A Genome-Wide Association Study of the Maize Hypersensitive Defense Response Identifies Genes That Cluster in Related Pathways


The hypersensitive pathogen defense response (HR) in plants typically consists of a rapid, localized cell death around the point of attempted pathogen penetration. It is found in all plant species and is associated with high levels of resistance to a wide range of pathogens and pests including bacteria, fungi, viruses, nematodes, parasitic plants and insects. Little is known about the control of HR after initiation, largely because it is so rapid and localized and therefore difficult to quantify. Here we use a mutant maize gene conferring an exaggerated HR to quantify HR levels in a set of 3,381 mapping lines characterised at 26.5 million loci to identify genes associated with naturally-occurring variation in HR. Many of these genes seem to be involved in a set of connected regulatory pathways including protein degradation, control of programmed cell death, recycling of cellular components and regulation of oxidative stress. We have also shown that several of these genes show high levels of expression induction during HR. The study provides the first comprehensive list of natural variants in maize genes that modulate HR and cluster within reported pathways underlying molecular events during HR.


Vyšlo v časopise: A Genome-Wide Association Study of the Maize Hypersensitive Defense Response Identifies Genes That Cluster in Related Pathways. PLoS Genet 10(8): e32767. doi:10.1371/journal.pgen.1004562
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pgen.1004562

Souhrn

The hypersensitive pathogen defense response (HR) in plants typically consists of a rapid, localized cell death around the point of attempted pathogen penetration. It is found in all plant species and is associated with high levels of resistance to a wide range of pathogens and pests including bacteria, fungi, viruses, nematodes, parasitic plants and insects. Little is known about the control of HR after initiation, largely because it is so rapid and localized and therefore difficult to quantify. Here we use a mutant maize gene conferring an exaggerated HR to quantify HR levels in a set of 3,381 mapping lines characterised at 26.5 million loci to identify genes associated with naturally-occurring variation in HR. Many of these genes seem to be involved in a set of connected regulatory pathways including protein degradation, control of programmed cell death, recycling of cellular components and regulation of oxidative stress. We have also shown that several of these genes show high levels of expression induction during HR. The study provides the first comprehensive list of natural variants in maize genes that modulate HR and cluster within reported pathways underlying molecular events during HR.


Zdroje

1. VauxDL, KorsmeyerSJ (1999) Cell death in development. Cell 96: 245–254.

2. CohenJJ, DukeRC, FadokVA, SellinsKS (1992) Apoptosis and programmed cell death in immunity. Ann Rev Immunol 10: 267–293.

3. KroemerG, GalluzziL, VandenabeeleP, AbramsJ, AlnemriES, et al. (2008) Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death & Differen 16: 3–11.

4. GalluzziL, MorselliE, VicencioJM, KeppO, JozaN, et al. (2008) Life, death and burial: multifaceted impact of autophagy. Biochem Soc Trans 36: 786–790.

5. KuriyamaH, FukudaH (2002) Developmental programmed cell death in plants. Curr Opin Plant Biol 5: 568–573.

6. Van DoornW, BeersE, DanglJ, Franklin-TongV, GalloisP, et al. (2011) Morphological classification of plant cell deaths. Cell Death & Differen 18: 1241–1246.

7. WuJ, BaldwinIT (2010) New insights into plant responses to the attack from insect herbivores. Ann Rev Genet 44: 1–24.

8. CollNS, EppleP, DanglJL (2011) Programmed cell death in the plant immune system. Cell Death Differ 18: 1247–1256.

9. Hammond-KosackKE, JonesJ (1996) Resistance gene-dependent plant defense responses. Plant Cell 8: 1773–1791.

10. BentAF, MackeyD (2007) Elicitors, effectors, and R Genes: The new paradigm and a lifetime supply of questions. Anne Rev Phytopath 45: 399–436.

11. JohalGS (2007) Disease lesion mimic mutants of maize. American Phytopath. Soc Feature Story http://www.apsnet.org/online/feature/mimics/.

