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G Proteins and Plant Innate Immunity

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Integrated G Proteins Signaling in Plants

Part of the book series: Signaling and Communication in Plants ((SIGCOMM))

Abstract

Under the peaceful appearance of lovely green meadow, the different plant communities are engaged in a continuous struggle for life. Plants use every imaginable mechanism to enhance their defenses in order to survive attacks from an enormous number of pathogens. Plant innate immunity strongly relies on signal transduction pathways connecting pathogen recognition with the establishment of specific defense responses. Heterotrimeric and small GTP-binding proteins provide such signaling between plasma membrane receptors and cytoplasm localized effector molecules. Recent studies, mostly in Arabidopsis and rice, have revealed very important roles for G proteins in plant resistance to fungal pathogens. Experimental evidence implicating G proteins in plant innate immunity and putative signaling mechanisms is presented and discussed in this chapter.

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References

  • Adjobo-Hermans MJW, Goedhart J, Gadella TWJ Jr (2006) Plant G protein heterotrimers require dual lipidation motifs of Ga and Gg and do not dissociate upon activation. J Cell Sci 119:5087–5097

    CAS  PubMed  Google Scholar 

  • Adie BAT, Perez-Perez J, Perez-Perez MM, Godoy M, Sanchez-Serrano JJ, Schmelz EA, Solano R (2007) ABA is an essential signal for plant resistance to pathogens affecting JA biosynthesis and the activation of defenses in Arabidopsis. Plant Cell 19:1665–1681

    Google Scholar 

  • Agrawal GK, Iwahashi H, Rakwal R (2003) Small GTPase 'Rop': molecular switch for plant defense responses. FEBS Letts 546:173–180

    CAS  Google Scholar 

  • Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16:3460–3479

    CAS  PubMed  Google Scholar 

  • Anthony RG, Henriques R, Helfer A, Meszaros T, Rios G, Testerink C, Munnik T, Deak M, Koncz C, Bogre L (2004) A protein kinase target of a PDK1 signalling pathway is involved in root hair growth in Arabidopsis. EMBO J 23:572–581

    CAS  PubMed  Google Scholar 

  • Anthony RG, Khan S, Costa J, Pais MS, Bogre L (2006) The Arabidopsis protein kinase PTI1–2 is activated by convergent phosphatidic acid and oxidative stress signaling pathways downstream of PDK1 and OXI1. J Biol Chem 281:37536–37546

    CAS  PubMed  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Ann Rev Plant Biol 55:373–399

    CAS  Google Scholar 

  • Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977–83

    Google Scholar 

  • Ashikari M, Wu JZ, Yano M, Sasaki T, Yoshimura A (1999) Rice gibberellin-insensitive dwarf mutant gene Dwarf 1 encodes the a-subunit of GTP-binding protein. Proc Nat Acad Sci USA 96:10284–10289

    CAS  PubMed  Google Scholar 

  • Assaad FF, Qiu JL, Youngs H, Ehrhardt D, Zimmerli L, Kalde M, Wanner G, Peck SC, Edwards H, Ramonell K, Somerville CR, Thordal-Christensen H (2004) The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papillae. Mol Biol Cell 15:5118–5129

    CAS  PubMed  Google Scholar 

  • Asselbergh B, De Vleesschauwer D, Hofte M (2008) Global switches and fine-tuning-ABA modulates plant pathogen defense. Molecular Plant-Microbe Interactions 21:709–719

    Google Scholar 

  • Ausubel FM (2005) Are innate immune signaling pathways in plants and animals conserved? Nature Immunology 6:973–979

    Google Scholar 

  • Beffa R, Szell M, Meuwly P, Pay A, Vogeli-Lange R, Metraux J-P, Neuhaus G, Meins F Jr, Nagy F (1995) Cholera toxin elevates pathogen resistance and induces pathogenesis-related gene expression in tobacco. EMBO J 14:5753–5761

    CAS  PubMed  Google Scholar 

  • Beindl W, Mitterauer T, Hohenegger M, Ijzerman AP, Nanoff C, Freissmuth M (1996) Inhibition of receptor/G protein coupling by suramin analogues. Mol Pharmacol 50:415–423

    CAS  PubMed  Google Scholar 

  • Berrocal-Lobo M, Molina A (2008) Arabidopsis defense response against Fusarium oxysporum. Trends Plant Sci 13:145–150

    CAS  PubMed  Google Scholar 

  • Bhat RA, Miklis M, Schmelzer E, Schulze-Lefert P, Panstruga R (2005) Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain. Proc Nat Acad Sci USA 102:3135–3140

    CAS  PubMed  Google Scholar 

  • Bilgin DD, Liu Y, Schiff M, Dinesh-Kumar SP (2003) P58(IPK), a plant ortholog of double-stranded RNA-dependent protein kinase PKR inhibitor, functions in viral pathogenesis. Dev Cell 4:651–661

    CAS  PubMed  Google Scholar 

  • Bos JL (1989) RAS oncogenes in human cancer. Canc Res 49:4682–4689

    CAS  Google Scholar 

  • Burns DL (1988) Subunit structure and enzymic activity of pertussis toxin. Microbiol Sci 5:285–287

    CAS  PubMed  Google Scholar 

  • Chang CC, Ball L, Fryer MJ, Baker NR, Karpinski S, Mullineaux PM (2004) Induction of ASCORBATE PEROXIDASE 2 expression in wounded Arabidopsis leaves does not involve known wound-signalling pathways but is associated with changes in photosynthesis. Plant J 38:499–511

    CAS  PubMed  Google Scholar 

  • Chen J-G, Gao Y, Jones AM (2006) Differential roles of Arabidopsis heterotrimeric G-protein subunits in modulating cell division in roots. Plant Physiol 141:887–897

    CAS  PubMed  Google Scholar 

  • Chen YL, Huang R, Xiao YM, Lu P, Chen J, Wang XC (2004) Extracellular calmodulin-induced stomatal closure is mediated by heterotrimeric G protein and H2O2. Plant Physiol 136:4096–4103

    CAS  PubMed  Google Scholar 

  • Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T, Jones JD, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497–500

    CAS  PubMed  Google Scholar 

  • Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, Garcia-Casado G, Lopez-Vidriero I, Lozano FM, Ponce MR, Micol JL, Solano R (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–671

    CAS  PubMed  Google Scholar 

  • Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu JL, Huckelhoven R, Stein M, Freialdenhoven A, Somerville SC, Schulze-Lefert P (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 42:973–977

    Google Scholar 

  • Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833

    CAS  PubMed  Google Scholar 

  • Delmer DP, Pear JR, Andrawis A, Stalker DM (1995) Genes encoding small GTP-binding proteins analogous to mammalian rac are preferentially expressed in developing cotton fibers. Mol Gen Genet 248:43–51

    CAS  PubMed  Google Scholar 

  • Dorjgotov D, Jurca ME, Fodor-Dunai C, Szucs A, Otvos K, Klement E, Biro J, Feher A (2009) Plant Rho-type (Rop) GTPase-dependent activation of receptor-like cytoplasmic kinases in vitro. FEBS Letts 583:1175–1182

    CAS  Google Scholar 

  • Edgar CI, Mcgrath KC, Dombrecht B, Manners JM, Maclean DC, Schenk PM, Kazan K (2006) Salicylic acid mediates resistance to the vascular wilt pathogen Fusarium oxysporum in the model host Arabidopsis thaliana. Australasian Plant Pathology 35:581–591

    Google Scholar 

  • Farfel Z, Bourne HR, Iiri T (1999) The expanding spectrum of G protein diseases. New Engl J Med 340:1012–1020

    CAS  PubMed  Google Scholar 

  • Fryer MJ, Ball L, Oxborough K, Karpinski S, Mullineaux PM, Baker NR (2003) Control of Ascorbate Peroxidase 2 expression by hydrogen peroxide and leaf water status during excess light stress reveals a functional organisation of Arabidopsis leaves. Plant J 33:691–705

    CAS  PubMed  Google Scholar 

  • Fryer MJ, Oxborough K, Mullineaux PM, Baker NR (2002) Imaging of photo-oxidative stress responses in leaves. J Exp Bot 53:1249–1254

    CAS  PubMed  Google Scholar 

  • Fujisawa Y, Kato H, Iwasaki Y (2001) Structure and function of heterotrimeric G proteins in plants. Plant Cell Physiol 42:789–794

    CAS  PubMed  Google Scholar 

  • Galletti R, Denoux C, Gambetta S, Dewdney J, Ausubel FM, De Lorenzo G, Ferrari S (2008) The AtrbohD-mediated oxidative burst elicited by oligogalacturonides in Arabidopsis is dispensable for the activation of defense responses effective against Botrytis cinerea. Plant Physiol 148:1695–1706

    CAS  PubMed  Google Scholar 

  • Gautam N, Downes GB, Yan K, Kisselev O (1998) The G-protein bg complex. Cell Signal 10:447–455

    CAS  PubMed  Google Scholar 

  • Gelli A, Higgins VJ, Blumwald E (1997) Activation of plant plasma membrane Ca2+-permeable channels by race-specific fungal elicitors. Plant Physiol 113:269–279

    CAS  PubMed  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annual Review of Phytopathology 43:205–227

    Google Scholar 

  • Grant M, Lamb C (2006) Systemic immunity. Current Opinion in Plant Biology 9:414–420

    Google Scholar 

  • Groom QJ, Torres MA, Fordham-Skelton AP, Hammond-Kosack KE, Robinson NJ, Jones JD (1996) rbohA, a rice homologue of the mammalian gp91phox respiratory burst oxidase gene. Plant J 10:515–522

    CAS  PubMed  Google Scholar 

  • Han RB, Yuan YJ (2004) Oxidative burst in suspension culture of Taxus cuspidata induced by a laminar shear stress in short-term. Biotech Prog 20:507–513

    CAS  Google Scholar 

  • Hematy K, Hofte H (2008) Novel receptor kinases involved in growth regulation. Curr Opin Plant Biol 11:321–328

