three times intermated generations in two populations of European flint maize (Zea mays L.). Theoretical and Applied Genetics 113, 857–866.Google Scholar
Foyer, C. H., Rasool, B., Davey, J. W. & Hancock, R. D. (2016). Cross tolerance to biotic and abiotic stresses in plants: a focus on resistance to aphid infestation. Journal of Experimental Botany 67, 2025–2037.CrossRefGoogle ScholarPubMed
Gardiner, J. M., Coe, E. H., Melia-Hancock, S., Hoisington, D. A. & Chao, S. (1993). Development of a core RFLP map in maize using an immortalized-F2 population. Genetics 134, 917–930.Google Scholar
Gorena, R. L. (2004). Characterization of Schizaphis graminum (R.) (Homoptera: Aphididae) biotype evolution via virulence and fitness on Sorghum bicolor (L.) Moench and Sorghum halepense (L.) Persoon. Ph.D. Dissertation, Texas A & M University, College Station, TX.Google Scholar
Harris, M. O., Friesen, T. L., Xu, S. S., Chen, M. S., Giron, D. & Stuart, J. J. (2015). Pivoting from Arabidopsis to wheat to understand how agricultural plants integrate responses to biotic stress. Journal of Experimental Botany 66, 513–531.Google Scholar
Harvey, T. L. & Hackerott, H. L. (1969). Recognition of a greenbug biotype injurious to sorghum. Journal of Economic Entomology 62, 776–779.Google Scholar
Harvey, T. L., Kofoid, K. D., Martin, T. J. & Sloderbeck, P. E. (1991). A new greenbug virulent to E-biotype resistant sorghum. Crop Science 31, 1689–1691.Google Scholar
Harvey, T. L., Wilde, G. E. & Kofoid, K. D. (1997). Designation of a new greenbug, biotype K, injurious to resistant sorghum. Crop Science 37, 989–991.Google Scholar
Holland, J. B., Nyquist, W. E. & Cervantes-Martinex, C. T. (2003). Estimating and interpreting heritability for plant breeding. Plant Breeding Reviews 22, 9–112.Google Scholar
Hua, J. P., Xing, Y. Z., Wu, W. R., Xu, C. G., Sun, X. L., Yu, S. B. & Zhang, Q. F. (2003). Single-locus heterotic effects and dominance by dominance interaction can adequately explain the genetic basis of heterosis in an elite hybrid. Proceedings of the National Academy of Sciences of the United States of America 100, 2574–2579.Google Scholar
Huang, Y. (2007). Phloem feeding regulates the plant defense pathways responding to both aphid infestation and pathogen infection. In Biotechnology and Sustainable Agriculture 2006 and Beyond (Eds Xu, Z., Li, J., Xue, Y. & Yang, W.), pp. 215–219. Dordrecht, The Netherlands: Springer.Google Scholar
Huang, Y. (2011). Improvement of crop protection against greenbug using the worldwide sorghum germplasm collection and genomics-based approaches. Plant Genetic Resources 9, 317–320.CrossRefGoogle Scholar
Huang, Y., Sharma, H. C. & Dillon, M. K. (2013). Bridging conventional and molecular genetics of sorghum insect resistance. In Genomics of the Saccharinae. Plant Genetics and Genomics: Crops and Models 11 (Ed. Paterson, A. H.), pp. 367–389. New York: Springer.CrossRefGoogle Scholar
INTSORMIL (2006). Pest and disease resistant hybrids for U.S. producers. In INTSORMIL: International Expertise Benefits U.S. Sorghum and Pearl Millet Producers. INTSORMIL Report no. 4, 1 August 2006. Lincoln, NE, USA: INTSORMIL.Google Scholar
Kao, C. H., Zeng, Z. B. & Teasdale, R. D. (1999). Multiple interval mapping for quantitative trait loci. Genetics 152, 1203–1216.Google Scholar
Katsar, C. S., Paterson, A. H., Teetes, G. L. & Peterson, G. C. (2002). Molecular analysis of sorghum resistance to the greenbug (Homoptera: Aphididae). Journal of Economic Entomology 95, 448–457.Google Scholar
