Erwinia carotovora elicitors and Botrytis cinerea activate defense responses in Physcomitrella patens
Tóm tắt
Vascular plants respond to pathogens by activating a diverse array of defense mechanisms. Studies with these plants have provided a wealth of information on pathogen recognition, signal transduction and the activation of defense responses. However, very little is known about the infection and defense responses of the bryophyte, Physcomitrella patens, to well-studied phytopathogens. The purpose of this study was to determine: i) whether two representative broad host range pathogens, Erwinia carotovora ssp. carotovora (E.c. carotovora) and Botrytis cinerea (B. cinerea), could infect Physcomitrella, and ii) whether B. cinerea, elicitors of a harpin (HrpN) producing E.c. carotovora strain (SCC1) or a HrpN-negative strain (SCC3193), could cause disease symptoms and induce defense responses in Physcomitrella. B. cinerea and E.c. carotovora were found to readily infect Physcomitrella gametophytic tissues and cause disease symptoms. Treatments with B. cinerea spores or cell-free culture filtrates from E.c. carotovoraSCC1 (CF(SCC1)), resulted in disease development with severe maceration of Physcomitrella tissues, while CF(SCC3193) produced only mild maceration. Although increased cell death was observed with either the CFs or B. cinerea, the occurrence of cytoplasmic shrinkage was only visible in Evans blue stained protonemal cells treated with CF(SCC1) or inoculated with B. cinerea. Most cells showing cytoplasmic shrinkage accumulated autofluorescent compounds and brown chloroplasts were evident in a high proportion of these cells. CF treatments and B. cinerea inoculation induced the expression of the defense-related genes: PR-1, PAL, CHS and LOX. B. cinerea and E.c. carotovora elicitors induce a defense response in Physcomitrella, as evidenced by enhanced expression of conserved plant defense-related genes. Since cytoplasmic shrinkage is the most common morphological change observed in plant PCD, and that harpins and B. cinerea induce this type of cell death in vascular plants, our results suggest that E.c. carotovora CFSCC1 containing HrpN and B. cinerea could also induce this type of cell death in Physcomitrella. Our studies thus establish Physcomitrella as an experimental host for investigation of plant-pathogen interactions and B. cinerea and elicitors of E.c. carotovora as promising tools for understanding the mechanisms involved in defense responses and in pathogen-mediated cell death in this simple land plant.
Tài liệu tham khảo
Lee HI, Leon J, Raskin I: Biosynthesis and metabolism of salicylic acid. Proc Natl Acad Sci USA. 1995, 92 (10): 4076-4079. 10.1073/pnas.92.10.4076.
Creelman RA, Mullet JE: Biosynthesis and action of jasmonates in plants. Annu Rev Plant Physiol Plant Mol Biol. 1997, 48: 355-381. 10.1146/annurev.arplant.48.1.355.
Enyedi AJ, Yalpani N, Silverman P, Raskin I: Signal molecules in systemic plant resistance to pathogens and pests. Cell. 1992, 70 (6): 879-886. 10.1016/0092-8674(92)90239-9.
Linthorst HJM: Pathogenesis-related proteins of plants. Crit Rev Plant Sci. 1991, 10: 123-150.
Dixon RA, Paiva NL: Stress-induced phenylpropanoid metabolism. Plant Cell. 1995, 7 (7): 1085-1097. 10.1105/tpc.7.7.1085.
Goodman RN, Novacky AJ: The Hypersensitive Reaction in Plants to Pathogens: A Resistance Phenomenon. St. Paul: American Phytopathological Society Press 1994.
Dangl JL, Dietrich RA, Richberg MH: Death don't have no mercy: Cell death programs in plant-microbe interactions. Plant Cell. 1996, 8 (10): 1793-1807. 10.1105/tpc.8.10.1793.
Dangl JL, Jones JD: Plant pathogens and integrated defence responses to infection. Nature. 2001, 411 (6839): 826-833. 10.1038/35081161.
Nimchuk Z, Eulgem T, Holt IB, Dangl JL: Recognition and response in the plant immune system. Annu Rev Genet. 2003, 37: 579-609. 10.1146/annurev.genet.37.110801.142628.
Greenberg JT: Programmed cell death in plant-pathogen interactions. Annu Rev Plant Physiol Plant Mol Biol. 1997, 48: 525-545. 10.1146/annurev.arplant.48.1.525.
Lam E, Kato N, Lawton M: Programmed cell death, mitochondria and the plant hypersensitive response. Nature. 2001, 411: 848-853. 10.1038/35081184.
Wang H, Li J, Bostock RM, Gilchrist DG: Apoptosis: A functional paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during development. Plant Cell. 1996, 8 (3): 375-391. 10.1105/tpc.8.3.375.
Greenberg JT, Yao N: The role and regulation of programmed cell death in plant-pathogen interactions. Cell Microbiol. 2004, 6 (3): 201-211. 10.1111/j.1462-5822.2004.00361.x.
Heckman DS, Geiser DM, Eidell BR, Stauffer RL, Kardos NL, Hedges SB: Molecular evidence for the early colonization of land by fungi and plants. Science. 2001, 293 (5532): 1129-1133. 10.1126/science.1061457.
Cove D, Benzanilla M, Harries P, Quatrano R: Mosses as model systems for the study of metabolism and development. Annu Rev Plant Biol. 2006, 57: 497-520. 10.1146/annurev.arplant.57.032905.105338.
Schaefer DG, Zrÿd JP: The moss Physcomitrella patens, now and then. Physcomitrella patens. 2001, 127 (4): 1430-1438.
Schaefer DG: A new moss genetics: targeted mutagenesis in Physcomitrella patens. Annu Rev Plant Biol. 2002, 53: 477-501. 10.1146/annurev.arplant.53.100301.135202.
Quatrano RS, McDaniel SF, Khandelwal A, Perroud PF, Cove DJ: Physcomitrella patens: mosses enter the genomic age. Current Opinion in Plant Biology. 2007, 10: 182-189. 10.1016/j.pbi.2007.01.005.
Nishiyama T, Fujita T, Shin-I T, Seki M, Nishide H, Uchiyama I, Kamiya A, Carninci P, Hayashizaki Y, Shinozaki K, Kohara Y, Hasebe M: Comparative genomics of Physcomitrella patens gametophytic transcriptome and Arabidopsis thaliana: implication for land plant evolution. Proc Natl Acad Sci USA. 2003, 100 (13): 8007-8012. 10.1073/pnas.0932694100.
Lang D, Eisinger J, Reski R, Rensing SA: Representation and high-quality annotation of the Physcomitrella patens transcriptome demonstrates a high proportion of proteins involved in metabolism in mosses. Plant Biology. 2005, 7 (3): 238-250. 10.1055/s-2005-837578.
Reski R: Physcomitrella and Arabidopsis: the David and Goliath of reverse genetics. Trends Plant Sci. 1998, 3: 209-210. 10.1016/S1360-1385(98)01257-6.
Akita M, Valkonen JP: A novel gene family in moss (Physcomitrella patens) shows sequence homology and a phylogenetic relationship with the TIR-NBS class of plant disease resistance genes. J Mol Evol. 2002, 55 (5): 595-605. 10.1007/s00239-002-2355-8.
Tsuneda A, Chen MH, Currah RS: Characteristics of a disease of Spagnum fuscum caused by Scleroconidioma sphagnicola. Can J Bot. 2001, 79: 1217-1224. 10.1139/cjb-79-10-1217.
Polischuk V, Budzanivska I, Shevchenko T, Oliynik S: Evidence for plant viruses in the region of Argentina islands, Antartica. FEMS Microbiol Ecol. 2007, 59: 409-417.
Pérombelon MCM, Kelman A: Ecology of the soft-rot Erwinia. Annu Rev Phytopathol. 1980, 12: 361-387. 10.1146/annurev.py.18.090180.002045.
Toth IK, Bell KS, Holeva MC, Birch PRJ: Soft rot erwiniae: From genes to genomes. Mol Plant Pathol. 2003, 4 (1): 17-30. 10.1046/j.1364-3703.2003.00149.x.
Collmer A, Keen NT: The role of pectic enzymes in plant pathogenesis. Annu Rev Phytopathol. 1986, 24: 383-409. 10.1146/annurev.py.24.090186.002123.
Palva TK, Holmström KO, Heino P, Palva ET: Induction of plant defense response by exoenzymes of Erwinia carotovora ssp. carotovora. Mol Plant-Microbe Interact. 1993, 6 (2): 190-196.
Vidal S, Ponce de León I, Denecke J, Palva ET: Salicylic acid and the plant pathogen Erwinia carotovora induce defense genes via antagonistic pathways. Plant J. 1997, 11 (1): 115-123. 10.1046/j.1365-313X.1997.11010115.x.
Vidal S, Eriksson ARB, Montesano M, Denecke J, Palva ET: Cell wall-degrading enzymes from Erwinia carotovora cooperate in the salicylic acid-independent induction of a plant defense response. Mol Plant-Microbe Interact. 1998, 11 (1): 23-32. 10.1094/MPMI.1998.11.1.23.
Montesano M, Brader G, Ponce de Leon I, Palva ET: Multiple defense signals induced by Erwinia carotovora ssp. carotovora in potato. Molecular Plant Pathol. 2005, 6 (5): 541-549. 10.1111/j.1364-3703.2005.00305.x.
Norman C, Vidal S, Palva ET: Interacting signal pathways control defense gene expression in Arabidopsis in response to the plant pathogen Erwinia carotovora. Mol Plant-Microbe Interact. 2000, 13 (4): 430-438. 10.1094/MPMI.2000.13.4.430.
Desikan R, Reynolds A, Hancock JT, Neill SJ: Harpin and hydrogen peroxide both initiate programmed cell death but have differential effects on defense gene expression in Arabidopsis suspension cultures. Biochem J. 1998, 330: 115-120.
Krause M, Durner J: Harpin inactivates mitochondria in Arabidopsis suspension cells. Mol Plant-Microbe Interact. 2004, 17 (2): 131-139. 10.1094/MPMI.2004.17.2.131.
Rantakari A, Virtaharju O, Vähämiko S, Taira S, Palva ET, Saarilahti HT, Romantschuk M: 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. 2001, 14 (8): 962-968. 10.1094/MPMI.2001.14.8.962.
Mattinen L, Tshuikina M, Mäe A, Pirhonen M: Identification and characterization of Nip, necrosis-inducing virulence protein of Erwinia carotovora subsp. carotovora. Mol Plant-Microbe Interact. 2004, 17 (12): 1366-1375. 10.1094/MPMI.2004.17.12.1366.
Elad Y, Williamson B, Tudzynski P, Delen N: Botrytis: Biology, Pathology and Control. Dordrecht Kluwer Academic Publishers 2004.
van Kan JAL: Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends in Plant Sci. 2006, 11 (5): 247-253. 10.1016/j.tplants.2006.03.005.
Reino JL, Hernández-Galán R, Durán-Patrón R, Collado IG: Virulence-toxin production relationship in isolates of the plant pathogenic fungus Botrytis cinerea. J Phytopathol. 2004, 152: 563-566. 10.1111/j.1439-0434.2004.00896.x.
Kars I, Geja H, Krooshof GH, Wagemakers L, Joosten R, Benen JAE, van Kan JAL: Necrotising activity of five Botrytis cinerea endopolygalacturonases produced in Pichia pastoris. Plant J. 2005, 43 (2): 213-225. 10.1111/j.1365-313X.2005.02436.x.
Brito N, Espino JJ, Gonzalez C: The endo-beta-1,4-xylanase xyn11A is required for virulence in Botrytis cinerea. Mol Plant-Microbe Interact. 2006, 19 (1): 25-32. 10.1094/MPMI-19-0025.
Mittler R, Simon L, Lam E: Pathogen-induced programmed cell death in tobacco. J Cell Science. 1997, 110: 1333-1344.
