Abstract
Key message
Epistasis and genetic background were important influences on expression of stripe rust resistance in two wheat RIL populations, one with resistance conditioned by two major genes and the other conditioned by several minor QTL.
Abstract
Stripe rust is a foliar disease of wheat (Triticum aestivum L.) caused by the air-borne fungus Puccinia striiformis f. sp. tritici and is present in most regions around the world where commercial wheat is grown. Breeding for durable resistance to stripe rust continues to be a priority, but also is a challenge due to the complexity of interactions among resistance genes and to the wide diversity and continuous evolution of the pathogen races. The goal of this study was to detect chromosomal regions for resistance to stripe rust in two winter wheat populations, ‘Tubbs’/‘NSA-98-0995’ (T/N) and ‘Einstein’/‘Tubbs’ (E/T), evaluated across seven environments and mapped with diversity array technology and simple sequence repeat markers covering polymorphic regions of ≈1480 and 1117 cM, respectively. Analysis of variance for phenotypic data revealed significant (P < 0.01) genotypic differentiation for stripe rust among the recombinant inbred lines. Results for quantitative trait loci/locus (QTL) analysis in the E/T population indicated that two major QTL located in chromosomes 2AS and 6AL, with epistatic interaction between them, were responsible for the main phenotypic response. For the T/N population, eight QTL were identified, with those in chromosomes 2AL and 2BL accounting for the largest percentage of the phenotypic variance.
Similar content being viewed by others
References
Agenbag GM, Pretorius ZA, Boyd LA, Bender CM, Prins R (2012) Identification of adult plant resistance to stripe rust in the wheat cultivar ‘Cappelle-Desprez’. Theor Appl Genet 125:109–120
Akbari M, Wenzl P, Caig V, Carling J, Xia L, Yang SY, Uszynski G, Mohler V, Lehmensiek A, Kuchel H, Hayden MJ, Howes N, Sharp P, Vaughan P, Rathmell B, Huttner E, Kilian A (2006) Diversity arrays technology (DArT) for high-throughput profiling of the hexaploid wheat genome. Theor Appl Genet 113:1409–1420
Allan RE, Peterson CJ, Rubenthaler GL, Line RF, Roberts DE (1989) Registration of ‘Madsen’ wheat. Crop Sci 26:1575
Asins MJ, Carbonell EA (2014) The effect of epistasis between linked genes on quantitative trait locus analysis. Mol Breed 34:1125–1135
Boukhatem N, Baret PV, Mingeot D, Jacquemin JM (2002) Quantitative trait loci for resistance against yellow rust in two wheat-derived recombinant inbred line populations. Theor Appl Genet 104:111–118
Caldwell RM (1968) Breeding for general and/or specific plant disease resistance. In: Finlay KW Shepherd KW (eds) Proceedings of 3rd international wheat genetics symposium Australian Academy of Science Canberra, pp 263–272
Capital Press (2013) New OSU wheat varieties promise yield, rust resistance. Accessed 02 March 2015. [Online] http://www.capitalpress.com/content/mw-Bobtail-Rosalyn-052113-mug
Chen XM (2005) Epidemiology and control of stripe rust Puccinia striiformis f. sp. tritici on wheat. Plant Pathol 27:314–337
Chen XM (2013) Review article: high-temperature adult-plant resistance key for sustainable control of stripe rust. Am J Plant Sci 4:608–627
Chen XM (2014) Integration of cultivar resistance and fungicide application for control of wheat stripe rust. Can J Plant Pathol 36:311–326
Chen XM, Moore M, Milus EA, Long DL, Line RF, Marshall D, Jackson L (2002) Wheat stripe rust epidemics and races of Puccinia striiformis f. sp. tritici in the United States in 2000. Plant Dis 86:39–46
Chen XM, Coram T, Huang X, Wang M, Dolezal A (2013) Understanding molecular mechanisms of durable and non-durable resistance to stripe rust in wheat using a transcriptomics approach. Curr Genomics 14:111–126
Churchill GA, Doerge RW (1994) Empirical threshold values for quantitative trait mapping. Genetics 138:963–971
Conti V, Roncallo PF, Beaufort V, Cervigni GL, Miranda R, Jensen CA, Echenique VC (2011) Mapping of main and epistatic effect QTLs associated to grain protein and gluten strength using a RIL population of durum wheat. J Appl Genet 52:287–298
Dedryver F, Paillard S, Mallard S, Robert O, Trottet M, Nègre S, Verplancke G, Jahier J (2009) Characterization of genetic components involved in durable resistance to stripe rust in the bread wheat ‘Renan’. Phytopathology 99:968–973
Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Longman, Burnt Mill, Harlow, Essex, England, pp 376
Fang T, Garland-Campbell KA, Liu Z, Chen XM, Wan A, Li S, Liu Z, Cao S, Chen Y, Bowden RL, Carver B, Yan L (2011) Stripe rust resistance in the wheat cultivar ‘Jagger’ is due to Yr17 plus a novel QTL. Crop Sci 51:2455–2465
FAO’s Plant Production and Protection Division (AGP). Wheat rust disease global programme. Accessed Sept 2014. [Online] http://www.faoorg/agriculture/crops/thematic-sitemap/theme/pests/wrdgp/en/
GrainGenes 2.0 (2013) A database for Triticeae and Avena maps tml. Accessed 23 Nov 2013. http://www.wheatpwusdagov/ggpages/map_shortlisth
Guest DI, Brown JF (1997) Plant defences against pathogens. In: Brown JF, Ogle JH (eds) Plant pathogens and plant diseases. Rockvale Publications, Armidale, pp 263–286
Haldane JBS (1919) The combination of linkage values and the calculation of distances between the loci of linked factors. J Genet 8:299–309
Hao Y, Chen Z, Wang Y, Bland D, Buck J, Brown-Guedira G, Johnson J (2011) Characterization of a major QTL for adult plant resistance to stripe rust in US soft red winter wheat. Theor Appl Genet 123:1401–1411
Hayes PM, Marquez-Cedillo L, Mundt CC, Richardson K, Vales MI (2006) Perspectives on finding and using quantitative disease resistance genes in barley. In: Lamkey KR, Lee M (eds) Plant breeding: the Arnel R Hallauer international symposium. Blackwell, Ames, pp 182–200
Helguera M, Khan IA, Kolmer J, Lijavetzky D, Zhong-Qi L, Dubcovsky J (2003) PCR assays for the cluster of rust resistance genes and their use to develop isogenic hard red spring wheat lines. Crop Sci 43:1839–1847
Holland JB, Nyquist WE, Cervantes-Martínez CT (2010) Estimating and interpreting heritability for plant breeding: an update plant breeding reviews. Wiley, Oxford, pp 9–112
Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329
Jones SS, Lyons SR, Balow KA, Gollnick MA, Murphy KM, Kuehner JS, Murray TD, Chen X, Engle DA, Garland Campbell KA (2010) Registration of ‘Xerpha’ Wheat. J Plant Regist 4:137–140
Knott DR (2000) Inheritance of resistance to stem rust in Medea durum wheat and the role of suppressors. Crop Sci 40:98–102
Limagrain UK (2013). Accessed 01 March 2013. [Online] http://www.limagraincouk/products/details/11html
Lin F, Chen XM (2009) Quantitative trait loci for non-race-specific high-temperature adult-plant resistance to stripe rust in wheat cultivar ‘Express’. Theor Appl Genet 118:631–642
Mackay TF (2013) Epistasis and quantitative traits: using model organisms to study gene-gene interactions. Nat Rev Genet 10:565–577
Mao D, Liu T, Xu C, Li X, Xing Y (2011) Epistasis and complementary gene action adequately account for the genetic bases of transgressive segregation of kilo-grain weight in rice. Euphytica 180:261–271
Paillard S, Trotoux-Verplancke G, Perretant M-R, Mohamadi F, Leconte M, Coëdel S, de Vallavieille-Pope C, Dedryver F (2012) Durable resistance to stripe rust is due to three specific resistance genes in French bread wheat cultivar ‘Apache’. Theor Appl Genet 125:955–965
Parlevliet JE (1979) Components of resistance that reduce the rate of epidemic development. Annu Rev Phytopathol 17:203–222
Parlevliet JE (1986) Pleiotropic association of infection frequency and latent period of two barley cultivars partially resistant to barley leaf rust. Euphytica 35:267–272
Parlevliet JE (2002) Durability of resistance against fungal bacterial and viral pathogens; present situation. Euphytica 124:147–156
Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ (2009) Shades of gray: the world of quantitative disease resistance. Trends Plant Sci 14:21–29
Purcell S, Sham PC (2004) Epistasis in quantitative trait locus linkage analysis: interaction or main effect? Behav Genet 34:143–152
Quincke MC, Peterson CJ, Zemetra RS, Hansen JL, Chen JL, Riera-Lizarazu O, Mundt CC (2011) Quantitative trait loci analysis for resistance to Cephalosporium stripe, a vascular wilt disease of wheat. Theor Appl Genet 122:1339–1349
Reif JC, Maurer HP, Korzun V, Ebmeyer E, Miedaner T, Wyrschum T (2011) Mapping QTLs with main and epistatic effects underlying grain yield and heading time in soft winter wheat. Theor Appl Genet 123:283–292
Riera-Lizarazu O, Vales IM, Ananiev EV, Rines HW, Phillips RL (2000) Production and characterization of maize chromosome radiation hybrids derived from an oat-maize addition line. Genetics 156:329–339
Roelfs AP, Singh RP, Saari EE (1992) Rust diseases of wheat: concepts and methods of disease management. Mexico, CIMMYT, p 45
Roncallo PF, Cervigni GL, Jensen C, Miranda R, Carrera AD, Helguera M, Echenique V (2012) QTL analysis of main and epistatic effects for flour color traits in durum wheat. Euphytica 185:77–92
Rosewarne GM, Herrera-Foessel SA, Singh RP, Huerta-Espino J, Lan CX, He ZH (2013) Quantitative trait loci of stripe rust resistance in wheat. Theor Appl Genet 126:2427–2449
Rouse MN, Talbert LE, Singh D, Sherman JD (2014) Complementary epistasis involving Sr12 explains adult plant resistance to stem rust in ‘Thatcher’ wheat (Triticum aestivum L.). Theor Appl Genet 127:1549–1559
SAS Institute Inc. (2004) SAS 9.1.3 Help and Documentation, Cary, NC: SAS Institute Inc., 2002–2004
Sharma-Poudyal D, Chen XM, Rupp R (2014) Potential oversummering and overwintering regions for the wheat stripe rust pathogen in the contiguous United States. Int J Biometeorol 58:987–997
Silva LDCE, Wang S, Zeng Z-B (2012) Composite interval mapping and multiple interval mapping: procedures and guidelines for using windows QTL cartographer. In: Rifkin SA (ed) Quantitative trait loci (QTL). Humana Press, New York, pp 75–119
Singh A, Knox RE, DePauw RM, Singh AK, Cuthbert RD, Campbell HL, Singh D, Bhavani S, Fetch T, Clarke F (2013) Identification and mapping in spring wheat of genetic factors controlling stem rust resistance and the study of their epistatic interactions across multiple environments. Theor Appl Genet 126:1951–1964
Singh A, Knox RE, DePauw RM, Singh AK, Cuthbert RD, Campbell HL, Shorter S, Bhavani S (2014) Stripe rust and leaf rust resistance QTL mapping epistatic interactions and co-localization with stem rust resistance loci in spring wheat evaluated over three continents. Theor Appl Genet 127:2465–2477
Sthapit J, Newcomb M, Bonman JM, Chen XM, See DR (2014) Genetic diversity for stripe rust resistance in wheat landraces and identification of accessions with resistance to stem rust and stripe rust. Crop Sci 54:2131–2139
Triticarte (2013) Wheat DArT Yarralumla ACT 2600 Australia. http://www.triticartecomau/content/wheat_diversity_analysishtml
US Wheat Associates (USW) Market and crop information. Retrieved Sept 2014. http://www.uswheatorg/commercialSales
USDA-AMS (2015) Plant variety protection office, Beltsville MD. Accessed 28 March 2015. http://www.ars-gringov/cgi-bin/npgs/html/pvplistpl? [Online]
Van Ooijen JW (2006) JoinMap 4.0 Software for the calculation of genetic linkage maps in experimental populations. Plant Research International, Wageningen
Vazquez MD, Peterson CJ, Riera-Lizarazu O, Chen XM, Heesacker A, Ammar K, Crossa J, Mundt CC (2012) Genetic analysis of adult plant quantitative resistance to stripe rust in wheat cultivar ‘Stephens’ in multi-environment trials. Theor Appl Genet 124:1–11
Vazquez MD, Zemetra R, Peterson CJ, Mundt CC (2014) Identification of Cephalosporium stripe resistance quantitative trait loci in two recombinant inbred line populations of winter wheat. Theor Appl Genet 128:329–341
Wan AM, Chen XM (2012) Virulence frequency and distribution of races of Puccinia striiformis f. sp. tritici and P striiformis f. sp. hordei identified in the United States in 2008 and 2009. Plant Dis 96:67–74
Wan AM, Chen XM (2014) Virulence characterization of Puccinia striiformis f. sp. tritici using a new set of Yr single-gene line differentials in the United States in 2010. Plant Dis 98:1534–1542
Wang S, Basten CJ, Zeng ZB (2007) Windows QTL Cartographer 2.5. Department of Statistics. North Carolina State University, Raleigh, NC. http://statgen.ncsu.edu/qtlcart/WQTLCart.htm
Wang C, Ulloa M, Mullens TR, Yu JZ, Robers PA (2012) QTL analysis for transgressive resistance to root-knot nematode in interspecific cotton (Gossypium spp.) progeny derived from susceptible parents. PLoS 1:e34874
Wang G, Leonard JM, Zitzewitz J, Peterson CJ, Ross AS, Riera-Lizarazu O (2014) Marker–trait association analysis of kernel hardness and related agronomic traits in a core collection of wheat lines. Mol Breed 34:177–184
Acknowledgments
We thank the Oregon Wheat Commission and Warren Kronstad Endowment for funding the project. We thank the Columbia Basin Agricultural Research Center staff, Kathryn Sackett, Larae Wallace, Mark Larson, and Paul Severns for their excellent technical assistance.
Conflict of interest
The authors declare that they have no conflict of interests.
Ethical standards
The experiments comply with the current US laws.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by F. Ordon.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Vazquez, M.D., Zemetra, R., Peterson, C.J. et al. Multi-location wheat stripe rust QTL analysis: genetic background and epistatic interactions. Theor Appl Genet 128, 1307–1318 (2015). https://doi.org/10.1007/s00122-015-2507-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-015-2507-z