    CAS  PubMed  Google Scholar 

  • Hernandez-Blanco C, Feng DX, Hu J, Sanchez-Vallet A, Deslandes L, Llorente F, Berrocal-Lobo M, Keller H, Barlet X, Sanchez-Rodriguez C, Anderson LK, Somerville S, Marco Y, Molina A (2007) Impairment of cellulose synthases required for Arabidopsis secondary cell wall formation enhances disease resistance. Plant Cell 19:890–903

    CAS  PubMed  Google Scholar 

  • Higashijima T, Uzu S, Nakajima T, Ross EM (1988) Mastoparan, a peptide toxin from wasp venom, mimics receptors by activating GTP-binding regulatory proteins (G proteins). J Biol Chem 263:6491–6494

    CAS  PubMed  Google Scholar 

  • Hong Z, Zhang Z, Olson JM, Verma DP (2001) A novel UDP-glucose transferase is part of the callose synthase complex and interacts with phragmoplastin at the forming cell plate. Plant Cell 13:769–779

    CAS  PubMed  Google Scholar 

  • Jelitto-Van Dooren EP, Vidal S, Denecke J (1999) Anticipating endoplasmic reticulum stress. A novel early response before pathogenesis-related gene induction. Plant Cell 11:1935–1944

    CAS  Google Scholar 

  • Joo J, Wang S, Chen J, Jones A, Fedoroff N (2005) Different signaling and cell death roles of heterotrimeric G protein a and b subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell 17:957–970

    CAS  PubMed  Google Scholar 

  • Joo JH, Bae YS, Lee JS (2001) Role of auxin-induced reactive oxygen species in root gravitropism. Plant Physiol 126:1055–1060

    CAS  PubMed  Google Scholar 

  • Jung YH, Agrawal GK, Rakwal R, Kim JA, Lee MO, Choi PG, Kim YJ, Kim MJ, Shibato J, Kim SH, Iwahashi H, Jwa NS (2006) Functional characterization of OsRacB GTPase–a potentially negative regulator of basal disease resistance in rice. Plant Physiol Biochem 44:68–77

    CAS  PubMed  Google Scholar 

  • Kachroo A, Kachroo P (2007) Salicylic acid-, jasmonic acid- and ethylene-mediated regulation of plant defense signaling. Genetic engineering 28:55–83

    Google Scholar 

  • Katou S, Yoshioka H, Kawakita K, Rowland O, Jones JD, Mori H, Doke N (2005) Involvement of PPS3 phosphorylated by elicitor-responsive mitogen-activated protein kinases in the regulation of plant cell death. Plant Physiology 139:1914–26

    Google Scholar 

  • Katsir L, Schilmiller AL, Staswick PE, He SY, Howe GA (2008) COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci USA 105:7100–7105

    CAS  PubMed  Google Scholar 

  • Kawasaki T, Henmi K, Ono E, Hatakeyama S, Iwano M, Satoh H, Shimamoto K (1999) The small GTP-binding protein Rac is a regulator of cell death in plants. Proc Natl Acad Sci USA 96:10922–10926

    CAS  PubMed  Google Scholar 

  • Kawasaki T, Koita H, Nakatsubo T, Hasegawa K, Wakabayashi K, Takahashi H, Urnemura K, Urnezawa T, Shimamoto K (2006) Cinnamoyl-CoA reductase, a key enzyme in lignin biosynthesis, is an effector of small GTPase Rac in defense signaling in rice. Proc Natl Acad Sci USA 103:230–235

    CAS  PubMed  Google Scholar 

  • Kemmerling B, Schwedt A, Rodriguez P, Mazzotta S, Frank M, Qamar SA, Mengiste T, Betsuyaku S, Parker JE, Mussig C, Thomma BP, Albrecht C, De Vries SC, Hirt H, Nurnberger T (2007) The BRI1-associated kinase 1, BAK1, has a brassinolide-independent role in plant cell-death control. Curr Biol 17:1116–1122

    CAS  PubMed  Google Scholar 

  • Klusener B, Young JJ, Murata Y, Allen GJ, Mori IC, Hugouvieux V, Schroeder JI (2002) Convergence of calcium signaling pathways of pathogenic elicitors and abscisic acid in Arabidopsis guard cells. Plant Physiol 130:2152–2163

    CAS  PubMed  Google Scholar 

  • Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5:325–331

    CAS  PubMed  Google Scholar 

  • Kurosaki F, Yamashita A, Arisawa M (2001) Involvement of GTP-binding protein in the induction of phytoalexin biosynthesis in cultured carrot cells. Plant Sci 161:273–278

    CAS  PubMed  Google Scholar 

  • Kwak JM, Mori IC, Pei ZM, Leonhardt N, Torres MA, Dangl JL, Bloom RE, Bodde S, Jones JD, Schroeder JI (2003) NADPH oxidase AtrbohD and AtrbohF genes function in ROS-dependent ABA signaling in Arabidopsis. EMBO J 22:2623–2633

    CAS  PubMed  Google Scholar 

  • Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–275

    CAS  PubMed  Google Scholar 

  • Lease KA, Wen J, Li J, Doke JT, Liscum E, Walker JC (2001) A mutant Arabidopsis heterotrimeric G-protein b subunit affects leaf, flower, and fruit development. Plant Cell 13:2631–2641

    CAS  PubMed  Google Scholar 

  • Legendre L, Heinstein P, Low P (1992) Evidence for participation of GTP-binding proteins in elicitation of the rapid oxidative burst in cultured soybean cells. J Biol Chem 267:20140–20147

    CAS  PubMed  Google Scholar 

  • Legendre L, Rueter S, Heinstein PF, Low PS (1993a) Characterization of the oligogalacturonide-induced oxidative burst in cultured soybean (Glycine max) cells. Plant Physiol 102:233–240

    CAS  PubMed  Google Scholar 

  • Legendre L, Yueh Y, Crain R, Haddock N, Heinstein P, Low P (1993b) Phospholipase C activation during elicitation of the oxidative burst in cultured plant cells. J Biol Chem 268:24559–24563

    CAS  PubMed  Google Scholar 

  • Lemichez E, Wu Y, Sanchez JP, Mettouchi A, Mathur J, Chua NH (2001) Inactivation of AtRac1 by abscisic acid is essential for stomatal closure. Genes Dev 15:1808–1816

    CAS  PubMed  Google Scholar 

  • Li H, Wu G, Ware D, Davis KR, Yang Z (1998) Arabidopsis Rho-related GTPases: differential gene expression in pollen and polar localization in fission yeast. Plant Physiol 118:407–417

    CAS  PubMed  Google Scholar 

  • Li J, Wang DY, Li Q, Xu YJ, Cui KM, Zhu YX (2004) PPF1 inhibits programmed cell death in apical meristems of both G2 pea and transgenic Arabidopsis plants possibly by delaying cytosolic Ca2+ elevation. Cell Calcium 35:71–77

    CAS  PubMed  Google Scholar 

  • Li JH, Liu YQ, Lu P, Lin HF, Bai Y, Wang XC, Chen YL (2009) A signaling pathway linking nitric oxide production to heterotrimeric G protein and H2O2 regulates extracellular calmodulin induction of stomatal closure in Arabidopsis. Plant Physiol 150(1):114–124

    CAS  PubMed  Google Scholar 

  • Lieberherr D, Thao NP, Nakashima A, Umemura K, Kawasaki T, Shimamoto K (2005) A sphingolipid elicitor-inducible mitogen-activated protein kinase is regulated by the small GTPase OsRac1 and heterotrimeric G-protein in rice. Plant Physiol 138:1644–1652

    CAS  PubMed  Google Scholar 

  • Llorente F, Alonso-Blanco C, Sanchez-Rodriguez C, Jorda L, Molina A (2005) ERECTA receptor-like kinase and heterotrimeric G protein from Arabidopsis are required for resistance to the necrotrophic fungus Plectosphaerella cucumerina. Plant J 43:165–180

    CAS  PubMed  Google Scholar 

  • Llorente F, Muskett P, Sanchez-Vallet A, Lopez G, Ramos B, Sanchez-Rodriguez C, Jorda L, Parker J, Molina A (2008) Repression of the auxin response pathway increases Arabidopsis susceptibility to necrotrophic fungi. Mol Plant 1:496–509

    CAS  PubMed  Google Scholar 

  • Lorenzo O, Chico JM, Sanchez-Serrano JJ, Solano R (2004) Jasmonate-insensitive1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16:1938–1950

    CAS  PubMed  Google Scholar 

  • Ma H (2001) Plant G proteins: the different faces of GPA1. Curr Biol 11:R869–R871

    CAS  PubMed  Google Scholar 

  • Ma H, Yanofsky MF, Meyerowitz EM (1990) Molecular cloning and characterization of GPA1, a G protein a subunit gene from Arabidopsis thaliana. Proc Natl Acad Sci USA 87:3821–3825

    CAS  PubMed  Google Scholar 

  • Mahady GB, Liu C, Beecher CW (1998) Involvement of protein kinase and G proteins in the signal transduction of benzophenanthridine alkaloid biosynthesis. Phytochemistry 48:93–102

    CAS  PubMed  Google Scholar 

  • Maleck K, Dietrich RA (1999) Defense on multiple fronts: how do plants cope with diverse enemies? Trends In Plant Science 4:215–219

    Google Scholar 

  • Mason MG, Botella J (2000) Completing the heterotrimer: Isolation and characterization of an Arabidopsis thaliana G protein g-subunit cDNA. Proc Natl Acad Sci USA 97:14784–14788

    CAS  PubMed  Google Scholar 

  • Mason MG, Botella J (2001) Isolation of a novel G-protein g-subunit from Arabidopsis thaliana and its interaction with Gb. Biochim Biophys Acta 1520:147–153

    CAS  PubMed  Google Scholar 

  • Mayrose M, Bonshtien A, Sessa G (2004) LeMPK3 is a mitogen-activated protein kinase with dual specificity induced during tomato defense and wounding responses. J Biol Chem 279:14819–14827

    CAS  PubMed  Google Scholar 

  • McDowell JM, Dangl JL (2000) Signal transduction in the plant immune response. Trends Biochem Sci 25:79–82

    CAS  PubMed  Google Scholar 

  • Menke FL, Van Pelt JA, Pieterse CM, Klessig DF (2004) Silencing of the mitogen-activated protein kinase MPK6 compromises disease resistance in Arabidopsis. Plant Cell 16:897–907

    CAS  PubMed  Google Scholar 

  • Miles GP, Samuel MA, Jones AM, Ellis BE (2004) Mastoparan rapidly activates plant MAP kinase signaling independent of heterotrimeric G proteins. Plant Physiol 134:1332–1336

    CAS  PubMed  Google Scholar 

  • Molendijk AJ, Ruperti B, Singh MK, Dovzhenko A, Ditengou FA, Milia M, Westphal L, Rosahl S, Soellick TR, Uhrig J, Weingarten L, Huber M, Palme K (2008) A cysteine-rich receptor-like kinase NCRK and a pathogen-induced protein kinase RBK1 are Rop GTPase interactors. Plant J 53:909–923

    CAS  PubMed  Google Scholar 

  • Morel J, Fromentin J, Blein JP, Simon-Plas F, Elmayan T (2004) Rac regulation of NtrbohD, the oxidase responsible for the oxidative burst in elicited tobacco cell. Plant J 37:282–293

    CAS  PubMed  Google Scholar 

  • Munnik T, Arisz SA, De Vrije T, Musgrave A (1995) G protein activation stimulates phospholipase D signaling in plants. Plant Cell 7:2197–2210

    CAS  PubMed  Google Scholar 

  • Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JD (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439

    CAS  PubMed  Google Scholar 

  • Nibau C, Wu HM, Cheung AY (2006) RAC/ROP GTPases: ‘hubs’ for signal integration and diversification in plants. Trends Plant Sci 11:309–315

    CAS  PubMed  Google Scholar 

  • Ono E, Wong HL, Kawasaki T, Hasegawa M, Kodama O, Shimamoto K (2001) Essential role of the small GTPase Rac in disease resistance of rice. Proc Natl Acad Sci USA 98:759–764

    CAS  PubMed  Google Scholar 

  • Opalski KS, Schultheiss H, Kogel KH, Huckelhoven R (2005) The receptor-like MLO protein and the RAC/ROP family G-protein RACB modulate actin reorganization in barley attacked by the biotrophic powdery mildew fungus Blumeria graminis f.sp. hordei. Plant J 41:291–303

    CAS  PubMed  Google Scholar 

  • Ortega X, Polanco R, Castaneda P, Perez LM (2002) Signal transduction in lemon seedlings in the hypersensitive response against Alternaria alternata: participation of calmodulin, G-protein and protein kinases. Biol Res 35:373–383

    CAS  PubMed  Google Scholar 

  • Overmyer K, Brosche M, Kangasjarvi J (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8:335–342

    CAS  PubMed  Google Scholar 

  • Patel S, Caplan J, Dinesh-Kumar SP (2006) Autophagy in the control of programmed cell death. Curr Opin Plant Biol 9:391–396

    CAS  PubMed  Google Scholar 

  • Pathuri IP, Zellerhoff N, Schaffrath U, Hensel G, Kumlehn J, Kogel KH, Eichmann R, Huckelhoven R (2008) Constitutively activated barley ROPs modulate epidermal cell size, defense reactions and interactions with fungal leaf pathogens. Plant Cell Rep 27:1877–1887

    CAS  PubMed  Google Scholar 

  • Pei ZM, Murata Y, Benning G, Thomine S, Klusener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signalling in guard cells. Nature 406:731–734

    CAS  PubMed  Google Scholar 

  • Perekhod EA, Chalenko GI, Il'inskaya LI, Vasyukova NI, Gerasimova NG, Babakov AV, Usov AI, Mel'nikova TM, Ozeretskovskaya OL (1998) Modulation of potato resistance by means of xyloglucan fragments. Appl Biochem Microbiol 34:91–96

    Google Scholar 

  • Philip B, Levin DE (2001) Wsc1 and Mid2 are cell surface sensors for cell wall integrity signaling that act through Rom2, a guanine nucleotide exchange factor for Rho1. Mol Cell Biol 21: 271–280

    CAS  PubMed  Google Scholar 

  • Pieterse CM, Van Loon LC (2004) NPR1: the spider in the web of induced resistance signaling pathways. Curr Opin Plant Biol 7:456–464

    CAS  PubMed  Google Scholar 

  • Rajasekhar VK, Lamb C, Dixon RA (1999) Early events in the signal pathway for the oxidative burst in soybean cells exposed to avirulent Pseudomonas syringae pv glycinea. Plant Physiol 120:1137–1146

    CAS  PubMed  Google Scholar 

  • Ren D, Liu Y, Yang KY, Han L, Mao G, Glazebrook J, Zhang S (2008) A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 105:5638–5643

    Google Scholar 

  • Rentel MC, Lecourieux D, Ouaked F, Usher SL, Petersen L, Okamoto H, Knight H, Peck SC, Grierson CS, Hirt H, Knight MR (2004) OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427:858–861

    CAS  PubMed  Google Scholar 

  • Robert-Seilaniantz A, Navarro L, Bari R, Jones JD (2007) Pathological hormone imbalances. Current Opinion in Plant Biology 10:372–379

    Google Scholar 

  • Roos W, Dordschbal B, Steighardt J, Hieke M, Weiss D, Saalbach G (1999) A redox-dependent, G-protein-coupled phospholipase A of the plasma membrane is involved in the elicitation of alkaloid biosynthesis in Eschscholtzia californica. Biochim Biophys Acta 1448:390–402

    CAS  PubMed  Google Scholar 

  • Ropers HH, Hamel BCJ (2005) X-linked mental retardation. Nat Rev Genet 6:46–57

    CAS  PubMed  Google Scholar 

  • Sagi M, Fluhr R (2001) Superoxide production by plant homologues of the gp91(phox) NADPH oxidase. Modulation of activity by calcium and by tobacco mosaic virus infection. Plant Physiol 126:1281–1290

    CAS  PubMed  Google Scholar 

  • Sánchez-Rodríguez C, Estévez JM, Llorente F, Hernández-Blanco C, Jordá L, Pagán I, Berrocal-Lobo M, Marco Y, Somerville S, Molina A (2009) The ERECTA receptor-like kinase regulates cell wall-mediated resistance to pathogens in Arabidopsis thaliana. Mol Plant-Microbe Interact 22(8):953–963

    PubMed  Google Scholar 

  • Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proceedings of the National Academy of Sciences of the United States of America 97:11655–11660

    Google Scholar 

  • Schenk PM, Kazan K, Manners JM, Anderson JP, Simpson RS, Wilson IW, Somerville SC, Maclean DJ (2003) Systemic gene expression in Arabidopsis during an incompatible interaction with Alternaria brassicicola. Plant Physiology 132:999–1010

    Google Scholar 

  • Schiene K, Puhler A, Niehaus K (2000) Transgenic tobacco plants that express an antisense construct derived from a Medicago sativa cDNA encoding a Rac-related small GTP-binding protein fail to develop necrotic lesions upon elicitor infiltration. Mol Gen Genet 263:761–770

    CAS  PubMed  Google Scholar 

  • Schopfer P, Liszkay A, Bechtold M, Frahry G, Wagner A (2002) Evidence that hydroxyl radicals mediate auxin-induced extension growth. Planta 214:821–828

    CAS  PubMed  Google Scholar 

  • Schroder M, Kaufman RJ (2005) The mammalian unfolded protein response. Ann Rev Biochem 74:739–789

    PubMed  Google Scholar 

  • Schultheiss H, Preuss J, Pircher T, Eichmann R, Huckelhoven R (2008) Barley RIC171 interacts with RACB in planta and supports entry of the powdery mildew fungus. Cell Microbiol 10:1815–1826

    CAS  PubMed  Google Scholar 

  • Schutz I, Gus-Mayer S, Schmelzer E (2006) Profilin and Rop GTPases are localized at infection sites of plant cells. Protoplasma 227:229–235

    CAS  PubMed  Google Scholar 

  • Schwechheimer C, Calderon Villalobos LI (2004) Cullin-containing E3 ubiquitin ligases in plant development. Curr Opin Plant Biol 7:677–686

    CAS  PubMed  Google Scholar 

  • Seifert R, Rosenthal W, Schultz G (1986) Guanine nucleotides stimulate NADPH oxidase in membranes of human neutrophils. FEBS Letts 205:161–165

    CAS  Google Scholar 

  • Sessa G, D'ascenzo M, Loh YT, Martin GB (1998) Biochemical properties of two protein kinases involved in disease resistance signaling in tomato. J Biol Chem 273:15860–15865

    Google Scholar 

  • Sharp GW, Hynie S (1971) Stimulation of intestinal adenyl cyclase by cholera toxin. Nature 229:266–269

    CAS  PubMed  Google Scholar 

  • Shiu SH, Karlowski WM, Pan R, Tzeng YH, Mayer KF, Li WH (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16:1220–1234

    CAS  PubMed  Google Scholar 

  • Shoji T, Ogawa T, Hashimoto T (2008) Jasmonate-induced nicotine formation in tobacco is mediated by tobacco COI1 and JAZ genes. Plant Cell Physiol 49:1003–12

    Google Scholar 

  • Spiegel AM (1996) Defects in G protein-coupled signal transduction in human disease. Ann Rev Physiol 58:143–170

    CAS  Google Scholar 

  • Suh PG, Park JI, Manzoli L, Cocco L, Peak JC, Katan M, Fukami K, Kataoka T, Yun S, Ryu SH (2008) Multiple roles of phosphoinositide-specific phospholipase C isozymes. BMB Rep 41:415–434

    CAS  PubMed  Google Scholar 

  • Suharsono U, Fujisawa Y, Kawasaki T, Iwasaki Y, Satoh H, Shimamoto K (2002) The heterotrimeric G protein alpha subunit acts upstream of the small GTPase Rac in disease resistance of rice. Proc Natl Acad Sci USA 99:13307–13312

    CAS  PubMed  Google Scholar 

  • Tao LZ, Cheung AY, Nibau C, Wu HM (2005) RAC GTPases in tobacco and Arabidopsis mediate auxin-induced formation of proteolytically active nuclear protein bodies that contain AUX/IAA proteins. Plant Cell 17:2369–2383

    CAS  PubMed  Google Scholar 

  • Takahashi H, Kanayama Y, Zheng MS, Kusano T, Hase S, Ikegami M, Shah J (2004) Antagonistic interactions between the SA and JA signaling pathways in Arabidopsis modulate expression of defense genes and gene-for-gene resistance to cucumber mosaic virus. Plant Cell Physiol 45:803–809

    Google Scholar 

  • Thao NP, Chen L, Nakashima A, Hara S, Umemura K, Takahashi A, Shirasu K, Kawasaki T, Shimamoto K (2007) RAR1 and HSP90 form a complex with Rac/Rop GTPase and function in innate-immune responses in rice. Plant Cell 19:4035–4045

    PubMed  Google Scholar 

  • Thatcher LF, Manners JM, Kazan K (2009) Fusarium oxysporum hijacks COI1-mediated jasmonate signaling to promote disease development in Arabidopsis. Plant J 58:927–939

    Google Scholar 

  • Thomma BPHJ, Eggermont K, A., PIAM, Mauch-Mani B, Vogelsang R, A., CBP, Broekaert WF (1998) Separate jasmonate-dependent and salicylate-dependent defense response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proceedings of the National Academy of Sciences of the United States of America 95:15107–15111

    Google Scholar 

  • Thomma BPHJ, Eggermont K, Tierens KFMJ, Broekaert WF (1999) Requirement of functional ethylene-insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea. Plant Physiology 121:1093–1101

    Google Scholar 

  • Thomma BPHJ, Penninckx IAMA, Cammue BPA, Broekaert WF (2001a) The complexity of disease signaling in Arabidopsis. Current Opinion in Immunology 13:63–68

    Google Scholar 

  • Thomma BPHJ, Tierens KFM, Penninckx IAMA, Mauch-Mani B, Broekaert WF, Cammue BPA (2001b) Different micro-organisms differentially induce Arabidopsis disease response pathways. Plant Physiology and Biochemistry 39:673–680

    Google Scholar 

  • Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 8:397–403

    CAS  PubMed  Google Scholar 

  • Trotochaud AE, Hao T, Wu G, Yang Z, Clark SE (1999) The CLAVATA1 receptor-like kinase requires CLAVATA3 for its assembly into a signaling complex that includes KAPP and a Rho-related protein. Plant Cell 11:393–406

    CAS  PubMed  Google Scholar 

  • Trusov Y, Rookes JE, Chakravorty D, Armour D, Schenk PM, Botella JR (2006) Heterotrimeric G-proteins facilitate Arabidopsis resistance to necrotrophic pathogens and are involved in jasmonate signaling. Plant Physiol 140:210–220

    CAS  PubMed  Google Scholar 

  • Trusov Y, Rookes JE, Tilbrook K, Chakravorty D, Mason MG, Anderson D, Chen JG, Jones AM, Botella JR (2007) Heterotrimeric G protein g subunits provide functional selectivity in G bg dimer signaling in Arabidopsis. Plant Cell 19:1235–1250

    CAS  PubMed  Google Scholar 

  • Trusov Y, Sewelam N, Rookes JE, Kunkel M, Nowak E, Schenk PM, Botella JR (2009) Heterotrimeric G proteins-mediated resistance to necrotrophic pathogens includes mechanisms independent of salicylic acid-, jasmonic acid/ethylene- and abscisic acid-mediated defense signaling. Plant J 58:69–81

    CAS  Google Scholar 

  • Trusov Y, Zhang W, Assmann SM, Botella JR (2008) Gg1+Gg2 not equal Gb: heterotrimeric G protein Gg-deficient mutants do not recapitulate all phenotypes of Gb-deficient mutants. Plant Physiol 147:636–649

    CAS  PubMed  Google Scholar 

  • Ullah H, Chen J-G, Temple B, Boyes DC, Alonso JM, Davis KR, Ecker JR, Jones AM (2003) The b-Subunit of the Arabidopsis G protein negatively regulates auxin-induced cell division and affects multiple developmental processes. Plant Cell 15:393–409

    CAS  PubMed  Google Scholar 

  • Van Wees SCM, Chang HS, Zhu T, Glazebrook J (2003) Characterization of the early response of Arabidopsis to Alternaria brassicicola infection using expression profiling. Plant Physiology 132:606–617

    Google Scholar 

  • Vera-Estrella R, Barkla BJ, Higgins VJ, Blumwald E (1994a) Plant defense response to fungal pathogens (activation of host-plasma membrane H+-ATPase by elicitor-iInduced enzyme dephosphorylation). Plant Physiol 104:209–215

    CAS  PubMed  Google Scholar 

  • Vera-Estrella R, Higgins VJ, Blumwald E (1994b) Plant defense response to fungal pathogens 2. G-protein-mediated changes in host plasma-membrane redox reactions. Plant Physiol 106: 97–102

    CAS  PubMed  Google Scholar 

  • Wang D, Weaver ND, Kesarwani M, Dong X (2005) Induction of protein secretory pathway is required for systemic acquired resistance. Science 308:1036–1040

    CAS  PubMed  Google Scholar 

  • Wang S, Narendra S, Fedoroff N (2007) Heterotrimeric G protein signaling in the Arabidopsis unfolded protein response. Proc Natl Acad Sci USA 104:3817–3822

    CAS  PubMed  Google Scholar 

  • Wei Q, Zhou W, Hu G, Wei J, Yang H, Huang J (2008) Heterotrimeric G-protein is involved in phytochrome A-mediated cell death of Arabidopsis hypocotyls. Cell Res 18:949–960

    CAS  PubMed  Google Scholar 

  • Weiss C, Garnaat C, Mukai K, Hu Y, Ma H (1994) Isolation of cDNAs encoding guanine nucleotide-binding protein b-subunit homologues from maize (ZGB1) and Arabidopsis (AGB1). Proc Natl Acad Sci USA 91:9554–9558

    CAS  PubMed  Google Scholar 

  • Wengier D, Valsecchi I, Cabanas ML, Tang WH, Mccormick S, Muschietti J (2003) The receptor kinases LePRK1 and LePRK2 associate in pollen and when expressed in yeast, but dissociate in the presence of style extract. Proc Natl Acad Sci USA 100:6860–6865

    CAS  PubMed  Google Scholar 

  • Winge P, Brembu T, Bones AM (1997) Cloning and characterization of rac-like cDNAs from Arabidopsis thaliana. Plant Mol Biol 35:483–495

    CAS  PubMed  Google Scholar 

  • Wong HL, Pinontoan R, Hayashi K, Tabata R, Yaeno T, Hasegawa K, Kojima C, Yoshioka H, Iba K, Kawasaki T, Shimamoto K (2007) Regulation of rice NADPH oxidase by binding of Rac GTPase to its N-terminal extension. Plant Cell 19:4022–4034

    CAS  PubMed  Google Scholar 

  • Wong HL, Sakamoto T, Kawasaki T, Umemura K, Shimamoto K (2004) Down-regulation of metallothionein, a reactive oxygen scavenger, by the small GTPase OsRac1 in rice. Plant Physiol 135:1447–1456

    CAS  PubMed  Google Scholar 

  • Xin Z, Zhao Y, Zheng ZL (2005) Transcriptome analysis reveals specific modulation of abscisic acid signaling by ROP10 small GTPase in Arabidopsis. Plant Physiol 139:1350–1365

    CAS  PubMed  Google Scholar 

  • Yang KY, Liu Y, Zhang S (2001) Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc Natl Acad Sci USA 98:741–746

    CAS  PubMed  Google Scholar 

  • Yang Z, Fu Y (2007) ROP/RAC GTPase signaling. Curr OpinPlant Biol 10:490–494

    CAS  Google Scholar 

  • Yang Z, Watson JC (1993) Molecular cloning and characterization of rho, a ras-related small GTP-binding protein from the garden pea. Proc Natl Acad Sci USA 90:8732–8736

    CAS  PubMed  Google Scholar 

  • Zeng Q, Wang X, Running MP (2007) Dual lipid modification of Arabidopsis Gg-subunits is required for efficient plasma membrane targeting. Plant Physiol 143:1119–1131

    CAS  PubMed  Google Scholar 

  • Zhang S, Liu Y (2001) Activation of salicylic acid-induced protein kinase, a mitogen-activated protein kinase, induces multiple defense responses in tobacco. Plant Cell 13:1877–1889

    CAS  PubMed  Google Scholar 

  • Zhang X, Zhang L, Dong F, Gao J, Galbraith DW, Song CP (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438–1448

    CAS  PubMed  Google Scholar 

  • Zhao J, Sakai K (2003) Multiple signalling pathways mediate fungal elicitor-induced b-thujaplicin biosynthesis in Cupressus lusitanica cell cultures. J Exp Bot 54:647–656

    CAS  PubMed  Google Scholar 

  • Zheng Z, Qamar SA, Chen Z, Mengiste T (2006) Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J 48:592–605

    CAS  PubMed  Google Scholar 

  • Zheng ZL, Nafisi M, Tam A, Li H, Crowell DN, Chary SN, Schroeder JI, Shen J, Yang Z (2002) Plasma membrane-associated ROP10 small GTPase is a specific negative regulator of abscisic acid responses in Arabidopsis. Plant Cell 14:2787–2797

    CAS  PubMed  Google Scholar 

  • Zheng ZL, Yang Z (2000) The Rop GTPase: an emerging signaling switch in plants. Plant Mol Biol 44:1–9

    CAS  PubMed  Google Scholar 

  • Zhou J, Loh YT, Bressan RA, Martin GB (1995) The tomato gene Pti1 encodes a serine/threonine kinase that is phosphorylated by Pto and is involved in the hypersensitive response. Cell 83:925–935

    Google Scholar 

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Acknowledgments

We thank Dr. Miguel Angel Torres for helpful discussions. Heterotrimeric G protein work in A. Molina’s laboratory is supported by Spanish MEC (Grant BIO2006-00488). G-protein research in J. Botella’s laboratory is supported by the Australian Research Council (grant DP0772145).

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Trusov, Y., Jordá, L., Molina, A., Botella, J.R. (2010). G Proteins and Plant Innate Immunity. In: Yalovsky, S., Baluška, F., Jones, A. (eds) Integrated G Proteins Signaling in Plants. Signaling and Communication in Plants. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-03524-1_12

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