Physcomitrella patens activates reinforcement of the cell wall, programmed cell death and accumulation of evolutionary conserved defence signals, such as salicylic acid and 12-oxo-phytodienoic acid, but not jasmonic acid, upon Botrytis cinerea infection

Molecular Plant Pathology

Volumn 13, Issue 8, 2012, Pages 960-974

  Ponce De León, Inés ^a   Schmelz, Eric A ^b   Gaggero, Carina ^a   Castro, Alexandra ^a   Álvarez, Alfonso ^a   Montesano, Marcos ^a,c  

^a INSTITUTO DE INVESTIGACIONES BIOLÓGICAS CLEMENTE ESTABLE   (Uruguay)

^b CENTER FOR MEDICAL   (United States)

^c Facultad de Ciencias   (Uruguay)

Author keywords

[No Author keywords available]

Indexed keywords

BOTRYOTINIA FUCKELIANA; BRYOPHYTA; MAGNOLIOPHYTA; PHYSCOMITRELLA PATENS;

EID: 85027952144     PISSN: 14646722     EISSN: 13643703     Source Type: Journal    
DOI: 10.1111/j.1364-3703.2012.00806.x     Document Type: Article

References (84)

1. AbuQamar, S., Chen, X., Dhawan, R., Bluhm, B., Salmeron, J., Lam, S., Dietrich, R.A. and Mengiste, T. (2006) Expression profiling and mutant analysis reveals complex regulatory networks involved in Arabidopsis response to Botrytis infection. Plant J. 48, 28-44.
2. Andersson, R.A., Akita, M., Pirhonen, M., Gammelgård, E. and Valkonen, J.P.T. (2005) Moss-Erwinia pathosystem reveals possible similarities in pathogenesis and pathogen defense in vascular and nonvascular plants. J. Gen. Plant Pathol. 71, 23-28.
3. Anterola, A., Göbel, C., Hornung, E., Sellhorn, G., Feussner, I. and Grimes, H. (2009) Physcomitrella patens has lipoxygenases for both eicosanoid and octadecanoid pathways. Phytochemistry, 70, 40-52.
4. Asai, S. and Yoshioka, H. (2009) Nitric oxide as a partner of reactive oxygen species participates in disease resistance to necrotrophic pathogen Botrytis cinerea in Nicotiana benthamiana. Mol. Plant-Microbe Interact. 22, 619-629.
5. Asai, S., Mase, K. and Yoshioka, H. (2010) Role of nitric oxide and reactive oxide species in disease resistance to necrotrophic pathogens. Plant Signal. Behav. 5, 872-874.
6. Asselbergh, B., Curvers, K., Franca, S.C., Audenaert, K., Vuylsteke, M., Van Breusegem, F. and Höfte, M. (2007) Resistance to Botrytis cinerea in sitiens, an abscisic acid-deficient tomato mutant, involves timely production of hydrogen peroxide and cell wall modifications in the epidermis. Plant Physiol. 144, 1863-1877.
7. Audenaert, K., De Meyer, G.B. and Höfte, M.M. (2002) Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms. Plant Physiol. 128, 491-501.
8. van Baarlen, P., Woltering, E.J., Staats, M. and van Kan, J.A.L. (2007) Histochemical and genetic analysis of host and non-host interactions of Arabidopsis with three Botrytis species: an important role for cell death control. Mol. Plant Pathol. 8, 41-54.
9. Bhuiyan, N.H., Selvaraj, G., Wei, Y. and King, J. (2009) Gene expression profiling and silencing reveal that monolignol biosynthesis plays a critical role in penetration defence in wheat against powdery mildew invasion. J. Exp. Bot. 60, 509-521.
10. Breithaupt, C., Kurzbauer, R., Schaller, F., Stintzi, A., Schaller, A., Huber, R., Macheroux, P. and Clausen, T. (2009) Structural basis of substrate specificity of plant 12-oxophytodienoate reductases. J. Mol. Biol. 392, 1266-1277.