Bestwick CS, Bennett MH, Mansfield JW: Hrp mutant of Pseudomonas syringae pv phaseolicola induces cell wall alterations but not membrane damage leading to the hypersensitive reaction in lettuce (Lactuca sativa). Plant Physiol. 1995, 108 (2): 503-516.
Bennett M, Gallagher M, Fagg J, Bestwick C, Paule T, Beale M, Mansfield J: The hypersensitive reaction, membrane damage, and accumulation of autofluorescent phenolics in lettuce cells challenged by Bremia lactucae. Plant J. 1996, 9 (6): 851-865. 10.1046/j.1365-313X.1996.9060851.x.
Gaff DF, Okong'o-Ogola O: The use of nonpermeating pigments for testing the survival of cells. J Exp Bot. 1971, 22: 756-758. 10.1093/jxb/22.3.756.
Feussner I, Wasternack C: The lipoxygenase pathway. Annu Rev Plant Biol. 2002, 53: 275-297. 10.1146/annurev.arplant.53.100301.135248.
Hahlbrock K, Scheel D: Physiology and molecular biology of phenylpropenoid metabolism. Annu Rev Plant Physiol Plant Mol Biol. 1989, 40: 347-369. 10.1146/annurev.pp.40.060189.002023.
Davey ML, Currah RS: Interactions between mosses (Bryophyta) and fungi. Can J Bot. 2006, 84: 1509-1519. 10.1139/B06-120.
He SY, Huang HC, Collmer A: Pseudomonas syringae pv. syringae harpinPss: a protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants. Cell. 1993, 2 (7): 1255-66. 10.1016/0092-8674(93)90354-S.
Wei ZM, Laby RJ, Zumoff CH, Bauer DW, He SY, Collmer A, Beer SV: Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science. 1992, 257 (5066): 85-88. 10.1126/science.1621099.
Yang CH, Gavilanes-Ruiz M, Okinaka Y, Vedel R, Berthuy L, Boccara M, Chen JW, Perna NT, Keen NT: hrp genes of erwinia chrysanthemi 3937 are important virulence factors. Mol Plant-Microbe Interact. 2002, 15 (5): 472-480. 10.1094/MPMI.2002.15.5.472.
Kariola T, Palomäki TA, Brader G, Palva ET: Erwinia carotovora subsp. carotovora and Erwinia -derived elicitors HrpN and PehA trigger distinct but interacting defense responses and cell death in Arabidopsis. Mol Plant-Microbe Interact. 2003, 16 (3): 179-187. 10.1094/MPMI.2003.16.3.179.
Levine A, Pennell RI, Alvarez ME, Palmer R, Lamb C: Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Curr Biol. 1996, 6: 427-437. 10.1016/S0960-9822(02)00510-9.
Morel J.-B, Dangl JL: The hypersensitive response and the induction of cell death in plants. Cell Death Differ. 1997, 4: 671-683. 10.1038/sj.cdd.4400309.
de Pinto MC, Paradiso A, Leonetti P, De Gara L: Hydrogen peroxide, nitric oxide and cytosolic ascorbate peroxidase at the crossroad between defence and cell death. Plant J. 2006, 48 (5): 784-95. 10.1111/j.1365-313X.2006.02919.x.
Yoshinaga K, Arimura SI, Hirata A, Niwa Y, Yun DJ, Tsutsumi N, Uchimiya H, Kawai-Yamada M: Mammalian Bax initiates plant cell death through organelle destruction. Plant Cell Rep. 2005, 24 (7): 408-17. 10.1007/s00299-005-0948-6.
Yao N, Tada Y, Park P, Nakayashiki H, Tosa Y, Mayama S: Novel evidence for apoptotic cell response and differential signals in chromatin condensation and DNA cleavage in victorin-treated oats. Plant J. 2001, 28 (1): 13-26. 10.1046/j.1365-313X.2001.01109.x.
Navarre DA, Wolpert TJ: Victorin induction of an apoptotic, senescence-like response in oats. Plant Cell. 1999, 11 (2): 237-250. 10.1105/tpc.11.2.237.
Keates SE, Kostman TA, Anderson JD, Bailey BA: Altered gene expression in three plant species in response to treatment with Nep1, a fungal protein that cause necrosis. Plant Physiol. 2003, 132 (3): 1610-1622. 10.1104/pp.102.019836.
Kariola T, Brader G, Li J, Palva ET: Chlorophyllase 1, a damage control enzyme, affects the balance between defense pathways in plants. Plant Cell. 2005, 17 (1): 282-294. 10.1105/tpc.104.025817.
Govrin EM, Levine A: The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea . Curr Biol. 2000, 10 (13): 751-757. 10.1016/S0960-9822(00)00560-1.
Jiang C, Schommer CK, Kim SY, Suh D-Y: Cloning and characterization of chalcone synthase from the moss, Physcomitrella patens . Phytochem. 2000, 67 (23): 2531-2540. 10.1016/j.phytochem.2006.09.030.
Senger T, Wichard T, Kunze S, Gobel C, Lerchl J, Pohnert G, Feussner I: A multifunctional lipoxygenase with fatty acid hydroperoxide cleaving activity from the moss Physcomitrella patens. J Biol Chem. 2005, 280 (9): 7588-7596. 10.1074/jbc.M411738200.
Aguilar I, Poza-Carrin C, Gui A, Rodrguez-Palenzuela P: Erwinia chrysanthemi genes specifically induced during infection in chicory leaves. Mol Plant Pathol. 2002, 3 (4): 271-275. 10.1046/j.1364-3703.2002.00118.x.
Vidal S: Molecular Defense responses against the plant pathogen Erwinia carotovora. Signal pathways in the regulation of pathogen-induced gene expression in plants. PhD thesis. 1998, Swedish University of Agricultural Sciences, Department of Plant Biology
Govrin EM, Levine A: Infection of Arabidopsis with a necrotrophic pathogen, Botrytis cinerea, elicits various defense responses but does not induce systemic acquired resistance (SAR). Plant Mol Biol. 2002, 48: 267-276. 10.1023/A:1013323222095.
Ferrari S, Plotnikova JM, De Lorenzo G, Ausubel FM: Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. Plant J. 2003, 35 (2): 193-205. 10.1046/j.1365-313X.2003.01794.x.
Schaefer D, Zryd JP, Knight CD, Cove DJ: Stable transformation of the moss Physcomitrella patens . Mol Gen Genet. 1991, 226: 418-424.
Ashton NW, Cove DJ: The isolation and preliminary characterization of auxotrophic and analogue resistant mutants in the moss Physcomitrella patens . Mol Gen Genet. 1977, 154: 87-95. 10.1007/BF00265581.
Saavedra L, Svensson J, Carballo V, Izmendi D, Welin B, Vidal S: A dehydrin gene in Physcomitrella patens is required for salt and osmotic stress tolerance. Plant J. 2006, 45 (2): 237-249. 10.1111/j.1365-313X.2005.02603.x.
Pirhonen M, Heino P, Helander I, Harju P, Palva ET: Bacteriophage T4-resistant mutants of the plant pathogen Erwinia carotovora . Microbe Pathog. 1988, 4: 359-367. 10.1016/0882-4010(88)90063-0.
Saarilahti HT, Palva ET: Major outer membrane proteins in the phytopathogenic bacteria Erwinia carotovora subsp. carotovora and subsp. atroseptica . FEMS Microbiol Lett. 1986, 35: 267-270. 10.1111/j.1574-6968.1986.tb01540.x.
Miller JH: Experiments in Molecular genetics. 1972, Cold Spring Harbor, Cold Spring Harbor Press
Koch E, Slusarenko A: Arabidopsis is susceptible to infection by downy mildew fungus. Plant Cell. 1990, 2: 437-455. 10.1105/tpc.2.5.437.
Dietrich RA, Delaney TP, Uknes SJ, Ward ER, Ryals JA, et al: Arabidopsis mutants simulating disease resistance response. Cell. 1994, 77: 565-577. 10.1016/0092-8674(94)90218-6.
Sambrook J, Fitsch EF, Maniatis T: Molecular Cloning: A Laboratory Manual. 1989, Cold Spring Harbor, Cold Spring Harbor Press