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Endocytosis and Endosymbiosis

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Book cover Plant Endocytosis

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 1))

Abstract

Symbioses are widespread in nature and occur between organisms that belong to a large variety of taxonomic divisions (Hentschel et al. 2000). Most often, only two partners are involved and the outcome may be either beneficial to both, i.e. mutualism, or detrimental to one of them, i.e. parasitism. Mutualism varies from simple protection against a hostile environment to an intimate cohabitation with exchange of essential nutrients. Important and well-studied examples are the symbiosis between nitrogen-fixing bacteria and plants of the Leguminosae family (approximately 750 genera and 20 000 species) and the arbuscular mycorrhizal interactions that involve more than 80% of land plants with fungi of the Glomeromycota. In the first case, plants profit through the supply of a nitrogen source, and in the second, through an uptake of phosphate. The microsymbionts benefit through the acquisition of carbon sources in a specific and exclusive ecological niche. In both types of interactions, the microsymbionts invade the plant host and the nutrient exchange takes place inside specialised plant cells. The establishment of the symbiosis is a complex process that requires the coordinated action of both symbionts and most probably the involvement of endocytosis in a number of critical events. In this chapter, we will describe both types of endosymbiosis in view of endocytosis and endocytosis-like processes.

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References

  1. Akiyama K, Matsuzaki K-I, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 432:824–827

    Article  Google Scholar 

  2. Ardourel M, Demont N, Debellé F, Maillet F, de Billy F, Promé J-C, Dénarié J, Truchet G (1994) Rhizobium meliloti lipooligosaccharide nodulation factors: different structural requirements for bacterial entry into target root hair cells and induction of plant symbiotic developmental responses. Plant Cell 6:1357–1374

    Article  PubMed  Google Scholar 

  3. Balestrini R, Romera C, Puigdomènech P, Bonfante P (1994) Location of cell-wall hydroxyproline-rich glycoprotein, cellulose and β-1,3-glucans in apical and differentiated regions of maize mycorrhizal roots. Planta 195:201–209

    Article  Google Scholar 

  4. Baluška F, Hlavacka A, Šamaj J, Palme K, Robinson DG, Matoh T, McCurdy DW, Menzel D, Volkmann D (2002) F-actin-dependent endocytosis of cell wall pectins in meristematic root cells. Insights from brefeldin A-induced compartments. Plant Physiol 130:422–431

    Article  PubMed  Google Scholar 

  5. Batut J, Andersson SGE, O'Callaghan D (2004) The evolution of chronic infection strategies in the α-proteobacteria. Nat Rev Microbiol 2:933–945

    Article  Google Scholar 

  6. Bénaben V, Duc G, Lefebvre V, Huguet T (1995) TE7, an inefficient symbiotic mutant of Medicago truncatula Gaertn. cv Jemalong. Plant Physiol 107:53–62

    PubMed  Google Scholar 

  7. Blancaflor EB, Zhao L, Harrison MJ (2001) Microtubule organization in root cells of Medicago truncatula during development of an arbuscular mycorrhizal symbiosis with Glomus versiforme. Protoplasma 217:154–165

    Article  PubMed  Google Scholar 

  8. Boisson-Dernier A, Chabaud M, Garcia F, Bécard G, Rosenberg G, Barker DG (2001) Agrobacterium rhizogenes-transformed roots of Medicago truncatula for the study of nitrogen-fixing and endomycorrhizal symbiotic associations. Mol Plant-Microbe Interact 14:695–700

    PubMed  Google Scholar 

  9. Bolaños L, Brewin NJ, Bonilla I (1996) Effects of boron on Rhizobium–legume cell-surface interactions and nodule development. Plant Physiol 110:1249–1256

    PubMed  Google Scholar 

  10. Bonfante P, Perotto S (1995) Strategies of arbuscular mycorrhizal fungi when infecting host plants. New Phytol 130:3–21

    Google Scholar 

  11. Bonfante P, Bergero R, Uribe X, Romera C, Rigau J, Puigdomenech P (1996) Transcriptional activation of a maize α-tubulin gene in mycorrhizal maize and transgenic tobacco plants. Plant J 9:737–743

    Article  Google Scholar 

  12. Bonfante P, Genre A, Faccio A, Martini I, Schauser L, Stougaard J, Webb J, Parniske M (2000) The Lotus japonicus LjSym4 gene is required for the successful symbiotic infection of root epidermal cells. Mol Plant-Microbe Interact 13:1109–1120

