Resistance to Gray Leaf Spot of Maize: Genetic Architecture and Mechanisms Elucidated through Nested Association Mapping and Near-Isogenic Line Analysis

English version České info

Gray leaf spot (GLS), a necrotrophic, foliar fungal disease of maize, contributes to maize yield losses worldwide. We identified and characterized regions of the maize genome that confer resistance to GLS and gained insight into the mechanisms associated with these quantitative trait loci (QTL). We provide evidence for structural and detoxification-related mechanisms underlying quantitative resistance. The distance between major veins of the maize leaf was positively correlated with the quantity of fungal conidiophores (reproductive structures) produced. Four of the GLS QTL were associated with inter-vein distance, and co-localization was confirmed for one of these QTL in near-isogenic lines. In addition, up-regulation of a putative detoxification-related flavin-monooxygenase gene was correlated with a fine-mapped QTL. Plant breeding decisions regarding development and deployment of disease resistance traits can be improved with better understanding of the mechanisms underlying quantitative disease resistance.

Vyšlo v časopise: Resistance to Gray Leaf Spot of Maize: Genetic Architecture and Mechanisms Elucidated through Nested Association Mapping and Near-Isogenic Line Analysis. PLoS Genet 11(3): e32767. doi:10.1371/journal.pgen.1005045
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005045

Souhrn

Zdroje

1. Wen L (2013) Cell death in plant immune response to necrotrophs. J Plant Biochem Physiol 1 : 1–3.

2. Lai Z, Wang F, Zheng Z, Fan B, Chen Z (2011) A critical role of autophagy in plant resistance to necrotrophic fungal pathogens. Plant J 66 : 953–968. doi: 10.1111/j.1365-313X.2011.04553.x 21395886

3. Sivasithamparam K, Barbetti MJ, Li H (2005) Recurring challenges from a necrotrophic fungal plant pathogen: a case study with Leptosphaeria maculans (causal agent of blackleg disease in Brassicas) in Western Australia. Ann Bot 96 : 363–377. 15994842

4. Crous PW, Groenewald JZ, Groenewald M, Caldwell P, Braun U, et al. (2006) Species of Cercospora associated with grey leaf spot of maize. Stud Mycol: 189–197.

5. Tehon L, Daniels E (1925) Notes on parasitic fungi of Illinois. Mycologia 71 : 240–249.

6. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43 : 205–227. 16078883

7. Ward JMJ, Stromberg EL, Nowell DC, Nutter FW (1999) Gray leaf spot—A disease of global importance in maize production. Plant Dis 83 : 884–895.

8. Latterell FM, Rossi AE (1983) Gray leaf spot of corn: A disease on the move. Plant Dis 67.

9. Ngoko Z, Cardwell KF, Marasas WFO, Wingfield MJ, Ndemah R, et al. (2002) Biological and physical constraints on maize production in the Humid Forest and Western Highlands of Cameroon. Eur J Plant Pathol 108 : 893–902.

10. Balint-Kurti PJ, Wisser R, Zwonitzer JC (2008) Use of an advanced intercross line population for precise mapping of quantitative trait loci for gray leaf spot resistance in maize. Crop Sci 48 : 1696–1704.

11. Bubeck DM, Goodman MM, Beavis WD, Grant D (1993) Quantitative trait loci controlling resistance to gray leaf spot in maize. Crop Sci 33 : 838–847.

12. Clements MJ, Dudley JW, White DG (2000) Quantitative trait loci associated with resistance to gray leaf spot of corn. Phytopathology 90 : 1018–1025. doi: 10.1094/PHYTO.2000.90.9.1018 18944528

13. Danson J, Lagat M, Kimani M, Kuria A (2008) Quantitative trait loci (QTLs) for resistance to gray leaf spot and common rust diseases of maize. Afr J Biotechnol 7 : 3247–3254.

14. Juliatti FC, Pedrosa MG, Silva HD, da Silva JVC (2009) Genetic mapping for resistance to gray leaf spot in maize. Euphytica 169 : 227–238.

15. Lehmensiek A, Esterhuizen AM, van Staden D, Nelson SW, Retief AE (2001) Genetic mapping of gray leaf spot (GLS) resistance genes in maize. Theor Appl Genet 103 : 797–803.

16. Maroof MAS, Yue YG, Xiang ZX, Stromberg EL, Rufener GK (1996) Identification of quantitative trait loci controlling resistance to gray leaf spot disease in maize. Theor Appl Genet 93 : 539–546. doi: 10.1007/BF00417945 24162345

17. Pozar G, Butruille D, Silva HD, McCuddin ZP, Penna JCV (2009) Mapping and validation of quantitative trait loci for resistance to Cercospora zeae-maydis infection in tropical maize (Zea mays L.). Theor Appl Genet 118 : 553–564. doi: 10.1007/s00122-008-0920-2 18989654

18. Gordon SG, Bartsch M, Matthies I, Gevers HO, Lipps PE, et al. (2004) Linkage of molecular markers to Cercospora zeae-maydis resistance in maize. Crop Sci 44 : 628–636.