Kim, J. S., Klein, P. E., Klein, R. R., Price, H. J., Mullet, J. E. & Stelly, D. M. (2005). Chromosome identification and nomenclature of Sorghum bicolor . Genetics 169, 1169–1173.CrossRefGoogle ScholarPubMed
Kofoid, K. D., Harvey, T. L. & Sloderbeck, P. E. (1991). A new greenbug, biotype I, damaging sorghum. In Proceedings of the 46th Annual Corn and Sorghum Research Conference (Ed. Wilkinson, D.), pp. 130–140. Washington, D.C.: American Seed Trade Association.Google Scholar
Kofoid, K. D., Perumal, R., Reese, J. C. & Campbell, L. R. (2012). Registration of twelve sorghum germplasm lines tolerant to greenbug feeding damage. Journal of Plant Registrations 6, 101–103.Google Scholar
Kosambi, D. D. (1943). The estimation of map distances from recombination values. Annals of Eugenics 12, 172–175.Google Scholar
Lander, E. S., Green, P., Abrahamson, J., Barlow, A., Daly, M. J., Lincoln, S. E. & Newburg, L. (1987). MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1, 174–181.Google Scholar
Lee, M., Sharopova, N., Beavis, W. D., Grant, D., Katt, M., Blair, D. & Hallauer, A. (2002). Expanding the genetic map of maize with the intermated B73 × Mo17 (IBM) population. Plant Molecular Biology 48, 453–461.Google Scholar
Liu, S. C., Kowalski, S. P., Lan, T. H., Feldmann, K. A. & Paterson, A. H. (1996). Genome-wide high-resolution mapping by recurrent intermating using Arabidopsis thaliana as a model. Genetics 142, 247–258.Google Scholar
Mace, E., Tai, S., Innes, D., Godwin, I., Hu, W., Campbell, B., Gilding, E., Cruickshank, A., Prentis, P., Wang, J. & Jordan, D. (2014). The plasticity of NBS resistance genes in sorghum is driven by multiple evolutionary processes. BMC Plant Biology 14, 253. doi: 10.1186/s12870-014-0253-z.Google Scholar
Mace, E. S., Rami, J.-F., Bouchet, S., Klein, P. E., Klein, R. R., Kilian, A., Wenzl, P., Xia, L., Halloran, K. & Jordan, D. R. (2009). A consensus genetic map of sorghum that integrates multiple component maps and high-throughput Diversity Array Technology (DArT) markers. BMC Plant Biology 9, 13. doi: 10.1186/1471-2229-9-13.CrossRefGoogle ScholarPubMed
Michaud, J. P., Whitworth, R. J. & Schwarting, H. (2015). Sorghum Insect Management 2015. MF742. Manhattan, KS: Kansas State University Agricultural Experiment Station and Cooperative Extension Service.Google Scholar
Mohan, M., Nair, S., Bhagwat, A., Krishna, T. G., Yano, M., Bhatia, C. R. & Sasaki, T. (1997). Genome mapping, molecular markers and marker-assisted selection in crop plants. Molecular Breeding 3, 87–103.Google Scholar
Morkunas, I., Mai, V. C. & Gabryś, B. (2011). Phytohormonal signaling in plant responses to aphid feeding. Acta Physiologiae Plantarum 33, 2057–2073.Google Scholar
Mullet, J. E., Klein, R. R. & Klein, P. E. (2002). Sorghum bicolor-an important species for comparative grass genomics and a source of beneficial genes for agriculture. Current Opinion in Plant Biology 5, 118–121.Google Scholar
Murray, M. G. & Thompson, W. F. (1980). Rapid isolation of high molecular weight plant DNA. Nucleic Acids Research 8, 4321–4325.CrossRefGoogle ScholarPubMed
Nagaraj, N., Reese, J. C., Tuinstra, M. R., Smith, C. M., Amand, P., Kirkham, M. B., Kofoid, K. D., Campbell, L. R. & Wilde, G. E. (2005). Molecular mapping of sorghum genes expressing tolerance to damage by greenbug (Homoptera: Aphididae). Journal of Economic Entomology 98, 595–602.Google Scholar
Park, S.-J., Huang, Y. & Ayoubi, P. (2006). Identification of expression profiles of sorghum genes in response to greenbug phloem-feeding using cDNA subtraction and microarray analysis. Planta 223, 932–947.Google Scholar