12. Walbot V, Hoisington D, Neuffer MG (1983) Disease lesion mimic mutations. In: Kosuge T, Meredith CP, Hollaender A, editors. Genetic Engineering of Plants. New York: Plenum Press. pp. 431–432.

13. LorrainS, VailleauF, BalagueC, RobyD (2003) Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends Plant Sci 8: 263–271.

14. WolterM, HollricherK, SalaminiF, Schulze-LefertP (1993) The mlo resistance alleles to powdery mildew infection in barley trigger a developmentally controlled defence mimic phenotype. Mol Gen Genet 239: 122–128.

15. YinZ, ChenJ, ZengL, GohM, LeungH, et al. (2000) Characterizing rice lesion mimic mutants and identifying a mutant with broad-spectrum resistance to rice blast and bacterial blight. Mol Plant Microbe Interact 13: 869–876.

16. NeufferMG, CalvertOH (1975) Dominant disease lesion mimics in maize. J Heredit 66: 265–270.

17. GrayJ, ClosePS, BriggsSP, JohalGS (1997) A novel suppressor of cell death in plants encoded by the Lls1 gene of maize. Cell 89: 25–31.

18. MachJM, CastilloAR, HoogstratenR, GreenbergJT (2001) The Arabidopsis-accelerated cell death gene ACD2 encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms. Proc Nat Acad Sci 98: 771–776.

19. HulbertSH (1997) Structure and evolution of the Rp1 complex conferring rust resistance in maize. Ann Rev Phytopath 35: 293–310.

20. SudupakMA, BennetzenJL, HulbertSH (1993) Unequal exchange and meiotic instability of disease-resistance genes in the Rp1 region of maize. Genetics 133: 119–125.

21. SmithS, SteinauM, TrickH, HulbertS (2010) Recombinant Rp1 genes confer necrotic or nonspecific resistance phenotypes. Mol Genet Genomics 283: 591–602.

22. CollinsN, DrakeJ, AyliffeM, SunQ, EllisJ, et al. (1999) Molecular characterization of the maize Rp1-D rust resistance haplotype and its mutants. Plant Cell 11: 1365–1376.

23. ChintamananiS, HulbertSH, JohalGS, Balint-KurtiPJ (2010) Identification of a maize locus that modulates the hypersensitive defense response, using mutant-assisted gene identification and characterization. Genetics 184: 813–825.

24. ChaikamV, NegeriA, DhawanR, PuchakaB, JiJ, et al. (2011) Use of mutant-assisted gene identification and characterization (MAGIC) to identify novel genetic loci that modify the maize hypersensitive response. Theor Appl Genet 123: 985–997.

25. NegeriA, WangG-F, BenaventeL, KibitiC, ChaikamV, et al. (2013) Characterization of temperature and light effects on the defense response phenotypes associated with the maize Rp1-D21 autoactive resistance gene. BMC Plant Biol 13: 106.

26. HuG, RichterTE, HulbertSH, PryorT (1996) Disease lesion mimicry caused by mutations in the rust resistance gene Rp1. Plant Cell 8: 1367–1376.

27. OlukoluBA, NegeriA, DhawanR, VenkataBP, SharmaP, et al. (2013) A connected set of genes associated with programmed cell death implicated in controlling the hypersensitive response in maize. Genetics 193: 609–620.

28. ChengC, GaoX, FengB, SheenJ, ShanL, et al. (2013) Plant immune response to pathogens differs with changing temperatures. Nat Commun 4: 2530.

29. ZhuY, QianW, HuaJ (2010) Temperature Modulates Plant Defense Responses through NB-LRR Proteins. PLoS Pathog 6: e1000844.

30. AlcázarR, ParkerJE (2011) The impact of temperature on balancing immune responsiveness and growth in Arabidopsis. Trends Plant Sci 16: 666–675.

31. JohalGS, Balint-KurtiP, WellCF (2008) Mining and harnessing natural variation: A little magic. Crop Sci 48: 2066–2073.