    PubMed  Google Scholar 

  13. Borg S, Brandstrup B, Jensen TJ, Poulsen C (1997) Identification of new protein species among 33 different small GTP-binding proteins encoded by cDNAs from Lotus japonicus, and expression of corresponding mRNAs in developing root nodules. Plant J 11:237–250

    Article  PubMed  Google Scholar 

  14. Brewin NJ (1998) Tissue and cell invasion by Rhizobium: The structure and development of infection threads and symbiosomes. In: Spaink HP, Kondorosi A, Hooykaas PJJ (eds) The Rhizobiaceae. Molecular biology of model plant-associated bacteria. Kluwer, Dordrecht, The Netherlands, pp 417–429

    Google Scholar 

  15. Brewin NJ (2004) Plant cell wall remodelling in the rhizobium–legume symbiosis. Crit Rev Plant Sci 23:293–316

    Article  Google Scholar 

  16. Buee M, Rossignol M, Jauneau A, Ranjeva R, Bécard G (2000) The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Mol Plant-Microbe Interact 13:693–698

    PubMed  Google Scholar 

  17. Campbell GRO, Reuhs BL, Walker GC (2002) Chronic intracellular infection of alfalfa nodules by Sinorhizobium meliloti requires correct lipopolysaccharide core. Proc Natl Acad Sci USA 99:3938–3943

    Article  PubMed  Google Scholar 

  18. Capoen W, Goormachtig S, Schroeyers K, Holsters M (2005) SrSymRK, a plant receptor essential for symbiosome formation. Proc Natl Acad Sci USA 102:10369–10374

    Article  PubMed  Google Scholar 

  19. Catoira R, Timmers ACJ, Maillet F, Galera C, Penmetsa RV, Cook D, Dénarié J, Gough C (2001) The HCL gene of Medicago truncatula controls Rhizobium-induced root hair curling. Development 128:1507–1518

    PubMed  Google Scholar 

  20. Cebolla A, Vinardell JM, Kiss E, Oláh B, Roudier F, Kondorosi A, Kondorosi E (1999) The mitotic inhibitor ccs52 is required for endoreduplication and ploidy-dependent cell enlargement in plants. EMBO J 18:4476–4484

    Article  PubMed  Google Scholar 

  21. Chabaud M, Venard C, Defaux-Petras A, Bécard G, Barker DG (2002) Targeted inoculation of Medicago truncatula in vitro root cultures reveals MtENOD11 expression during early stages of infection by arbuscular mycorrhizal fungi. New Phytol 156:265–273

    Article  Google Scholar 

  22. Cheon C-I, Lee N-G, Siddique A-BM, Bal AK, Verma DPS (1993) Roles of plant homologs of Rab1p and Rab7p in the biogenesis of the peribacteroid membrane, a subcellular compartment formed de novo during root nodule symbiosis. EMBO J 12:4125–4135

    PubMed  Google Scholar 

  23. Collins NC, Thordal-Christensen H, Lipka V, Bau S, Kombrink E, Qiu J-L, Hückelhoven R, Stein M, Freialdenhoven A, Somerville SC, Schulze-Lefert P (2003) SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425:973–977

    Article  PubMed  Google Scholar 

  24. Conner SD, Schmid SL (2003) Regulated portals of entry into the cell. Nature 422:37–44

    Article  PubMed  Google Scholar 

  25. D'Haeze W, Holsters M (2002) Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 12:79R–105R

    Article  PubMed  Google Scholar 

  26. D'Haeze W, Gao M, De Rycke R, Van Montagu M, Engler G, Holsters M (1998) Roles for azorhizobial Nod factors and surface polysaccharides in intercellular invasion and nodule penetration, respectively. Mol Plant-Microbe Interact 11:999–1008

    Google Scholar 

  27. Davidson AL, Newcomb W (2001) Changes in actin microfilament arrays in developing pea nodule cells. Can J Bot 79:767–776

    Article  Google Scholar 

  28. Davidson AL, Newcomb W (2001) Organization of microtubules in developing pea root nodule cells. Can J Bot 79:777–786

    Article  Google Scholar 

  29. Demchenko K, Winzer T, Stougaard J, Parniske M, Pawlowski K (2004) Distinct roles of Lotus japonicus SYMRK and SYM15 in root colonization and arbuscule formation. New Phytol 163:381–392

    Article  Google Scholar 

  30. Dénarié J, Debellé F, Promé J-C (1996) Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu Rev Biochem 65:503–535

    Article  PubMed  Google Scholar 

  31. Dickstein R, Scheirer DC, Fowle WH, Ausubel FM (1991) Nodules elicited by Rhizobium meliloti heme mutants are arrested at an early stage of development. Mol Gen Genet 230:423–432

    Article  PubMed  Google Scholar 

  32. Downie JA, Walker SA (1999) Plant responses to nodulation factors. Curr Opin Plant Biol 2:483–489

    Article  PubMed  Google Scholar 

  33. El Yahyaoui F, Küster H, Ben Amor B, Hohnjec N, Pühler A, Becker A, Gouzy J, Vernié T, Gough C, Niebel A, Godiard L, Gamas P (2004) Expression profiling in Medicago truncatula identifies more than 750 genes differentially expressed during nodulation, including many potential regulators of the symbiotic program. Plant Physiol 136:3159–3176

    Article  PubMed  Google Scholar 

  34. Esseling JJ, Lhuissier FGP, Emons AMC (2003) Nod factor-induced root hair curling: continuous polar growth towards the point of Nod factor application. Plant Physiol 132:1982–1988

    Article  PubMed  Google Scholar 

  35. Esseling JJ, Lhuissier FGP, Emons AMC (2004) A nonsymbiotic root hair tip growth phenotype in NORK-mutated legumes: implications for nodulation factor-induced signaling and formation of a multifaceted root hair pocket for bacteria. Plant Cell 16:933–944

    Article  PubMed  Google Scholar 

  36. Ferguson GP, Datta A, Baumgartner J, Roop RM II, Carlson RW, Walker GC (2004) Similarity to peroxisomal-membrane protein family reveals that Sinorhizobium and Brucella BacA affect lipid-A fatty acids. Proc Natl Acad Sci USA 101:5012–5017

    Article  PubMed  Google Scholar 

  37. Fraysse N, Couderc F, Poinsot V (2003) Surface polysaccharide involvement in establishing the rhizobium–legume symbiosis. Eur J Biochem 270:1365–1380

    Article  PubMed  Google Scholar 

  38. Gage DJ (2004) Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68:280–300

    Article  PubMed  Google Scholar 

  39. Genre A, Bonfante P (1997) A mycorrhizal fungus changes microtubule orientation in tobacco root cells. Protoplasma 199:30–38

    Google Scholar 

  40. Giovannetti M, Sbrana C, Citernesi AS, Logi C (1993) Differential hyphal morphogenesis in arbuscular mycorrhizal fungi during pre-infection stages. New Phytol 125:587–593

    Google Scholar 

  41. Goethals K, Gao M, Tomekpe K, Van Montagu M, Holsters M (1989) Common nodABC genes in Nod locus 1 of Azorhizobium caulinodans: nucleotide sequence and plant-inducible expression. Mol Gen Genet 219:289–298

    Article  PubMed  Google Scholar 

  42. Goedhart J, Hink MA, Visser AJWG, Bisseling T, Gadella TWJ Jr (2000) In vivo fluorescence correlation microscopy (FCM) reveals accumulation and immobilization of Nod factors in root hair cell walls. Plant J 21:109–119

    Article  PubMed  Google Scholar 

  43. Goormachtig S, Capoen W, James EK, Holsters M (2004) Switch from intracellular to intercellular invasion during water stress-tolerant legume nodulation. Proc Natl Acad Sci USA 101:6303–6308

    Article  PubMed  Google Scholar 

  44. Greene EA, Erard M, Dedieu A, Barker DG (1998) MtENOD16 and 20 are members of a family of phytocyanin-related early nodulins. Plant Mol Biol 36:775–783

    Article  PubMed  Google Scholar 

  45. Gross A, Kapp D, Nielsen T, Niehaus K (2005) Endocytosis of Xanthomonas campestris pathovar campestris lipopolysaccharides in non-host plant cells of Nicotiana tabacum. New Phytol 165:215–226

    Article  PubMed  Google Scholar 

  46. Harrison MJ, Dewbre GR, Liu J (2002) A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14:2413–2429

    Article  PubMed  Google Scholar 

  47. Hentschel U, Steinert M, Hacker J (2000) Common molecular mechanisms of symbiosis and pathogenesis. Trends Microbiol 8:226–230