Paterson, A. H., Bowers, J. E., Bruggmann, R., Dubchak, I., Grimwood, J., Gundlach, H., Haberer, G., Hellsten, U., Mitros, T., Poliakov, A., Schmutz, J., Spannagl, M., Tang, H., Wang, X., Wicker, T., Bharti, A. K., Chapman, J., Feltus, F. A., Gowik, U., Grigoriev, I. V., Lyons, E., Maher, C. A., Martis, M., Narechania, A., Otillar, R. P., Penning, B. W., Salamov, A. A., Wang, Y., Zhang, L., Carpita, N. C., Freeling, M., Gingle, A. R., Hash, C. T., Keller, B., Klein, P., Kresovich, S., McCann, M. C., Ming, R., Peterson, D. G., Mehboob-ur-Rahman, , Ware, D., Westhoff, P., Mayer, K. F., Messing, J. & Rokhsar, D. S. (2009). The Sorghum bicolor genome and the diversification of grasses. Nature 457, 551–556.Google Scholar
Porter, K. B., Peterson, G. L. & Vise, O. (1982). A new greenbug biotype. Crop Science 22, 847–850.Google Scholar
Porter, D. R., Burd, J. D., Shufran, K. A., Webster, J. A. & Teetes, G. L. (1997). Greenbug (Homoptera: Aphididae) biotypes: selected by resistant cultivars or preadapted opportunists. Journal of Economic Entomology 90, 1055–1065.Google Scholar
Punnuri, S. M. (2011). Genetic mapping of greenbug resistance loci in sorghum [Sorghum bicolor (L.) Moench] & expression analysis of candidate genes in response to greenbug infestation . Ph.D. Dissertation, Oklahoma State University, Stillwater, OK.Google Scholar
Punnuri, S. M., Huang, Y., Steets, J. & Wu, Y. (2013). Developing new markers and QTL mapping for greenbug resistance in sorghum [Sorghum bicolor (L.) Moench]. Euphytica 191, 191–203.Google Scholar
Puterka, G. J. & Peters, D. C. (1989). Inheritance of greenbug, Schizaphis graminum (Rondani), virulence to Gb2 and Gb3 resistance genes in wheat. Genome 32, 109–114.Google Scholar
Puterka, G. J. & Peters, D. C. (1995). Genetics of greenbug (Homoptera, Aphididae) virulence to resistance in sorghum. Journal of Economic Entomology 88, 421–429.Google Scholar
Radchenko, E. E. & Lychagina, N. S. (2003). Physiological and genetic variation in Schizaphis graminum (Sternorrhyncha: Aphididae) populations. Acta Societatis Zoologicae Bohemicae 67, 15–23.Google Scholar
Reddy, P. S., Fakrudin, B., Rajkumar, , Punnuri, S. M., Arun, S. S., Kuruvinashetti, M. S., Das, I. K. & Seetharama, N. (2008). Molecular mapping of genomic regions harboring QTLs for stalk rot resistance in sorghum. Euphytica 159, 191–198.Google Scholar
Rooney, W. L. (2004). Sorghum improvement-integrating traditional and new technology to produce improved genotypes. Advances in Agronomy 83, 37–109.Google Scholar
Royer, T. A., Pendleton, B. B., Elliott, N. C. & Giles, K. L. (2015). Greenbug (Hemiptera: Aphididae) biology, ecology, and management in wheat and sorghum. Journal of Integrated Pest Management 6, 19. doi: 10.1093/jipm/pmv018.Google Scholar
SAS Institute (2008). SAS Proprtary Software version 9.2. Cary, NC: SAS Institute.Google Scholar
Satish, K., Srinivas, G., Madhusudhana, R., Padmaja, P. G., Reddy, R. N., Mohan, S. M. & Seetharama, N. (2009). Identification of quantitative trait loci for resistance to shoot fly in sorghum [Sorghum bicolor (L.) Moench]. Theoretical and Applied Genetics 119, 1425–1439.Google Scholar
Sekhwal, M. K., Li, P., Lam, I., Wang, X., Cloutier, S. & You, F. M. (2015). Disease resistance gene analogs (RGAs) in plants. International Journal of Molecular Sciences 16, 19248–19290.Google Scholar
Sharma, H. C. & Ortiz, R. (2002). Host plant resistance to insects: an eco-friendly approach for pest management and environment conservation. Journal of Environmental Biology 23, 111–135.Google Scholar