32. McMullenMD, KresovichS, VilledaHS, BradburyP, LiHH, et al. (2009) Genetic properties of the maize nested association mapping population. Science 325: 737–740.

33. Benson J (2013) Resistance to gray leaf spot of maize: underlying genetic architecture and associated mechanisms. Thesis. Cornell University.

34. KumpKL, BradburyPJ, WisserRJ, BucklerES, BelcherAR, et al. (2011) Genome-wide association study of quantitative resistance to southern leaf blight in the maize nested association mapping population. Nat Genet 43: 163–168.

35. PolandJA, BradburyPJ, BucklerES, NelsonRJ (2011) Genome-wide nested association mapping of quantitative resistance to northern leaf blight in maize. Proc Nat Acad Sci 108: 6893–6898.

36. Balint-KurtiPJ, JohalGS (2011) Use of mutant-assisted gene identification and characterization (magic) to identify useful alleles for crop improvement. ISB News Reports January 2011: 1–3.

37. PenningBW, JohalGS, McMullenMM (2004) A major suppressor of cell death, slm1, modifies the expression of the maize (Zea mays L.) lesion mimic mutation les23. Genome 47: 961–969.

38. OliverRP, IpchoSVS (2004) Arabidopsis pathology breathes new life into the necrotrophs-vs.-biotrophs classification of fungal pathogens. Mol Plant Pathol 5: 347–352.

39. JenningsP, UllstrupAJ (1957) A histological study of three Helminthosporium leaf blights on corn. Phytopath 47: 707–714.

40. OhmRA, FeauN, HenrissatB, SchochCL, HorwitzBA, et al. (2012) Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen Dothideomycete fungi. PLoS Pathog 8: e1003037.

41. NagyED, BennetzenJL (2008) Pathogen corruption and site-directed recombination at a plant disease resistance gene cluster. Genome Res 18: 1918–1923.

42. FarisJD, ZhangZ, LuH, LuS, ReddyL, et al. (2010) A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proc Nat Acad Sci 107: 13544–13549.

43. MengisteT (2012) Plant immunity to necrotrophs. Ann Rev Phytopathol 50: 267–294.

44. MackayTF (2013) Epistasis and quantitative traits: using model organisms to study gene-gene interactions. Nature Rev Genet 15: 22–33.

45. WallaceJ, LarssonS, BucklerE (2014) Entering the second century of maize quantitative genetics. Heredity 112: 30–38.

46. TianF, BradburyPJ, BrownPJ, HungH, SunQ, et al. (2011) Genome-wide association study of leaf architecture in the maize nested association mapping population. Nat Genet 43: 159–162.

47. BucklerES, HollandJB, BradburyPJ, AcharyaCB, BrownPJ, et al. (2009) The genetic architecture of maize flowering time. Science 325: 714–718.

48. PhillipsPC (2008) Epistasis—the essential role of gene interactions in the structure and evolution of genetic systems. Nature Reviews Genetics 9: 855–867.

49. YuJ, HollandJB, McMullenMD, BucklerES (2008) Genetic design and statistical power of nested association mapping in maize. Genetics 178: 539–551.

50. CookJP, McMullenMD, HollandJB, TianF, BradburyP, et al. (2012) Genetic architecture of maize kernel composition in the nested association mapping and inbred association panels. Plant Physiol 158: 824–834.

51. TianF, BradburyPJ, BrownPJ, HungH, SunQ, et al. (2011) Genome-wide association study of leaf architecture in the maize nested association mapping population. Nat Genet 43: 159–162.

52. HungH-Y, ShannonL, TianF, BradburyP, ChenC, et al. (2012) ZmCCT and the genetic basis of day-length adaptation underlying the postdomestication spread of maize. Proc Natl Acad Sci USA 109: 1913–1921.

53. LaiJ, LiY, MessingJ, DoonerHK (2005) Gene movement by Helitron transposons contributes to the haplotype variability of maize. Proc Nat Acad Sci 102: 9068–9073.

