Theoretical and Applied Genetics

, Volume 122, Issue 8, pp 1617–1630 | Cite as

Identification and validation of genomic regions that affect shoot fly resistance in sorghum [Sorghum bicolor (L.) Moench]

  • C. Aruna
  • V. R. Bhagwat
  • R. Madhusudhana
  • Vittal Sharma
  • T. Hussain
  • R. B. Ghorade
  • H. G. Khandalkar
  • S. Audilakshmi
  • N. Seetharama
Original Paper


Shoot fly is one of the most important pests affecting the sorghum production. The identification of quantitative trait loci (QTL) affecting shoot fly resistance enables to understand the underlying genetic mechanisms and genetic basis of complex interactions among the component traits. The aim of the present study was to detect QTL for shoot fly resistance and the associated traits using a population of 210 RILs of the cross 27B (susceptible) × IS2122 (resistant). RIL population was phenotyped in eight environments for shoot fly resistance (deadheart percentage), and in three environments for the component traits, such as glossiness, seedling vigor and trichome density. Linkage map was constructed with 149 marker loci comprising 127 genomic-microsatellite, 21 genic-microsatellite and one morphological marker. QTL analysis was performed by using MQM approach. 25 QTL (five each for leaf glossiness and seedling vigor, 10 for deadhearts, two for adaxial trichome density and three for abaxial trichome density) were detected in individual and across environments. The LOD and R 2 (%) values of QTL ranged from 2.44 to 24.1 and 4.3 to 44.1%, respectively. For most of the QTLs, the resistant parent, IS2122 contributed alleles for resistance; while at two QTL regions, the susceptible parent 27B also contributed for resistance traits. Three genomic regions affected multiple traits, suggesting the phenomenon of pleiotrophy or tight linkage. Stable QTL were identified for the traits across different environments, and genetic backgrounds by comparing the QTL in the study with previously reported QTL in sorghum. For majority of the QTLs, possible candidate genes were identified. The QTLs identified will enable marker assisted breeding for shoot fly resistance in sorghum.


Deadheart percentage Quantitative trait loci Candidate genes Co-localization Gene pyramiding 



The authors wish to thank Dr CN Neeraja, Principal Scientist, DRR, Hyderabad, India for her help during the preparation of the manuscript.


  1. Agarwal BL, Abraham CV (1985) Breeding sorghum for resistance to shoot fly and midge. In: Proceedings of the international sorghum entomology workshop, Texas A&M University, College Station, Texas, USA, 15–21 July 1984. International Crops Research Institute for the Semi-Arid Tropics, Patancheru 502324, Andhra Pradesh, India, pp 371–383Google Scholar
  2. Agarwal BL, House LR (1982) Breeding for pest resistance in sorghum. In: Sorghum in eighties, Proceedings of the International symposium on sorghum, 2–7 November 1981. International Crops Research Institute for the Semi-Arid Tropics, Patancheru 502324, Andhra Pradesh, India, pp 435–446Google Scholar
  3. Agrama HA, Widle GE, Reeses JC, Campbell LR, Tuinstra MR (2002) Genetic mapping of QTL associated with green bug resistance and tolerance in Sorghum bicolor. Theor Appl Genet 104:1373–1378PubMedCrossRefGoogle Scholar
  4. Alonso JM, Hirayama T, Roman G, Nourizadeh S, Ecker JR (1999) EIN 2, a bifunctional transducer of Ethylene and stress responases in Arabidopsis. Science 284:2148–2152PubMedCrossRefGoogle Scholar
  5. Anandan A, Huliraj H, Veerabadhiran P (2009) Analysis of resistance mechanism to Atherigona soccata in crosses of sorghum. Plant Breed 128:443–450CrossRefGoogle Scholar
