Arabidopsis thaliana DM2h (R8) within the Landsberg RPP1-like Resistance Locus Underlies Three Different Cases of EDS1-Conditioned Autoimmunity

PLoS Genetics

Volumn 12, Issue 4, 2016, Pages

  Stuttmann, Johannes ^a,b   Peine, Nora ^a   Garcia, Ana V ^a   Wagner, Christine ^b   Choudhury, Sayan R ^a   Wang, Yiming ^a   James, Geo Velikkakam ^a   Griebel, Thomas ^a   Alcázar, Ruben ^c   Tsuda, Kenichi ^a   Schneeberger, Korbinian ^a   Parker, Jane E ^a  

^a MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

^c UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

EDS1 PROTEIN; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; ARABIDOPSIS PROTEIN; CARBOXYLESTERASE; COG1 PROTEIN, ARABIDOPSIS; DNA BINDING PROTEIN; EDS1 PROTEIN, ARABIDOPSIS; PAD4 PROTEIN, ARABIDOPSIS; TRANSCRIPTION FACTOR;

ARABIDOPSIS THALIANA; ARTICLE; AUTOIMMUNITY; DM2H GENE; GENE LOCUS; GENE MAPPING; GENE MUTATION; GENE REPRESSION; GENETIC INCOMPATIBILITY; GENETIC POLYMORPHISM; GENETIC SCREENING; GENETIC TRANSCRIPTION; NONHUMAN; PHENOTYPE; PLANT GENE; PLANT GENETICS; PLANT IMMUNITY; PROTEIN EXPRESSION; PROTEIN FUNCTION; ARABIDOPSIS; DISEASE RESISTANCE; GENE DELETION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; AUTOIMMUNITY; CARBOXYLIC ESTER HYDROLASES; DISEASE RESISTANCE; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, PLANT; PLANTS, GENETICALLY MODIFIED; SEQUENCE DELETION; TRANSCRIPTION FACTORS;

EID: 84964802244     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1005990     Document Type: Article

References (89)

1. Dodds PN, Rathjen JP, Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet. 2010;11(8):539–48. Epub 2010/06/30. nrg2812 [pii] doi: 10.1038/nrg281220585331.
2. Maekawa T, Kracher B, Vernaldi S, Ver Loren van Themaat E, Schulze-Lefert P, Conservation of NLR-triggered immunity across plant lineages. Proc Natl Acad Sci. 2012;109(49):20119–23. Epub 2012/11/24. 1218059109 [pii] doi: 10.1073/pnas.121805910923175786; PubMed Central PMCID: PMC3523848.
3. Vance RE, The NAIP/NLRC4 inflammasomes. Curr Opin Immunol. 2015;32:84–9. WOS:000350781300014. 25621709
4. Takken FLW, Goverse A, How to build a pathogen detector: structural basis of NB-LRR function. Curr Opin Plant Biol. 2012;15:375–84. doi: 10.1016/j.pbi.2012.05.00122658703.
5. Griebel T, Maekawa T, Parker JE, NOD-like receptor cooperativity in effector-triggered immunity. Trends Immunol. 2014;35(11):562–70. doi: 10.1016/J.It.2014.09.005 WOS:000345478500008. 25308923
6. Cui HT, Tsuda K, Parker JE, Effector-Triggered Immunity: From Pathogen Perception to Robust Defense. Annu Rev Plant Biol, Vol 66. 2015;66:487–511. doi: 10.1146/annurev-arplant-050213-040012 WOS:000353711400020.
7. Clark RM, Schweikert G, Toomajian C, Ossowski S, Zeller G, Shinn P, et al. Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science. 2007;317(5836):338–42. doi: 10.1126/science.1138632 WOS:000248150200037. 17641193
8. Guo YL, Fitz J, Schneeberger K, Ossowski S, Cao J, Weigel D, Genome-Wide Comparison of Nucleotide-Binding Site-Leucine-Rich Repeat-Encoding Genes in Arabidopsis. Plant Physiol. 2011;157(2):757–69. doi: 10.1104/pp.111.181990 WOS:000295625700020. 21810963
9. Jacob F, Vernaldi S, Maekawa T, Evolution and conservation of plant NLR functions. Front Immunol. 2013;4. doi: 10.3389/Fimmu.2013.00297 WOS:000209374100292.