Smith, C. M. (2004). Insect/host plant resistance in crops. In Encyclopedia of Plant and Crop Science (Ed. Goodman, R. M.), pp. 605–608. Boca Raton, FL: CRC Press.Google Scholar
Smith, C. M. & Boyko, E. V. (2007). The molecular bases of plant resistance and defense responses to aphid feeding: current status. Entomologia Experimentalis et Applicata 122, 1–16.Google Scholar
Smith, C. M. & Clement, S. L. (2012). Molecular bases of plant resistance to arthropods. Annual Review of Entomology 57, 309–328.Google Scholar
Song, W. Y., Want, G. L., Chen, L. L., Kim, H. S., Pi, L. Y., Holsten, T., Gardner, J., Wang, B., Zhai, W. X., Zhu, G. L., Fauquet, C. & Ronald, P. (1995). A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270, 1804–1806.Google Scholar
Starks, K. J. & Burton, R. L. (1977). Greenbugs: Determining Biotypes, Culturing, and Screening for Plant Resistance. Technical Bulletin No. 1556. Washington, DC: USDA-ARS.Google Scholar
Tanksley, S. D. (1993). Mapping polygenes. Annual Review of Genetics 27, 205–233.Google Scholar
Tuinstra, M. R., Wilde, G. E. & Kriegshauser, T. (2001). Genetic analysis of biotype I greenbug resistance in sorghum. Euphytica 121, 87–91.Google Scholar
Wang, S., Basten, C. J. & Zeng, Z. B. (2010). Windows QTL Cartographer 2.5. Raleigh, NC: Department of Statistics, North Carolina State University.Google Scholar
Wang, Y.-S., Pi, L.-Y., Chen, X., Chakrabarty, P. K., Jiang, J., De Leon, A. L., Liu, G.-Z., Li, L., Benny, U., Oard, J., Ronald, P. C. & Song, W.-Y. (2006). Rice XA21 binding protein 3 is a ubiquitin ligase required for full Xa21-mediated disease resistance. Plant Cell 18, 3635–3646.Google Scholar
Wilde, G. E. & Tuinstra, M. R. (2000). Registration of KS 97 sorghum. Crop Science 40, 866.Google Scholar
Winkler, C. R., Jensen, N. M., Cooper, M., Podlich, D. W. & Smith, O. S. (2003). On the determination of recombination rates in intermated recombinant inbred populations. Genetics 164, 741–745.Google Scholar
Wu, Y. Q. & Huang, Y. (2008). Molecular mapping of QTLs for resistance to the greenbug Schizaphis graminum; (Rondani) in Sorghum bicolor, L (Moench). Theoretical and Applied Genetics 117, 117–124.Google Scholar
Wu, Y. Q., Huang, Y., Tauer, C. G. & Porter, D. R. (2006). Genetic diversity of sorghum accessions resistant to greenbugs as assessed with AFLP markers. Genome 49, 143–149.Google Scholar
Wu, Y. Q., Huang, Y., Porter, D. R., Tauer, C. G. & Hollaway, L. (2007). Identification of a major quantitative trait locus conditioning resistance to greenbug biotype E in sorghum PI 550610 using simple sequence repeat markers. Journal of Economic Entomology 100, 1672–1678.Google Scholar
Yencho, G. C., Cohen, M. B. & Byrne, P. F. (2000). Applications of tagging and mapping insect resistance loci in plants. Annual Review of Entomology 45, 393–422.Google Scholar
Young, D. N. (2000). Constructing a plant genetic linkage map with DNA markers. In DNA-based Markers in Plants (Eds Philips, R. L. & Vasil, J. K.), pp. 31–47. Dordrecht, The Netherlands: Kluwer Academic Publishers.Google Scholar
Zeng, Z. B., Kao, C.-H. & Basten, C. J. (1999). Estimating the genetic architecture of quantitative traits. Genetics Research 74, 279–289.Google Scholar
Zhu-Salzman, K., Salzman, R. A., Ahn, J.-E. & Koiwa, H. (2004). Transcriptional regulation of sorghum defense determinants against a phloem-feeding aphid. Plant Physiology 134, 420–431.Google Scholar
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