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PLOS ONE 2013

Dynamics of Defense Responses and Cell Fate Change during Arabidopsis-Pseudomonas syringae Interactions

DOI: 10.1371/journal.pone.0083219

Safae Hamdoun, Zhe Liu, Manroop Gill, Nan Yao, Hua Lu

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Abstract:

Plant-pathogen interactions involve sophisticated action and counteraction strategies from both parties. Plants can recognize pathogen derived molecules, such as conserved pathogen associated molecular patterns (PAMPs) and effector proteins, and subsequently activate PAMP-triggered immunity (PTI) and effector-triggered immunity (ETI), respectively. However, pathogens can evade such recognitions and suppress host immunity with effectors, causing effector-triggered susceptibility (ETS). The differences among PTI, ETS, and ETI have not been completely understood. Toward a better understanding of PTI, ETS, and ETI, we systematically examined various defense-related phenotypes of Arabidopsis infected with different Pseudomonas syringae pv. maculicola ES4326 strains, using the virulence strain DG3 to induce ETS, the avirulence strain DG34 that expresses avrRpm1 (recognized by the resistance protein RPM1) to induce ETI, and HrcC- that lacks the type three secretion system to activate PTI. We found that plants infected with different strains displayed dynamic differences in the accumulation of the defense signaling molecule salicylic acid, expression of the defense marker gene PR1, cell death formation, and accumulation/localization of the reactive oxygen species, H2O2. The differences between PTI, ETS, and ETI are dependent on the doses of the strains used. These data support the quantitative nature of PTI, ETS, and ETI and they also reveal qualitative differences between PTI, ETS, and ETI. Interestingly, we observed the induction of large cells in the infected leaves, most obviously with HrcC- at later infection stages. The enlarged cells have increased DNA content, suggesting a possible activation of endoreplication. Consistent with strong induction of abnormal cell growth by HrcC-, we found that the PTI elicitor flg22 also activates abnormal cell growth, depending on a functional flg22-receptor FLS2. Thus, our study has revealed a comprehensive picture of dynamic changes of defense phenotypes and cell fate determination during Arabidopsis-P. syringae interactions, contributing to a better understanding of plant defense mechanisms.

References

[1]	Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11: 539-548. doi:10.1038/nrm2939. PubMed: 20585331.
[2]	Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60: 379-406. doi:10.1146/annurev.arplant.57.032905.105346. PubMed: 19400727.
[3]	Jones JD, Dangl JL (2006) The plant immune system. Nature 444: 323-329. doi:10.1038/nature05286. PubMed: 17108957.
[4]	Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD et al. (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428: 764-767. doi:10.1038/nature02485. PubMed: 15085136.
[5]	Gómez-Gómez L, Felix G, Boller T (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J 18: 277-284. doi:10.1046/j.1365-313X.1999.00451.x. PubMed: 10377993.
[6]	Mudgett MB (2005) New insights to the function of phytopathogenic bacterial type III effectors in plants. Annu Rev Plant Biol 56: 509-531. doi:10.1146/annurev.arplant.56.032604.144218. PubMed: 15862106.
[7]	Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Phytopathol 42: 185-209. doi:10.1146/annurev.phyto.42.040803.140421. PubMed: 15283665.
[8]	Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY et al. (1996) Systemic acquired resistance. Plant Cell 8: 1809-1819. doi:10.2307/3870231. PubMed: 12239363.
[9]	Maleck K, Levine A, Eulgem T, Morgan A, Schmid J et al. (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26: 403-410. doi:10.1038/82521. PubMed: 11101835.
[10]	Tao Y, Xie Z, Chen W, Glazebrook J, Chang HS et al. (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15: 317-330. doi:10.1105/tpc.007591. PubMed: 12566575.
[11]	Wang D, Amornsiripanitch N, Dong X (2006) A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathog 2: e123. doi:10.1371/journal.ppat.0020123. PubMed: 17096590.
[12]	Scheideler M, Schlaich NL, Fellenberg K, Beissbarth T, Hauser NC et al. (2002) Monitoring the switch from housekeeping to pathogen defense metabolism in Arabidopsis thaliana using cDNA arrays. J Biol Chem 277: 10555-10561. doi:10.1074/jbc.M104863200. PubMed: 11748215.