10. Allen RL, Bittner-Eddy PD, Grenville-Briggs LJ, Meitz JC, Rehmany AP, Rose LE, et al. Host-parasite coevolutionary conflict between Arabidopsis and downy mildew. Science. 2004;306(5703):1957–60. 15591208.
11. Seeholzer S, Tsuchimatsu T, Jordan T, Bieri S, Pajonk S, Yang W, et al. Diversity at the Mla powdery mildew resistance locus from cultivated barley reveals sites of positive selection. Mol Plant Microbe Interact. 2010;23:497–509. doi: 10.1094/MPMI-23-4-049720192836.
12. Karasov TL, Horton MW, Bergelson J, Genomic variability as a driver of plant-pathogen coevolution?Curr Opin Plant Biol. 2014;18:24–30. WOS:000335619700005. 24491596
13. Thrall PH, Laine AL, Ravensdale M, Nemri A, Dodds PN, Barrett LG, et al. Rapid genetic change underpins antagonistic coevolution in a natural host-pathogen metapopulation. Ecol Lett. 2012;15(5):425–35. doi: 10.1111/j.1461-0248.2012.01749.x WOS:000302288900004. 22372578
14. Mukhtar MS, Carvunis AR, Dreze M, Epple P, Steinbrenner J, Moore J, et al. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science. 2011;333(6042):596–601. doi: 10.1126/science.120365921798943; PubMed Central PMCID: PMC3170753.
15. Cesari S, Bernoux M, Moncuquet P, Kroj T, Dodds PN, A novel conserved mechanism for plant NLR protein pairs: the "integrated decoy" hypothesis. Front Plant Sci. 2014;5. doi: 10.3389/Fpls.2014.00606 WOS:000347323700001.
16. Le Roux C, Huet G, Jauneau A, Camborde L, Tremousaygue D, Kraut A, et al. A Receptor Pair with an Integrated Decoy Converts Pathogen Disabling of Transcription Factors to Immunity. Cell. 2015;161(5):1074–88. doi: 10.1016/j.cell.2015.04.025 WOS:000355152600015. 26000483
17. Sarris PF, Duxbury Z, Huh SU, Ma Y, Segonzac C, Sklenar J, et al. A Plant Immune Receptor Detects Pathogen Effectors that Target WRKY Transcription Factors. Cell. 2015;161(5):1089–100. doi: 10.1016/j.cell.2015.04.024 WOS:000355152600016. 26000484
18. Chae E, Bomblies K, Kim ST, Karelina D, Zaidem M, Ossowski S, et al. Species-wide genetic incompatibility analysis identifies immune genes as hot spots of deleterious epistasis. Cell. 2014;159(6):1341–51. doi: 10.1016/j.cell.2014.10.04925467443; PubMed Central PMCID: PMC4269942.
19. Alcázar R, Parker JE, The impact of temperature on balancing immune responsiveness and growth in Arabidopsis. Trends Plant Sci. 2011;16(12):666–75. doi: 10.1016/j.tplants.2011.09.001 WOS:000298724900004. 21963982
20. Sohn KH, Segonzac C, Rallapalli G, Sarris PF, Woo JY, Williams SJ, et al. The nuclear immune receptor RPS4 is required for RRS1SLH1-dependent constitutive defense activation in Arabidopsis thaliana. PLoS Genet. 2014;10(10):e1004655. doi: 10.1371/journal.pgen.100465525340333; PubMed Central PMCID: PMCPMC4207616.
21. Heidrich K, Tsuda K, Blanvillain-Baufume S, Wirthmueller L, Bautor J, Parker JE, Arabidopsis TNL-WRKY domain receptor RRS1 contributes to temperature-conditioned RPS4 auto-immunity. Front Plant Sci. 2013;4:403. doi: 10.3389/fpls.2013.0040324146667; PubMed Central PMCID: PMC3797954.
