The mitochondrial outer membrane AAA ATPase AtOM66 affects cell death and pathogen resistance in Arabidopsis thaliana

Plant Journal

Volumn 80, Issue 4, 2014, Pages 709-727

  Zhang, Botao ^a,b   Van Aken, Olivier ^a   Thatcher, Louise ^c   De Clercq, Inge ^d   Duncan, Owen ^a   Law, Simon R ^b   Murcha, Monika W ^a   Van Der Merwe, Margaretha ^a   Seifi, Hamed Soren ^d   Carrie, Chris ^a,f   Cazzonelli, Christopher ^e,g   Radomiljac, Jordan ^b   Höfte, Monica ^d   Singh, Karam B ^a,c   Van Breusegem, Frank ^d   Whelan, James ^b  

^a UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^b LA TROBE UNIVERSITY   (Australia)

^c CSIRO   (Australia)

^d GHENT UNIVERSITY   (Belgium)

^e AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^f University of Western Australia ^*  (Germany)

^g WESTERN SYDNEY UNIVERSITY   (Australia)

Author keywords

Arabidopsis; ATPase; cell death; mitochondria; pathogen defence; stress

Indexed keywords

CELL DEATH; CELL SIGNALING; GENES; MAMMALS; MITOCHONDRIA; PATHOGENS; PLANTS (BOTANY); SALICYLIC ACID; STRESSES; BIOLOGICAL MEMBRANES; CELL MEMBRANES; CELLS; CYTOLOGY; PROTEINS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; ATPASE; INDUCIBLE EXPRESSION; MITOCHONDRIAL PROTEIN; OUTER MITOCHONDRIAL MEMBRANES; PSEUDOMONAS SYRINGAE; STRESS-RESPONSIVE GENE;

PROTEINS; GENE EXPRESSION;

ARABIDOPSIS; ARABIDOPSIS THALIANA; BOTRYOTINIA FUCKELIANA; FUNGI; MAMMALIA; PSEUDOMONAS SYRINGAE;

ARABIDOPSIS PROTEIN; CYCLOPENTANE DERIVATIVE; JASMONIC ACID; MITOCHONDRIAL PROTEIN; MULTIPROTEIN COMPLEX; OM66 PROTEIN, ARABIDOPSIS; OXYLIPIN; SALICYLIC ACID;

ARABIDOPSIS; BOTRYTIS; CELL DEATH; CYTOLOGY; DROUGHT; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; MITOCHONDRIAL MEMBRANE; MUTATION; PATHOGENICITY; PHENOTYPE; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT DISEASE; PLANT LEAF; PSEUDOMONAS SYRINGAE; TRANSGENIC PLANT;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BOTRYTIS; CELL DEATH; CYCLOPENTANES; DROUGHTS; GENE EXPRESSION REGULATION, PLANT; HOST-PATHOGEN INTERACTIONS; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL PROTEINS; MULTIPROTEIN COMPLEXES; MUTATION; OXYLIPINS; PHENOTYPE; PLANT DISEASES; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; PSEUDOMONAS SYRINGAE; SALICYLIC ACID; STRESS, PHYSIOLOGICAL;

EID: 84920202450     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12665     Document Type: Article

References (82)

1. Bartoli, C.G., Gomez, F., Martinez, D.E., and, Guiamet, J.J., (2004) Mitochondria are the main target for oxidative damage in leaves of wheat (Triticum aestivum L.). J. Exp. Bot. 55, 1663-1669.
2. Brauc, S., De Vooght, E., Claeys, M., Hofte, M., and, Angenon, G., (2011) Influence of over-expression of cytosolic aspartate aminotransferase on amino acid metabolism and defence responses against Botrytis cinerea infection in Arabidopsis thaliana. J. Plant Physiol. 168, 1813-1819.
3. Carrie, C., Murcha, M.W., Kuehn, K., Duncan, O., Barthet, M., Smith, P.M., Eubel, H., Meyer, E., Day, D.A., Millar, A.H., and, Whelan, J., (2008) Type II NAD(P)H dehydrogenases are targeted to mitochondria and chloroplasts or peroxisomes in Arabidopsis thaliana. FEBS Lett. 582, 3073-3079.
4. Chacinska, A., Koehler, C.M., Milenkovic, D., Lithgow, T., and, Pfanner, N., (2009) Importing mitochondrial proteins: machineries and mechanisms. Cell, 138, 628-644.
5. Clifton, R., Lister, R., Parker, K.L., Sappl, P.G., Elhafez, D., Millar, A.H., Day, D.A., and, Whelan, J., (2005) Stress-induced co-expression of alternative respiratory chain components in Arabidopsis thaliana. Plant Mol. Biol. 58, 193-212.
6. Clough, S.J., and, Bent, A.F., (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.
7. Cserzö, M., Wallin, E., Simon, I., von Heijne, G., and, Elofsson, A., (1997) Prediction of transmembrane alpha-helices in prokaryotic membrane proteins: the dense alignment surface method. Protein Eng. 10, 673-676.
8. Curvers, K., Seifi, H., Mouille, G., et al. (2010) Abscisic acid deficiency causes changes in cuticle permeability and pectin composition that influence tomato resistance to Botrytis cinerea. Plant Physiol. 154, 847-860.
9. Cvetkovska, M., and, Vanlerberghe, G.C., (2013) Alternative oxidase impacts the plant response to biotic stress by influencing the mitochondrial generation of reactive oxygen species. Plant Cell Environ. 36, 721-732.
10. Cvetkovska, M., Dahal, K., Alber, N.A., Jin, C., Cheung, M., and, Vanlerberghe, G.C., (2014) Knockdown of mitochondrial alternative oxidase induces the 'stress state' of signaling molecule pools in Nicotiana tabacum, with implications for stomatal function. New Phytol. 203, 449-461.
11. Danon, A., Rotari, V.I., Gordon, A., Mailhac, N., and, Gallois, P., (2004) Ultraviolet-C overexposure induces programmed cell death in Arabidopsis, which is mediated by caspase-like activities and which can be suppressed by caspase inhibitors, p35 and Defender against Apoptotic Death. J. Biol. Chem. 279, 779-787.
12. De Clercq, I., Vermeirssen, V., Van Aken, O., et al. (2013) The membrane-bound NAC transcription factor ANAC013 functions in mitochondrial retrograde regulation of the oxidative stress response in Arabidopsis. Plant Cell, 25, 3472-3490.
13. Diaz, J., ten Have, A., and, van Kan, J.A., (2002) The role of ethylene and wound signaling in resistance of tomato to Botrytis cinerea. Plant Physiol. 129, 1341-1351.
14. Doukhanina, E.V., Chen, S., van der Zalm, E., Godzik, A., Reed, J., and, Dickman, M.B., (2006) Identification and functional characterization of the BAG protein family in Arabidopsis thaliana. J. Biol. Chem. 281, 18793-18801.
15. Duncan, O., Taylor, N.L., Carrie, C., Eubel, H., Kubiszewski-Jakubiak, S., Zhang, B., Narsai, R., Millar, A.H., and, Whelan, J., (2011) Multiple lines of evidence localize signaling, morphology, and lipid biosynthesis machinery to the mitochondrial outer membrane of Arabidopsis. Plant Physiol. 157, 1093-1113.
16. Dutilleul, C., Garmier, M., Noctor, G., Mathieu, C., Chetrit, P., Foyer, C.H., and, de Paepe, R., (2003) Leaf mitochondria modulate whole cell redox homeostasis, set antioxidant capacity, and determine stress resistance through altered signaling and diurnal regulation. Plant Cell, 15, 1212-1226.
17. Erdmann, R., Wiebel, F.F., Flessau, A., Rytka, J., Beyer, A., Frohlich, K.U., and, Kunau, W.H., (1991) PAS1, a yeast gene required for peroxisome biogenesis, encodes a member of a novel family of putative ATPases. Cell, 64, 499-510.
18. Erzberger, J.P., and, Berger, J.M., (2006) Evolutionary relationships and structural mechanisms of AAA+ proteins. Annu. Rev. Biophys. Biomol. Struct. 35, 93-114.
19. Frickey, T., and, Lupas, A.N., (2004) Phylogenetic analysis of AAA proteins. J. Struct. Biol. 146, 2-10.
20. Fu, Z.Q., and, Dong, X., (2013) Systemic acquired resistance: turning local infection into global defense. Annu. Rev. Plant Biol. 64, 839-863.
21. Fu, H., Girod, P.A., Doelling, J.H., van Nocker, S., Hochstrasser, M., Finley, D., and, Vierstra, R.D., (1999) Structure and functional analysis of the 26S proteasome subunits from plants. Mol. Biol. Rep. 26, 137-146.
22. Fujita, M., Fujita, Y., Noutoshi, Y., Takahashi, F., Narusaka, Y., Yamaguchi-Shinozaki, K., and, Shinozaki, K., (2006) Crosstalk between abiotic and biotic stress responses: a current view from the points of convergence in the stress signaling networks. Curr. Opin. Plant Biol. 9, 436-442.
23. Gadjev, I., Vanderauwera, S., Gechev, T.S., Laloi, C., Minkov, I.N., Shulaev, V., Apel, K., Inze, D., Mittler, R., and, Van Breusegem, F., (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol. 141, 436-445.
24. Gao, M., Liu, J., Bi, D., Zhang, Z., Cheng, F., Chen, S., and, Zhang, Y., (2008) MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Res. 18, 1190-1198.
25. Gibala, M., Kicia, M., Sakamoto, W., Gola, E.M., Kubrakiewicz, J., Smakowska, E., and, Janska, H., (2009) The lack of mitochondrial AtFtsH4 protease alters Arabidopsis leaf morphology at the late stage of rosette development under short-day photoperiod. Plant J. 59, 685-699.
26. Giraud, E., Ho, L.H., Clifton, R., et al. (2008) The absence of ALTERNATIVE OXIDASE1a in Arabidopsis results in acute sensitivity to combined light and drought stress. Plant Physiol. 147, 595-610.
27. Giraud, E., Van Aken, O., Uggalla, V., and, Whelan, J., (2012) REDOX regulation of mitochondrial function in plants. Plant Cell Environ. 35, 271-280.
28. Gleason, C., Huang, S., Thatcher, L.F., Foley, R.C., Anderson, C.R., Carroll, A.J., Millar, A.H., and, Singh, K.B., (2011) Mitochondrial complex II has a key role in mitochondrial-derived reactive oxygen species influence on plant stress gene regulation and defense. Proc. Natl Acad. Sci. USA, 108, 10768-10773.
29. Gomez, L., Bancel, D., Rubio, E., and, Vercambre, G., (2007) The microplate reader: an efficient tool for the separate enzymatic analysis of sugars in plant tissues-validation of a micro-method. J. Sci. Food Agric. 87, 1893-1905.
30. Hanson, P.I., and, Whiteheart, S.W., (2005) AAA+ proteins: have engine, will work. Nat. Rev. Mol. Cell Biol. 6, 519-529.
31. Hellens, R.P., Edwards, E.A., Leyland, N.R., Bean, S., and, Mullineaux, P.M., (2000) pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation. Plant Mol. Biol. 42, 819-832.
32. Hinson, J.T., Fantin, V.R., Schonberger, J., et al. (2007) Missense mutations in the BCS1L gene as a cause of the Bjornstad syndrome. N. Engl. J. Med. 356, 809-819.
33. Ho, L.H., Giraud, E., Uggalla, V., Lister, R., Clifton, R., Glen, A., Thirkettle-Watts, D., Van Aken, O., and, Whelan, J., (2008) Identification of regulatory pathways controlling gene expression of stress-responsive mitochondrial proteins in Arabidopsis. Plant Physiol. 147, 1858-1873.
34. Iyer, L.M., Leipe, D.D., Koonin, E.V., and, Aravind, L., (2004) Evolutionary history and higher order classification of AAA+ ATPases. J. Struct. Biol. 146, 11-31.
35. Kang, H.G., Kuhl, J.C., Kachroo, P., and, Klessig, D.F., (2008) CRT1, an Arabidopsis ATPase that interacts with diverse resistance proteins and modulates disease resistance to turnip crinkle virus. Cell Host Microbe, 3, 48-57.
36. Kang, H.G., Oh, C.S., Sato, M., Katagiri, F., Glazebrook, J., Takahashi, H., Kachroo, P., Martin, G.B., and, Klessig, D.F., (2010) Endosome-associated CRT1 functions early in resistance gene-mediated defense signaling in Arabidopsis and tobacco. Plant Cell, 22, 918-936.
37. Karimi, M., Inze, D., and, Depicker, A., (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193-195.
38. Kuhn, K., Richter, U., Meyer, E.H., Delannoy, E., de Longevialle, A.F., O'Toole, N., Borner, T., Millar, A.H., Small, I.D., and, Whelan, J., (2009) Phage-type RNA polymerase RPOTmp performs gene-specific transcription in mitochondria of Arabidopsis thaliana. Plant Cell, 21, 2762-2779.
39. Lam, E., Kato, N., and, Lawton, M., (2001) Programmed cell death, mitochondria and the plant hypersensitive response. Nature, 411, 848-853.
40. Lee, M.H., and, Sano, H., (2007) Attenuation of the hypersensitive response by an ATPase associated with various cellular activities (AAA) protein through suppression of a small GTPase, ADP ribosylation factor, in tobacco plants. Plant J. 51, 127-139.
41. Liebrand, T.W., van den Berg, G.C., Zhang, Z., et al. (2013) Receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection. Proc. Natl Acad. Sci. USA, 110, 10010-10015.
42. Lin, S.S., Martin, R., Mongrand, S., Vandenabeele, S., Chen, K.C., Jang, I.C., and, Chua, N.H., (2008) RING1 E3 ligase localizes to plasma membrane lipid rafts to trigger FB1-induced programmed cell death in Arabidopsis. Plant J. 56, 550-561.
43. Lister, R., Carrie, C., Duncan, O., Ho, L.H., Howell, K.A., Murcha, M.W., and, Whelan, J., (2007) Functional definition of outer membrane proteins involved in preprotein import into mitochondria. Plant Cell, 19, 3739-3759.
44. Lupas, A., Van Dyke, M., and, Stock, J., (1991) Predicting coiled coils from protein sequences. Science, 252, 1162-1164.
45. Meyer, E.H., Tomaz, T., Carroll, A.J., Estavillo, G., Delannoy, E., Tanz, S.K., Small, I.D., Pogson, B.J., and, Millar, A.H., (2009) Remodeled respiration in ndufs4 with low phosphorylation efficiency suppresses Arabidopsis germination and growth and alters control of metabolism at night. Plant Physiol. 151, 603-619.
46. Millar, A.H., and, Leaver, C.J., (2000) The cytotoxic lipid peroxidation product, 4-hydroxy-2-nonenal, specifically inhibits decarboxylating dehydrogenases in the matrix of plant mitochondria. FEBS Lett. 481, 117-121.
47. Miura, K., Okamoto, H., Okuma, E., Shiba, H., Kamada, H., Hasegawa, P.M., and, Murata, Y., (2012) SIZ1 deficiency causes reduced stomatal aperture and enhanced drought tolerance via controlling salicylic acid-induced accumulation of reactive oxygen species in Arabidopsis. Plant J. 73, 91-104.
48. Nakagami, H., Soukupova, H., Schikora, A., Zarsky, V., and, Hirt, H., (2006) A Mitogen-activated protein kinase kinase kinase mediates reactive oxygen species homeostasis in Arabidopsis. J. Biol. Chem. 281, 38697-38704.
49. Nemhauser, J.L., Hong, F., and, Chory, J., (2006) Different plant hormones regulate similar processes through largely nonoverlapping transcriptional responses. Cell, 126, 467-475.
50. Ng, S., Ivanova, A., Duncan, O., et al. (2013) A membrane-bound NAC transcription factor, ANAC017, mediates mitochondrial retrograde signaling in Arabidopsis. Plant Cell, 25, 3450-3471.
51. Nobrega, F.G., Nobrega, M.P., and, Tzagoloff, A., (1992) BCS1, a novel gene required for the expression of functional Rieske iron-sulfur protein in Saccharomyces cerevisiae. EMBO J. 11, 3821-3829.
52. Ogura, T., and, Wilkinson, A.J., (2001) AAA+ superfamily ATPases: common structure-diverse function. Genes Cells, 6, 575-597.
53. Park, S.Y., Yu, J.W., Park, J.S., et al. (2007) The senescence-induced staygreen protein regulates chlorophyll degradation. Plant Cell, 19, 1649-1664.
54. Patel, S., and, Latterich, M., (1998) The AAA team: related ATPases with diverse functions. Trends Cell Biol. 8, 65-71.
55. Peters, K., Niessen, M., Peterhansel, C., Spath, B., Holzle, A., Binder, S., Marchfelder, A., and, Braun, H.P., (2012) Complex I-complex II ratio strongly differs in various organs of Arabidopsis thaliana. Plant Mol. Biol. 79, 273-284.
56. Pieterse, C.M., Leon-Reyes, A., Van der Ent, S., and, Van Wees, S.C., (2009) Networking by small-molecule hormones in plant immunity. Nat. Chem. Biol. 5, 308-316.
57. Rancour, D.M., Park, S., Knight, S.D., and, Bednarek, S.Y., (2004) Plant UBX domain-containing protein 1, PUX1, regulates the oligomeric structure and activity of Arabidopsis CDC48. J. Biol. Chem. 279, 54264-54274.
58. Schwab, R., Ossowski, S., Riester, M., Warthmann, N., and, Weigel, D., (2006) Highly specific gene silencing by artificial microRNAs in Arabidopsis. Plant Cell, 18, 1121-1133.
59. Senthil-Kumar, M., and, Mysore, K.S., (2012) Ornithine-delta-aminotransferase and proline dehydrogenase genes play a role in non-host disease resistance by regulating pyrroline-5-carboxylate metabolism-induced hypersensitive response. Plant Cell Environ. 35, 1329-1343.
60. Shahriari, M., Keshavaiah, C., Scheuring, D., Sabovljevic, A., Pimpl, P., Hausler, R.E., Hulskamp, M., and, Schellmann, S., (2010) The AAA-type ATPase AtSKD1 contributes to vacuolar maintenance of Arabidopsis thaliana. Plant J. 64, 71-85.
61. Singer, S.J., (1990) The structure and insertion of integral proteins in membranes. Annu. Rev. Cell Biol. 6, 247-296.
62. Stettler, M., Eicke, S., Mettler, T., Messerli, G., Hortensteiner, S., and, Zeeman, S.C., (2009) Blocking the metabolism of starch breakdown products in Arabidopsis leaves triggers chloroplast degradation. Mol. Plant, 2, 1233-1246.
63. Sugimoto, M., Yamaguchi, Y., Nakamura, K., Tatsumi, Y., and, Sano, H., (2004) A hypersensitive response-induced ATPase associated with various cellular activities (AAA) protein from tobacco plants. Plant Mol. Biol. 56, 973-985.
64. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and, Kumar, S., (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731-2739.
65. Taylor, N.L., Tan, Y.F., Jacoby, R.P., and, Millar, A.H., (2009) Abiotic environmental stress induced changes in the Arabidopsis thaliana chloroplast, mitochondria and peroxisome proteomes. J. Proteomics, 72, 367-378.
66. Thatcher, L.F., Powell, J.J., Aitken, E.A., Kazan, K., and, Manners, J.M., (2012) The lateral organ boundaries domain transcription factor LBD20 functions in Fusarium wilt Susceptibility and jasmonate signaling in Arabidopsis. Plant Physiol. 160, 407-418.
67. Tomoyasu, T., Yuki, T., Morimura, S., Mori, H., Yamanaka, K., Niki, H., Hiraga, S., and, Ogura, T., (1993) The Escherichia coli FtsH protein is a prokaryotic member of a protein family of putative ATPases involved in membrane functions, cell cycle control, and gene expression. J. Bacteriol. 175, 1344-1351.
68. Van Aken, O., and, Whelan, J., (2012) Comparison of transcriptional changes to chloroplast and mitochondrial perturbations reveals common and specific responses in Arabidopsis. Front. Plant Sci. 3, 281.
69. Van Aken, O., Pecenkova, T., van de Cotte, B., et al. (2007) Mitochondrial type-I prohibitins of Arabidopsis thaliana are required for supporting proficient meristem development. Plant J. 52, 850-864.
70. Van Aken, O., Zhang, B., Carrie, C., Uggalla, V., Paynter, E., Giraud, E., and, Whelan, J., (2009) Defining the mitochondrial stress response in Arabidopsis thaliana. Mol. Plant, 2, 1310-1324.
71. Van Aken, O., Zhang, B., Law, S., Narsai, R., and, Whelan, J., (2013) AtWRKY40 and AtWRKY63 modulate the expression of stress-responsive nuclear genes encoding mitochondrial and chloroplast proteins. Plant Physiol. 162, 254-271.
72. Van Leene, J., Eeckhout, D., Persiau, G., Van De Slijke, E., Geerinck, J., Van Isterdael, G., Witters, E., and, De Jaeger, G., (2011) Isolation of transcription factor complexes from Arabidopsis cell suspension cultures by tandem affinity purification. Methods Mol. Biol. 754, 195-218.
73. Verniquet, F., Gaillard, J., Neuburger, M., and, Douce, R., (1991) Rapid inactivation of plant aconitase by hydrogen peroxide. Biochem J. 276 (Pt 3), 643-648.
74. Visapaa, I., Fellman, V., Vesa, J., et al. (2002) GRACILE syndrome, a lethal metabolic disorder with iron overload, is caused by a point mutation in BCS1L. Am. J. Hum. Genet. 71, 863-876.
75. Wagener, N., Ackermann, M., Funes, S., and, Neupert, W., (2011) A pathway of protein translocation in mitochondria mediated by the AAA-ATPase Bcs1. Mol. Cell, 44, 191-202.
76. Woo, N.S., Badger, M.R., and, Pogson, B.J., (2008) A rapid, non-invasive procedure for quantitative assessment of drought survival using chlorophyll fluorescence. Plant Methods, 4, 27.
77. Yang, Z.T., Wang, M.J., Sun, L., Lu, S.J., Bi, D.L., Song, Z.T., Zhang, S.S., Zhou, S.F., and, Liu, J.X., (2014) The membrane-associated transcription factor NAC089 controls ER-stress-induced programmed cell death in plants. PLoS Genet. 10, e1004243.
78. Zhang, Y., Marcillat, O., Giulivi, C., Ernster, L., and, Davies, K.J., (1990) The oxidative inactivation of mitochondrial electron transport chain components and ATPase. J. Biol. Chem. 265, 16330-16336.
79. Zhang, X., Shaw, A., Bates, P.A., et al. (2000) Structure of the AAA ATPase p97. Mol. Cell, 6, 1473-1484.
80. Zhang, B., Carrie, C., Ivanova, A., et al. (2012) LETM proteins play a role in the accumulation of mitochondrially encoded proteins in Arabidopsis thaliana and AtLETM2 displays parent of origin effects. J. Biol. Chem. 287, 41757-41773.
81. Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L., and, Gruissem, W., (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol. 136, 2621-2632.
82. Zipfel, C., Robatzek, S., Navarro, L., Oakeley, E.J., Jones, J.D., Felix, G., and, Boller, T., (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature, 428, 764-767.