  6. Aruna C, Bhagwat VR, Sharma V, Hussain T, Ghorade RB, Khandalkar HG, Audilakshmi S, Seetharama N (2011) Genotype × environment interactions for shoot fly resistance in sorghum (Sorghum bicolor (L.) Moench): response of recombinant inbred lines. Crop prot (Accepted)Google Scholar
  7. Aruna C, Padmaja PG (2009) Evaluation of genetic potential of shoot fly resistant sources in sorghum (Sorghum bicolor (L.)). J Agri Sci 147:71–80Google Scholar
  8. Audilakshmi S, Stenhouse JW, Reddy TP (2000) Genetic analysis of grain mould resistance in coloured sorghum genotypes. Euphytica 116:95–103CrossRefGoogle Scholar
  9. Aubert G, Morin J, Jacquin F, Loridon K, Quillet MC, Petit A, Rameau C, Lejeune-He’naut I, Huguet T, Burstin J (2006) Functional mapping in pea, as an aid to the candidate gene selection and for investigating synteny with the model legume Medicago truncatula. Theor Appl Genet 112:1024–1041PubMedCrossRefGoogle Scholar
  10. Belkhadir Y, Subramanian R, Dangi J (2004) Plant disease resistance protein signaling: NBS-LRR protein and their parameters. Curr Opin Plant Boil 7:391–399CrossRefGoogle Scholar
  11. Blakeslee JJ, Peer WA, Murphy AS (2005) Auxin transport. Curr Opin Plant Biol 8:494–500PubMedCrossRefGoogle Scholar
  12. Brooks TD, Willcox MC, Williams WP, Luthe DS (2004) Quantitative trait loci conferring resistance to fall Army worm and southern corn borer leaf feeding damage. Crop Sci 45:2430–2434CrossRefGoogle Scholar
  13. Chen M, Wang QY, Cheng XG, Xu ZS, Li LC, Ye X, Xia L, Ma Y (2006a) Gm DREB2, a soybean DRE binding transcription factor, conferred drought and high salt tolerance in transgenic plants. Biochem Biophys Res Comm 353:299–305PubMedCrossRefGoogle Scholar
  14. Chen X, Shang J, Chen D, Lei C, Zou Y, Zhai W, Liu G, Xu J, Ling Z, Cao G, Ma B, Wang Y, Zhao X, Li S, Zhu L (2006b) AB-lectin receptor kinase gene conferring rice blast resistance. Plant J 46:794–804PubMedCrossRefGoogle Scholar
  15. Cosio C, Dunand C (2009) Specific functions of individual class III peroxidase genes. J Expt Bot 60:391–408CrossRefGoogle Scholar
  16. Datta K, Velazhahan R, Oliva N, Ona I, Mew T, Khush GS, MuthuKrishnan S, Datta SK (1998) Over expression of the cloned rice thaumatin like protein (PR-5) gene in transgenic rice plants enhances environmental friendly resistance to Rhizoctonia solani causing sheath blight disease. Theo Appl Genet 98:1138–1145CrossRefGoogle Scholar
  17. Deeming JC (1971) Some species of Atherigona rondani (Diptera: Muscidae) from northern Nigeria, with special reference to those injurious to cereal crops. Bull Entomol Res 61:133–190CrossRefGoogle Scholar
  18. Deu M, Ratnadass A, Hamada MA, Noyer JL, Diabate M, Chantereau J (2005) Quantitative trait loci for head-bug resistance in sorghum. African J Biotech 4:247–250Google Scholar
  19. Dhillon MK, Sharma HC, Reddy BVS, Ram S, Naresh JS, Kaizhu (2005) Relative susceptibility of different male-sterile cytoplasms in sorghum to shoot fly, Atherigona soccata. Euphytica 144:275–283CrossRefGoogle Scholar
  20. Dhillon MK, Sharma HC, Reddy BVS, Ram-Singh, Naresh JS (2006) Inheritance of resistance to sorghum shoot fly, Atherigona soccata. Crop Sci 46:1377–1383CrossRefGoogle Scholar
  21. Dilworth ES, Beese S, Paris R, Belfanti E, Tartarini S, Sansavini S, Patocchi A, Gessler C (2005) Identification of functional apple scab resistance gene promoters. Theor Appl Genet 110:1119–1126CrossRefGoogle Scholar
  22. Duval M, Hsieh TF, Kim SY, Thomas TL (2002) Molecular characterization of AtNAM: a member of the Arabidopsis NAC domain superfamily. Plant Mol Biol 50:237–248PubMedCrossRefGoogle Scholar
  23. Eulgem T, Rushton PJ, Robartzek S, Somssich IE (2000) The WRKY super family of plant transcription factors. Trends Plant Sci 5:199–206PubMedCrossRefGoogle Scholar
  24. Falconer DS (1989) Introduction to quantitative genetics. Wiley, New YorkGoogle Scholar
  25. Faris JD, Haen KM, Gill BS (2000) Saturation mapping of a gene-rich recombination hot spot region in wheat. Genetics 154:823–835PubMedGoogle Scholar
  26. Fritz AK, Caldwell S, Worral WD (1999) Molecular mapping of Russsian wheat aphid resistance from triticale accession, PI 386156. Crop Sci 39:1707–1710CrossRefGoogle Scholar
  27. Gibson PT, Maiti RK (1983) Trichomes in segregating generations of sorghum matings. I. Inheritance of presence and density. Crop Sci 23:73–75CrossRefGoogle Scholar
  28. Haussmann BIG, Mahalakshmi V, Reddy BVS, Seetharama N, Hash CT, Geiger HH (2002) QTL mapping of stay-green in two sorghum recombinant inbred populations. Theor Appl Genet 106:133–142PubMedGoogle Scholar
  29. Hulbert SH, Webb CA, Smith SM, Sun Q (2001) Resistance gene complexes: evolution and utilization. Annu Rev Phytopathol 39:285–312PubMedCrossRefGoogle Scholar
  30. Jadhav SS, Mote UN, Bapat DR (1986) Biophysical plant characters contributing to shoot fly resistance. Sorghum Newsletter 29:70Google Scholar
  31. Jansen RC (1993) Interval mapping of multiple quantitative trait loci. Genetics 135:205–211PubMedGoogle Scholar
  32. Jansen RC, Stam P (1994) High resolution of quantitative traits into multiple loci via interval mapping. Genetics 136:1447–1455PubMedGoogle Scholar
  33. Jayanthi PDK, Reddy BVS, Gour TB, Reddy DDR (2002) Early seedling vigour in sorghum and its relationship with resistance to shoot fly Atherigona soccata (Rond). J Entomological Res 26:93–100Google Scholar
  34. Jotwani MG (1982) Factors reducing sorghum yields-insect pests. In: Sorghum in Eighties. Proceedings International Symposium on sorghum. 2–7 Nov. 1981. ICRISAT, Patancheru, pp 251–255Google Scholar
  35. Jotwani MG, Marawaha KK, Srivastava KM, Young WR (1970) Seasonal incidence of shoot fly (Atherigona soccata Rond.) in jowar hybrids at Delhi. Indian J Ento 32:7–15Google Scholar
  36. Kamatar MY, Salimath PM (2003) Morphological traits of sorghum associated with resistance to shoot fly, Atherigona soccata Rondani. Indian J Plant Prot 31:73–77Google Scholar
  37. Kim JS, Klein PE, Klein RR, Price HJ, Mullet JE, Stelly DM (2005) Chromosome identification and nomenclature of Sorghum bicolor. Genetics 169:1169–1173PubMedCrossRefGoogle Scholar
  38. Knoll J, Ejeta G (2008) Marker-assisted selection for early-season cold tolerance in sorghum: QTL validation across populations and environments. Theor Appl Genet 116:541–553PubMedCrossRefGoogle Scholar
  39. Knoll J, Gunaratna N, Ejeta G (2008) QTL analysis of early season cold tolerance in sorghum. Theor Appl Genet 116:577–587PubMedCrossRefGoogle Scholar
  40. Khurana AD, Verma AN (1985) Some physical plant characters in relation to stemborer and shoot fly resistance in sorghum. Indian J Entom 47:14–19Google Scholar
  41. Kulaeva ON, Prokoptseva OS (2004) Recent advances in the study of mechanism of action of phytohormones. Biochem Mosc 69:233–247CrossRefGoogle Scholar
  42. Lander ES, Botstein D (1989) Mapping Mendelian factors underlying quantitative traits by using RFLP linkage maps. Genetics 121:1447–1455Google Scholar
  43. Maiti RK, Bidinger FR (1979) A simple approach to identification of shoot fly tolerance in sorghum. Indian J Plant Prot 7:135–140Google Scholar
  44. Maiti RK, Gibson PT (1983) Trichomes in segregating generations of sorghum matings. II. Association with shoot fly resistance. Crop Sci 23:76–79CrossRefGoogle Scholar
  45. Maiti RK, Prasada Rao KE, Raju PS, House LR (1984) The glossy trait in sorghum: its characteristics and significance in crop improvement. Field Crops Res 9:279–289CrossRefGoogle Scholar
  46. Mathews BF, Devine TE, Weisemann JM, Beard HS, Lewers KS, McDonald MH, Park Y-B, Maiti R, Lin J-J, Kuo J, Pedroni MJ, Cregan PB, Saunders JA (2001) Incorporation of sequenced cDNA and genomic markers into the soybean genetic map. Crop Sci 41:516–521CrossRefGoogle Scholar
  47. Munro AW, Girvan HM, McLean KJ (2007) Cytochrome P450-redox partner fusion enzymes. Biochim Biophys Acta 1770:345–359Google Scholar
  48. Mote UN, Kadam JR, Bapat DR (1986) Antibiosis mechanisms of resistance to sorghum shoot fly. J Maharashtra Agric Univ 11:43–46Google Scholar
  49. Nagaraj N, Reese JC, Tuinstra MR, Smith CM, Amand PS, Kirkham MB, Kofoid KD, Campbell LR, Wild GE (2005) Molecular mapping of sorghum genes expressing tolerance to damage by green bug (Homoptera: Aphididae). J Econ Entomol 98:595–602PubMedCrossRefGoogle Scholar
  50. Nwanze KF, Reddy YVR, Soman P (1990) The role of leaf surface wetness in larval behavior of the sorghum shoot fly Atherigona soccata. Entomol Exp Appl 56:187–195CrossRefGoogle Scholar
  51. Padmaja PG, Madhusudhana R, Seetharama N (2010a) Epicuticular wax and morphological traits associated with resistance to shoot fly, Atherigona soccata Rondani in sorghum, Sorghum bicolor. Entomon 34:137–146Google Scholar
  52. Padmaja PG, Madhusudhana R, Seetharama N (2010b) Sorghum shoot fly. Directorate of Sorghum Research, Rajendranagar, Hyderabad 500 030, Andhra Pradesh, India. ISBN 81-89335-29-4. Pp 82Google Scholar
  53. Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A et al (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457:551–556PubMedCrossRefGoogle Scholar
  54. Pechan T, Cohen A, Williams QP, Luther DS (2002) Insect feeding mobilizes a unique plant defense protease that disrupts the pleiotrophic matrix of caterpillar. Proc Natl Acad Sci USA 99:13319–13323PubMedCrossRefGoogle Scholar
  55. Rana BS, Tripathi DP, Balakotaiah K, Damodar R, Rao NGP (1975) Genetic analysis of some exotic x Indian crosses in sorghum. XI. Selection of shoot fly resistance. Indian J Genet 35:350–354Google Scholar
  56. Rao M, Gowda S (1967) A short note on the bionomics and control of jowar fly. Sorghum Newsletter 10:55–57Google Scholar
  57. Rotheberg JM, Jacobs JR, Goodman CS, Artavanis-Tsakonas S (1990) Slit: an extra cellular protein necessary for development of midline glia and commissural axon pathways contains both EGF and LRR domains. Genes Dev 4:2169–2187CrossRefGoogle Scholar
  58. Saghai-Maroof MA, Soliman KM, Jordensen RA, Allard RW (1984) Ribosomal DNA spacer-length polymorphism in barley: Mendelian inheritance, chromosomal location, and population dynamics. Proc Natl Acad Sci USA 81:8014–8018PubMedCrossRefGoogle Scholar
  59. Sandhu D, Champoux JA, Bondareva SN, Gill KS (2001) Identification and physical localization of useful genes and markers to a major gene-rich region on wheat group IA chromosomes. Genetics 157:1735–1747PubMedGoogle Scholar
  60. Satish K, Srinivas G, Madhusudhana R, Padmaja PG, Nagaraja Reddy R, Murali Mohan S, Seetharama N (2009) Identification of quantitative trait loci for resistance to shoot fly in sorghum [Sorghum bicolor (L.) Moench]. Theo Appl Genet 119:1425–1439CrossRefGoogle Scholar
  61. Sharma HC (1993) Host plant resistance to insects in sorghum and its role in integrated pest management. Crop Prot 12:11–34CrossRefGoogle Scholar
  62. Sharma HC, Dhillon MK, Reddy BVS (2006) Expression of resistance to Atherigona soccata in F1 hybrids involving shoot fly resistant and susceptible cytoplasmic male-sterile and restorer lines of sorghum. Plant Breed 125:473–477CrossRefGoogle Scholar
  63. Singh BU, Padmaja PG, Seetharama N (2004) Stability of biochemical constituents and their relationship with resistance to shoot fly Atherigona soccata (Rond.) in seedling sorghum. Euphytica 136:279–289CrossRefGoogle Scholar
  64. Singh H, Grewal TS, Pannu PPS, Dhaliwal HS (1999) Genetics of resistance to Karnal bunt disease of wheat. Euphytica 105:125–131CrossRefGoogle Scholar
  65. Smith JSC, Kresovich S, Hopkins MS, Mitchell SE, Dean RE, Woodman WL, Lee M, Porter K (2000) Genetic diversity among elite sorghum inbred lines assessed with simple sequence repeats. Crop Sci 40:226–232CrossRefGoogle Scholar
  66. Soto PE (1974) Ovipositional preference and antibiosis in relation to resistance to sorghum shoot fly. J Econ Entomol 67:165–167Google Scholar
  67. Srinivas G, Satish K, Madhusudhana R, Seetharama N (2009a) Exploration and mapping of microsatellite markers from subtracted drought stress ESTs in Sorghum bicolor (L.) Moench. Theor Appl Genet 118:703–717PubMedCrossRefGoogle Scholar
  68. Srinivas G, Satish K, Madhusudhana R, Nagaraja Reddy R, Murali Mohan S, Seetharama N (2009b) Identification of quantitative trait loci for agronomically important traits and their association with genic-microsatellite markers in sorghum. Theor Appl Genet 118:1439–1454PubMedCrossRefGoogle Scholar
  69. Taneja SL, Leuschner K (1985) Resistance screening and mechanisms of resistance in sorghum to shoot fly. In: Proceedings of the international sorghum entomology workshop, 15–21 July, 1984, Texas A&M University, College Station, Texas, USA, International Crops Research Institute for the Semi-Arid Tropics, Patancheru 502324, Andhra Pradesh, India, pp 115–129Google Scholar
  70. Tao YZ, Hardy A, Drenth J, Henzell RG, Franzmann BA, Jordan DR, Butler DG, McIntyre CL (2003) Identification of two different mechanisms for sorghum midge resistance through QTL mapping. Theor Appl Genet 107:116–122PubMedGoogle Scholar
  71. Van Ooijen JW (2005) Map-QTL 5: Software for the mapping quantitative trait loci in mapping populations. Kyazma BV, WageningenGoogle Scholar
  72. Van Ooijen JW, Voorrips RE (2001) JoinMap 3.0 Software for the calculation of genetic linkage maps. Plant Res Int, WageningenGoogle Scholar
  73. Vander Biezen EA, Jones D (1998) The NB-ARC domain: a novel signaling motif shared by plant resistance gene products and regulators of cell death in animals. Curr Biol 8:226–227CrossRefGoogle Scholar
  74. Veldboom LR, Lee M, Woodman WL (1994) Molecular facilitated studies of morphological traits in an elite maize population. II. Determination of QTL for grain yield and yield components. Theor Appl Genet 89:451–458CrossRefGoogle Scholar
  75. Vij S, Tyagi AK (2006) Genome-wide analysis of the stress associated protein (SAP) gene family containing A20/AN1 Zinc-finger(s) in rice and their phylogenetic relationship with Arabidopsis. Mol Genet Genom 276:565–575CrossRefGoogle Scholar
  76. Wu Y, Huang Y (2008) Molecular mapping of QTL for resistance to the green bug Schizaphis graminum (Rondani) in Sorghum bicolor (Moench). Theor Appl Genet 117:117–124PubMedCrossRefGoogle Scholar
  77. Xiao J, Li J, Tanksley SD (1996) Identification of QTL affecting traits of agronomic importance in a recombinant inbred population derived from a sub specific rice cross. Theor Appl Genet 92:230–244CrossRefGoogle Scholar
  78. Xu C, Jing R, Mao X, Jia X, Chang X. (2007) A wheat (Triticum aestivum) protein phosphatase 2A catalytic subunit gene provides enhanced drought tolerance in Tobacco. Ann Bot. doi: 10.1093/aob/mc1285
  79. Zhang WK, Wang YJ, Luo GZ, Zhang JS, He CY, Wu XL, Gai JY, Chen SY (2004) QTL mapping of ten agronomic traits on the soybean (Glycine max L. Merr.) genetic map and their association with EST markers. Theor Appl Genet 108:1131–1139PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • C. Aruna
    • 1
  • V. R. Bhagwat
    • 1
  • R. Madhusudhana
    • 1
  • Vittal Sharma
    • 2
  • T. Hussain
    • 2
  • R. B. Ghorade
    • 3
  • H. G. Khandalkar
    • 3
  • S. Audilakshmi
    • 1
  • N. Seetharama
    • 1
  1. 1.Directorate of Sorghum ResearchHyderabadIndia
  2. 2.MPUATUdaipurIndia
  3. 3.PDKVAkolaIndia

Personalised recommendations