22. Bomblies K, Lempe J, Epple P, Warthmann N, Lanz C, Dangl JL, et al. Autoimmune response as a mechanism for a Dobzhansky-Muller-type incompatibility syndrome in plants. PLoS Biol. 2007;5(9):e236. doi: 10.1371/journal.pbio.005023617803357; PubMed Central PMCID: PMC1964774.
23. Bomblies K, Weigel D, Hybrid necrosis: autoimmunity as a potential gene-flow barrier in plant species. Nat Rev Genet. 2007;8(5):382–93. doi: 10.1038/nrg208217404584.
24. Bikard D, Patel D, Le Mette C, Giorgi V, Camilleri C, Bennett MJ, et al. Divergent evolution of duplicate genes leads to genetic incompatibilities within A. thaliana. Science. 2009;323(5914):623–6. doi: 10.1126/science.116591719179528.
25. Alcázar R, Garcia AV, Kronholm I, de Meaux J, Koornneef M, Parker JE, et al. Natural variation at Strubbelig Receptor Kinase 3 drives immune-triggered incompatibilities between Arabidopsis thaliana accessions. Nat Genet. 2010;42(12):1135–9. doi: 10.1038/ng.70421037570.
26. Kruger J, Thomas CM, Golstein C, Dixon MS, Smoker M, Tang S, et al. A tomato cysteine protease required for Cf-2-dependent disease resistance and suppression of autonecrosis. Science. 2002;296(5568):744–7. doi: 10.1126/science.106928811976458.
27. Alcázar R, Garcia AV, Parker JE, Reymond M, Incremental steps toward incompatibility revealed by Arabidopsis epistatic interactions modulating salicylic acid pathway activation. Proc Natl Acad Sci. 2009;106(1):334–9. doi: 10.1073/pnas.081173410619106299; PubMed Central PMCID: PMC2629243.
28. Jeuken MJ, Zhang NW, McHale LK, Pelgrom K, den Boer E, Lindhout P, et al. Rin4 causes hybrid necrosis and race-specific resistance in an interspecific lettuce hybrid. Plant Cell. 2009;21(10):3368–78. doi: 10.1105/tpc.109.07033419855048; PubMed Central PMCID: PMCPMC2782268.
29. Yamamoto E, Takashi T, Morinaka Y, Lin S, Wu J, Matsumoto T, et al. Gain of deleterious function causes an autoimmune response and Bateson-Dobzhansky-Muller incompatibility in rice. Mol Genet Genomics. 2010;283(4):305–15. doi: 10.1007/s00438-010-0514-y20140455.
30. Meyers BC, Kozik A, Griego A, Kuang HH, Michelmore RW, Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell. 2003;15(4):809–34. ISI:000185078100003. 12671079
31. Feys BJ, Moisan LJ, Newman MA, Parker JE, Direct interaction between the Arabidopsis disease resistance signaling proteins, EDS1 and PAD4. EMBO Journal. 2001;20(19):5400–11. ISI:000171501200012. 11574472
32. Wirthmueller L, Zhang Y, Jones JD, Parker JE, Nuclear accumulation of the Arabidopsis immune receptor RPS4 is necessary for triggering EDS1-dependent defense. Curr Biol. 2007;17(23):2023–9. 17997306.
33. Li X, Clarke JD, Zhang Y, Dong X, Activation of an EDS1-mediated R-gene pathway in the snc1 mutant leads to constitutive, NPR1-independent pathogen resistance. Mol Plant Microbe Interact: MPMI. 2001;14:1131–9. doi: 10.1094/MPMI.2001.14.10.113111605952.
34. Hu G, deHart AK, Li Y, Ustach C, Handley V, Navarre R, et al. EDS1 in tomato is required for resistance mediated by TIR-class R genes and the receptor-like R gene Ve. Plant J. 2005;42(3):376–91. doi: 10.1111/j.1365-313X.2005.02380.x15842623.
35. Kim T-H, Kunz H-H, Bhattacharjee S, Hauser F, Park J, Engineer C, et al. Natural Variation in Small Molecule-Induced TIR-NB-LRR Signaling Induces Root Growth Arrest via EDS1- and PAD4-Complexed R Protein VICTR in Arabidopsis. Plant Cell. 2012;24:5177–92. doi: 10.1105/tpc.112.10723523275581.
36. Heidrich K, Wirthmueller L, Tasset C, Pouzet C, Deslandes L, Parker JE, Arabidopsis EDS1 connects pathogen effector recognition to cell compartment-specific immune responses. Science. 2011;334(6061):1401–4. Epub 2011/12/14. 334/6061/1401 [pii] doi: 10.1126/science.121164122158818.
37. Bhattacharjee S, Halane MK, Kim SH, Gassmann W, Pathogen effectors target Arabidopsis EDS1 and alter its interactions with immune regulators. Science. 2011;334(6061):1405–8. Epub 2011/12/14. 334/6061/1405 [pii] doi: 10.1126/science.121159222158819.
38. Garcia AV, Blanvillain-Baufume S, Huibers RP, Wiermer M, Li G, Gobbato E, et al. Balanced nuclear and cytoplasmic activities of EDS1 are required for a complete plant innate immune response. PLoS Pathog. 2010;6:e1000970. Epub 2010/07/10. doi: 10.1371/journal.ppat.100097020617163; PubMed Central PMCID: PMC2895645.
39. Cheng YT, Germain H, Wiermer M, Bi D, Xu F, Garcia AV, et al. Nuclear pore complex component MOS7/Nup88 is required for innate immunity and nuclear accumulation of defense regulators in Arabidopsis. Plant Cell. 2009;21(8):2503–16. doi: 10.1105/tpc.108.06451919700630; PubMed Central PMCID: PMC2751965.
40. Wagner S, Stuttmann J, Rietz S, Guerois R, Brunstein E, Bautor J, et al. Structural basis for signaling by exclusive EDS1 heteromeric complexes with SAG101 or PAD4 in plant innate immunity. Cell Host Microbe. 2013;14(6):619–30. doi: 10.1016/j.chom.2013.11.00624331460.
41. Bartsch M, Gobbato E, Bednarek P, Debey S, Schultze JL, Bautor J, et al. Salicylic acid-independent ENHANCED DISEASE SUSCEPTIBILITY1 signaling in Arabidopsis immunity and cell death is regulated by the monooxygenase FMO1 and the Nudix hydrolase NUDT7. Plant Cell. 2006;18(4):1038–51. 16531493.
42. Stenvik GE, Tandstad NM, Guo Y, Shi CL, Kristiansen W, Holmgren A, et al. The EPIP peptide of INFLORESCENCE DEFICIENT IN ABSCISSION is sufficient to induce abscission in Arabidopsis through the receptor-like kinases HAESA and HAESA-LIKE2. Plant Cell. 2008;20(7):1805–17. doi: 10.1105/tpc.108.05913918660431; PubMed Central PMCID: PMC2518227.
43. Kalderon D, Richardson WD, Markham AF, Smith AE, Sequence requirements for nuclear location of simian virus 40 large-T antigen. Nature. 1984;311(5981):33–8. 6088992.
44. Narusaka M, Shirasu K, Noutoshi Y, Kubo Y, Shiraishi T, Iwabuchi M, et al. RRS1 and RPS4 provide a dual Resistance-gene system against fungal and bacterial pathogens. Plant J. 2009;60:218–26. doi: 10.1111/j.1365-313X.2009.03949.x19519800.
45. Birker D, Heidrich K, Takahara H, Narusaka M, Deslandes L, Narusaka Y, et al. A locus conferring resistance to Colletotrichum higginsianum is shared by four geographically distinct Arabidopsis accessions. Plant J. 2009;60(4):602–13. doi: 10.1111/j.1365-313X.2009.03984.x WOS:000271811700003. 19686535
46. Williams SJ, Sohn KH, Wan L, Bernoux M, Sarris PF, Segonzac C, et al. Structural basis for assembly and function of a heterodimeric plant immune receptor. Science. 2014;344(6181):299–303. doi: 10.1126/science.124735724744375.
47. van der Biezen EA, Freddie CT, Kahn K, Parker JE, Jones JD, Arabidopsis RPP4 is a member of the RPP5 multigene family of TIR-NB-LRR genes and confers downy mildew resistance through multiple signalling components. Plant J. 2002;29(4):439–51. 11846877.
48. Zhu Y, Qian W, Hua J, Temperature Modulates Plant Defense Responses through NB-LRR Proteins. PLoS Pathogens. 2010;6(4). doi: 10.1371/journal.ppat.1000844 WOS:000277722400016.
49. Mang H-G, Qian W, Zhu Y, Qian J, Kang H-G, Klessig DF, et al. Abscisic Acid Deficiency Antagonizes High-Temperature Inhibition of Disease Resistance through Enhancing Nuclear Accumulation of Resistance Proteins SNC1 and RPS4 in Arabidopsis. Plant Cell. 2012;24(3):1271–84. doi: 10.1105/tpc.112.096198 WOS:000303763000031. 22454454
50. Yang SH, Hua J, A haplotype-specific Resistance gene regulated by BONZAI1 mediates temperature-dependent growth control in Arabidopsis. Plant Cell. 2004;16(4):1060–71. ISI:000220731900025. 15031411
51. Feys BJ, Wiermer M, Bhat RA, Moisan LJ, Medina-Escobar N, Neu C, et al. Arabidopsis SENESCENCE-ASSOCIATED GENE101 stabilizes and signals within an ENHANCED DISEASE SUSCEPTIBILITY1 complex in plant innate immunity. Plant Cell. 2005;17(9):2601–13. 16040633.
52. Rietz S, Stamm A, Malonek S, Wagner S, Becker D, Medina-Escobar N, et al. Different roles of Enhanced Disease Susceptibility1 (EDS1) bound to and dissociated from Phytoalexin Deficient4 (PAD4) in Arabidopsis immunity. New Phytol. 2011;191(1):107–19. Epub 2011/03/26. doi: 10.1111/j.1469-8137.2011.03675.x21434927.
53. Jirage D, Tootle TL, Reuber TL, Frost LN, Feys BJ, Parker JE, et al. Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc Natl Acad Sci. 1999;96(23):13583–8. Epub 1999/11/11. 10557364; PubMed Central PMCID: PMC23991.
54. Tsuda K, Sato M, Stoddard T, Glazebrook J, Katagiri F, Network Properties of Robust Immunity in Plants. Plos Genetics. 2009;5(12). doi: 10.1371/journal.pgen.1000772 WOS:000273469700023.
55. Glazebrook J, Chen W, Estes B, Chang HS, Nawrath C, Metraux JP, et al. Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. Plant J. 2003;34(2):217–28. 12694596.
56. Zhang YL, Goritschnig S, Dong XN, Li X, A gain-of-function mutation in a plant disease resistance gene leads to constitutive activation of downstream signal transduction pathways in suppressor of npr1-1, constitutive 1. Plant Cell. 2003;15(11):2636–46. ISI:000186578900014. 14576290
57. Wildermuth MC, Dewdney J, Wu G, Ausubel FM, Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature. 2001;414(6863):562–5. doi: 10.1038/3510710811734859.
58. Cao H, Glazebrook J, Clarke JD, Volko S, Dong X, The arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell. 1997;88:57–63. 9019406
59. Hartwig B, James GV, Konrad K, Schneeberger K, Turck F, Fast isogenic mapping-by-sequencing of ethyl methanesulfonate-induced mutant bulks. Plant Phys. 2012;160(2):591–600. doi: 10.1104/pp.112.20031122837357; PubMed Central PMCID: PMC3461541.
60. Abe A, Kosugi S, Yoshida K, Natsume S, Takagi H, Kanzaki H, et al. Genome sequencing reveals agronomically important loci in rice using MutMap. Nature biotechnology. 2012;30(2):174–8. doi: 10.1038/nbt.209522267009.
61. Schneeberger K, Using next-generation sequencing to isolate mutant genes from forward genetic screens. Nat Rev Genet. 2014;15(10):662–76. doi: 10.1038/nrg374525139187.