11. Browse, J. (2009) Jasmonate passes muster: a receptor and targets for the defense hormone. Annu. Rev. Plant Biol. 60, 183-205.
12. Chakravarthy, S., Velásquez, A.C., Ekengren, S.K., Collmer, A. and Martin, G.B. (2010) Identification of Nicotiana benthamiana genes involved in pathogen-associated molecular pattern-triggered immunity. Mol. Plant-Microbe Interact. 23, 715-726.
13. Chehab, E.W., Kim, S., Savchenko, T., Kliebenstein, D., Dehesh, K. and Braam, J. (2011) Intronic T-DNA insertion renders Arabidopsis opr3 a conditional jasmonic acid-producing mutant. Plant Physiol. 156, 770-778.
14. Chico, J.M., Chini, A., Fonseca, S. and Solano, R. (2008) JAZ repressors set the rhythm in jasmonate signaling. Curr. Opin. Plant Biol. 11, 1-9.
15. Chini, A., Boter, M. and Solano, R. (2009) Plant oxylipins: COI1/JAZs/MYC2 as the core jasmonic acid-signalling module. FEBS J. 276, 4682-4692.
16. Christianson, M.L. and Duffy, S.H. (2002) Dose-dependent effect of salicylates in a moss, Funaria hygrometrica. J. Plant Growth Regul. 21, 200-208.
17. Coram, T.E., Wang, M. and Chen, X. (2008) Transcriptome analysis of the wheat-Puccinia striiformis f. sp. tritici interaction. Mol. Plant Pathol. 9, 157-169.
18. Curvers, K., Seifi, H., Mouille, G., de Rycke, R., Asselbergh, B., Van Hecke, A., Vanderschaeghe, D., Höfte, H., Callewaert, N., Van Breusegem, F. and Höfte, M. (2010) Abscisic acid deficiency causes changes in cuticle permeability and pectin composition that influence tomato resistance to Botrytis cinerea. Plant Physiol. 154, 847-860.
19. Davey, M.L. and Currah, R.S. (2006) Interactions between mosses (Bryophyta) and fungi. Can. J. Bot. 84, 1509-1519.
20. Davin, L.B. and Lewis, N.G. (2000) Dirigent proteins and dirigent sites explain the mystery of specificity of radical precursor coupling in lignan and lignin biosynthesis. Plant Physiol. 123, 453-462.
21. Dickman, M.B., Park, Y.K., Oltersdorf, T., Li, W., Clemente, T. and French, R. (2001) Abrogation of disease development in plants expressing animal antiapoptotic genes. Proc. Natl. Acad. Sci. USA, 98, 6957-6962.
22. van Doorn, W.G., Beers, E.P., Dangl, J.L., Franklin-Tong, V.E., Gallois, P., Hara-Nishimura, I., Jones, A.M., Kawai-Yamada, M., Lam, E., Mundy, J., Mur, L.A., Petersen, M., Smertenko, A., Taliansky, M., Van Breusegem, F., Wolpert, T., Woltering, E., Zhivotovsky, B. and Bozhkov, P.V. (2011) Morphological classification of plant cell deaths. Cell Death Differ. 18, 1241-1246.
23. Edelmann, H.G., Neinhuis, C., Jarvis, M., Evans, B., Fischer, E. and Barthlott, W. (1998) Ultrastructure and chemistry of the cell wall of the moss Rhacocarpus purpurascens (Rhacocarpaceae): a puzzling architecture among plants. Planta, 206, 315-321.
24. El Oirdi, M. and Bouarab, K. (2007) Plant signalling components EDS1 and SGT1 enhance disease caused by the necrotrophic pathogen Botrytis cinerea. New Phytol. 175, 131-139.
25. El Oirdi, M., El Rahman, T.A., Rigano, L., El Hadrami, A., Rodriguez, M.C., Daayf, F., Vojnov, A. and Bouarab, K. (2011) Botrytis cinerea manipulates the antagonistic effects between immune pathways to promote disease development in tomato. Plant Cell, 23, 2405-2421.
26. Espiñeira, J.M., Novo, U.E., Gómez Ros, L.V., Carrión, J.S., Merino, F., Ros Barceló, A. and Pomar, F. (2011) Distribution of lignin monomers and the evolution of lignification among lower plants. Plant Biol. 13, 59-68.
27. Ferrari, S., Plotnikova, J.M., De Lorenzo, G. and Ausubel, F.M. (2003) Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. Plant J. 35, 193-205.
28. Fonseca, S., Chini, A., Hamberg, M., Adie, B., Porzel, A., Kramell, R., Miersch, O., Wasternack, C. and Solano, R. (2009) (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat. Chem. Biol. 5, 344-350.
29. Fung, R.W., Gonzalo, M., Fekete, C., Kovacs, L.G., He, Y., Marsh, E., McIntyre, L.M., Schachtman, D.P. and Qiu, W. (2008) Powdery mildew induces defense oriented reprogramming of the transcriptome in a susceptible but not in a resistant grapevine. Plant Physiol. 146, 236-249.
30. Gachon, C. and Saindrenan, P. (2004) Real-time PCR monitoring of fungal development in Arabidopsis thaliana infected by Alternaria brassicicola and Botrytis cinerea. Plant Physiol. Biochem. 42, 367-371.
31. Glazebrook, J. (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43, 205-227.
32. Govrin, E.M. and Levine, A. (2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr. Biol. 10, 751-757.
33. Govrin, E.M. and Levine, A. (2002) Infection of Arabidopsis with a necrotrophic pathogen, Botrytis cinerea, elicits various defense responses but does not induce systemic acquired resistance (SAR). Plant Mol. Biol. 1, 267-276.
34. Greenberg, J.T. and Yao, N. (2004) The role and regulation of programmed cell death in plant-pathogen interactions. Cell. Microbiol. 6, 201-211.
35. Hoch, H.C., Galvani, C.D., Szarowski, D.H. and Turner, J.N. (2005) Two new fluorescent dyes applicable for visualization of fungal cell walls. Mycologia, 97, 580-588.
36. van Kan, J.A. (2006) Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends Plant Sci. 11, 247-253.
37. Lam, E. (2004) Controlled cell death, plant survival and development. Nat. Rev. Mol. Cell. Biol. 5, 305-315.
38. Lam, E. (2008) Programmed cell death in plants: orchestrating an intrinsic suicide program within walls. Crit. Rev. Plant Sci. 27, 413-423.
39. Lawton, M. and Saidasan, H. (2009) Pathogenesis in mosses. Annu. Plant Rev. 36, 298-339.
40. Lee, K.J.D., Knight, C.D. and Knox, J.P. (2005) Physcomitrella patens: a moss system for the study of plant cell walls. Plant Biosyst. 139, 16-19.
41. 2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell, 79, 583-593.
42. Li, W., Liu, B., Yu, L., Feng, D., Wang, H. and Wang, J. (2009) Phylogenetic analysis, structural evolution and functional divergence of the 12-oxophytodienoate acid reductase gene family in plants. BMC Evol. Biol. 9, 90.
43. Llorente, F., Muskett, P., Sánchez-Vallet, A., López, G., Ramos, B., Sánchez-Rodríguez, C., Jordá, L., Parker, J. and Molina, A. (2008) Repression of the auxin response pathway increases Arabidopsis susceptibility to necrotrophic fungi. Mol. Plant, 1, 496-509.
44. López, M.A., Bannenberg, G. and Castresana, C. (2008) Controlling hormone signaling is a plant and pathogen challenge for growth and survival. Curr. Opin. Plant Biol. 11, 420-427.
45. Lucena, M.A., Romero-Aranda, R., Mercado, J.A., Cuartero, J., Valpuesta, V. and Quesada, M.A. (2003) Structural and physiological changes in the roots of tomato plants over-expressing a basic peroxidase. Physiol. Plant. 118, 422-429.
46. Maor, R., Haskin, S., Levi-Kedmi, H. and Sharon, A. (2004) Inplanta production of indole-3-acetic acid by Colletotrichum gloeosporioides f. sp. aeschynomene. Appl. Environ. Microbiol. 70, 1852-1854.
47. 2 plays different roles in determining penetration failure in three diverse plant-fungal interactions. Plant J. 29, 257-268.
48. Morel, J.B. and Dangl, J.L. (1997) The hypersensitive response and the induction of cell death in plants. Cell Death Differ. 4, 671-683.
49. Mueller, S., Hilbert, B., Dueckershoff, K., Roitsch, T., Krischke, M., Mueller, M.J. and Berger, S. (2008) General detoxification and stress responses are mediated by oxidized lipids through TGA transcription factors in Arabidopsis. Plant Cell, 20, 768-785.
50. Nishiyama, T., Fujita, T., Shin-I, T., Seki, M., Nishide, H., Uchiyama, I., Kamiya, A., Carninci, P., Hayashizaki, Y., Shinozaki, K., Kohara, Y. and Hasebe, M. (2003) Comparative genomics of Physcomitrella patens gametophytic transcriptome and Arabidopsis thaliana: implication for land plant evolution. Proc. Natl. Acad. Sci. USA, 100, 8007-8012.
51. Oliver, J.P., Castro, A., Gaggero, C., Cascón, T., Schmelz, E.A., Castresana, C. and Ponce de León, I. (2009) Pythium infection activates conserved plant defense responses in mosses. Planta, 230, 569-579.
52. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, 45.
53. Ponce de León, I. (2011) The moss Physcomitrella patens as a model system to study interactions between plants and phytopathogenic fungi and oomycetes. J. Pathog. 2011, Article ID 719873, 6.
54. Ponce de León, I., Oliver, J.P., Castro, A., Gaggero, C., Bentancor, M. and Vidal, S. (2007) Erwinia carotovora elicitors and Botrytis cinerea activate defense responses in Physcomitrella patens. BMC Plant Biol. 8, 52.
55. Popper, Z.A. (2008) Evolution and diversity of green plant cell walls. Curr. Opin. Plant Biol. 11, 286-292.
56. Prost, I., Dhondt, S., Rothe, G., Vicente, J., Rodriguez, M.J., Kift, N., Carbonne, F., Griffiths, G., Esquerré-Tugayé, M.-T., Rosahl, S., Castresana, C., Hamberg, M. and Joëlle Fournier, J. (2005) Evaluation of the antimicrobial activities of plant oxylipins supports their involvement in defense against pathogens. Plant Physiol. 139, 1902-1913.
57. Rantakari, A., Virtaharju, O., Vähämiko, S., Taira, S., Palva, E.T., Saarilahti, H.T. and Romantschuk, M. (2001) Type III secretion contributes to the pathogenesis of the soft-rot pathogen Erwinia carotovora. Partial characterization of the hrp gene cluster. Mol. Plant-Microbe Interact. 14, 962-968.
58. Rensing, S.A., Lang, D., Zimmer, A.D., Terry, A., Salamov, A., Shapiro, H., Nishiyama, T., Perroud, P.F., Lindquist, E.A., Kamisugi, Y., Tanahashi, T., Sakakibara, K., Fujita, T., Oishi, K., Shin -I, T., Kuroki, Y., Toyoda, A., Suzuki, Y., Hashimoto, S., Yamaguchi, K., Sugano, S., Kohara, Y., Fujiyama, A., Anterola, A., Aoki, S., Ashton, N., Barbazuk, W.B., Barker, E., Bennetzen, J.L., Blankenship, R., Cho, S.H., Dutcher, S.K., Estelle, M., Fawcett, J.A., Gundlach, H., Hanada, K., Heyl, A., Hicks, K.A., Hughes, J., Lohr, M., Mayer, K., Melkozernov, A., Murata, T., Nelson, D.R., Pils, B., Prigge, M., Reiss, B., Renner, T., Rombauts, S., Rushton, P.J., Sanderfoot, A., Schween, G., Shiu, S.H., Stueber, K., Theodoulou, F.L., Tu, H., Van de Peer, Y., Verrier, P.J., Waters, E., Wood, A., Yang, L., Cove, D., Cuming, A.C., Hasebe, M., Lucas, S., Mishler, B.D., Reski, R., Grigoriev, I.V., Quatrano, R.S. and Boore, J.L. (2008) The Physcomitrella genome reveals evolutionary insights into the conquest of land by plants. Science, 4, 64-69.
59. Robert-Seilaniantz, A., Navarro, L., Bari, R. and Jones, J.D. (2007) Pathological hormone imbalances. Curr. Opin. Plant Biol. 10, 372-379.
60. Robert-Seilaniantz, A., Grant, M. and Jones, J.D. (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu. Rev. Phytopathol. 8, 317-343.
61. Schaefer, D., Zrÿd, J.P., Knight, C.D. and Cove, D.J. (1991) Stable transformation of the moss Physcomitrella patens. Mol. Gen. Genet. 226, 418-424.
62. Schaefer, D.G. (2002) A new moss genetics: targeted mutagenesis in Physcomitrella patens. Annu. Rev. Plant Biol. 53, 477-501.
63. Schaefer, D.G. and Zrÿd, J.P. (2001) The moss Physcomitrella patens, now and then. Plant Physiol. 127, 1430-1438.
64. Schmelz, E.A., Engelberth, J., Tumlinson, J.H., Block, A. and Alborn, H.T. (2004) The use of vapor phase extraction in metabolic profiling of phytohormones and other metabolites. Plant J. 39, 790-808.
65. Siewers, V., Smedsgaard, J. and Tudzynski, P. (2004) The P450 monooxygenase BcABA1 is essential for abscisic acid biosynthesis in Botrytis cinerea. Appl. Environ. Microbiol. 70, 3868-3876.
66. Staswick, P.E., Su, W.P. and Howell, S.H. (1992) Methyl jasmonate inhibition of root-growth and induction of a leaf protein are decreased in an Arabidopsis thaliana mutant. Proc. Natl. Acad. Sci. USA, 89, 6837-6840.
67. Stintzi, A., Weber, H., Reymond, P., Browse, J. and Farmer, E.E. (2001) Plant defense in the absence of jasmonic acid: the role of cyclopentenones. Proc. Natl. Acad. Sci. USA, 98, 12837-12842.
68. Stumpe, M., Göbel, C., Faltin, B., Beike, A.K., Hause, B., Himmelsbach, K., Bode, J., Kramell, R., Wasternack, C., Frank, W., Reski, R. and Feussner, I. (2010) The moss Physcomitrella patens contains cyclopentenones but no jasmonates: mutations in allene oxide cyclase lead to reduced fertility and altered sporophyte morphology. New Phytol. 188, 740-749.
69. Swiatek, A., Lenjou, M., Van Bockstaele, D., Inze, D. and Van Onckelen, H. (2002) Differential effect of jasmonic acid and abscisic acid on cell cycle progression in tobacco BY-2 cells. Plant Physiol. 128, 201-211.
70. Taki, N., Sasaki-Sekimoto, Y., Obayashi, T., Kikuta, A., Kobayashi, K., Ainai, T., Yagi, K., Sakurai, N., Suzuki, H., Masuda, T., Takamiya, K., Shibata, D., Kobayashi, Y. and Ohta, H. (2005) 12-Oxo-phytodienoic acid triggers expression of a distinct set of genes and plays a role in wound-induced gene expression in Arabidopsis. Plant Physiol. 139, 1268-1283.
71. Tanaka, E., Koga1, H., Mori, M. and Mori, M. (2011) Auxin production by the rice blast fungus and its localization in host tissue. J. Phytopathol. 159, 522-530.
72. Ton, J., Flors, V. and Mauch-Mani, B. (2009) The multifaceted role of ABA in disease resistance. Trends Plant Sci. 14, 310-317.
73. Vellosillo, T., Martinez, M., Lopez, M.A., Vicente, J., Cascon, T., Dolan, L., Hamberg, M. and Castresana, C. (2007) Oxylipins produced by the 9-lipoxygenase pathway in Arabidopsis regulate lateral root development and defense responses through a specific signaling cascade. Plant Cell, 19, 831-846.
74. Veronese, P., Nakagami, H., Bluhm, B., Abuqamar, S., Chen, X., Salmeron, J., Dietrich, R.A., Hirt, H. and Mengiste, T. (2006) The membrane-anchored Botrytis-induced kinase1 plays distinct roles in Arabidopsis resistance to necrotrophic and biotrophic pathogens. Plant Cell, 18, 257-273.
75. Vicedo, B., Flors, V., de la O Leyva, M., Finiti, I., Kravchuk, Z., Real, M.D., García-Agustín, P. and González-Bosch, C. (2009) Hexanoic acid-induced resistance against Botrytis cinerea in tomato plants. Mol. Plant-Microbe Interact. 22, 1455-1465.
76. Vidal, S., Ponce de León, I., Denecke, J. and Palva, E.T. (1997) Salicylic acid and the plant pathogen Erwinia carotovora induce defense genes via antagonistic pathways. Plant J. 11, 115-123.
77. Wang, D., Pajerowska-Mukhtar, K., Culler, A.H. and Dong, X. (2007) Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Curr. Biol. 17, 1784-1790.
78. Wang, Y., Nowak, G., Culley, D., Hadwiger, L.A. and Fristensky, B. (1999) Constitutive expression of pea defense gene DRR206 confers resistance to blackleg (Leptosphaeria maculans) disease in transgenic canola (Brassica napus). Mol. Plant-Microbe Interact. 12, 410-418.
79. Wang, Y.P. and Fristensky, B. (2001) Transgenic canola lines expressing pea defense gene DRR206 have resistance to aggressive blackleg isolates and to Rhizoctonia solani. Mol. Breed. 8, 263-271.
80. Wolf, L., Rizzini, L., Stracke, R., Ulm, R. and Rensing, S.A. (2010) The molecular and physiological responses of Physcomitrella patens to ultraviolet-B radiation. Plant Physiol. 153, 1123-1134.
81. Xu, Z., Zhang, D., Hu, J., Zhou, X., Ye, X., Reichel, K.L., Stewart, N.R., Syrenne, R.D., Yang, X., Gao, P., Shi, W., Doeppke, C., Sykes, R.W., Burris, J.N., Bozell, J.J., Cheng, M.Z., Hayes, D.G., Labbe, N., Davis, M., Stewart, C.N. Jr. and Yuan, J.S. (2009) Comparative genome analysis of lignin biosynthesis gene families across the plant kingdom. BMC Bioinformatics, 10, S3.
82. Yan, Y., Stolz, S., Chételat, A., Reymond, P., Pagni, M., Dubugnon, L. and Farmer, E.E. (2007) A downstream mediator in the growth repression limb of the jasmonate pathway. Plant Cell, 19, 2470-2483.
83. Yang, W., Devaiah, S.P., Pan, X., Isaac, G., Welti, R. and Wang, X. (2007) AtPLAI is an acyl hydrolase involved in basal jasmonic acid production and Arabidopsis resistance to Botrytis cinerea. J. Biol. Chem. 22, 18116-18128.
84. Yasuda, M., Ishikawa, A., Jikumaru, Y., Seki, M., Umezawa, T., Asami, T., Maruyama-Nakashita, A., Kudo, T., Shinozaki, K., Yoshida, S. and Nakashita, H. (2008) Antagonistic interaction between systemic acquired resistance and the abscisic acid-mediated abiotic stress response in Arabidopsis. Plant Cell, 20, 1678-1692.