Practical breeding strategies to improve resistance to Septoria tritici blotch of wheat

Euphytica

Volumn 214, Issue 7, 2018, Pages

  Ghaffary, Seyed Mahmoud Tabib ^a,d   Chawade, Aakash ^b   Singh, Pawan Kumar ^c  

^a Safiabad Agricultural and Natural Resources Research and Education Center   (Iran)

^b SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^c INTERNATIONAL MAIZE AND WHEAT IMPROVEMENT CENTER CIMMYT   (Mexico)

^d International Maize and Wheat Improvement Center (CIMMYT)   (Iran)

Author keywords

Breeding; Resistance; Septoria tritici blotch; Wheat

Indexed keywords

EID: 85049145900     PISSN: 00142336     EISSN: 15735060     Source Type: Journal    
DOI: 10.1007/s10681-018-2205-4     Document Type: Review

References (136)

1. Adhikari TB, Anderson JM, Goodwin SB (2003) Identification and molecular mapping of a gene in wheat conferring resistance to Mycosphaerella graminicola. Phytopathology 93:1158–1164
2. Adhikari TB, Cavaletto JR, Dubcovsky J, Gieco JO, Schlatter AR, Goodwin SB (2004a) Molecular mapping of the Stb4 gene for resistance to Septoria tritici blotch in wheat. Phytopathology 94:1198–1206
3. Adhikari TB, Wallwork H, Goodwin SB (2004b) Microsatellite markers linked to the Stb2 and Stb3 genes for resistance to Septoria tritici blotch in wheat. Crop Sci 44:1403–1411
4. Adhikari TB, Yang X, Cavaletto JR, Hu X, Buechley G, Ohm HW, Shaner G, Goodwin SB (2004c) Molecular mapping of Stb1, a potentially durable gene for resistance to Septoria tritici blotch in wheat. Theor Appl Genet 109:944–953
5. Agrios GN (2005) Plant Pathology, 5th edn. Department of Plant Pathology, University of Florida, Gainesville
6. Alexander H (1992) Evolution of disease resistance in natural plant populations. In: Plant resistance to herbivores and pathogens: ecology, evolution, and genetics. The University of Chicago Press, Chicago, pp 237–326
7. Arraiano LS, Brown JKM (2006) Identification of isolate-specific and partial resistance to Septoria tritici blotch in 238 European wheat cultivars and breeding lines. Plant Pathol 55:726–738
8. Arraiano L, Brading P, Brown J (2001a) A detached seedling leaf technique to study resistance to Mycosphaerella graminicola (anamorph Septoria tritici) in wheat. Plant Pathol 50:339–346
9. Arraiano LS, Worland AJ, Ellerbrook C, Brown JKM (2001b) Chromosomal location of a gene for resistance to Septoria tritici blotch (Mycosphaerella graminicola) in the hexaploid wheat ‘Synthetic 6x’. Theor Appl Genet 103:758–764
10. Arraiano LS, Chartrain L, Bossolini E, Slatter HN, Keller B, Brown JKM (2007) A gene in European wheat cultivars for resistance to an African isolate of Mycosphaerella graminicola. Plant Pathol 56:73–78
11. Arraiano LS, Balaam N, Fenwick PM, Chapman C, Feuerhelm D, Howell P, Smith SJ, Widdowson JP, Brown JKM (2009) Contributions of disease resistance and escape to the control of Septoria tritici blotch of wheat. Plant Pathol 58:910–922
12. Assefa S, Fehrmann H (1998) Resistance in Aegilops species against leaf rust, stem rust, Septoria tritici blotch, eyespot and powdery mildew of wheat. Zeitschrift Fur Pflanzenkrankheiten Und Pflanzenschutz-J Plant Dis Prot 105:624–631
13. Battisti D (2009) Historical warnings of future food insecurity with unprecedented seasonal heat. Science 323:240
14. Bearchell SJ, Fraaije BA, Shaw MW, Fitt BDL (2005) Wheat archive links long-term fungal pathogen population dynamics to air pollution. Proc Natl Acad Sci USA 102:5438–5442
