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2009 | 56 | 2 | 199-210
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Annexins - calcium- and membrane-binding proteins in the plant kingdom Potential role in nodulation and mycorrhization in Medicago truncatula

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Annexins belong to a family of multi-functional membrane- and Ca2+-binding proteins. The characteristic feature of these proteins is that they can bind membrane phospholipids in a reversible, Ca2+-dependent manner. While animal annexins have been known for a long time and are fairly well characterized, their plant counterparts were discovered only in 1989, in tomato, and have not been thoroughly studied yet. In the present review, we discuss the available information about plant annexins with special emphasis on biochemical and functional properties of some of them. In addition, we propose a link between annexins and symbiosis and Nod factor signal transduction in the legume plant, Medicago truncatula. A specific calcium response, calcium spiking, is an essential component of the Nod factor signal transduction pathway in legume plants. The potential role of annexins in the generation and propagation of this calcium signal is considered in this review. M. truncatula annexin 1 (MtAnn1) is a typical member of the plant annexin family, structurally similar to other members of the family. Expression of the MtAnn1 gene is specifically induced during symbiotic associations with both Sinorhizobium meliloti and the mycorrhizal fungus Glomus intraradices. Furthermore, it has been reported that the MtAnn1 protein is preferentially localized at the nuclear periphery of rhizobial-activated cortical cells, suggesting a possible role of this annexin in the calcium response signal elicited by symbiotic signals from rhizobia and mycorrhizal fungi.
Physical description
  • Department of Biochemistry, Nencki Institute of Experimental Biology, Warszawa, Poland
  • Department of Biochemistry, Nencki Institute of Experimental Biology, Warszawa, Poland
  • Laboratoire des Interactions Plantes-Microorganismes, INRA-CNRS, Castanet-Tolosan, France
  • Department of Molecular Microbiology, John Innes Centre, Norwich Research Park, Norwich, UK
  • Laboratoire des Interactions Plantes-Microorganismes, INRA-CNRS, Castanet-Tolosan, France
  • Department of Biochemistry, Nencki Institute of Experimental Biology, Warszawa, Poland
  • Amiour N, Recorbet G, Robert F, Gianinazzi S, Dumas-Gaudot E (2006) Mutations in DMI3 and SUNN modify the appressorium-responsive root proteome in arbuscular mycorrhiza. Mol Plant Microbe Interact 19: 988-997.
  • Amor BB, Shaw SL, Oldroyd GED, Maillet F, Penmetsa RV, Cook D, Long SR, Dénarié J, Gough C (2003) The NFP locus of Medicago truncatula controls an early step of Nod factor signal transduction upstream of a rapid calcium flux and root hair deformation. Plant J 34: 495-506.
  • Andrawis A, Solomon M, Delmer DP (1993) Cotton fibre annexins: a potential role in the regulation of callose synthase. Plant J 3: 763-772.
  • Battey NH, James NC, Greenland AJ (1996) cDNA isolation and gene expression of the maize annexins p33 and p35. Plant Physiol 112: 1391-1396.
  • Balasubramanian K, Bevers EM, Willems GM, Schroit AJ (2001) Binding of annexin 5 to membrane products of lipid peroxidation. Biochemistry 40: 8672-8676.
  • Blackbourn HD, Walker JH, Battey NH (1991) Calcium-dependent phospholipid-binding proteins in plants - their characterization and potential for regulating cell-growth. Planta 184: 67-73.
  • Blackbourn HD, Barker PJ, Huskisson NS, Battey NH (1992) Properties and partial protein sequence of plant annexins. Plant Physiol 99: 864-871.
  • Brewin NJ (1998) Tissue and cell invasion by Rhizobium: the structure and development of infection threads and symbiosomes. In The Rhizobiaceae. Spaink HP, Kondorosi A, Hooykaas PJJ, eds, pp 417-429. Kluwer Academic Publishers, Dordrecht.
  • Boustead CM, Smallwood M, Small H, Bowles DJ, Walker JH (1989) Identification of Ca2+-dependent phospholipid-binding proteins in higher plant cells. FEBS Lett 244: 456-460.
  • Calvert CM, Gant SJ, Bowles DJ (1996) Tomato annexins p34 and p35 bind to F-actin and display nucleotide phosphodiesterase activity inhibited by phospholipid binding. Plant Cell 8: 333-342.
  • Catoira R, Galera C, de Billy F, Penmetsa RV, Journet EP, Maillet F, Rosenberg C, Cook D, Gough C, Denarie J (2000) Four genes of Medicago truncatula controlling components of a Nod factor transduction pathway. Plant Cell 12: 1647-1666.
  • Charpentier M, Bredemeier R, Wanner G, Takeda N, Schleiff E, Parniske M (2008) Lotus japonicus CASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis. Plant Cell 20: 3467-3479.
  • Clark GB, Roux SJ (1995) Annexins of plant cells. Plant Physiol 109: 1133-1139.
  • Clark GB, Dauwalder M, Roux SJ (1992) Purification and immunolocalization of an annexin-like protein in pea seedings. Planta 187: 1-9.
  • Clark GB, Dauwalder M, Roux SJ (1994) Immunolocalization of an annexin-like protein in corn. Adv Space Res 14: 341-346.
  • Clark GB, Dauwalder M, Roux SJ (1998) Immunological and biochemical evidence for nuclear localization of annexin in peas. Plant Physiol Biochem 36: 621-627.
  • Clark GB, Rafati DS, Bolton RJ, Dauwalder M, Roux SJ (2000) Redistribution of annexin in gravistimulated pea plumules. Plant Physiol Biochem 38: 937-947.
  • Clark GB, Sessions A, Eastburn DJ, Roux SJ (2001) Differential expression of members of the annexin multigene family in Arabidopsis. Plant Physiol 126: 1072-1084.
  • Dabitz N, Hu N-J, Yusof A, Tranter N, Winter A, Daley M, Zschornig O, Brisson A, Hofmann A (2005) Structural determinants for plant annexin-membrane interactions. Biochemistry 44: 16292-16300.
  • de Carvalho-Niebel F, Lescure N, Cullimore JV, Gamas P (1998) The Medicago truncatula MtAnn1 gene encoding an annexin is induced by nod factors and during the symbiotic interaction with Rhizobium meliloti. Mol Plant-Microbe Interact 11: 504-513.
  • de Carvalho-Niebel F, Timmers ACJ, Chabaud M, Defaux-Petras A, Barker DG (2002) The Nod factor-elicited annexin MtAnn1 is preferentially localized at the nuclear periphery in symbiotically activated root tissues of Medicago truncatula. Plant J 32: 343-352.
  • Delmer DP, Potikha TS (1997) Structures and functions of annexins in plants. Cell Mol Life Sci 53: 546-553.
  • Dénarié J, Debellé F, Promé JC (1996) Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu Rev Biochem 65: 503-535.
  • Dénarié J, Cullimore J (1993) Lipo-oligosaccharide nodulation factors: a mnireview new class of signaling molecules mediating recognition and morphogenesis. Cell 74: 951-954.
  • den Hartog M, Musgrave A, Munnik T (2001) Nod factor induced phosphatidic acid and diacylglycerol pyrophosphate formation: a role for phospholipase C and D in root hair deformation. Plant J 25: 55-65.
  • den Hartog M, Verhoef N, Munnik T (2003) Nod factor and elicitors activate different phospholipid signaling pathways in suspension-cultured alfalfa cells. Plant Physiol 132: 311-317.
  • Edwards A, Heckmann AB, Yousafzai F, Duc G, Downie JA (2007) Structural implications of mutations in the pea SYM8 symbiosis gene, the DMI1 ortholog, encoding a predicted ion channel. Mol Plant Microbe Interact 20: 1183-1191.
  • Engstrom EM, Ehrhardt DW, Mitra RM, Long SR (2002) Pharmacological analysis of nod factor-induced calcium spiking in Medicago truncatula. Evidence for the requirement of type IIA calcium pumps and phosphoinositide signaling. Plant Physiol 128: 1390-1401.
  • Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422: 442-446.
  • Gage DJ, Margolin W (2000) Hanging by a thread: invasion of legume plants by rhizobia. Curr Opin Microbiol 3: 613-617.
  • Gapper C, Dolan L (2006) Control of plant development by reactive oxygen species. Plant Physiol 141: 341-345.
  • Geisow M, Fritsche U, Hexham JM, Dash B, Johnson T (1986) A consensus amino acid sequence repeat in Torpedo and mammalian Ca2+-dependent membrane-binding proteins. Nature 320: 636-638.
  • Gerke V, Moss SE (2002) Annexins: from structure to function. Physiol Rev 82: 331-371.
  • Gerke V, Creutz CE, Moss SE (2005) Annexins: linking Ca2+ signaling to membrane dynamics. Nat Rev Mol Cell Biol 6: 449-461.
  • Geurts R, Fedorova E, Bisseling T (2005) Nod factor signaling genes and their function in the early stages of Rhizobium infection. Curr Opin Plant Biol 8: 346-352.
  • Gidrol X, Sabelli PA, Fern YS, Kush AK (1996) Annexin-like protein from Arabidopsis thaliana rescues ∆oxyR mutant of Escherichia coli from H2O2 stress. Proc Natl Acad Sci USA 93: 11268-11273.
  • Gorecka KM, Konopka-Postupolska D, Hennig J, Buchet R, Pikula S (2005) Peroxidase activity of annexin 1 from Arabidopsis thaliana. Biochem Biophys Res Commun 336: 868-875.
  • Gorecka KM, Thouverey C, Buchet R, Pikula S (2007) Potential role of Annexin AnnAt1 from Arabidopsis thaliana in pH-mediated cellular response to environmental stimuli. Plant Cell Physiol 48: 792-803.
  • Hofmann A (2004) Annexins in the plant kingdom: perspectives and potentials. Annexins 1: 51-61.
  • Hofmann A, Proust J, Dorowski A, Schantz R, Huber R (2000) Annexin 24 from Capsicum annuum - X-ray structure and biochemical characterization. J Biol Chem 275: 8072-8082.
  • Hofmann A, Delmer DP, Wlodawer A (2003) The crystal structure of annexin Gh1 from Gossypium hirsutum reveals an unusual S3 cluster - implication for cellulose synthase complex formation and oxidative stress response. Eur J Biochem 270: 2557-2564.
  • Hoshino D, Hayashi A, Temmei Y, Kanzawa N, Tsuchiya T (2004) Biochemical and immunohistochemical characterization of mimosa annexin. Planta 219: 867-875.
  • Hu SQ, Brady SR, Kovar DR, Staiger CJ, Clark GB, Roux SJ, Muday GK (2000) Identification of plant actin-binding proteins by F-actin affinity chromatography. Plant J 24: 127-137.
  • Hu NJ, Yusof AM, Winter A, Osman A, Reeve AK, Hofmann A (2008) The crystal structure of calcium-bound annexin Gh1 from Gossypium hirsutum and its implications for membrane binding mechanisms of plant annexins. J Biol Chem 283: 18314-18322.
  • Kirilenko A, Golczak M, Pikula S, Buchet R, Bandorowicz-Pikula J (2002) GTP-induced membrane binding and ion channel activity of annexin VI: Is annexin VI a GTP biosensor? Biophys J 82: 2737-2745.
  • Kistner C, Parniske M (2002) Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci 7: 511-851.
  • Kosuta S, Hazledine S, Sun J, Miwa H, Morris RJ, Downie JA, Oldroyd GE (2008) Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proc Natl Acad Sci USA 105: 9823-9828.
  • Kovacs I, Ayaydin F, Oberschall A, Ipacs I, Bottka S, Pongor S, Dudits D, Toth EC (1998) Immunolocalization of novel annexin-like protein encoded by a stress and abscicic acid responsive gene in alfalfa. Plant J 15: 185-197.
  • Kush A, Sabapathy K (2001) Oxy5, a novel protein from Arabidopsis thaliana, protects mammalian cells from oxidative stress. Int J Biochem Cell Biol 33: 591-602.
  • Ladokhin AS, Haigler HT (2005) Reversible transition between the surface trimer and membrane-inserted monomer annexin 12. Biochemistry 44: 3402-3409.
  • Lee S, Lee EJ, Yang EJ, Lee JE, Park AR, Song WH, Park OK (2004) Proteomic identification of annexins, calcium-dependent membrane binding proteins that mediate osmotic stress and abscisic acid signal transduction in Arabidopsis. Plant Cell 16: 1378-1391.
  • Lefebvre B, Furt F, Hartmann M-A, Michaelson LV, Carde J-P, Sargueil-Boiron F, Rossignol M, Napier JA, Cullimore J, Bessoulie J-J, Mongrand S (2007) Characterization of lipid rafts from Medicago truncatula root plasma membranes: A proteomic study reveals the presence of a raft-associated redox system. Plant Physiol 144: 402-418.
  • Liemann S, Benz J, Burger A, Voges D, Hofmann A, Huber R, Gottig P (1996) Structural and functional characterization of the voltage sensor in the ion channel human annexin V. J Mol Biol 258: 555-561.
  • Lim E, Roberts MR, Bowles DJ (1998) Biochemical characterization of tomato annexin p35. J Biol Chem 273: 34920-34925.
  • Lindermayr C, Saalbach G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol 137: 921-930.
  • Manthey K, Krajinski F, Hohnjec N, Firnhaber C, Puhler A, Perlick AM, Kuster H (2004) Transcriptome profiling in root nodules and arbuscular mycorrhiza identifies a collection of novel genes induced during Medicago truncatula root endosymbioses. Mol Plant Microbe Interact 17: 1063-1077.
  • McClung AD, Carroll AD, Battey NH (1994) Identification and characterization of ATPase activity associated with maize (Zea mays) annexins. Biochem J 303: 709-712.
  • Miwa H, Sun J, Oldroyd GE, Downie JA (2006) Analysis of Nod-factor-induced calcium signaling in root hairs of symbiotically defective mutants of Lotus japonicus. Mol Plant Microbe Interact 19: 914-923.
  • Morgan RO, Fernandez MP (1997) Distinct annexin subfamilies in Plants and Protists diverged prior to animal annexins and from a common ancestor. J Mol Evol 44: 178-188.
  • Morgan RO, Jenkins NA, Gilbert DJ, Copeland NG, Balsara BR, Testa JR, Fernandez MP (1999) Novel human and mouse annexin A10 are linked to the genome duplications during early chordate evolution. Genomics 60: 40-49.
  • Morgan RO, Martin-Almedina S, Iglesias JM, Gonzalez-Florez MI, Fernandez MP (2004) Evolutionary perspective on annexin calcium-binding domains. Biochem Biophys Acta 1742: 133-140.
  • Mortimer JC, Laohavisit A, Macpherson N, Webb A, Brownlee C, Battey NH, Davies JM (2008) Annexins: multifunctional components of growth and adaptation. J Exp Bot 59: 533-544.
  • Nichols C (2005) Functional characterization of plant annexins. PhD thesis, University of Cambridge.
  • Oldroyd GED, Downie JA (2004) Calcium, kinases and nodulation signaling in legumes. Nat Rev Mol Cell Biol 5: 566-576.
  • Oldroyd GE, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59: 519-546.
  • Peiter E, Sun J, Heckmann AB, Venkateshwaran M, Riely BK, Otegui MS, Edwards A, Freshour G, Hahn MG, Cook DR, Sanders D, Oldroyd GE, Downie JA, Ane JM (2007) The Medicago truncatula DMI1 protein modulates cytosolic calcium signaling. Plant Physiol 145: 192-203.
  • Pirck M, Hirt H, Heberle-Bors E (1994) The cDNA sequence encoding an annexin from Medicago sativa. Plant Physiol 104: 1463-1464.
  • Pollard HB, Rojas E (1988) Ca2+activated synexin forms highly-selective voltage-gated Ca2+ channels in phosphatidylserine bilayer-membranes. Proc Nat Acad Sci USA 85: 2974-2978.
  • Radutoiu S, Madsen LH, Madsen EB, Jurkiewicz A, Fukai E, Quistgaard EM, Albrektsen AS, James EK, Thirup S, Stougaard J (2007) LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO J 26: 3923-3935.
  • Reddy ASN (2001) Calcium: silver bullet in signaling. Plant Sci 160: 381-404.
  • Riely BK, Lougnon GR, Ané JM, Cook DR (2007) The symbiotic ion channel homolog DMI1 is localized in the nuclear membrane of Medicago truncatula roots. Plant J 49: 208-216.
  • Seals DF, Randall SK (1997) A vacuole-associated annexin protein, VCaB42, correlates with the expansion of Tobacco cells. Plant Physiol 115: 753-761.
  • Seals DF, Parrish ML, Randall SK (1994) A 42-kilodalton annexin-like protein is associated with plant vacuoles. Plant Physiol 106: 1403-1412.
  • Shaw SL, Long SR (2003) Nod factor elicits two separable calcium responses in Medicago truncatula root hair cells. Plant Physiol 131: 976-984.
  • Shin HS, Brown RM (1999) GTPase activity and biochemical characterization of a recombinant cotton fibre annexin. Plant Physiol 119: 925-934.
  • Smallwood M, Keen JN, Bowles DJ (1990) Purification and partial sequence analysis of plant annexins. Biochem J 270: 157-161.
  • Smallwood MF, Gurr SJ, McPherson MJ, Roberts K, Bowles DJ (1992) The pattern of plant annexin gene expression. Biochem J 281: 501-505.
  • Smit P, Limpens E, Geurts R, Fedorova E, Dolgikh E, Gough C, Bisseling T (2007) Medicago LYK3, an entry receptor in rhizobial nodulation factor signaling. Plant Physiol 145: 183-191.
  • Thonat C, Mathieu C, Crevecoeur M, Penel C, Gaspar T, Boyer N (1997) Effects of a mechanical stimulation of localization of annexin-like proteins in Bryonia dioica internodes. Plant Physiol 114: 981-988.
  • Thoquet P, Gherardi M, Journet EP, Kereszt A, Ane JM, Prosperi JM, Huguet T (2002) The molecular genetic linkage map of the model legume Medicago truncatula: an essential tool for comparative legume genomics and the isolation of agronomically important genes. BMC Plant Biol 2: 1-13.
  • Wilkinson JQ, Lanahan MB, Conner TW, Klee HJ (1995) Identification of mRNAs with enhanced expression in ripening strawberry fruit using polymerase chain reaction differential display. Plant Mol Biol 27: 1097-1108.
  • White PJ, Bowen HC, Demidchik V, Nichols C, Davies JM (2002) Genes for calcium-permeable channels in the plasma membrane of plant root cells. Biochim Biophys Acta 1564: 299-309.
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