54. ZhengP, AllenWB, RoeslerK, WilliamsME, ZhangS, et al. (2008) A phenylalanine in DGAT is a key determinant of oil content and composition in maize. Nat Genet 40: 367–372.

55. SalviS, SponzaG, MorganteM, TomesD, NiuX, et al. (2007) Conserved noncoding genomic sequences associated with a flowering-time quantitative trait locus in maize. Proc Natl Acad Sci 104: 11376–11381.

56. BucklerES, HollandJB, BradburyPJ, AcharyaCB, BrownPJ, et al. (2009) The genetic architecture of maize flowering time. Science 325: 714–718.

57. ChiaJM, SongC, BradburyPJ, CostichD, de LeonN, et al. (2012) Maize HapMap2 identifies extant variation from a genome in flux. Nat Genet 44: 803–807.

58. Flint-GarciaSA, ThuilletAC, YuJM, PressoirG, RomeroSM, et al. (2005) Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J 44: 1054–1064.

59. RomayM, MillardM, GlaubitzJ, PeifferJ, SwartsK, et al. (2013) Comprehensive genotyping of the USA national maize inbred seed bank. Genome Biol 14: R55.

60. MoerschbacherBM, NollU, GorrichonL, ReisenerH-J (1990) Specific inhibition of lignification breaks hypersensitive resistance of wheat to stem rust. Plant Physiol 93: 465–470.

61. BhuiyanNH, SelvarajG, WeiY, KingJ (2009) Role of lignification in plant defense. Plant Sig Behavior 4: 158–159.

62. MohrPG, CahillDM (2001) Relative roles of glyceollin, lignin and the hypersensitive response and the influence of ABA in compatible and incompatible interactions of soybeans with Phytophthora sojae. Physiol Mol Plant Pathol 58: 31–41.

63. BoerjanW, RalphJ, BaucherM (2003) Lignin biosynthesis. Ann Rev Plant Biol 54: 519–546.

64. HofiusD, MunchD, BressendorffS, MundyJ, PetersenM (2011) Role of autophagy in disease resistance and hypersensitive response-associated cell death. Cell Death Differ 18: 1257–1262.

65. LiuY, SchiffM, CzymmekK, TalloczyZ, LevineB, et al. (2005) Autophagy regulates programmed cell death during the plant innate immune response. Cell 121: 567–577.

66. PatelS, Dinesh-KumarSP (2008) Arabidopsis ATG6 is required to limit the pathogen-associated cell death response. Autophagy 4: 20–27.

67. CodognoP, MeijerAJ (2005) Autophagy and signaling: their role in cell survival and cell death. Cell Death Differ 12 (Suppl 2) 1509–1518.

68. LaiZ, WangF, ZhengZ, FanB, ChenZ (2011) A critical role of autophagy in plant resistance to necrotrophic fungal pathogens. Plant J 66: 953–968.

69. LenzHD, HallerE, MelzerE, KoberK, WursterK, et al. (2011) Autophagy differentially controls plant basal immunity to biotrophic and necrotrophic pathogens. Plant J 66: 818–830.

70. HofiusD, Schultz-LarsenT, JoensenJ, TsitsigiannisDI, PetersenNHT, et al. (2009) Autophagic Components Contribute to Hypersensitive Cell Death in Arabidopsis. Cell 137: 773–783.

71. LevineB, YuanJ (2005) Autophagy in cell death: an innocent convict? The Journal of Clinical Investigation 115: 2679–2688.

72. SpitzerC, SchellmannS, SabovljevicA, ShahriariM, KeshavaiahC, et al. (2006) The Arabidopsis elch mutant reveals functions of an ESCRT component in cytokinesis. Development 133: 4679–4689.

73. BacheKG, SlagsvoldT, CabezasA, RosendalKR, RaiborgC, et al. (2004) The growth-regulatory protein HCRP1/hVps37A is a subunit of mammalian ESCRT-I and mediates receptor down-regulation. Mol. Biol. Cell 15: 4337–4346.

