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Alerted Defense System Attenuates Hypersensitive Response-Associated Cell Death in Arabidopsis siz1 Mutant

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Abstract

Plants defend themselves by inducing sophisticated multilevel defense responses against pathogenic attack. The first line of defense against microbial pathogens is the process of nonself-recognition, which mediates the activation of the necessary defense repertoire. The hypersensitive response (HR), a macroscopic collapse of plant leaves in primary infection site, is one of such plant resistance responses. Subsequently, the HR triggers a general resistance mechanism called systemic acquired resistance (SAR), rendering uninfected parts of the plants less sensitive to further pathogenic attacks. Here, we show that SIZ1 mutation-mediated preexisting SAR attenuates HR-associated cell death in Arabidopsis thaliana. In siz1 mutant, the amount of PR1 and PR5 stayed high level, and the growth of pathogenic bacteria Pseudomonas syringae pv. maculicola (Pma) strain M6CΔE was reduced. Early callose deposition, spontaneous formation of microscopic cell death, and reactive oxygen species (ROS) were also observed in siz1 mutant.

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References

  • Atkinson MM, Keppler LD, Orlandi EW, Baker CJ, Mischke CF (1990) Involvement of plasma membrane calcium influx in bacterial induction of the K+/H+ and hypersensitive responses in tobacco. Plant Physiol 92:215–221

    Article  CAS  PubMed  Google Scholar 

  • Atkinson MM, Midlan SL, Sims JJ, Keen NT (1996) Syringolide 1 triggers Ca2+ influx, K+ efflux and extracellular alkalinization in soybean cells carrying the disease-resistance gene Rpg4. Plant Physiol 112:297–302

    CAS  PubMed  Google Scholar 

  • Bogre L, Ligterink W, Meskiene I, Barker PJ, Heberle-Bors E, Huskisson NS, Hirt H (1997) Wounding induces the rapid and transient activation of a specific MAP kinase pathway. Plant Cell 9:75–83

    Article  PubMed  Google Scholar 

  • Bowling SA, Clarke JD, Liu Y, Klessig DF, Dong X (1997) The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell 9:1573–1584

    Article  CAS  PubMed  Google Scholar 

  • Boyes DC, Nam J, Dangl JL (1998) The Arabidopsis thaliana RPM1 disease resistance gene product is a peripheral plasma membrane protein that is degraded coincident with the hypersensitive response. Proc Natl Acad Sci U S A 95:15849–15854

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Chang JH, Goel AK, Grant SR, Dangl JL (2004) Wake of the flood: ascribing functions to the wave of type III effector proteins of phytopathogenic bacteria. Curr Opin Microbiol 7:11–18

    Article  CAS  PubMed  Google Scholar 

  • Chang JH, Urbach JM, Law TF, Arnold LW, Hu A, Gombar S, Grant SR, Ausubel FM, Dangl JL (2005) A high-throughput, near-saturating screen for type III effector genes from Pseudomonas syringae. Proc Natl Acad Sci U S A 102:2549–2554

    Article  CAS  PubMed  Google Scholar 

  • Cheong MS, Park HC, Hong MJ, Choi W, Jin JB, Bohnert HJ, Lee SY, Bressan RA, Yun DJ (2009) Specific domain structures control ABA, SA, and stress mediated SIZ1 phenotypes. Plant Physiol 151:1930–1942

    Google Scholar 

  • Clough SJ, Fengler KA, Yu IC, Lippok B, Smith RK Jr, Bent AF (2000) The Arabidopsis dnd1 “defense, no death” gene encodes a mutated cyclic nucleotide-gated ion channel. Proc Natl Acad Sci U S A 97:9323–9328

    Article  CAS  PubMed  Google Scholar 

  • Collmer A, Lindeberg M, Petnicki-Ocwieja T, Schnieder DJ, Alfano JR (2002) Genomic mining type III secretion system effectors in Pseudomonas syringae yields new picks for all TTSS prospectors. Trends Microbiol 10:462–469

    Article  CAS  PubMed  Google Scholar 

  • Donofrio NM, Delaney TP (2001) Abnormal callose response phenotype and hypersusceptibility to Peronospoara parasitica in defence-compromised Arabidopsis nim1-1 and salicylate hydroxylase-expressing plants. Mol Plant Microbe Interact 14:439–450

    Article  CAS  PubMed  Google Scholar 

  • Duan K, Yi K, Dang L, Huang H, Wu W, Wu P (2008) Characterization of a sub-family of Arabidopsis genes with the SPX domain reveals their diverse functions in plant tolerance to phosphorus starvation. Plant J 54:965–975

    Article  CAS  PubMed  Google Scholar 

  • Felix G, Duran JD, Volko S, Boller T (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18:265–276

    Article  CAS  PubMed  Google Scholar 

  • Gálan JE, Collmer A (1999) Type III secretion machines: bacterial devices for protein delivery into host cells. Science 284:1322–1328

    Article  PubMed  Google Scholar 

  • Gomez-Gomez L, Felix G, Boller T (1999) A single locus determines sensitivity to bacterial flagellin in Arabidopsis thaliana. Plant J 18:277–284

    Article  CAS  PubMed  Google Scholar 

  • Ham JH, Kim MG, Lee SY, Mackey D (2007) Layered basal defenses underlie non-host resistance of Arabidopsis to Pseudomonas syringae pv. phaseolicola. Plant J 51:604–616

    Article  CAS  PubMed  Google Scholar 

  • Hammond-Kosack KE, Jones JDG (1996) Resistance-gene dependent plant defense mechanisms. Plant Cell 8:1773–1791

    Article  CAS  PubMed  Google Scholar 

  • Hanania U, Furman-Matarasso N, Ron M, Avni A (1999) Isolation of a novel SUMO protein from tomato that suppresses EIX-induced cell death. Plant J 19:533–541

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Holt BF 3rd, Mackey D, Dangl JL (2000) Recognition of pathogens by plants. Curr Biol 10:R5–R7

    Article  CAS  PubMed  Google Scholar 

  • Hotson A, Chosed R, Shu H, Orth K, Mudgett MB (2003) Xanthomonas type III effector XopD targets SUMO-conjugated proteins in planta. Mol Microbiol 50:377–389

    Article  CAS  PubMed  Google Scholar 

  • Ishida T, Fujiwara S, Miura K, Stacey N, Yoshimura M, Schneider K, Adachi S, Minamisawa K, Umeda M, Sugimoto K (2009) SUMO E3 Ligase HIGH PLOIDY2 regulates endocycle onset and meristem maintenance in Arabidopsis. Plant Cell 21:2284–2297

    Article  CAS  PubMed  Google Scholar 

  • Jacobs AK, Lipka V, Burton RA, Panstruga R, Strizhov N, Schulze-Lefert P, Fincher GB (2003) An Arabidopsis callose synthase, GSL5, is required for wound and papillary callose formation. Plant Cell 15:2503–2513

    Article  CAS  PubMed  Google Scholar 

  • Jensen ON (2004) Modification-specific proteomics: characterization of post-translational modifications by mass spectrometry. Curr Opin Chem Biol 8:33–41

    Article  PubMed  Google Scholar 

  • Jin JB, Jin YH, Lee J, Miura K, Yoo CY, Kim WY, Van Oosten M, Hyun Y, Somers DE, Lee I, Yun DJ, Bressan RA, Hasegawa PM (2008) The SUMO E3 ligase, AtSIZ1, regulates flowering by controlling a salicylic acid-mediated floral promotion pathway and through affects on FLC chromatin structure. Plant J 53:530–540

    Article  CAS  PubMed  Google Scholar 

  • Jing HC, Dijkwel PP (2008) CPR5: a Jack of all trades in plants. Plant Signal Behav 3:562–563

    PubMed  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Kerscher O, Felberbaum R, Hochstrasser M (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 22:159–180

    Article  CAS  PubMed  Google Scholar 

  • Kim HS, Desveaux D, Singer AU, Patel P, Sondek J, Dangl JL (2005a) The Pseudomonas syringae effector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation. Proc Natl Acad Sci U S A 102:6496–6501

    Article  CAS  PubMed  Google Scholar 

  • Kim MG, da Cunha L, McFall AJ, Belkhadir Y, DebRoy S, Dangl JL, Mackey D (2005b) Two Pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in Arabidopsis. Cell 121:749–759

    Article  CAS  PubMed  Google Scholar 

  • Kirik V, Bouyer D, Schobinger U, Bechtold N, Herzog M, Bonneville JM, Hulskamp M (2001) CPR5 is involved in cell proliferation and cell death control and encodes a novel transmembrane protein. Curr Biol 11:1891–1895

    Article  CAS  PubMed  Google Scholar 

  • Kliebenstein DJ, Dietrich RA, Martin AC, Last RL, Dangl JL (1999) LSD1 regulates salicylic acid induction of copper–zinc superoxide dismutase in Arabidopsis thaliana. Mol Plant–Microbe Interact 12:1022–1026

    Article  CAS  PubMed  Google Scholar 

  • Kloek AP, Verbsky ML, Sharma SB, Schoelz JE, Vogel J, Klessig DF, Kunkel BN (2001) Resistance to Pseudomonas syringae conferred by an Arabidopsis thaliana coronatine-insensitive (coi1) mutation occurs through two distinct mechanisms. Plant J 26:509–522

    Article  CAS  PubMed  Google Scholar 

  • Kurepa J, Walker JM, Smalle J, Gosink MM, Davis SJ, Durham TL, Sung DY, Vierstra RD (2003) The small ubiquitin-like modifier (SUMO) protein modification system in Arabidopsis. Accumulation of SUMO1 and -2 conjugates is increased by stress. J Biol Chem 278:6862–6872

    Article  CAS  PubMed  Google Scholar 

  • Laxalt AM, Munnik T (2002) Phospholipid signalling in plant defence. Curr Opin Plant Biol 5:332–338

    Article  CAS  PubMed  Google Scholar 

  • Laxalt AM, Raho N, Have AT, Lamattina L (2007) Nitric oxide is critical for inducing phosphatidic acid accumulation in xylanase-elicited tomato cells. J Biol Chem 282:21160–21168

    Article  CAS  PubMed  Google Scholar 

  • Lee SC, Hwang BK (2005) Induction of some defense-related genes and oxidative burst is required for the establishment of systemic acquired resistance in Capsicum annuum. Planta 221:790–800

    Article  CAS  PubMed  Google Scholar 

  • Lee J, Nam J, Park HC, Na G, Miura K, Jin JB, Yoo CY, Baek D, Kim DH, Jeong JC, Kim D, Lee SY, Salt DE, Mengiste T, Gong Q, Ma S, Bohnert HJ, Kwak SS, Bressan RA, Hasegawa PM, Yun DJ (2007) Salicylic acid-mediated innate immunity in Arabidopsis is regulated by SIZ1 SUMO E3 ligase. Plant J 49:79–90

    Article  CAS  PubMed  Google Scholar 

  • Ligterink W, Kroj T, Zur Nieden U, Hirt H, Scheel D (1997) Receptor-mediated activation of a MAP kinase in pathogen defense of plants. Science 276:2054–2057

    Article  CAS  PubMed  Google Scholar 

  • Lindgren PB, Peet RC, Panapoulos NJ (1986) Gene cluster of Pseudomonas syringae pv. phaseolicola controls pathogenicity on bean plants and hypersensitivity on nonhost plants. J Bacteriol 168:512–522

    CAS  PubMed  Google Scholar 

  • Lu H, Liu Y, Greenberg JT (2005) Structure–function analysis of the plasma membrane-localized Arabidopsis defense component ACD6. Plant J 44:798–809

    Article  CAS  PubMed  Google Scholar 

  • Lu H, Salimian S, Gamelin E, Wang G, Fedorowski J, LaCourse W, Greenberg JT (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

    Article  CAS  PubMed  Google Scholar 

  • Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL (2003) Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112:379–389

    Article  CAS  PubMed  Google Scholar 

  • Matunis MJ, Coutavas E, Blobel G (1996) A novel ubiquitin-like modification modulates the partitioning of the Ran-GTPase-activating protein RanGAP1 between the cytosol and the nuclear pore complex. J Cell Biol 135:1457–1470

    Article  CAS  PubMed  Google Scholar 

  • Miura K, Jin JB, Hasegawa PM (2007a) Sumoylation, a post-translational regulatory process in plants. Curr Opin Plant Biol 10:495–502

    Article  CAS  PubMed  Google Scholar 

  • Miura K, Jin JB, Lee J, Yoo CY, Stirm V, Miura T, Ashworth EN, Bressan RA, Yun DJ, Hasegawa PM (2007b) SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. Plant Cell 19:1403–1414

    Article  CAS  PubMed  Google Scholar 

  • Miura K, Lee J, Jin JB, Yoo CY, Miura T, Hasegawa PM (2009) Sumoylation of ABI5 by the Arabidopsis SUMO E3 ligase SIZ1 negatively regulates abscisic acid signaling. Proc Natl Acad Sci U S A 106:5418–5423

    Article  CAS  PubMed  Google Scholar 

  • Morel JB, Dangl JL (1997) The hypersensitive response and the induction of cell death in plants. Cell Death Differ 4:671–683

    Article  CAS  PubMed  Google Scholar 

  • Mudgett MB (2005) New insights to the function of phytopathogenic bacterial type III effectors in plants. Annu Rev Plant Biol 56:509–531

    Article  CAS  PubMed  Google Scholar 

  • Nishimura MT, Stein M, Hou BH, Vogel JP, Edwards H, Somerville SC (2003) Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301:969–972

    Article  CAS  PubMed  Google Scholar 

  • Novatchkova M, Budhiraja R, Coupland G, Eisenhaber F, Bachmair A (2004) SUMO conjugation in plants. Planta 220:1–8

    Article  CAS  PubMed  Google Scholar 

  • Nurnberger T, Scheel D (2001) Signal transmission in the plant immune response. Trends Plant Sci 6:372–379

    Article  CAS  PubMed  Google Scholar 

  • Pegadaraju V, Knepper C, Reese J, Shah J (2005) Premature leaf senescence modulated by the Arabidopsis PHYTOALEXIN DEFICIENT4 gene is associated with defense against the phloem-feeding green peach aphid. Plant Physiol 139:1927–1934

    Article  CAS  PubMed  Google Scholar 

  • Rohmer L, Kjemtrup S, Marchesini P, Dangl JL (2003) Nucleotide sequence, functional characterization and evolution of pFKN, a virulence plasmid in Pseudomonas syringae pathovar maculicola. Mol Microbiol 47:1545–1562

    Article  CAS  PubMed  Google Scholar 

  • Ryals JL, Neuenschwander UH, Willits MC, Molina A, Steiner H-Y, Hunt MD (1996) Systemic acquired resistance. Plant Cell 8:1809–1819

    Article  CAS  PubMed  Google Scholar 

  • Saracco SA, Miller MJ, Kurepa J, Vierstra RD (2007) Genetic analysis of SUMOylation in Arabidopsis: conjugation of SUMO1 and SUMO2 to nuclear proteins is essential. Plant Physiol 145:119–134

    Article  CAS  PubMed  Google Scholar 

  • Shan L, He P, Sheen J (2007) Intercepting host MAPK signaling cascades by bacterial type III effectors. Cell Host Microbe 1:167–174

    Article  CAS  PubMed  Google Scholar 

  • Shirasu K, Schulze-Lefert P (2003) Complex formation, promiscuity and multi-functionality: protein interactions in disease-resistance pathways. Trends Plant Sci 8:252–258

    Article  CAS  PubMed  Google Scholar 

  • Stone B, Clarke A (1992) Chemistry and biology of (1-3)-β-D-glucans. La Trobe University Press, Victoria

    Google Scholar 

  • Stone B, Evans N, Bonig I, Clarke A (1985) The application of sirofluor, a chemically defined fluorochrome from aniline blue, for the histochemical detection of callose. Protoplasma 122:191–195

    Article  Google Scholar 

  • Stulemeijer IJ, Joosten MH (2008) Post-translational modification of host proteins in pathogen-triggered defence signalling in plants. Mol Plant Pathol 9:545–560

    Article  CAS  PubMed  Google Scholar 

  • Vance CP, Kirk TK, Sherwood RT (1980) Lignification as a mechanism of disease resistance. Annu Rev Phytopathol 18:259–288

    Article  CAS  Google Scholar 

  • Veronese P, Nakagami H, Bluhm B, Abuqamar S, Chen X, Salmeron J, Dietrich RA, Hirt H, 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

    Article  CAS  PubMed  Google Scholar 

  • Ward ER, Uknes SJ, Williams SC, Dincher SS, Wiederhold DL, Alexander DC, Ahl-Goy P, Metraux JP, Ryals JA (1991) Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 3:1085–1094

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Shah J, Klessig DF (1997) Signal perception and transduction in plant defense responses. Genes Dev 11:1621–1639

    Article  CAS  PubMed  Google Scholar 

  • Yoo CY, Miura K, Jin JB, Lee J, Park HC, Salt DE, Yun DJ, Bressan RA, Hasegawa PM (2006) SIZ1 small ubiquitin-like modifier E3 ligase facilitates basal thermotolerance in Arabidopsis independent of salicylic acid. Plant Physiol 142:1548–1558

    Article  CAS  PubMed  Google Scholar 

  • Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764–767

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the National Academy of Agricultural Sciences and Rural Development Administration to M.G. Kim and a MEST/NRF to the EB-NCRC (grant #: 20090091494).

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  1. National Academy of Agricultural Science, RDA, Suwon, South Korea

    Min Gab Kim

  2. Division of Applied Life Science (BK21 Program), Environmental Biotechnology National Core Research Center, Jinju, South Korea

    Min Gab Kim

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Kim, M.G. Alerted Defense System Attenuates Hypersensitive Response-Associated Cell Death in Arabidopsis siz1 Mutant. J. Plant Biol. 53, 70–78 (2010). https://doi.org/10.1007/s12374-009-9089-8

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