[13]	Thilmony R, Underwood W, He SY (2006) Genome-wide transcriptional analysis of the Arabidopsis thaliana interaction with the plant pathogen Pseudomonas syringae pv. tomato DC3000 and the human pathogen Escherichia coli O157:H7. Plant J 46: 34-53. doi:10.1111/j.1365-313X.2006.02725.x. PubMed: 16553894.
[14]	Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414: 562-565. doi:10.1038/35107108. PubMed: 11734859.
[15]	Cao H, Glazebrook J, Clarke JD, Volko S, Dong X (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88: 57-63. doi:10.1016/S0092-8674(00)81858-9. PubMed: 9019406.
[16]	Shah J, Tsui F, Klessig DF (1997) Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA- inducible expression of the tms2 gene. Mol Plant Microbe Interact 10: 69-78. doi:10.1094/MPMI.1997.10.1.69. PubMed: 9002272.
[17]	Ryals J, Weymann K, Lawton K, Friedrich L, Ellis D et al. (1997) The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor I kappa B. Plant Cell 9: 425-439. doi:10.1105/tpc.9.3.425. PubMed: 9090885.
[18]	Metraux JP, Ahl-Goy P, Staub T, Speich J, Steinemann A et al. (1991) Induced resistance in cucumber in response to 2,6-dichloroisonicotinic acid and pathogens; H. HeneckeDPS Verma. Dordrecht, The Netherlands: Kluwer Academic Publishers.
[19]	Friedrich L, Lawton K, Wilhelm R, Masner P, Specker N et al. (1996) A benzothiadiazole derivative induces systemic acquired resistance. Plant J 10: 61-70. doi:10.1046/j.1365-313X.1996.10010061.x.
[20]	Lawton KA, Friedrich L, Hunt M, Weymann K, Delaney T et al. (1996) Benzothiadiazole induces disease resistance in Arabidopsis by activation of the systemic acquired resistance signal transduction pathway. Plant J 10: 71-82. doi:10.1046/j.1365-313X.1996.10010071.x. PubMed: 8758979.
[21]	Torres MA, Jones JD, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141: 373-378. doi:10.1104/pp.106.079467. PubMed: 16760490.
[22]	Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48: 251-275. doi:10.1146/annurev.arplant.48.1.251. PubMed: 15012264.
[23]	de Almeida Engler J, De Vleesschauwer V, Burssens S, Celenza JL Jr., Inzé D et al. (1999) Molecular markers and cell cycle inhibitors show the importance of cell cycle progression in nematode-induced galls and syncytia. Plant Cell 11: 793-808. doi:10.2307/3870815. PubMed: 10330466.
[24]	Chandran D, Inada N, Hather G, Kleindt CK, Wildermuth MC (2010) Laser microdissection of Arabidopsis cells at the powdery mildew infection site reveals site-specific processes and regulators. Proc Natl Acad Sci U S A 107: 460-465. PubMed: 20018666.
[25]	Braun AC (1956) The activation of two growth-substance systems accompanying the conversion of normal to tumor cells in crown gall. Cancer Res 16: 53-56. PubMed: 13284730.
[26]	Chalupowicz L, Barash I, Schwartz M, Aloni R, Manulis S (2006) Comparative anatomy of gall development on Gypsophila paniculata induced by bacteria with different mechanisms of pathogenicity. Planta 224: 429-437. doi:10.1007/s00425-006-0229-9. PubMed: 16477460.
[27]	Marois E, Van den Ackerveken G, Bonas U (2002) The Xanthomonas type III effector protein AvrBs3 modulates plant gene expression and induces cell hypertrophy in the susceptible host. Mol Plant Microbe Interact 15: 637-646. doi:10.1094/MPMI.2002.15.7.637. PubMed: 12118879.
[28]	Wang GF, Seabolt S, Hamdoun S, Ng G, Park J et al. (2011) Multiple roles of WIN3 in regulating disease resistance, cell death, and flowering time in Arabidopsis. Plant Physiol 156: 1508-1519. doi:10.1104/pp.111.176776. PubMed: 21543726.
[29]	Wang GY, Shi JL, Ng G, Battle SL, Zhang C et al. (2011) Circadian clock-regulated phosphate transporter PHT4;1 plays an important role in Arabidopsis Defense. Mol Plant 4: 516-526. doi:10.1093/mp/ssr016. PubMed: 21447757.
[30]	Lu H, Rate DN, Song JT, Greenberg JT (2003) ACD6, a novel ankyrin protein, is a regulator and an effector of salicylic acid signaling in the Arabidopsis defense response. Plant Cell 15: 2408-2420. doi:10.1105/tpc.015412. PubMed: 14507999.
[31]	Guttman DS, Vinatzer BA, Sarkar SF, Ranall MV, Kettler G et al. (2002) A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science 295: 1722-1726. doi:10.1126/science.295.5560.1722. PubMed: 11872842.
[32]	Lu H, Zhang C, Albrecht U, Shimizu R, Wang G et al. (2013) Overexpression of a citrus NDR1 ortholog increases disease resistance in Arabidopsis. Front - Plant Sci 4: 157. PubMed: 23761797.
[33]	Ng G, Seabolt S, Zhang C, Salimian S, Watkins TA et al. (2011) Genetic dissection of salicylic acid-mediated defense signaling networks in Arabidopsis. Genetics 189: 851-859. doi:10.1534/genetics.111.132332. PubMed: 21900271.
[34]	Lu H, Salimian S, Gamelin E, Wang G, Fedorowski J et al. (2009) Genetic analysis of acd6-1 reveals complex defense networks and leads to identification of novel defense genes in Arabidopsis. Plant J 58: 401-412. doi:10.1111/j.1365-313X.2009.03791.x. PubMed: 19144005.
[35]	Ruzin SE (1999) Plant Microtechnique and Microscopy. New York: Oxford University Press.
[36]	Vanacker H, Lu H, Rate DN, Greenberg JT (2001) A role for salicylic acid and NPR1 in regulating cell growth in Arabidopsis. Plant J 28: 209-216. doi:10.1046/j.1365-313X.2001.01158.x. PubMed: 11722764.
[37]	Kasili R, Walker JD, Simmons LA, Zhou J, De Veylder L et al. (2010) SIAMESE cooperates with the CDH1-like protein CCS52A1 to establish endoreplication in Arabidopsis thaliana trichomes. Genetics 185: 257-268. doi:10.1534/genetics.109.113274. PubMed: 20194967.
[38]	Bestwick CS, Brown IR, Bennett MH, Mansfield JW (1997) Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv phaseolicola. Plant Cell 9: 209-221. doi:10.1105/tpc.9.2.209. PubMed: 9061952.
[39]	Yao N, Tada Y, Sakamoto M, Nakayashiki H, Park P et al. (2002) Mitochondrial oxidative burst involved in apoptotic response in oats. Plant J 30: 567-579. doi:10.1046/j.1365-313X.2002.01314.x. PubMed: 12047631.
[40]	Grant MR, Godiard L, Straube E, Ashfield T, Lewald J et al. (1995) Structure of the Arabidopsis RPM1 gene enabling dual specificity disease resistance. Science 269: 843-846. doi:10.1126/science.7638602. PubMed: 7638602.
[41]	Alfano JR, Charkowski AO, Deng WL, Badel JL, Petnicki-Ocwieja T et al. (2000) The Pseudomonas syringae Hrp pathogenicity island has a tripartite mosaic structure composed of a cluster of type III secretion genes bounded by exchangeable effector and conserved effector loci that contribute to parasitic fitness and pathogenicity in plants. Proc Natl Acad Sci U S A 97: 4856-4861. doi:10.1073/pnas.97.9.4856. PubMed: 10781092.
[42]	Tsuda K, Glazebrook J, Katagiri F (2008) The interplay between MAMP and SA signaling. Plant Signal Behav 3: 359-361. doi:10.4161/psb.3.6.5702. PubMed: 19513222.
[43]	Wang L, Tsuda K, Sato M, Cohen JD, Katagiri F et al. (2009) Arabidopsis CaM binding protein CBP60g contributes to MAMP-induced SA accumulation and is involved in disease resistance against Pseudomonas syringae. PLoS Pathog 5: e1000301. PubMed: 19214217.
[44]	Hauck P, Thilmony R, He SY (2003) A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc Natl Acad Sci U S A 100: 8577-8582. doi:10.1073/pnas.1431173100. PubMed: 12817082.
