Abstract
Stagonospora nodorum glume blotch (SNG), caused by the necrotrophic fungus Stagonospora nodorum, is one of the economically important diseases of bread wheat (Triticum aestivum L.). Resistance to SNG is known to be quantitative and previous studies of a recombinant inbred line (RIL) population identified a major quantitative trait locus (QTL) for resistance to SNG on the short arm of chromosome 3B. To localize this QTL (QSng.sfr-3BS) with high resolution, we constructed a genetic map for the QTL target region using information from sequenced flow-sorted chromosomes 3B of the two parental cultivars ‘Arina’ and ‘Forno’, the physical map of chromosome 3B of cultivar ‘Chinese Spring’ and BAC-clone sequences. The mapping population of near-isogenic lines (NIL) was evaluated for SNG resistance in field infection tests. NILs segregated for disease resistance as well as for plant height; additionally, we observed a high environmental influence on the trait. Our analysis detected a strong negative correlation of SNG resistance and plant height. Further analysis of the target region identified two linked loci associated with SNG resistance. One of them was also associated with plant height, revealing an effect of QSng.sfr-3BS on plant height that was hidden in the RIL population. This result demonstrates an unexpectedly high genetic complexity of resistance controlled by QSng.sfr-3BS and shows the importance of the study of QTL in mendelized form in NILs.
Similar content being viewed by others
References
Aguilar V, Stamp P, Winzeler M, Winzeler H, Schachermayr G, Keller B, Zanetti S, Messmer MM (2005) Inheritance of field resistance to Stagonospora nodorum leaf and glume blotch and correlations with other morphological traits in hexaploid wheat (Triticum aestivum L.). Theor Appl Genet 111:325–336
Akhunov ED, Goodyear AW, Geng S, Qi L-L, Echalier B, Gill BS, Miftahudin, Gustafson JP, Lazo G, Chao S, Anderson OD, Linkiewicz AM, Dubcovsky J, Rota ML, Sorrells ME, Zhang D, Nguyen HT, Kalavacharla V, Hossain K, Kianian SF, Peng J, Lapitan NLV, Gonzalez-Hernandez JL, Anderson JA, Choi D-W, Close TJ, Dilbirligi M, Gill KS, Walker-Simmons MK, Steber C, McGuire PE, Qualset CO, Dvorak J (2003) The organization and rate of evolution of wheat genomes are correlated with recombination rates along chromosome arms. Genome Res 13:753–763
Bennett MD, Smith JB (1976) Nuclear DNA amounts in angiosperms. Philos Trans R Soc Lond B Biol Sci 274:227–274
Bostwick DE, Ohm HW, Shaner G (1993) Inheritance of Septoria glume blotch resistance in wheat. Crop Sci 33:439–443
Broennimann A (1968) Untersuchungen über Septoria nodorum Berk. des Weizens. Mitteil Schweiz Landw 16:65–76
Broennimann A (1975) Contributions to genetics of tolerance towards Septoria nodorum Berk. in wheat (Triticum aestivum L.). J Plant Breed 75:138–160
Broennimann A, Fossati A, Hani F (1973) Spreading of Septoria nodorum Berk. and damage to artificially induced mutants of winter wheat cultivar Zenith (Triticum aestivum L.). J Plant Breed 70:230–245
Bryan GJ, Stepherson P, Collins A, Kirby J, Smith JB, Gale MD (1999) Low level of DNA sequence variation among adapted genotypes of hexaploid wheat. Theor Appl Genet 99:192–198
Choulet F, Wicker T, Rustenholz C, Paux E, Salse J, Leroy P, Schlub S, Paslier M-CL, Magdelenat G, Gonthier C, Couloux A, Budak H, Breen J, Pumphrey M, Liu S, Kong X, Jia J, Gut M, Brunel D, Anderson JA, Gill BS, Appels R, Keller B, Feuillet C (2010) Megabase level sequencing reveals contrasted organization and evolution patterns of the wheat gene and transposable element spaces. Plant Cell 22:1686–1701
Crawley MJ (2007) The R book. Wiley, England
Draeger R, Gosman N, Steed A, Chandler E, Thomsett M, Srinivasachary, Schondelmaier J, Buerstmayr H, Lemmens M, Schmolke M, Mesterhazy A, Nicholson P (2007) Identification of QTLs for resistance to Fusarium head blight, DON accumulation and associated traits in the winter wheat variety Arina. Theor Appl Genet 115:617–625
Duczek LJ, Sutherland KA, Reed SL, Bailey KL, Lanford GP (1999) Survival of leaf spot pathogens on crop residues of wheat and barley in Saskatchewan. Can J Plant Pathol 21:165–173
Ellis MH, Rebetzke GJ, Azanza F, Richards RA, Spielmeyer W (2005) Molecular mapping of gibberillin-responsive dwarfing genes in bread wheat. Theor Appl Genet 111:423–430
Eriksen L, Borum F, Jahoor A (2003) Inheritance and localisation of resistance to Mycosphaerella graminicola causing septoria tritici blotch and plant height in the wheat (Triticum aestivum L.) genome with DNA markers. Theor Appl Genet 107:515–527
Eyal Z, Scharen AL, Prescott JM and van Ginkel M (1987) The Septoria diseases of wheat: concepts and methods of disease management. CIMMYT, Mexico, DF
FAO stat (2010) Food and Agriculture organization of the United Nations. Available at http://faostat.fao.org
Faris JD, Haen KM, Gill BS (2000) Saturation mapping of a gene-rich recombination hot spot region in wheat. Genetics 154:823–835
Fridman E, Liu YS, Carmel-Goren L, Gur A, Shoresh M, Pleban T, Eshed Y, Zamir D (2002) Two tightly linked QTLs modify tomato sugar content via different physiological pathways. Mol Genet Genomics 266:821–826
Fried PM, Meister E (1987) Inheritance of leaf and head resistance of winter wheat to Septoria nodorum in a diallel cross. Phytopathology 77:1371–1375
Gervais L, Dedryver F, Morlais J-Y, Bodusseau V, Negre S, Bilous M, Groos C, Trottet M (2003) Mapping of quantitative trait loci for field resistance to Fusarium head blight in an European winter wheat. Theor Appl Genet 106:961–970
Halama P (2002) Mating relationships between isolates of Phaeosphaeria nodorum, (anamorph Stagonospora nodorum) from geographical locations. Eur J Plant Pathol 108:593–596
Hallauer AR, Miranda Fo JB (1981) Quantitative genetics in maize breeding. The Iowa University Press, Ames
Hollister JD, Gaut BS (2009) Epigenetic silencing of transposable elements: a trade-off between reduced transposition and deleterious effects on neighboring gene expression. Genome Res 19:1419–1428
Jeger MJ, Viljanen-Rollinson SLH (2001) The use of the area under the disease progress curve (AUDPC) to assess quantitative disease resistance in crop cultivars. Theor Appl Genet 102:32–40
Keurentjes JJB, Bentsink L, Alonso-Blanco C, Hanhart CJ, Vries HB-D, Effgen S, Vreugdenhil D, Koornneef M (2007) Development of a near-isogenic line population of Arabidopsis thaliana and comparison of mapping power with a recombinant inbred line population. Genetics 175:891–905
Kroymann J, Mitchell-Olds T (2005) Epistasis and balanced polymorphism influencing complex trait variation. Nature 435:95–98
Laubscher FX, von Wechmar B, van Schalkwyk D (1966) Heritable resistance of wheat varieties to Glume Blotch (Septoria nodorum Berk.). J Phytopathol 56:260–264
Mesterhazy A (1995) Types and components of resistance to Fusarium head blight of wheat. Plant Breed 114:377–386
Monna L, Lin X, Kojima S, Sasaki T, Yano M (2002) Genetic dissection of a genomic region for a quantitative trait locus, Hd3, into two loci, Hd3a and Hd3b, controlling heading date in rice. Theor Appl Genet 104:772–778
Nelson LR, Gates CE (1982) Genetics of host plant resistance of wheat to Septoria nodorum. Crop Sci 22:771–773
Oliver RP, Friesen TL, Faris JD, Solomon PS (2012) Stagonospora nodorum: from pathology to genomics and host resistance. Annu Rev Phytopathol 50:23–43
Paillard S, Schnurbusch T, Winzeler M, Messmer M, Sourdille P, Abderhalden O, Keller B, Schachermayr G (2003) An integrative genetic linkage map of winter wheat (Triticum aestivum L.). Theor Appl Genet 107:1235–1242
Paux E, Sourdille P, Salse J, Saintenac C, Choulet F, Leroy P, Korol A, Michalak M, Kianian S, Spielmeyer W, Lagudah E, Somers D, Kilian A, Alaux M, Vautrin S, Bergès H, Eversole K, Appels R, Safar J, Simkova H, Dolezel J, Bernard M, Feuillet C (2008) A physical map of the 1-gigabase bread wheat chromosome 3B. Science 322:101–104
Paux E, Faure S, Choulet F, Roger D, Gauthier V, Martinant J-P, Sourdille P, Balfourier F, Paslier M-CL, Chauveau A, Cakir M, Gandon B, Feuillet C (2010) Insertion site-based polymorphism markers open new perspectives for genome saturation and marker-assisted selection in wheat. Plant Biotechnol J 8:196–210
Pea G, Paulstephenraj P, Canè MA, Sardaro MLS, Landi P, Morgante M, Porceddu E, Pè ME, Frascaroli E (2009) Recombinant near-isogenic lines: a resource for the mendelization of heterotic QTL in maize. Mol Genet Genomics 281:447–457
Rustenholz C, Choulet F, Laugier C, Šafář J, Šimková H, Doležel J, Magni F, Scalabrin S, Cattonaro F, Vautrin S, Bellec A, Bergès H, Feuillet C, Paux E (2011) A 3,000-loci transcription map of chromosome 3B unravels the structural and functional features of gene islands in hexaploid wheat. Plant Physiol 157:1596–1608
R Development Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org. ISBN 3-900051-07-0
Schnurbusch T, Paillard S, Fossati D, Messmer M, Schachermayr G, Winzeler M, Keller B (2003) Detection of QTLs for Stagonospora glume blotch resistance in Swiss winter wheat. Theor Appl Genet 107:1226–1234
Scott PR, Benedikz PW, Cox CJ (1982) A genetic study of the relationship between height, time of ear emergence and resistance to Septoria nodorum in wheat. Plant Pathol 31:45–60
Scott PR, Benedikz PW, Zones HG, Ford MA (1985) Some effects of canopy structure and microclimate on infection of tall and short wheats by Septoria nodorum. Plant Pathol 34:587–593
Shah DA, Bergstrom GC (2002) A rainfall-based model for predicting the regional incidence of wheat seed infection by Stagonospora nodorum in New York. Phytopathology 92:511–518
Shatalina M, Wicker T, Buchmann JP, Oberhaensli S, Simková H, Doležel J, Keller B (2013) Genotype-specific SNP map based on whole chromosome 3B sequence information from wheat cultivars Arina and Forno. Plant Biotechnol J 11:23–32
Shaw MW, Bearchell SJ, Fitt BDL, Fraaije BA (2008) Long-term relationships between environment and abundance in wheat of Phaeosphaeria nodorum and Mycosphaerella graminicola. New Phytol 177:229–238
Srinivasachary Gosman N, Steed A, Hollins TW, Bayles R, Jennings P, Nicholson P (2009) Semi-dwarfing Rht-B1 and Rht-D1 loci of wheat differ significantly in their influence on resistance to Fusarium head blight. Theor Appl Genet 118:695–702
The International Rice Genome Sequencing Project (2005) The map-based sequence of the rice genome. Nature 436:793–800
Thomson MJ, Edwards JD, Septiningsih EM, Harrington SE, McCouch SR (2006) Substitution mapping of dth1.1, a flowering-time quantitative trait locus (QTL) associated with transgressive variation in rice, reveals multiple sub-QTL. Genetics 172:2501–2514
Tommasini L, Schnurbusch T, Fossati D, Mascher F, Keller B (2007) Association mapping of Stagonospora nodorum blotch resistance in modern European winter wheat varieties. Theor Appl Genet 115:697–708
Van Ginkel M, Rajaram S (1999) Breeding for resistance to the Septoria/Stagonospora blights of wheat. In: van Ginkel M, McNab A, Krupinsky JM (eds) Septoria and Stagonospora diseases of cereals: a compilation of global research. CIMMYT, Mexico
Wanjugi H, Coleman-Derr D, Huo N, Kianian SF, Luo M-C, Wu J, Anderson O, Gu YQ (2009) Rapid development of PCR-based genome-specific repetitive DNA junction markers in wheat. Genome 52:576–587
Wicki W, Winzeler M, Schmid JE, Stamp P, Messmer M (1999) Inheritance of resistance to leaf and glume blotch caused by Septoria nodorum Berk. in winter wheat. Theor Appl Genet 99:1265–1272
Wolf EDD, Francl LJ (2000) Neural network classification of tan spot and Stagonospora blotch infection periods in a wheat field environment. Phytopathology 90:108–113
Acknowledgments
We thank Bea Senger and Stefan Kellenberger for excellent technical assistance with the field experiments. We thank Philip Streckeisen for the guidance on SNB field scorings. We also thank Bea Senger for the technical help with the plant material in the greenhouse. We thank Hana Simkova and Jaroslav Dolezel for isolation of chromosome 3B by flow cytometry. We also thank Matthias Helling for the help with the statistical analysis. The research leading to these results received funding from the European Community’s Seventh Framework Programme (FP7/2007-2013) under the grant agreement FP7-212019 (Triticeae Genome) and was supported in the framework of the European Cooperation in Science and Technology FA0604 (Tritigen). This work was also supported by a grant from the Swiss National Science Foundation 31003A_127061. The experiments in this study comply with the current laws of Switzerland.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by S. Dreisigacker.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Shatalina, M., Messmer, M., Feuillet, C. et al. High-resolution analysis of a QTL for resistance to Stagonospora nodorum glume blotch in wheat reveals presence of two distinct resistance loci in the target interval. Theor Appl Genet 127, 573–586 (2014). https://doi.org/10.1007/s00122-013-2240-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-013-2240-4