62. Schneeberger K, Ossowski S, Lanz C, Juul T, Petersen AH, Nielsen KL, et al. SHOREmap: simultaneous mapping and mutation identification by deep sequencing. Nat Methods. 2009;6(8):550–1. doi: 10.1038/nmeth0809-55019644454.
63. Botella MA, Parker JE, Frost LN, Bittner-Eddy PD, Beynon JL, Daniels MJ, et al. Three genes of the Arabidopsis RPP1 complex resistance locus recognize distinct Peronospora parasitica avirulence determinants. Plant Cell. 1998;10(11):1847–60. 9811793; PubMed Central PMCID: PMC143951.
64. Rehmany AP, Gordon A, Rose LE, Allen RL, Armstrong MR, Whisson SC, et al. Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. Plant Cell. 2005;17(6):1839–50. doi: 10.1105/tpc.105.03180715894715; PubMed Central PMCID: PMCPMC1143081.
65. Tahir J, Watanabe M, Jing HC, Hunter DA, Tohge T, Nunes-Nesi A, et al. Activation of R-mediated innate immunity and disease susceptibility is affected by mutations in a cytosolic O-acetylserine (thiol) lyase in Arabidopsis. Plant J. 2013;73(1):118–30. doi: 10.1111/tpj.1202122974487.
66. Shirzadian-Khorramabad R, Jing HC, Everts GE, Schippers JH, Hille J, Dijkwel PP, A mutation in the cytosolic O-acetylserine (thiol) lyase induces a genome-dependent early leaf death phenotype in Arabidopsis. BMC plant biology. 2010;10:80. doi: 10.1186/1471-2229-10-8020429919; PubMed Central PMCID: PMC2890954.
67. Alcázar R, von Reth M, Bautor J, Chae E, Weigel D, Koornneef M, et al. Analysis of a plant complex resistance gene locus underlying immune-related hybrid incompatibility and its occurrence in nature. PLoS Genet. 2014;10(12):e1004848. doi: 10.1371/journal.pgen.100484825503786; PubMed Central PMCID: PMC4263378.
68. Nemri A, Atwell S, Tarone AM, Huang YS, Zhao K, Studholme DJ, et al. Genome-wide survey of Arabidopsis natural variation in downy mildew resistance using combined association and linkage mapping. Proc Natl Acad Sci. 2010;107(22):10302–7. doi: 10.1073/pnas.091316010720479233; PubMed Central PMCID: PMCPMC2890483.
69. Holub EB, Beynon JL, Symbiology of mouse-ear cress (Arabidopsis thaliana) and oomycetes. Adv Bot Res. 1997;24:227–73. WOS:A1997BH33E00007.
70. Krasileva KV, Dahlbeck D, Staskawicz BJ, Activation of an Arabidopsis resistance protein is specified by the in planta association of its leucine-rich repeat domain with the cognate oomycete effector. Plant Cell. 2010;22(7):2444–58. doi: 10.1105/tpc.110.07535820601497; PubMed Central PMCID: PMC2929106.
71. Steinbrenner AD, Goritschnig S, Staskawicz BJ, Recognition and activation domains contribute to allele-specific responses of an Arabidopsis NLR receptor to an oomycete effector protein. PLoS Pathog. 2015;11(2):e1004665. doi: 10.1371/journal.ppat.100466525671309; PubMed Central PMCID: PMC4335498.
72. Kobe B, Deisenhofer J, Proteins with leucine-rich repeats. Curr Opin Struct Biol. 1995;5:409–16. 7583641
73. Manavalan B, Basith S, Choi S, Similar Structures but Different Roles—An Updated Perspective on TLR Structures. Front Physiol. 2011;2:41. doi: 10.3389/fphys.2011.0004121845181; PubMed Central PMCID: PMCPMC3146039.
74. Yi H, Richards EJ, Gene duplication and hypermutation of the pathogen Resistance gene SNC1 in the Arabidopsis bal variant. Genetics. 2009;183(4):1227–34. doi: 10.1534/genetics.109.10556919797048; PubMed Central PMCID: PMC2787416.
75. Wicker T, Yahiaoui N, Keller B, Illegitimate recombination is a major evolutionary mechanism for initiating size variation in plant resistance genes. Plant J. 2007;51(4):631–41. doi: 10.1111/j.1365-313X.2007.03164.x17573804.
76. Lucht JM, Mauch-Mani B, Steiner HY, Metraux JP, Ryals J, Hohn B, Pathogen stress increases somatic recombination frequency in Arabidopsis. Nat Genet. 2002;30(3):311–4. doi: 10.1038/ng84611836502.
77. Kovalchuk I, Kovalchuk O, Kalck V, Boyko V, Filkowski J, Heinlein M, et al. Pathogen-induced systemic plant signal triggers DNA rearrangements. Nature. 2003;423(6941):760–2. doi: 10.1038/nature0168312802336.
78. Molinier J, Ries G, Zipfel C, Hohn B, Transgeneration memory of stress in plants. Nature. 2006;442(7106):1046–9. doi: 10.1038/nature0502216892047.
79. Glazebrook J, Zook M, Mert F, Kagan I, Rogers EE, Crute IR, et al. Phytoalexin-deficient mutants of Arabidopsis reveal that PAD4 encodes a regulatory factor and that four PAD genes contribute to downy mildew resistance. Genetics. 1997;146(1):381–92. 9136026
80. Bowling SA, Guo A, Cao H, Gordon S, Klessig DF, Dong X, A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. Plant Cell. 1994;6:1845–57. 7866028
81. Stuttmann J, Hubberten HM, Rietz S, Kaur J, Muskett P, Guerois R, et al. Perturbation of Arabidopsis amino acid metabolism causes incompatibility with the adapted biotrophic pathogen Hyaloperonospora arabidopsidis. Plant Cell. 2011;23(7):2788–803. Epub 2011/07/26. tpc.111.087684 [pii] doi: 10.1105/tpc.111.08768421784950; PubMed Central PMCID: PMC3226217.
82. Wu ZJ, Irizarry RA, Preprocessing of oligonucleotide array data. Nature biotechnology. 2004;22(6):656–8. doi: 10.1038/nbt0604-656b WOS:000221785300012.
83. Storey J, Tibshirani R, Statistical methods for identifying differentially expressed genes in DNA microarrays. Methods Mol Biol2003;224:149–57. 12710672
84. Eisen MB, Spellman PT, Brown PO, Botstein D, Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci. 1998;95(25):14863–8. doi: 10.1073/pnas.95.25.14863 WOS:000077436700051. 9843981
85. Straus MR, Rietz S, Ver Loren van Themaat E, Bartsch M, Parker JE, Salicylic acid antagonism of EDS1-driven cell death is important for immune and oxidative stress responses in Arabidopsis. Plant J. 2010;62(4):628–40. 20163553. doi: 10.1111/j.1365-313X.2010.04178.x
86. Ossowski S, Schneeberger K, Clark RM, Lanz C, Warthmann N, Weigel D, Sequencing of natural strains of Arabidopsis thaliana with short reads. Genome Research. 2008;18(12):2024–33. doi: 10.1101/gr.080200.10818818371; PubMed Central PMCID: PMC2593571.
87. Schneeberger K, Ossowski S, Ott F, Klein JD, Wang X, Lanz C, et al. Reference-guided assembly of four diverse Arabidopsis thaliana genomes. Proc Natl Acad Sci. 2011;108(25):10249–54. doi: 10.1073/pnas.110773910821646520; PubMed Central PMCID: PMC3121819.
88. Engler C, Kandzia R, Marillonnet S, A one pot, one step, precision cloning method with high throughput capability. PLoS ONE. 2008;3(11):e3647. Epub 2008/11/06. doi: 10.1371/journal.pone.000364718985154; PubMed Central PMCID: PMC2574415.
89. Folta KM, Kaufman LS, Isolation of Arabidopsis nuclei and measurement of gene transcription rates using nuclear run-on assays. Nat Protoc. 2006;1(6):3094–100. doi: 10.1038/nprot.2006.47117406505.