[45]	Melillo MT, Leonetti P, Bongiovanni M, Castagnone-Sereno P, Bleve-Zacheo T (2006) Modulation of reactive oxygen species activities and H2O2 accumulation during compatible and incompatible tomato-root-knot nematode interactions. New Phytol 170: 501-512. doi:10.1111/j.1469-8137.2006.01724.x. PubMed: 16626472.
[46]	May MJ, Hammond-Kosack KE, Jones JDG (1996) Involvement of reactive oxygen species, glutathione metabolism, and lipid peroxidation in the Cf-gene-dependent defense response of tomato cotyledons induced by race-specific elicitors of Cladosporium fulvum. Plant Physiol 110: 1367-1379. PubMed: 12226267.
[47]	Walker JD, Oppenheimer DG, Concienne J, Larkin JC (2000) SIAMESE, a gene controlling the endoreduplication cell cycle in Arabidopsis thaliana trichomes. Development 127: 3931-3940. PubMed: 10952891.
[48]	De Veylder L, Larkin JC, Schnittger A (2011) Molecular control and function of endoreplication in development and physiology. Trends Plant Sci 16: 624-634. doi:10.1016/j.tplants.2011.07.001. PubMed: 21889902.
[49]	Hammond-Kosack KE, Jones JD (1996) Resistance gene-dependent plant defense responses. Plant Cell 8: 1773-1791. doi:10.2307/3870229. PubMed: 8914325.
[50]	Tsuda K, Sato M, Glazebrook J, Cohen JD, Katagiri F (2008) Interplay between MAMP-triggered and SA-mediated defense responses. Plant J 53: 763-775. doi:10.1111/j.1365-313X.2007.03369.x. PubMed: 18005228.
[51]	Legendre L, Rueter S, Heinstein PF, Low PS (1993) Characterization of the oligogalacturonide-induced oxidative burst in cultured soybean (Glycine max) cells. Plant Physiol 102: 233-240. PubMed: 12231814.
[52]	Olmos E, Martínez-Solano JR, Piqueras A, Hellín E (2003) Early steps in the oxidative burst induced by cadmium in cultured tobacco cells (BY-2 line). J Exp Bot 54: 291-301. doi:10.1093/jxb/erg028. PubMed: 12493856.
[53]	Cazalé AC, Rouet-Mayer MA, Barbier-Brygoo H, Mathieu Y, Laurière C (1998) Oxidative burst and hypoosmotic stress in tobacco cell suspensions. Plant Physiol 116: 659-669. doi:10.1104/pp.116.2.659. PubMed: 9490766.
[54]	Kauss H, Jeblick W (1995) Pretreatment of parsley suspension cultures with salicylic acid enhances spontaneous and elicited production of H2O2. Plant Physiol 108: 1171-1178. PubMed: 12228535.
[55]	Fauth M, Merten A, Hahn MG, Jeblick W, Kauss H (1996) Competence for elicitation of H2O2 in hypocotyls of cucumber is induced by breaching the cuticle and is enhanced by salicylic acid. Plant Physiol 110: 347-354. PubMed: 12226186.
[56]	Grant M, Brown I, Adams S, Knight M, Ainslie A 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. doi:10.1046/j.1365-313x.2000.00804.x. PubMed: 10972870.
[57]	Brown I, Trethowan J, Kerry M, Mansfield J, Bolwell GP (1998) Localization of components of the oxidative cross-linking of glycoproteins and of callose synthesis in papillae formed during the interaction between non-pathogenic strains of Xanthomonas campestris and French bean mesophyll cells. Plant J 15: 333-343. doi:10.1046/j.1365-313X.1998.00215.x.
[58]	Schouten A, Tenberge KB, Vermeer J, Stewart J, Wagemakers L et al. (2002) Functional analysis of an extracellular catalase of Botrytis cinerea. Mol Plant Pathol 3: 227-238. doi:10.1046/j.1364-3703.2002.00114.x. PubMed: 20569330.
[59]	Rubio MC, James EK, Clemente MR, Bucciarelli B, Fedorova M et al. (2004) Localization of superoxide dismutases and hydrogen peroxide in legume root nodules. Mol Plant Microbe Interact 17: 1294-1305. doi:10.1094/MPMI.2004.17.12.1294. PubMed: 15597735.
[60]	Otulak K, Garbaczewska G (2010) Localisation of hydrogen peroxide accumulation during Solanum tuberosum cv. Rywal hypersensitive response to Potato virus Y. Micron 41: 327-335. doi:10.1016/j.micron.2009.12.004. PubMed: 20117938.
[61]	Cohen JJ (1999) Apoptosis: mechanisms of life and death in the immune system. J Allergy Clin Immunol 103: 548-554. doi:10.1016/S0091-6749(99)70222-8. PubMed: 10199999.
[62]	Greenberg JT, Yao N (2004) The role and regulation of programmed cell death in plant-pathogen interactions. Cell Microbiol 6: 201-211. doi:10.1111/j.1462-5822.2004.00361.x. PubMed: 14764104.
[63]	Bertout J, Thomas-Tikhonenko A (2006) Infection & neoplastic growth 101: the required reading for microbial pathogens aspiring to cause cancer. Cancer Treat Res 130: 167-197. PubMed: 16610708.
[64]	Tapinos N, Rambukkana A (2005) Insights into regulation of human Schwann cell proliferation by Erk1/2 via a MEK-independent and p56Lck-dependent pathway from leprosy bacilli. Proc Natl Acad Sci U S A 102: 9188-9193. doi:10.1073/pnas.0501196102. PubMed: 15967991.
[65]	Niebel A, de Almeida Engler J, Hemerly A, Ferreira P, Inzé D et al. (1996) Induction of cdc2a and cyc1At expression in Arabidopsis thaliana during early phases of nematode-induced feeding cell formation. Plant J 10: 1037-1043. doi:10.1046/j.1365-313X.1996.10061037.x. PubMed: 9011085.
[66]	Hansen CE, Meins F Jr. (1986) Evidence for a cellular gene with potential oncogenic activity in plants. Proc Natl Acad Sci U S A 83: 2492-2495. doi:10.1073/pnas.83.8.2492. PubMed: 3458211.
[67]	Nissan G, Manulis-Sasson S, Chalupowicz L, Teper D, Yeheskel A et al. (2012) The type III effector HsvG of the gall-forming Pantoea agglomerans mediates expression of the host gene HSVGT. Mol Plant Microbe Interact 25: 231-240. doi:10.1094/MPMI-06-11-0173. PubMed: 21995766.
[68]	Kay S, Hahn S, Marois E, Hause G, Bonas U (2007) A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 318: 648-651. doi:10.1126/science.1144956. PubMed: 17962565.
[69]	Swarup S, de Feyter R, Brlansky RH, Gabriel DW (1991) A pathogenicity locus from Xanthomonas citri enables strains from several pathovars of X. campestris to elicit cankerlike lesions on citrus. Phytopathology 81: 802-809. doi:10.1094/Phyto-81-802.
[70]	Duan YP, Castaneda A, Zhao G, Erdos G, Gabriel DW (1999) Expression of a single, host-specific, bacterial pathogenicity gene in plant cells elicits division, enlargement, and cell death. Mol Plant-Microbe Interact 12: 556-560. doi:10.1094/MPMI.1999.12.6.556.
[71]	Bao Z, Yang H, Hua J (2013) Perturbation of cell cycle regulation triggers plant immune response via activation of disease resistance genes. Proc Natl Acad Sci U S A 110: 2407-2412. doi:10.1073/pnas.1217024110. PubMed: 23345424.
[72]	Rate DN, Cuenca JV, Bowman GR, Guttman DS, Greenberg JT (1999) The gain-of-function Arabidopsis acd6 mutant reveals novel regulation and function of the salicylic acid signaling pathway in controlling cell death, defenses, and cell growth. Plant Cell 11: 1695-1708. doi:10.1105/tpc.11.9.1695. PubMed: 10488236.
[73]	Rate DN, Greenberg JT (2001) The Arabidopsis aberrant growth and death2 mutant shows resistance to Pseudomonas syringae and reveals a role for NPR1 in suppressing hypersensitive cell death. Plant J 27: 203-211. doi:10.1046/j.0960-7412.2001.1075umedoc.x. PubMed: 11532166.
[74]	Kondorosi E, Roudier F, Gendreau E (2000) Plant cell-size control: growing by ploidy? Curr Opin Plant Biol 3: 488-492. doi:10.1016/S1369-5266(00)00118-7. PubMed: 11074380.

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