15. Bowers JH, Bailey BA, Hebbar PK, Sanogo S, Lumsden RD (2001) The impact of plant diseases on world chocolate production. Plant Health Prog. 10.1094/PHP-2001-0709-01-RV
16. Brading PA, Verstappen ECP, Kema GHJ, Brown JKM (2002) A gene-for-gene relationship between wheat and Mycosphaerella graminicola, the Septoria tritici blotch pathogen. Phytopathology 92:439–445
17. Brenchley R, Spannagl M, Pfeifer M, Barker GLA, D’Amore R, Allen AM, McKenzie N, Kramer M, Kerhornou A, Bolser D, Kay S, Waite D, Trick M, Bancroft I, Gu Y, Huo N, Luo M-C, Sehgal S, Gill B, Kianian S, Anderson O, Kersey P, Dvorak J, McCombie WR, Hall A, Mayer KFX, Edwards KJ, Bevan MW, Hall N (2012) Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 491:705–710
18. Brown JK, Chartrain L, Lasserre-Zuber P, Saintenac C (2015) Genetics of resistance to Zymoseptoria tritici and applications to wheat breeding. Fungal Genet Biol 79:33–41
19. Chartrain L, Brading PA, Widdowson JP, Brown JKM (2004) Partial resistance to Septoria tritici blotch (Mycosphaerella graminicola) in wheat cultivars Arina and Riband. Phytopathology 94:497–504
20. Chartrain L, Berry S, Brown J (2005a) Resistance of wheat line Kavkaz-K4500 L. 6. A. 4 to Septoria tritici blotch controlled by isolate-specific resistance genes. Phytopathology 95:664–671
21. Chartrain L, Brading PA, Brown JKM (2005b) Presence of the Stb6 gene for resistance to Septoria tritici blotch (Mycosphaerella graminicola) in cultivars used in wheat-breeding programmes worldwide. Plant Pathol 54:134–143
22. Chartrain L, Joaquim P, Berry ST, Arraiano LS, Azanza F, Brown JKM (2005c) Genetics of resistance to Septoria tritici blotch in the Portuguese wheat breeding line TE 9111. Theor Appl Genet 110:1138–1144
23. Chartrain L, Sourdille P, Bernard M, Brown JKM (2009) Identification and location of Stb9, a gene for resistance to Septoria tritici blotch in wheat cultivars Courtot and Tonic. Plant Pathol 58:547–555
24. Chawade A, Sandin M, Teleman J, Malmstrom J, Levander F (2015) Data processing has major impact on the outcome of quantitative label-free LC-MS analysis. J Proteome Res 14:676–687
25. Chawade A, Alexandersson E, Bengtsson T, Andreasson E, Levander F (2016) Targeted proteomics approach for precision plant breeding. J Proteome Res 15:638–646
26. Choulet F, Alberti A, Theil S, Glover N, Barbe V, Daron J, Pingault L, Sourdille P, Couloux A, Paux E, Leroy P, Mangenot S, Guilhot N, Le Gouis J, Balfourier F, Alaux M, Jamilloux V, Poulain J, Durand C, Bellec A, Gaspin C, Safar J, Dolezel J, Rogers J, Vandepoele K, Aury JM, Mayer K, Berges H, Quesneville H, Wincker P, Feuillet C (2014) Structural and functional partitioning of bread wheat chromosome 3B. Science 345:1249721
27. Cook R, Polley R, Thomas M (1991) Disease-induced losses in winter wheat in England and Wales 1985–1989. Crop Prot 10:504–508
28. Cools HJ, Fraaije BA (2008) Are azole fungicides losing ground against Septoria wheat disease? Resistance mechanisms in Mycosphaerella graminicola. Pest Manag Sci 64:681–684
29. Cuthbert RD (2011) Molecular mapping of Septoria tritici blotch resistance in hexaploid wheat (Triticum aestivum L.). University of Manitoba, Winniepeg, Canada
30. Dreisigacker S, Wang X, Cisneros BAM, Jing R, Singh PK (2015) Adult-plant resistance to Septoria tritici blotch in hexaploid spring wheat. Theor Appl Genet 128:2317–2329
31. Dubcovsky J, Dvorak J (2007) Genome plasticity a key factor in the success of polyploid wheat under domestication. Science 316:1862
32. Duveiller E, Singh RP, Nicol JM (2007) The challenges of maintaining wheat productivity: pests, diseases, and potential epidemics. Euphytica 157:417–430
33. Dvorak J, Akhunov E, Akhunov A, Deal K, Luo M (2006) Molecular characterization of a diagnostic DNA marker for domesticated tetraploid wheat provides evidence for gene flow from wild tetraploid wheat to hexaploid wheat. Mol Biol Evol 23:1386
34. Eyal Z (1999) The Septoria tritici and Stagonospora nodorum blotch diseases of wheat. Eur J Plant Pathol 105:629–641
35. Ferjaoui S, M’Barek S, Bahri B, Slimane R, Hamza S (2015) Identification of resistance sources to Septoria tritici blotch in old Tunisian durum wheat germplasm applied for the analysis of Zymoseptoria tritici-durum wheat interaction. J Plant Pathol 97:471–481
36. Fischer RAT, Edmeades GO (2010) Breeding and cereal yield progress. Crop Sci 50:S85–S98
37. Flor H (1971) Current status of the gene-for-gene concept. Annu Rev Phytopathol 9:275–296
38. Fones H, Gurr S (2015) The impact of Septoria tritici Blotch disease on wheat: an EU perspective. Fungal Genet Biol 79:3–7
39. Forrer H, Zadoks J (1983) Yield reduction in wheat in relation to leaf necrosis caused by Septoria tritici. Eur J Plant Pathol 89:87–98
40. Fraaije B, Lucas J, Clark W, Burnett F (2003) QoI resistance development in populations of cereal pathogens in the UK. In: The BCPC International Congress Crop Science or Technology: Proceedings of the international congress held in Glasgow, UK, 10–12 Nov 2003
41. Fraaije BA, Bayon C, Atkins S, Cools HJ, Lucas JA, Fraaije MW (2012) Risk assessment studies on succinate dehydrogenase inhibitors, the new weapons in the battle to control Septoria leaf blotch in wheat. Mol Plant Pathol 13:263–275
42. Ghaffary SMT, Robert O, Laurent V, Lonnet P, Margalé E, van der Lee TA, Visser RG, Kema GH (2011) Genetic analysis of resistance to Septoria tritici blotch in the French winter wheat cultivars Balance and Apache. Theor Appl Genet 123:741–754
43. Ghaffary SMT, Faris JD, Friesen TL, Visser RG, van der Lee TA, Robert O, Kema GH (2012) New broad-spectrum resistance to Septoria tritici blotch derived from synthetic hexaploid wheat. Theor Appl Genet 124:125–142
44. Gooding M (2007) Influence of foliar diseases and their control by fungicides on grain yield and quality in wheat. In: Buck HT, Nisi JE, Salomon N (ed) Wheat production in stressed environments. Springer, Berlin, pp 567–581
45. Goodwin SB (2007) Back to basics and beyond: increasing the level of resistance to Septoria tritici blotch in wheat. Australas Plant Pathol 36:532–538
46. Goodwin S, Thompson I (2011) Development of isogenic lines for resistance to Septoria tritici blotch in wheat. Czech J Genet Plant Breed 47:S98–S101
47. Goodwin SB, M’Barek SB, Dhillon B, Wittenberg AH, Crane CF, Hane JK, Foster AJ, Van der Lee TA, Grimwood J, Aerts A (2011) Finished genome of the fungal wheat pathogen Mycosphaerella graminicola reveals dispensome structure, chromosome plasticity, and stealth pathogenesis. PLoS Genet 7:e1002070
48. Gorash A, Henriksson T, Himanen K, Ingver A, Johansson E, Jørgensen LN, Koppel M, Koppel R, Makela P, Ortiz R, Podyma W, Roitsch T, Ronis A, Svensson JT, Vallenback P, Weih M (2018) A transnational and holistic breeding approach is needed for sustainable wheat production in the Baltic Sea region. Physiol Plant. 10.1111/ppl.12726
49. Gough F, Lee T (1985) Moisture effects on the discharge and survival of conidia of Septoria tritici. Phytopathology 75:180–182
50. Gullino M, Kuijpers L (1994) Social and political implications of managing plant diseases with restricted fungicides in Europe. Annu Rev Phytopathol 32:559–581
51. Hahn M (2014) The rising threat of fungicide resistance in plant pathogenic fungi: Botrytis as a case study. J Chem Biol 7:133–141
52. Hajjar R, Hodgkin T (2007) The use of wild relatives in crop improvement: a survey of developments over the last 20 years. Euphytica 156:1–13
53. Handa H, Namiki N, Xu D, Ban T (2008) Dissecting of the FHB resistance QTL on the short arm of wheat chromosome 2D using a comparative genomic approach: from QTL to candidate gene. Mol Breed 22:71–84
54. Hardwick N, Jones D, Slough J (2001) Factors affecting diseases of winter wheat in England and Wales, 1989–98. Plant Pathol 50:453–462
55. Henze M, Beyer M, Klink H, Verreet JA (2007) Characterizing meteorological scenarios favorable for Septoria tritici infections in wheat and estimation of latent periods. Plant Dis 91:1445–1449
56. INRA-Genoplant (2011) (http://grain.jouy.inra.fr/grain/export/home/infoservices/htdocs/ggpages/SSRclub/GeneticPhysical/textggmsatgpw.html)
57. Jackson L, Dubcovsky J, Gallagher L, Wennig R, Heaton J, Vogt H, Gibbs L, Kirby D, Canevari M, Carlson H (2000) Regional barley and common and durum wheat performance tests in California. Agron Prog Rep 272:1–56
58. Jenkins J, Morgan W (1969) The effect of Septoria diseases on the yield of winter wheat. Plant Pathol 18:152–156
59. Jing HC, Lovell D, Gutteridge R, Jenk D, Kornyukhin D, Mitrofanova OP, Kema GHJ, Hammond-Kosack KE (2008) Phenotypic and genetic analysis of the Triticum monococcum-Mycosphaerella graminicola interaction. New Phytol 179:1121–1132
60. Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329
61. Jorgensen LN (2008) Resistance situation with fungicides in cereals. Zemdirbyste-Agriculture 95:373–378
62. Jørgensen LN, Hovmøller MS, Hansen JG, Lassen P, Clark B, Bayles R, Rodemann B, Flath K, Jahn M, Goral T (2014) IPM strategies and their dilemmas including an introduction to www. eurowheat.org. J Integr Agric 13:265–281
63. Juroszek P, von Tiedemann A (2013) Climate change and potential future risks through wheat diseases: a review. Eur J Plant Pathol 136:21–33
64. Kema GHJ, vanSilfhout CH (1997) Genetic variation for virulence and resistance in the wheat Mycosphaerella graminicola pathosystem. 3. Comparative seedling and adult plant experiments. Phytopathology 87:266–272
65. Kema GHJ, Lange W, Vansilfhout CH (1995) Differential suppression of stripe rust resistance in synthetic wheat hexaploids derived from Triticum-turgidum subsp dicoccoides and Aegilops squarrosa. Phytopathology 85:425–429
66. Kema GHJ, Annone JG, Sayoud R, VanSilfhout CH, VanGinkel M, deBree J (1996a) Genetic variation for virulence and resistance in the wheat-Mycosphaerella graminicola pathosystem. 1. Interactions between pathogen isolates and host cultivars. Phytopathology 86:200–212
67. Kema GHJ, Sayoud R, Annone JG, VanSilfhout CH (1996b) Genetic variation for virulence and resistance in the wheat-Mycosphaerella graminicola pathosystem. 2. Analysis of interactions between pathogen isolates and host cultivars. Phytopathology 86:213–220
68. Kema GHJ, Verstappen ECP, Todorova M, Waalwijk C (1996c) Successful crosses and molecular tetrad and progeny analyses demonstrate heterothallism in Mycosphaerella graminicola. Curr Genet 30:251–258
69. Kema GHJ, Yu DZ, Rijkenberg FHJ, Shaw MW, Baayen RP (1996d) Histology of the pathogenesis of Mycosphaerella graminicola in wheat. Phytopathology 86:777–786
70. Kema G, Verstappen E, Waalwijk C (2000) Avirulence in the wheat Septoria tritici leaf blotch fungus Mycosphaerella graminicola is controlled by a single locus. Mol Plant Microbe Interact 13:1375–1379
71. Keon J, Antoniw J, Carzaniga R, Deller S, Ward JL, Baker JM, Beale MH, Hammond-Kosack K, Rudd JJ (2007) Transcriptional adaptation of Mycosphaerella graminicola to programmed cell death (PCD) of its susceptible wheat host. Mol Plant Microbe Interact 20:178–193
72. King J, Jenkins J, Morgan W (1983) The estimation of yield losses in wheat from severity of infection by Septoria species. Plant Pathol 32:239–249
73. Kohli M, Skovmand B (1997) Wheat varieties of South America: Names, parentage, pedigrees, and origins. Cimmyt, Mexico
74. Korzun V, Röder M, Ganal M, Worland A, Law C (1998) Genetic analysis of the dwarfing gene (Rht8) in wheat. Part I. Molecular mapping of Rht8 on the short arm of chromosome 2D of bread wheat (Triticum aestivum L.). Theor Appl Genet 96:1104–1109
75. Lantican M, Dubin H, Morris M, Heisey P (2005) Impacts of international wheat breeding research in the developing world, 1988–2002. Cimmyt, Mexico
76. Linde CC, Zhan J, McDonald BA (2002) Population structure of Mycosphaerella graminicola: from lesions to continents. Phytopathology 92:946–955
77. Liu Y, Zhang L, Thompson IA, Goodwin SB, Ohm HW (2013) Molecular mapping re-locates the Stb2 gene for resistance to Septoria tritici blotch derived from cultivar Veranopolis on wheat chromosome 1BS. Euphytica 190:145–156
78. Madden L (1987) Potential effects of air pollutants on epidemics of plant diseases. Agric Ecosyst Environ 18:251–262
79. Mayer KFX, Rogers J, el Dole J, Pozniak C, Eversole K, Feuillet C, Gill B, Friebe B, Lukaszewski AJ, Sourdille P, Endo TR, Kubalakova M, Mihalikova J, Dubska Z, Vrana J, Perkova R, Imkova H, Febrer M, Clissold L, McLay K, Singh K, Chhuneja P, Singh NK, Khurana J, Akhunov E, Choulet F, Alberti A, Barbe V, Wincker P, Kanamori H, Kobayashi F, Itoh T, Matsumoto T, Sakai H, Tanaka T, Wu J, Ogihara Y, Handa H, Maclachlan PR, Sharpe A, Klassen D, Edwards D, Batley J, Olsen OA, Sandve SR, Lien S, Steuernagel B, Wulff B, Caccamo M, Ayling S, Ramirez-Gonzalez RH, Clavijo BJ, Wright J, Pfeifer M, Spannagl M, Martis MM, Mascher M, Chapman J, Poland JA, Scholz U, Barry K, Waugh R, Rokhsar DS, Muehlbauer GJ, Stein N, Gundlach H, Zytnicki M, Jamilloux V, Quesneville H, Wicker T, Faccioli P, Colaiacovo M, Stanca AM, Budak H, Cattivelli L, Glover N, Pingault L, Paux E, Sharma S, Appels R, Bellgard M, Chapman B, Nussbaumer T, Bader KC, Rimbert H, Wang S, Knox R, Kilian A, Alaux M, Alfama F, Couderc L, Guilhot N, Viseux C, Loaec M, Keller B, Praud S (2014) A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome. Science 345:1251788
80. McCartney C, Brule-Babel A, Lamari L, Somers D (2003) Chromosomal location of a race-specific resistance gene to Mycosphaerella graminicola in the spring wheat ST6. Theor Appl Genet 107:1181–1186
81. McIntosh R, Wellings C, Park R (1995) Wheat rusts: an atlas of resistance genes. Springer, Netherlands
82. McNeal F, Konzak C, Smith E, Tate W, Russell T (1971) A uniform system for recording and processing cereal research data. US Agric Res Serv 42:31–121
83. Mergoum M, Singh P, Ali S, Elias E, Anderson J, Glover K, Adhikari T (2007) Reaction of elite wheat genotypes from the northern Great Plains of North America to Septoria diseases. Plant Dis 91:1310–1315
84. Morton V, Staub T (2008) A short history of fungicides. APSnet Features
85. Mujeeb-Kazi A, Gilchrist LI, Villareal RL, Delgado R (2000) Registration of 10 wheat germplasms resistant to Septoria tritici leaf blotch. Crop Sci 40:590–591
86. Mujeeb-Kazi A, Fuentes-Davilla G, Gul A, Mirza JI (2006) Karnal bunt resistance in Synthetic Hexaploid wheats (SH) derived from durum wheat x Aegilops tauschii combinations and in some SH x bread wheat derivatives. Cereal Res Commun 34:1199–1205
87. Mujeeb-Kazi A, Gul A, Ahmad I, Farooq M, Rizwan S, Bux H, Iftikhar S, Asad S, Delgado R (2007) Aegilops tauschii, as a spot blotch (Cochliobolus sativus) resistance source for bread wheat improvement. Pak J Bot 39:1207–1216
88. Narvaez I, Caldwell R (1957) Inheritance of resistance to leaf blotch of wheat caused by Septoria tritici. Phytopathology 47:529–530
89. Odilbekov F, Armoniené R, Henriksson T, Chawade A (2018) Proximal phenotyping and machine learning methods to identify septoria tritici blotch disease symptoms in wheat. Front Plant Sci. 10.3389/fpls.2018.00685
90. Oerke E, Dehne H, Schohnbeck F, Weber A (1995) Crop production and crop protection: estimated losses in major food and cash crops. Elsevier, Amsterdam, p 808
91. Ogbonnaya FC, Imtiaz M, Ye G, Hearnden PR, Hernandez E, Eastwood RF, Van Ginkel M, Shorter S, Winchester J (2008) Genetic and QTL analyses of seed dormancy and preharvest sprouting resistance in the wheat germplasm CN10955. Theor Appl Genet 116:891–902
92. Palma-Guerrero J, Ma X, Torriani SFF, Zala M, Francisco CS, Hartmann FE, Croll D, McDonald BA (2017) Comparative transcriptome analyses in Zymoseptoria tritici reveal significant differences in gene expression among strains during plant infection. Mol Plant-Microbe Interact MPMI-07-16-0146
93. Pastircak M (2005) Occurrence of Mycosphaerella graminicola, teleomorph of Septoria tritici, in Slovakia. Phytoparasitica 33:377–379
94. Polley R, Thomas M (1991) Surveys of diseases of winter wheat in England and Wales, 1976–1988. Ann Appl Biol 119:1–20
95. Ponomarenko A, Goodwin SB, Kema GH (2011) Septoria tritici blotch (STB) of wheat. Plant Health Instr. 10.1094/PHI-I-2011-0407-01
96. Prestes A, Hendrix J (1975) Evaluation of wheat response to Septorialeaf blotch//Ann. Wheat Newslett 21:163–164
97. Quaedvlieg W, Kema GHJ, Groenewald JZ, Verkley GJM, Seifbarghi S, Razavi M, Gohari AM, Mehrabi R, Crous PW (2011) Zymoseptoria gen. nov.: a new genus to accommodate Septoria-like species occurring on graminicolous hosts. Persoonia 25:57–69
98. Ragsdale N, Sisler H (1994) Social and political implications of managing plant diseases with decreased availability of fungicides in the United States. Annu Rev Phytopathol 32:545–557
99. Raman R, Milgate A, Imtiaz M, Tan M-K, Raman H, Lisle C, Coombes N, Martin P (2009) Molecular mapping and physical location of major gene conferring seedling resistance to Septoria tritici blotch in wheat. Mol Breed 24:153–164
100. Roder MS, Korzun V, Wendehake K, Plaschke J, Tixier MH, Leroy P, Ganal MW (1998) A microsatellite map of wheat. Genetics 149:2007–2023
101. Roos J, Hopkins R, Kvarnheden A, Dixelius C (2010) The impact of global warming on plant diseases and insect vectors in Sweden. Eur J Plant Pathol 1:9–19
102. Rosenzweig C, Iglesias A, Yang X, Epstein P, Chivian E (2001) Climate change and extreme weather events. Glob Change Hum Health 2:90–104
103. Rudd JJ, Kanyuka K, Hassani-Pak K, Derbyshire M, Andongabo A, Devonshire J, Lysenko A, Saqi M, Desai NM, Powers SJ, Hooper J, Ambroso L, Bharti A, Farmer A, Hammond-Kosack KE, Dietrich RA, Courbot M (2015) Transcriptome and metabolite profiling of the infection cycle of Zymoseptoria tritici on wheat reveals a biphasic interaction with plant immunity involving differential pathogen chromosomal contributions and a variation on the hemibiotrophic lifestyle definition. Plant Physiol 167:1158–1185
104. Saintenac C, Cambon F, Faris JD, Xu S, Marande W, Berges H, Tabib Ghaffary SM, Aouini L, Kema GHJ, Robert O, Langin T (2017) Stb16q-mediated resistance against Zymoseptoria tritici is conferred by a new class of R gene. In: Proceedings 13th international wheat genetics symposium, p 61
105. Sande DN, Mullen JD, Matekole AN (2010) Environmental benefits from reduced pesticide use and returns to research: an application to the US cotton industry. In: 2010 Annual meeting, Feb 6–9, 2010, Orlando, Florida. Southern Agricultural Economics Association
106. Sanderson F (1976) Mycosphaerella graminicola (Fuckel) Sanderson comb. nov., the ascogenous state of Septoria tritici Rob. apud Desm. N Z J Bot 14:359–360
107. Shaw M, Bearchell S, Fitt B, Fraaije B (2008) Long-term relationships between environment and abundance in wheat of Phaeosphaeria nodorum and Mycosphaerella graminicola. New Phytol 177:229–238
108. Shetty NP, Kristensen BK, Newman MA, Moller K, Gregersen PL, Jorgensen HJL (2003) Association of hydrogen peroxide with restriction of Septoria tritici in resistant wheat. Physiol Mol Plant Pathol 62:333–346
109. Shetty NP, Mehrabi R, Lutken H, Haldrup A, Kema GHJ, Collinge DB, Jorgensen HJL (2007) Role of hydrogen peroxide during the interaction between the hemibiotrophic fungal pathogen Septoria tritici and wheat. New Phytol 174:637–647
110. Shetty NP, Jensen JD, Knudsen A, Finnie C, Geshi N, Blennow A, Collinge DB, Jorgensen HJL (2009) Effects of beta-1,3-glucan from Septoria tritici on structural defence responses in wheat. J Exp Bot 60:4287–4300
111. Song QJ, Shi JR, Singh S, Fickus EW, Costa JM, Lewis J, Gill BS, Ward R, Cregan PB (2005) Development and mapping of microsatellite (SSR) markers in wheat. Theor Appl Genet 110:550–560
112. Sprague R (1938) The status of Septoria graminum. Mycologia 30:672–678
113. Stukenbrock EH, McDonald BA (2008) The origins of plant pathogens in agro-ecosystems. Annu Rev Phytopathol 46:75–100
114. te Beest D, Shaw M, Pietravalle S, van den Bosch F (2009) A predictive model for early-warning of Septoria leaf blotch on winter wheat. Eur J Plant Pathol 124:413–425
115. Torriani SFF, Brunner PC, McDonald BA, Sierotzki H (2009) QoI resistance emerged independently at least 4 times in European populations of Mycosphaerella graminicola. Pest Manag Sci 65:155–162
116. Triticartwheatmap (2011). http://www.triticarte.com.au/pdf/WheatDArTmapsVersion1.2.xls. Accessed 1 Feb 2018
117. USDA-Annual wheat news letter volume 53. http://wheat.pw.usda.gov/ggpages/awn/53/Textfile/WGC.html
118. Valkoun J (2001) Wheat pre-breeding using wild progenitors. Wheat in a global environment. Springer, Berlin, pp 699–707
119. van Ginkel M, Ogbonnaya F (2007) Novel genetic diversity from synthetic wheats in breeding cultivars for changing production conditions. Field Crops Res 104:86–94
120. Varshney RK, Langridge P, Graner A (2007) Application of genomics to molecular breeding of wheat and barley. Adv Genet 58:121–155
121. Waalwijk C, Mendes O, Verstappen EC, de Waard MA, Kema GH (2002) Isolation and characterization of the mating-type idiomorphs from the wheat Septoria leaf blotch fungus Mycosphaerella graminicola. Fungal Genet Biol 35:277–286
122. Warburton ML, Crossa J, Franco J, Kazi M, Trethowan R, Rajaram S, Pfeiffer W, Zhang P, Dreisigacker S, van Ginkel M (2006) Bringing wild relatives back into the family: recovering genetic diversity in CIMMYT improved wheat germplasm. Euphytica 149:289–301
123. Ware SB, Verstappen ECP, Breeden J, Cavaletto JR, Goodwin SB, Waalwijk C, Crous PW, Kema GHJ (2007) Discovery of a functional Mycosphaerella teleomorph in the presumed asexual barley pathogen Septoria passerinii. Fungal Genet Biol 44:389–397
124. White FF, Frommer W (2015) Deciphering durable resistance one R gene at a time. Nat Genet 47:1376–1377
125. Wiik L, Rosenqvist H (2010) The economics of fungicide use in winter wheat in southern Sweden. Crop Prot 29:11–19
126. Wilson R (1979) Resistance to Septoria tritici in two wheat cultivars, determined by independent, single dominant genes. Australas Plant Pathol 8:16–18
127. Wilson R (1985) Inheritance of resistance to Septoria tritici in wheat. ARS-US Department of Agriculture, Agricultural Research Service (USA), Stoneville
128. Wittenberg AHJ, van der Lee TAJ, Ben M’Barek S, Ware SB, Goodwin SB, Kilian A, Visser RGF, Kema GHJ, Schouten HJ (2009) Meiosis drives extraordinary genome plasticity in the hexaploid fungal plant pathogen Mycosphaerella graminicola. Plos One 4(6):e5863
129. Yang WY, Liu DC, Li J, Zhang LQ, Wei HT, Hu XR, Zheng YL, He ZH, Zou YC (2009) Synthetic hexaploid wheat and its utilization for wheat genetic improvement in China. J Genet Genomics 36:539–546
130. Yang F, Li W, Derbyshire M, Larsen MR, Rudd JJ, Palmisano G (2015) Unraveling incompatibility between wheat and the fungal pathogen Zymoseptoria tritici through apoplastic proteomics. BMC Genomics 16:362
131. Zhan J, McDonald BA (2011) Thermal adaptation in the fungal pathogen Mycosphaerella graminicola. Mol Ecol 20:1689–1701
132. Zhan J, McDonald BA (2013) Experimental measures of pathogen competition and relative fitness. Annu Rev Phytopathol 51:131–153
133. Zhan J, Mundt CC, McDonald BA (2007) Sexual reproduction facilitates the adaptation of parasites to antagonistic host environments: evidence from empirical study in the wheat-Mycosphaerella graminicola system. Int J Parasitol 37:861–870
134. Zhang XY, Loyce C, Meynard JM, Monod H (2007) Modeling the effect of cultivar resistance on yield losses of winter wheat in natural multiple disease conditions. Eur J Agron 26:384–393
135. Zhang KP, Chen GF, Zhao L, Liu B, Xu XB, Tian JC (2009) Molecular genetic analysis of flour color using a doubled haploid population in bread wheat (Triticum aestivum L.). Euphytica 165:471–484
136. Zhong Z, Marcel TC, Hartmann FE, Ma X, Plissonneau C, Zala M, Ducasse A, Confais J, Compain J, Lapalu N, Amselem J, McDonald BA, Croll D, Palma-Guerrero J (2017) A small secreted protein in Zymoseptoria tritici is responsible for avirulence on wheat cultivars carrying the Stb6 resistance gene. New Phytol 214:619–631