19. Zhang Y, Xu L, Fan X, Tan J, Chen W, et al. (2012) QTL mapping of resistance to gray leaf spot in maize. Theor Appl Genet: 1–12.

20. Berger DK, Carstens M, Korsman JN, Middleton F, Kloppers FJ, et al. (2014) Mapping QTL conferring resistance in maize to gray leaf spot disease caused by Cercospora zeina. BMC genetics 15 : 60. doi: 10.1186/1471-2156-15-60 24885661

21. Chung CL, Poland J, Kump K, Benson J, Longfellow J, et al. (2011) Targeted discovery of quantitative trait loci for resistance to northern leaf blight and other diseases of maize. Theor Appl Genet 123 : 307–326. doi: 10.1007/s00122-011-1585-9 21526397

22. Zwonitzer JC, Coles ND, Krakowsky MD, Arellano C, Holland JB, et al. (2010) Mapping resistance quantitative trait Loci for three foliar diseases in a maize recombinant inbred line population-evidence for multiple disease resistance? Phytopathology 100 : 72–79. doi: 10.1094/PHYTO-100-1-0072 19968551

23. McMullen MD, Kresovich S, Villeda HS, Bradbury P, Li H, et al. (2009) Genetic properties of the maize nested association mapping population. Science 325 : 737–740. doi: 10.1126/science.1174320 19661427

24. Berger R (1977) Application of epidemiological principles to achieve plant disease control. Annu Rev Phytopathol 15 : 165–181.

25. Chung CL, Longfellow JM, Walsh EK, Kerdieh Z, Van Esbroeck G, et al. (2010) Resistance loci affecting distinct stages of fungal pathogenesis: use of introgression lines for QTL mapping and characterization in the maize-Setosphaeria turcica pathosystem. BMC plant biology 10 : 103. doi: 10.1186/1471-2229-10-103 20529319

26. 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. doi: 10.1016/j.tplants.2008.10.006 19062327

27. Fu D, Uauy C, Distelfeld A, Blechl A, Epstein L, et al. (2009) A kinase-START gene confers temperature-dependent resistance to wheat stripe rust. Science 323 : 1357–1360. doi: 10.1126/science.1166289 19228999

28. Fukuoka S, Saka N, Koga H, Ono K, Shimizu T, et al. (2009) Loss of function of a proline-containing protein confers durable disease resistance in rice. Science 325 : 998–1001. doi: 10.1126/science.1175550 19696351

29. Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, et al. (2009) A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323 : 1360–1363. doi: 10.1126/science.1166453 19229000

30. Manosalva PM, Davidson RM, Liu B, Zhu X, Hulbert SH, et al. (2009) A germin-like protein gene family functions as a complex quantitative trait locus conferring broad-spectrum disease resistance in rice. Plant Physiol 149 : 286–296. doi: 10.1104/pp.108.128348 19011003

31. Cook DE, Lee TG, Guo X, Melito S, Wang K, et al. (2012) Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science 338 : 1206–1209. doi: 10.1126/science.1228746 23065905

32. St. Clair DA(2010) Quantitative disease resistance and quantitative resistance loci in breeding. Annu Rev Phytopathol 48 : 247–268. doi: 10.1146/annurev-phyto-080508-081904 19400646

33. Kimura M, Anzai H, Yamaguchi I (2001) Microbial toxins in plant-pathogen interactions: Biosynthesis, resistance mechanisms, and significance. J Gen Appl Microbiol 47 : 149–160. 12483615

34. Daub M (1982) Cercosporin, a photosensitizing toxin from Cercospora species. Phytopathology 72 : 370–374.

35. Ramel F, Birtic S, Cuiné S, Triantaphylidès C, Ravanat JL, et al. (2012) Chemical quenching of singlet oxygen by carotenoids in plants. Plant Physiol 158 : 1267–1278. doi: 10.1104/pp.111.182394 22234998

36. Daub ME, Payne GA (1989) The role of carotenoids in resistance of fungi to cercosporin. Phytopathology 79 : 180–185.

37. Daub ME, Leisman GB, Clark RA, Bowden EF (1992) Reductive detoxification as a mechanism of fungal resistance to singlet oxygen-generating photosensitizers. Proc Natl Acad Sci 89 : 9588–9592. 1409670

38. Daub ME (1987) The fungal photosensitizer cercosporin and its role in plant disease. In: Heitz JR, Downum KR, editors. Light-activated pesticides. Washington, DC: ACS Symposium Series, American Chemical Society. pp. 271–280.

39. Ververidis P, Davrazou F, Diallinas G, Georgakopoulos D, Kanellis A, et al. (2001) A novel putative reductase (Cpd1p) and the multidrug exporter Snq2p are involved in resistance to cercosporin and other singlet oxygen-generating photosensitizers in Saccharomyces cerevisiae. Curr Genet 39 : 127–136. 11409174

40. Poland JA, Bradbury PJ, Buckler ES, Nelson RJ (2011) Genome-wide nested association mapping of quantitative resistance to northern leaf blight in maize. Proc Natl Acad Sci 108 : 6893. doi: 10.1073/pnas.1010894108 21482771

41. Wisser RJ, Balint-Kurti PJ, Nelson RJ (2006) The genetic architecture of disease resistance in maize: a synthesis of published studies. Phytopathology 96 : 120–129. doi: 10.1094/PHYTO-96-0120 18943914

42. Berger R, Filho AB, Amorim L (1997) Lesion expansion as an epidemic component. Phytopathology 87 : 1005–1013. doi: 10.1094/PHYTO.1997.87.10.1005 18945033

43. Hung H, Browne C, Guill K, Coles N, Eller M, et al. (2012) The relationship between parental genetic or phenotypic divergence and progeny variation in the maize nested association mapping population. Heredity 108 : 490–499. doi: 10.1038/hdy.2011.103 22027895

44. Tuinstra M, Ejeta G, Goldsbrough P (1997) Heterogeneous inbred family (HIF) analysis: a method for developing near-isogenic lines that differ at quantitative trait loci. Theor Appl Genet 95 : 1005–1011.

45. Buckler ES, Holland JB, Bradbury PJ, Acharya CB, Brown PJ, et al. (2009) The genetic architecture of maize flowering time. Science 325 : 714–718. doi: 10.1126/science.1174276 19661422

46. Kump KL, Bradbury PJ, Wisser RJ, Buckler ES, Belcher AR, et al. (2011) Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population. Nature Genet 43 : 163–168. doi: 10.1038/ng.747 21217757

47. Tong AHY, Lesage G, Bader GD, Ding H, Xu H, et al. (2004) Global mapping of the yeast genetic interaction network. Sci STKE 303 : 808. 14764870

48. Byrne AB, Weirauch MT, Wong V, Koeva M, Dixon SJ, et al. (2007) A global analysis of genetic interactions in Caenorhabditis elegans. J Biol 6. doi: 10.1186/jbiol60 18177504

49. Tian F, Bradbury PJ, Brown PJ, Hung H, Sun Q, et al. (2011) Genome-wide association study of leaf architecture in the maize nested association mapping population. Nature Genet 43 : 159–162. doi: 10.1038/ng.746 21217756

50. Studer AJ, Doebley JF (2011) Do large effect QTL fractionate? A case study at the maize domestication QTL teosinte branched1. Genetics 188 : 673–681. doi: 10.1534/genetics.111.126508 21515578

51. Johnson EB, Haggard JE, Clair DAS (2012) Fractionation, stability, and isolate-specificity of QTL for resistance to Phytophthora infestans in cultivated tomato (Solanum lycopersicum). G3 (Bethesda) 2 : 1145–1159. doi: 10.1534/g3.112.003459 23050225

52. Jamann TM, Poland JA, Kolkman JM, Smith LG, Nelson RJ (2014) Unraveling genomic complexity at a quantitative disease resistance locus in maize. Genetics: In press.

53. Hansen BG, Kliebenstein DJ, Halkier BA (2007) Identification of a Flavin-monooxygenase as the S-oxygenating enzyme in aliphatic glucosinolate biosynthesis in Arabidopsis. Plant J 50 : 902–910. 17461789

54. Li J, Hansen BG, Ober JA, Kliebenstein DJ, Halkier BA (2008) Subclade of flavin-monooxygenases involved in aliphatic glucosinolate biosynthesis. Plant Physiol 148 : 1721–1733. doi: 10.1104/pp.108.125757 18799661

55. Mithen R (1992) Leaf glucosinolate profiles and their relationship to pest and disease resistance in oilseed rape. Euphytica 63 : 71–83.

56. Mishina TE, Zeier J (2006) The Arabidopsis flavin-dependent monooxygenase FMO1 is an essential component of biologically induced systemic acquired resistance. Plant Physiol 141 : 1666–1675. 16778014

57. Taylor TV, Mitchell TK, Daub ME (2006) An oxidoreductase is involved in cercosporin degradation by the bacterium Xanthomonas campestris pv. zinniae. Appl Environ Microbiol 72 : 6070–6078. 16957231

58. Wisser RJ, Kolkman JM, Patzoldt ME, Holland JB, Yu J, et al. (2011) Multivariate analysis of maize disease resistances suggests a pleiotropic genetic basis and implicates a GST gene. Proc Natl Acad Sci 108 : 7339–7344. doi: 10.1073/pnas.1011739108 21490302

59. Yu J, Holland JB, McMullen MD, Buckler ES (2008) Genetic design and statistical power of nested association mapping in maize. Genetics 178 : 539–551. doi: 10.1534/genetics.107.074245 18202393

60. Hsieh L-S (2011) Coexistence of sibling species of Cercospora causing gray leaf spot on maize in southern New York State [Master's]. Ithaca, NY: Cornell University. 90 p.

61. Batchvarova R, Reddy V, Bennett J (1992) Cellular resistance in rice to cercosporin, a toxin of Cercospora. Phytopathology 82 : 642–646.

62. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3 : 1101–1108. 18546601

63. Shi L-Y, Li X-H, Hao Z-F, Xie C-X, Ji H-L, et al. (2007) Comparative QTL mapping of resistance to gray leaf spot in maize based on bioinformatics. Agric Sci China 6 : 1411–1419.