    Article  PubMed  Google Scholar 

  48. Hirsch AM, LaRue TA (1997) Is the legume nodule a modified root or stem or an organ sui generis? Crit Rev Plant Sci 16:361–392

    Google Scholar 

  49. Hubbell DH (1981) Legume infection by Rhizobium: a conceptual approach. BioScience 31:832–837

    Google Scholar 

  50. Imaizumi-Anraku H, Kawaguchi M, Koiwa H, Akao S, Syōno K (1997) Two ineffective-nodulating mutants of Lotus japonicus–-different phenotypes caused by the blockage of endocytic bacterial release and nodule maturation. Plant Cell Physiol 38:871–881

    Google Scholar 

  51. Journet EP, Pichon M, Dedieu A, de Billy F, Truchet G, Barker DG (1994) Rhizobium meliloti Nod factors elicit cell-specific transcription of the ENOD12 gene in transgenic alfalfa. Plant J 6:241–249

    Article  PubMed  Google Scholar 

  52. Journet E-P, El-Gachtouli N, Vernoud V, de Billy F, Pichon M, Dedieu A, Arnould C, Morandi D, Barker DG, Gianinazzi-Pearson V (2001) Medicago truncatula ENOD11: a novel RPRP-encoding early nodulin gene expressed during mycorrhization in arbuscule-containing cells. Mol Plant-Microbe Interact 14:737–748

    PubMed  Google Scholar 

  53. Karandashov V, Bucher M (2005) Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci 10:22–29

    Article  PubMed  Google Scholar 

  54. Kijne JW (1992) The Rhizobium infection process. In: Stacey G, Burris RH, Evans HJ (eds) Biological nitrogen fixation. Chapman & Hall, New York, pp 349–398

    Google Scholar 

  55. Kistner C, Parniske M (2002) Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci 7:511–518

    Article  PubMed  Google Scholar 

  56. Kneen BE, LaRue TA, Hirsch AM, Smith CA, Weeden NF (1990) sym13–-a gene conditioning ineffective nodulation in Pisum sativum. Plant Physiol 94:899–905

    Google Scholar 

  57. Kosuta S, Chabaud M, Lougnon G, Gough C, Dénarié J, Barker DG, Bécard G (2003) A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiol 131:952–962

    Article  PubMed  Google Scholar 

  58. Król J, Wielbo J, Mazur A, Kopcińska J, Łotocka B, Golinowski W, Skorupska A (1998) Molecular characterization of pssCDE genes of Rhizobium leguminosarum bv. trifolii strain TA1: pssD mutant is affected in exopolysaccharide synthesis and endocytosis of bacteria. Mol Plant-Microbe Interact 11:1142–1148

    PubMed  Google Scholar 

  59. LeVier K, Phillips RW, Grippe VK, Roop RM II, Walker GC (2000) Similar requirements of a plant symbiont and a mammalian pathogen for prolonged intracellular survival. Science 287:2492–2493

    Article  PubMed  Google Scholar 

  60. Limpens E, Franken C, Smit P, Willemse J, Bisseling T, Geurts R (2003) LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302:630–633

    Article  PubMed  Google Scholar 

  61. Limpens E, Mirabella R, Federova E, Franken C, Franssen H, Bisseling T, Geurts R (2005) Formation of organelle-like N2-fixing symbiosomes in legume root nodules is controlled by DIM2. Proc Natl Acad Sci USA 102:10375–10380

    Article  PubMed  Google Scholar 

  62. Manthey K, Krajinski F, Hohnjec N, Firnhaber C, Pühler A, Perlick AM, Küster 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

    PubMed  Google Scholar 

  63. Marsh JF, Schultze M (2001) Analysis of arbuscular mycorrhizas using symbiosis-defective plant mutants. New Phytol 150:525–532

    Article  Google Scholar 

  64. Mathis R, Van Gijsegem F, De Rycke R, D'Haeze W, Van Maelsaeke E, Anthonio E, Van Montagu M, Holsters M, Vereecke D (2005) Lipopolysaccharides as a communication signal for progression of legume endosymbiosis. Proc Natl Acad Sci USA 102:2655–2660

    Article  PubMed  Google Scholar 

  65. Miaczynska M, Pelkmans L, Zerial M (2004) Not just a sink: endosomes in control of signal transduction. Curr Opin Cell Biol 16:400–406

    Article  PubMed  Google Scholar 

  66. Miklashevichs E, Röhrig H, Schell J, Schmidt J (2001) Perception and signal transduction of rhizobial NOD factors. Crit Rev Plant Sci 20:373–394

    Google Scholar 

  67. Mithöfer A (2002) Suppression of plant defence in rhizobia–legume symbiosis. Trends Plant Sci 7:440–444

    Article  PubMed  Google Scholar 

  68. Mitra RM, Long SR (2004) Plant and bacterial symbiotic mutants define three transcriptionally distinct stages in the development of the Medicago truncatula=Sinorhizobium meliloti symbiosis. Plant Physiol 134:595–604

    Article  PubMed  Google Scholar 

  69. Mitra RM, Shaw SL, Long SR (2004) Six nonnodulating plant mutants defective for Nod factor-induced transcriptional changes associated with the legume–rhizobia symbiosis. Proc Natl Acad Sci USA 101:10217–10222

    Article  PubMed  Google Scholar 

  70. Morrison N, Verma DPS (1987) A block in the endocytosis of Rhizobium allows cellular differentiation in nodules but affects the expression of some peribacteroid membrane nodulins. Plant Mol Biol 9:185–196

    Article  Google Scholar 

  71. Morzhina EV, Tsyganov VE, Borisov AY, Lebsky VK, Tikhonovich IA (2000) Four developmental stages identified by genetic dissection of pea (Pisum sativum L.) root nodule morphogenesis. Plant Sci 155:75–83

    Article  PubMed  Google Scholar 

  72. Müller P, Ahrens K, Keller T, Klaucke A (1995) A TnphoA insertion with the Bradyrhizobium japonicum sipS gene, homologous to prokaryotic signal peptidases, results in extensive changes in the expression of PBM-specific nodulins of infected soybean (Glycine max) cells. Mol Microbiol 18:831–840

    Article  PubMed  Google Scholar 

  73. Niehaus K, Lagares A, Pühler A (1998) A Sinorhizobium meliloti lipopolysaccharide mutant induces effective nodules on the host plant Medicago sativa (alfalfa) but fails to establish a symbiosis with Medicago truncatula. Mol Plant-Microbe Interact 11:906–914

    Google Scholar 

  74. Novero M, Faccio A, Genre A, Stougaard J, Webb KJ, Mulder L, Parniske M, Bonfante P (2002) Dual requirement of the LjSym4 gene for mycorrhizal development in epidermal and cortical cells of Lotus japonicus. New Phytol 154:741–749

    Article  Google Scholar 

  75. Oke V, Long SR (1999) Bacteroid formation in the Rhizobium–legume symbiosis. Curr Opin Microbiol 2:641–646

    Article  PubMed  Google Scholar 

  76. Oke V, Long SR (1999) Bacterial genes induced within the nodule during the Rhizobium–legume symbiosis. Mol Microbiol 32:837–849

    Article  PubMed  Google Scholar 

  77. Oldroyd GED, Downie JA (2004) Calcium, kinases and nodulation signalling in legumes. Nat Rev Mol Cell Biol 5:566–576

    Article  PubMed  Google Scholar 

  78. Parniske M (2000) Intracellular accommodation of microbes by plants: a common developmental program for symbiosis and disease? Curr Opin Plant Biol 3:320–328

    Article  PubMed  Google Scholar 

  79. Parniske M (2004) Molecular genetics of the arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 7:414–421

    Article  PubMed  Google Scholar 

  80. Perotto S, Brewin NJ, Bonfante P (1994) Colonization of pea roots by the mycorrhizal fungus Glomus versiforme and by Rhizobium bacteria: immunological comparison using monoclonal antibodies as probes for plant cell surface components. Mol Plant-Microbe Interact 7:91–98

    Google Scholar 

  81. Philip-Hollingsworth S, Dazzo FB, Hollingsworth RI (1997) Structural requirements of Rhizobium chitolipooligosaccharides for uptake and bioactivity in legume roots as revealed by synthetic analogs and fluorescent probes. J Lipid Res 38:1229–1241

    PubMed  Google Scholar 

  82. Rathbun EA, Naldrett MJ, Brewin NJ (2002) Identification of a family of extensin-like glycoproteins in the lumen of Rhizobium-induced infection threads in pea root nodules. Mol Plant-Microbe Interact 15:350–359

    PubMed  Google Scholar 

  83. Rausch C, Daram P, Brunner S, