Abstract
The associations of candidate genes with quantitative trait loci (QTL) for insect resistance provide primary insight into the molecular mechanisms of resistance. The objectives of the present study were to genetically map the candidate genes and identify their association with shoot fly resistance, and update the genetic map with new markers to locate additional QTL. In this study, 80 candidate gene (CG)-based markers were developed, targeting the seven most important shoot fly resistance genomic regions reported in our previous study. Of the 17 polymorphic CGs, the allelic polymorphisms of seven genes were significantly associated with 18 major QTL for component traits of resistance in multiple QTL mapping (MQM), and two genes in the single-marker analysis. MQM with an updated map revealed 20 new QTL with LOD and R 2 (%) values ranging from 2.6 to 15.6 and 5.5 to 34.5 %, respectively. The susceptible parent 296B contributed resistance at 10 QTL. Interestingly, an orthologous insect resistance gene Cysteine protease-Mir1 (XnhsbmSFC34/SBI-10), previously presumed to be a CG based on synteny with maize, was significantly associated with major QTL for all traits (except seedling vigor) explaining 22.1 % of the phenotypic variation for deadhearts%, a direct measure of shoot fly resistance. Similarly, a NBS–LRR gene (XnhsbmSFCILP2/SBI-10), involved in rice brown planthopper resistance, was associated with deadhearts% and number of eggs per plant. Beta-1,3-glucanase (XnhsbmSFC4/SBI-10), involved in aphid and brown planthopper resistance, was associated with deadhearts% and leaf glossiness. Comparative QTL analysis revealed the existence of common QTL for shoot fly and other important sorghum insect pests such as greenbug, head bug, and midge. Finally, the associated CGs should aid in elucidating the molecular basis of resistance, high-resolution mapping, and map-based cloning of major QTL, besides providing powerful gene tags for marker-assisted selection of shoot fly resistance.
Similar content being viewed by others
References
Agrama HA, Wilde GE, Reese JC, Campbell LR, Tuinstra MR (2002) Genetic mapping of QTLs associated with greenbug resistance and tolerance in Sorghum bicolor. Theor Appl Genet 104:1371–1378
Aruna C, Bhagwat VR, Madhusudhana R, Sharma V, Hussain T, Ghorade RB, Khandalkar HG, Audilakshmi S, Seetharama N (2011) Identification and validation of genomic regions that affect shoot fly resistance in sorghum [Sorghum bicolor (L.) Moench]. Theor Appl Genet 122:1617–1630
Aubert G, Morin J, Jacquin F, Loridon K, Quillet MC, Petit A, Rameau C, Lejeune-Hénaut 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 112:1024–1041
Bhattramakki D, Dong J, Chabra AK, Hart GE (2000) An integrated SSR and RFLP linkage map of Sorghum bicolor (L.) Moench. Genome 43:988–1002
Bierne N, Lehnert SA, Bédier E et al (2000) Screening for intron-length polymorphisms in penaeid shrimps using exon-primed intron-crossing (EPIC)-PCR. Mol Ecol 9:233–235
Blum A (1963) The penetration and development of the sorghum shoot fly in susceptible sorghum plants. Hassadeh (Hebrew) 44:23–25
Brooks TD, Willcox MC, Williams WP, Buckley PM (2005) Quantitative trait loci conferring resistance to fall armyworm and southwestern corn borer leaf feeding damage. Crop Sci 45:2430–2434
Collard BCY, Jahufer MZZ, Brouwer JB, Pang ECK (2005) An introduction to markers, quantitative trait loci (QTL) mapping and marker-assisted selection for crop improvement: the basic concepts. Euphytica 142:169–196
Deu M, Ratnadass A, Hamada MA, Noyer JL, Diabate M, Chantereau J (2005) Quantitative trait loci for head-bug resistance in sorghum. Afr J Biotechnol 4:247–250
Dhillon MK, Sharma HC, Reddy BVS, Singh R, Naresh JS, Kai Z (2005) Relative susceptibility of different male-sterile cytoplasms in sorghum to shoot fly, Atherigona soccata. Euphytica 144:275–283
Du B, Zhanga W, Liua B, Hua J, Wei Z, Shi Z, He R, Zhu L, Chen R, Han B, He G (2009) Identification and characterization of Bph14, a gene conferring resistance to brown planthopper in rice. Proc Natl Acad Sci USA 106:22163–22168
Fatouros NE, Bukovinszkine’Kiss G, Kalkers LA, Gamborena RS, Dicke M, Hilker M (2005) Oviposition-induced plant cues: do they arrest Trichogramma wasps during host location? Entomol Exp Appl 115:207–215
Fritz AK, Reddy AS, Pammi S, Ayres NM (1995) Silver staining as a low-cost, non-radioactive method of detecting PCR products. In: Meisinger JJ (ed) Agronomy abstracts. ASA, Madison, p 184
Han SK, Delaney TP (2002) Over-expression of TGA5, which encodes a bZIP transcription factor that interacts with NIM1/NPR1, confers SAR-independent resistance in Arabidopsis thaliana to Peronospora parasitica. Plant J 32:151–163
Hao P, Liu C, Wang Y, Chen R, Tang M, Du B, Zhu L, He G (2008) Herbivore-induced callose deposition on the sieve plates of rice: an important mechanism for host resistance. Plant Physiol 146:1810–1820
Ishimaru K, Ono K, Kashiwagi T (2004) Identification of a new gene controlling plant height in rice using the candidate-gene strategy. Planta 218:388–395
Jotwani MG (1982) Factors reducing sorghum yields-insect pests. In: Sorghum the eighties. Proceedings of the international symposium on sorghum, 2–7 November, 1981. ICRISAT, Patancheru, pp 251–255
Katsar CS, Paterson AH, Teetes GL, Peterson GC (2002) Molecular analysis of sorghum resistance to the greenbug (Homoptera: Aphididae). J Econ Entomol 95:448–457
Kim JS, Klein PE, Klein RR, Price HJ, Mullet JE, Stelly DM (2005) Chromosome identification and nomenclature of Sorghum bicolor. Genetics 169:1169–1173
Klingler J, Creasy R, Gao L, Nair RM, Calix AS, Jacob HS, Edwards OR, Singh KB (2005) Aphid resistance in Medicago truncatula involves antixenosis and phloem-specific, inducible antibiosis, and maps to a single locus flanked by NBS–LRR resistance gene analogs. Plant Physiol 137:1445–1455
Krishnaveni S, Muthukrishnan S, Liang G, Wilde G, Manickam A (1999) Induction of chitinases and beta-1,3-glucanases in resistant and susceptible cultivars of sorghum in response to insect attack, fungal infection and wounding. Plant Sci 144:9–16
Li Q, Yang X, Bai G, Warburton ML, Mahuku G, Gore M, Dai J, Li J, Yan J (2010) Cloning and characterization of a putative GS3 ortholog involved in maize kernel development. Theor Appl Genet 120:753–763
Little D, Gouhier-Darimont C, Bruessow F, Reymond P (2007) Oviposition by pierid butterflies triggers defense responses in Arabidopsis. Plant Physiol 143:784–800
Mace ES, Jordan DR (2011) Integrating sorghum whole genome sequence information with a compendium of sorghum QTL studies reveals uneven distribution of QTL and of gene-rich regions with significant implications for crop improvement. Theor Appl Genet 123:169–191
McHale L, Tan X, Koehl P, Michelmore RW (2006) Plant NBS–LRR proteins: adaptable guards. Genome Biol 7:212
McWhorter CG, Paul RN, OuztsSource JK (1995) Bicellular trichomes of Johnsongrass (Sorghum halepense) leaves: morphology, histochemistry, and function. Weed Sci 43:201–208
Meng XB, Zhao WS, Lin RM, Wang M, Peng YL (2005) Identification of a novel rice bZIP-type transcription factor gene, OsbZIP1, involved in response to infection of Magnaporthe grisea. Plant Mol Biol Rep 23:301a–301m
Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM (1998) The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10:1307–1319
Nagaraj N, Reese JC, Tuinstra MR, Smith CM, Amand PS, Kirkham MB, Kofoid KD, Campbell LR, Wilde GE (2005) Molecular mapping of sorghum genes expressing tolerance to damage by greenbug (Homoptera: Aphididae). J Econ Entomol 98:595–602
Nagaraja Reddy R, Madhusudhana R, Murali Mohan S, Chakravarthi DVN, Seetharama N (2012) Characterization, development and mapping of unigene-derived microsatellite markers in sorghum [Sorghum bicolor (L.) Moench]. Mol Breed 29:543–564
Nombela G, Williamson VM, Muniz M (2003) The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. Mol Plant Microbe Interact 16:645–649
Padmaja PG, Madhusudhana R, Seetharama N (2010) Epicuticular wax and morphological traits associated with resistance to shoot fly, Atherigona soccata Rondani in sorghum, Sorghum bicolor. Entomon 34:137–146
Park DS, Lee SK, Lee JH, Song MY, Song SY, Kwak DY, Yeo US, Jeon NS, Park SK, Yi G, Song YC, Nam MH, Ku YC, Jeon JS (2007) The identification of candidate rice genes that confer resistance to the brown planthopper (Nilaparvata lugens) through representational difference analysis. Theor Appl Genet 115:537–547
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 457:551–556
Pechan T, Ye L, Chang YM, Mitra A, Lin L, Davis FM, Williams WP, Luthe DS (2000) A unique 33-kD cysteine proteinase accumulates in response to larval feeding in maize genotypes resistant to fall armyworm and other Lepidoptera. Plant Cell 12:1031–1040
Pflieger S, Lefebvre V, Causse M (2001) The candidate gene approach in plant genetics: a review. Mol Breed 7:275–291
Pieterse CM, Van Loon LC (2004) NPR1: the spider in the web of induced resistance signaling pathways. Curr Opin Plant Biol 7:456–464
Price AH (2006) Believe it or not, QTLs are accurate. Trends Plant Sci 11:213–216
Romeis T, Ludwig AA, Martin R, Jones DGJ (2001) Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO J 20:5556–5567
Rossi M, Goggin FL, Milligan SB, Kaloshian I, Ullman DE, Williamson VM (1998) The nematode resistance gene Mi of tomato confers resistance against the potato aphid. Proc Natl Acad Sci USA 95:9750–9754
Sardesai N, Subramanyam S, Nemacheck J, Williams C (2005) Modulation of defense response gene expression in wheat during Hessian fly larval feeding. J Plant Interact 1:39–50
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]. Theor Appl Genet 119:1425–1439
Scheer JM Jr, Ryan CA (2002) The systemin receptor SR160 from Lycopersicon peruvianum is a member of the LRR receptor kinase family. Proc Natl Acad Sci USA 99:9585–9590
Seino Y, Suzuki Y, Sogawa K (1996) An ovicidal substance produced by rice plants in response to oviposition by the whitebacked planthopper, Sogatella furcifera (HORVATH) (Homoptera: Delphacidae). Appl Entomol Zool 31:467–473
Shapiro AM, Devay JE (1987) Hypersensitivity reaction of Brassica nigra L. (Cruciferae) kills eggs of Pieris butterflies (Lepidoptera, Pieridae). Oecologia 71:631–632
Sharma HC (1993) Host plant resistance to insects in sorghum and its role in integrated pest management. Crop Prot 12:11–34
Sharma HC (2006) Integrated pest management research at ICRISAT: present status and future priorities. International Crops Research Institute for the Semi-Arid Tropics, Patancheru 502324, Andhra Pradesh, India, p 48
Smith CM, Boyko EV (2007) The molecular bases of plant resistance and defense responses to aphid feeding: current status. Entomol Exp Appl 122:1–16
Soto PE (1974) Ovipositional preference and antibiosis in relation to resistance to sorghum shoot fly. J Econ Entomol 67:165–167
Srinivas G, Satish K, Murali Mohan S, Nagaraja Reddy R, Madhusudhana R, Balakrishna D, Venkatesh Bhat B, Howarth CJ, Seetharama N (2008) Development of genic-microsatellite markers for sorghum staygreen QTL using a comparative genomic approach with rice. Theor Appl Genet 117:283–296
Sukhani TR, Jotwani MG (1980) Efficacy of some newer systemic insecticides for the control of sorghum shootfly [Atherigona soccata (Rondani)]. Indian J Entomol 42:76–81
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, TX, USA, International Crops Research Institute for the Semi-Arid Tropics, Patancheru 502324, Andhra Pradesh, India, pp 115–129
Tao YZ, Hardy A, Drenth J, Henzell RG, Franzmann BA, Jordan DR, Butler DG, McIntyre CL (2003) Identifications of two different mechanisms for sorghum midge resistance through QTL mapping. Theor Appl Genet 107:116–122
Van Ooijen JW (2005) Map-QTL5: software for the mapping quantitative trait loci in mapping populations. Kyazma BV, Wageningen
Van Ooijen JW, Voorrips RE (2001) JoinMap 3.0 software for the calculation of genetic linkage maps. Plant Research International, Wageningen
Varshney RK, Graner A, Sorrells ME (2005) Genic microsatellite markers in plants: features and applications. Trends Biotechnol 23:48–55
Wu Y, Huang Y (2008) Molecular mapping of QTL for resistance to the greenbug Schizaphis graminum (Rondani) in Sorghum bicolor (Moench). Theor Appl Genet 117:117–124
Zhao Q, Dixon RA (2011) Transcriptional networks for lignin biosynthesis: more complex than we thought? Trends Plant Sci 16:227–233
Acknowledgments
The authors sincerely acknowledge the Director, Directorate of Sorghum Research (DSR) and ICAR, New Delhi for the kind support for undertaking this study. The authors also acknowledge Mr. Venkata Ramana for his technical assistance in the laboratory.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Satish, K., Madhusudhana, R., Padmaja, P.G. et al. Development, genetic mapping of candidate gene-based markers and their significant association with the shoot fly resistance quantitative trait loci in sorghum [Sorghum bicolor (L.) Moench]. Mol Breeding 30, 1573–1591 (2012). https://doi.org/10.1007/s11032-012-9740-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11032-012-9740-9