74. BenbrookDM, LongA (2012) Integration of autophagy, proteasomal degradation, unfolded protein response and apoptosis. Exp Oncol 34: 286–297.

75. WrightonKH (2011) Autophagy: ESCRTing proteins for microautophagy. Nat Rev Mol Cell Biol 12: 136–137.

76. ZengLR, QuS, BordeosA, YangC, BaraoidanM, et al. (2004) Spotted leaf11, a negative regulator of plant cell death and defense, encodes a U-box/armadillo repeat protein endowed with E3 ubiquitin ligase activity. Plant Cell 16: 2795–2808.

77. BouchezO, HuardC, LorrainS, RobyD, BalagueC (2007) Ethylene is one of the key elements for cell death and defense response control in the Arabidopsis lesion mimic mutant vad1. Plant Physiol 145: 465–477.

78. EitasTK, DanglJL (2010) NB-LRR proteins: pairs, pieces, perception, partners, and pathways. Current Opinion in Plant Biol 13: 472–477.

79. WilliamsSJ, SohnKH, WanL, BernouxM, SarrisPF, et al. (2014) Structural basis for assembly and function of a heterodimeric plant immune receptor. Science 344: 299–303.

80. BonardiV, CherkisK, NishimuraMT, DanglJL (2012) A new eye on NLR proteins: focused on clarity or diffused by complexity? Curr Opin Immunol 24: 41–50.

81. HwangIS, HwangBK (2011) The pepper mannose-binding lectin gene CaMBL1 is required to regulate cell death and defense responses to microbial pathogens. Plant Physiol 155: 447–463.

82. MaccarroneM, MelinoG, Finazzi-AgroA (2001) Lipoxygenases and their involvement in programmed cell death. Cell Death Differ 8: 776–784.

83. CacasJ-L, VailleauF, DavoineC, EnnarN, AgnelJ-P, et al. (2005) The combined action of 9 lipoxygenase and galactolipase is sufficient to bring about programmed cell death during tobacco hypersensitive response. Plant, Cell & Environ 28: 1367–1378.

84. GaoX, ShimWB, GobelC, KunzeS, FeussnerI, et al. (2007) Disruption of a maize 9-lipoxygenase results in increased resistance to fungal pathogens and reduced levels of contamination with mycotoxin fumonisin. Mol Plant Microbe Interact 20: 922–933.

85. MarinoD, PeetersN, RivasS (2012) Ubiquitination during plant immune signaling. Plant Physiol 160: 15–27.

86. ChengYT, LiY, HuangS, HuangY, DongX, et al. (2011) Stability of plant immune-receptor resistance proteins is controlled by SKP1-CULLIN1-F-box (SCF)-mediated protein degradation. Proc Nat Acad Sci 108: 14694–14699.

87. GrantM, BrownI, AdamsS, KnightM, AinslieA, et al. (2000) The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death. Plant J 23: 441–450.

88. LecourieuxD, MazarsC, PaulyN, RanjevaR, PuginA (2002) Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells. Plant Cell 14: 2627–2641.

89. XuH, HeathMC (1998) Role of calcium in signal transduction during the hypersensitive response caused by basidiospore-derived infection of the cowpea rust fungus. Plant Cell 10: 585–597.

90. LevineA, PennellRI, AlvarezME, PalmerR, LambC (1996) Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Curr Biol 6: 427–437.

91. AliR, MaW, Lemtiri-ChliehF, TsaltasD, LengQ, et al. (2007) Death don't have no mercy and neither does calcium: Arabidopsis CYCLIC NUCLEOTIDE GATED CHANNEL2 and innate immunity. Plant Cell 19: 1081–1095.

92. LambC, DixonRA (1997) The oxidative burst in plant disease resistance. Ann. Rev. Plant Physiol. Plant Mol Biol 48: 251–275.

93. DokeN, OhashiY (1988) Involvement of an O2− generating system in the induction of necrotic lesions on tobacco leaves infected with tobacco mosaic virus. Physiol Mol Plant Pathol 32: 163–175.

94. MurraySL, AdamsN, KliebensteinDJ, LoakeGJ, DenbyKJ (2005) A constitutive PR-1::luciferase expression screen identifies Arabidopsis mutants with differential disease resistance to both biotrophic and necrotrophic pathogens. Mol Plant Pathol 6: 31–41.

95. EtaloDW, StulemeijerIJE, Peter van EsseH, de VosRCH, BouwmeesterHJ, et al. (2013) System-Wide Hypersensitive Response-Associated Transcriptome and Metabolome Reprogramming in Tomato. Plant Physiology 162: 1599–1617.

96. LeeM, SharopovaN, BeavisWD, GrantD, KattM, et al. (2002) Expanding the genetic map of maize with the intermated B73×Mo17 (IBM) population. Plant Mol Biol 48: 453–461.

97. BloomJC, HollandJB (2012) Genomic localization of the maize cross-incompatibility gene, gametophyte factor 1 (ga1). Maydica 56: 1782.

98. ShanerG, FinneyPE (1977) The effect of nitrogen fertilizer on expression of slow mildewing resistance in Knox wheat. Phytopathol 67: 1051–1056.

99. SAS (2004) Help and Documentation. Cary, NC: SAS Institute.

100. Littell RC, Milliken GA, Stroup WA, Wolfinger RD, Schabenberger O (2006) SAS System for mixed models. Cary, NC: SAS institute.

101. ElshireRJ, GlaubitzJC, SunQ, PolandJA, KawamotoK, et al. (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6: e19379.

102. Silva LdaC, WangS, ZengZB (2012) Composite interval mapping and multiple interval mapping: procedures and guidelines for using Windows QTL Cartographer. Methods Mol Biol 871: 75–119.

103. VoorripsRE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93: 77–78.

104. HollandJ (1998) EPISTACY: A SAS Program for detecting two-locus epistatic interactions using genetic marker information. Heredity 89: 374–375.

105. ValdarW, HolmesCC, MottR, FlintJ (2009) Mapping in structured populations by resample model averaging. Genetics 182: 1263–1277.

106. PanagiotouOA, IoannidisJP (2012) What should the genome-wide significance threshold be? Empirical replication of borderline genetic associations. Int J Epidemiol 41: 273–286.

107. AndorfCM, LawrenceCJ, HarperLC, SchaefferML, CampbellDA, et al. (2010) The Locus lookup tool at MaizeGDB: Identification of genomic regions in maize by integrating sequence information with physical and genetic maps. Bioinformatics 26: 434–436.

108. SchnablePS, WareD, FultonRS, SteinJC, WeiF, et al. (2009) The B73 maize genome: complexity, diversity, and dynamics. Science 326: 1112–1115.

109. AltschulSF, MaddenTL, SchafferAA, ZhangJ, ZhangZ, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389–3402.

110. Marchler-BauerA, AndersonJB, CherukuriPF, DeWeese-ScottC, GeerLY, et al. (2005) CDD: a Conserved Domain Database for protein classification. Nucleic Acids Res 33: D192–196.

111. TrapnellC, PachterL, SalzbergSL (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25: 1105–1111.

112. RobinsonMD, McCarthyDJ, SmythGK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139–140.

113. BenjaminiY, HochbergY (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. . J Royal Stat Soc Series B (Methodol.) 57: 289–300.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2014 Číslo 8
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Eozinofilní granulomatóza s polyangiitidou
nový kurz

Betablokátory a Ca antagonisté z jiného úhlu
Autori: prof. MUDr. Michal Vrablík, Ph.D., MUDr. Petr Janský

Autori: doc. MUDr. Petr Čáp, Ph.D.

Farmakoterapie akutní a chronické bolesti

Získaná hemofilie - Povědomí o nemoci a její diagnostika

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Nemáte účet?  Registrujte sa

Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa