Abstract
Hessian fly (Mayetiola destructor (Say)) is a major pest in wheat producing areas of United States, Canada, Europe, and North Africa but has not been found in Australia. Host plant resistance is thought to involve a similar strategy used against plant pathogen, and in this study, we sought to investigate whether disease-resistance gene markers can also be useful in selecting against Hessian fly attack. The genome-wide association study involved 251 wheat genotypes of diverse origin and 72 SNPs, selected on the basis of significant similarity of their associated contig sequences to putative disease resistance genes. A novel statistical approach for genome-wide scan was applied, which utilised genotype data scored as Null alleles in the mixed model, instead of deleting or treating them as missing alleles. The analyses identified four markers with significant associations at the 5% level, after applying the false discovery rate. These were located on chromosomes 4A, 4B, 5A and 7D, with the 5A locus mapping to the cluster of major genes that confer resistance to multiple Hessian fly biotypes. Amongst the diverse wheat accessions analysed, most of the susceptible phenotypes carried the A–G–C–C haplotype at the BS00064369, BS00007416, BS00077047 and HfrDrd_nt_143 loci, respectively. When heterozygotes were excluded, all the Australian wheat accessions carried this allelic combination. The combination of alleles conferring resistance depended on the origin of the wheat accessions, with ICARDA accessions carrying a preponderance of the C–C–CG–T. Of the 11 USA accessions used for this study, only Lola carried a favourable combination of alleles for resistance at these loci.
Similar content being viewed by others
References
Allen AM, Barker GL, Berry ST, Coghill JA, Gwilliam R, Kirby S, Robinson P, Brenchley RC, D’Amore R, McKenzie N, Waite D, Hall A, Bevan M, Hall N, Edwards KJ (2011) Transcript-specific, single‐nucleotide polymorphism discovery and linkage analysis in hexaploid bread wheat (Triticum aestivum L.). Plant Biotechnol J 9:1086–1099
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B (Methodol) 57:289–300
Buntin GD (1999) Hessian fly (Diptera: Cecidomyiidae) injury and loss of winter wheat grain yield and quality. J Econ Entomol 92:1190–1197
Butler DG, Cullis BR, Gilmour AR, Gogel BJ (2009) ASReml-R reference manual, release 3 edition
Byers RA, Gallun RL (1972) Ability of Hessian fly to stunt winter wheat. 1. Effect of larval feeding on elongation of leaves. J Econ Entomol 65:955–958
Chapman JA, Mascher M, Buluç A, Barry K, Georganas E, Session A, Strnadova V, Jenkins J, Sehgal S, Oliker L, Schmutz J (2015) A whole-genome shotgun approach for assembling and anchoring the hexaploid bread wheat genome. Genome Biol 16:26. https://doi.org/10.1186/s13059-015-0582-8
Chen J, Souza EJ, Zemetra RS, Bosque-Pérez NA, Guttieri MJ, Schotzko D, O’Brien KL, Windes JM, Guy SO, Brown BD, Chen XM (2009) Registration of ‘cataldo’ wheat. J Plant Regist 3:264–268
Cook RJ (1998) The molecular mechanisms responsible for resistance in plant–pathogen interactions of the gene-for-gene type function more broadly than previously imagined. Proc Natl Acad Sci USA 95:9711–9712 (Commentary)
Dweikat I, Zhang W, Ohm H (2002) Development of STS markers linked to Hessian fly resistance gene H6 in wheat. Theor Appl Genet 105:766–770
El Bouhssini M, Lhaloui S, Amri A, Jlibene M, Hatchett JH, Nssarellah N, Nachitt M (1996) Wheat genetic control of Hessian fly (Diptera: Cecidomyiidae) in Morocco. Field Crops Res 45:111–114
El Bouhssini M, Nachit MM, Valkoun J, Abdalla O, Rihawi F (2008) Sources of resistance to Hessian fly (Diptera: Cecidomyiidae) in Syria identified among Aegilops species and synthetic derived bread wheat lines. Genet Resour Crop Evol 55:1215–1219
El Bouhssini M, Chen M, Lhaloui S, Zharmukhamedova G, Rihawi F (2009) Virulence of Hessian fly (Diptera: Cecidomyiidae) in the fertile crescent. J Appl Entomol 133:381–385
Emebiri LC, Tan MK, El-Bouhssini M, Wildman O, Jighly A, Tadesse W, Ogbonnaya FC (2017) QTL mapping identifies a major locus for resistance in wheat to Sunn pest (Eurygaster integriceps) feeding at the vegetative growth stage. Theor Appl Genet 130:309–318
Friebe B, Kynast RG, Hatchett JH, Sears RG, Wilson DL, Gill BS (1999) Transfer of wheat-rye translocation chromosomes conferring resistance to Hessian fly from bread wheat into durum wheat. Crop Sci 39:1692–1696
Giovanini MP, Saltzmann KD, Puthoff DP, Gonzalo M, Ohm HW, Williams CE (2007) A novel wheat gene encoding a putative chitin-binding lectin is associated with resistance against Hessian fly. Mol Plant Pathol 8:69–82
Harris MO, Freeman TP, Moore JA, Anderson KG, Payne SA, Anderson KM, Rohfritsch O (2010) H-gene-mediated resistance to Hessian fly exhibits features of penetration resistance to fungi. Phytopathology 100:279–289
Joukhadar R, El Bouhssini M, Jighly A, Ogbonnaya FC (2013) Genome-wide association mapping for five major pest resistances in wheat. Mol Breed 32:943–960
Kolesik P (2015) A review of gall midges (Diptera: Cecidomyiidae: Cecidomyiinae) of Australia and Papua New Guinea: morphology, biology, classification and key to adults. Austr Entomol 54:127–148
Liu M, Lei L, Powers C, Liu Z, Campbell KG, Chen X, Bowden RL, Carver BF, Yan L (2016) TaXA21–A1 on chromosome 5AL is associated with resistance to multiple pests in wheat. Theor Appl Genet 129:345–355
Mittapalli O, Neal JJ, Shukle RH (2007) Antioxidant defense response in a galling insect. Proc Natl Acad Sci 104:1889–1894
Naber N, El Bouhssini M, Lhaloui S (2003) Biotypes of Hessian fly (Dipt., Cecidomyiidae) in Morocco. J Appl Entomol 127:174–176
Ogbonnaya FC, Abdalla O, Mujeeb-Kazi A, Kazi AG, Xu SS, Gosman N, Lagudah ES, Bonnett D, Sorrells, ME, Tsujimoto H (2013) Synthetic hexaploids: harnessing species of the primary gene pool for wheat improvement. Plant Breed Rev Volume 37, Edited by Jules Janick, Wiley-Blackwell
Ohm HW, Sharma HC, Patterson FL, Ratcliffe RH, Obanni M (1995) Linkage relationships among genes on wheat chromosome 5A that condition resistance to Hessian fly. Crop Sci 35:1603–1607
Ohm HW, Ratcliffe RH, Patterson FL, Camborn SE (1997) Resistance to Hessian fly conditioned by genes H19 and proposed gene H27 (renamed as H29) of Durum wheat line PI422297. Crop Sci 37:113–115
Ratcliffe RH, Hatchett JH (1997) Biology and genetics of the Hessian fly and resistance in wheat. In: Bondari K (ed) New developments in entomology. Research Signpost, Trivandrum, pp 47–56
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
Smiley RW, Gourlie JA, Whittaker RG, Easley SA, Kidwell KK (2004) Economic impact of Hessian fly (Diptera: Cecidomyiidae) on spring wheat in Oregon and additive yield losses with Fusarium crown rot and lesion nematode. J Econ Entomol 97:397–408
Staskawicz BJ, Ausubel FM, Baker BJ, Ellis JG, Jones JD (1995) Molecular genetics of plant disease resistance. Science (New York, NY) 268:661–667
Stuart JJ, Chen M-S, Shukle R, Harris MO (2012) Gall midges (Hessian flies) as plant pathogens. Annu Rev Phytopathol 50:339–357
Subramanyam S, Zheng C, Shukle JT, Williams CE (2013) Hessian fly larval attack triggers elevated expression of disease resistance dirigent-like protein-encoding gene, HfrDrd, in resistant wheat. Arthropod-Plant Interact 7:389–402
Tan CT, Carver BF, Chen M-S, Gu Y-Q, Yan L (2013) Genetic association of OPR genes with resistance to Hessian fly in hexaploid wheat. BMC Genom 14:369
Tan M-K, El Bouhssini M, Emebiri LC, Wildman O, Tadesse W, Ogbonnaya FC (2015) A SNP marker for the selection of HfrDrd, a Hessian fly-response gene in wheat. Mol Breed 35:216
Tan CT, Yu H, Yang Y, Xu X, Chen M, Rudd JC, Xue Q, Ibrahim AM, Garza L, Wang S, Sorrells ME (2017) Development and validation of KASP markers for the greenbug resistance gene Gb7 and the Hessian fly resistance gene H32 in wheat. Theor Appl Genet 130:1867–1884
VanRaden PM (2008) Efficient methods to compute genomic predictions. J Dairy Sci 91:4414–4423
Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York
Wilkinson PA, Winfield MO, Barker GL, Allen AM, Burridge A, Coghill JA, Edwards KJ (2012) CerealsDB 2.0: an integrated resource for plant breeders and scientists. BMC Bioinform 13(1):219
Wise IL, Lamb RJ, McKenzie RIH, Whistlecraft JW (2006) Resistance to Hessian fly (Diptera cecidomyiidae) in a Canadian spring wheat cultivar. Can Entomol 138:638–646
Acknowledgements
This study was Funded jointly by Grants from the Grains Research & Development Corporation (GRDC), The NSW Department of Primary Industry (NSW DPI), and International Center for Agricultural Research in Dry Areas (ICARDA), under Grant Number DAN00174.
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
Collins, D., Emebiri, L., Tan, MK. et al. Association of KASP markers with Hessian fly resistance in wheat of diverse origin. Euphytica 214, 144 (2018). https://doi.org/10.1007/s10681-018-2228-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10681-018-2228-x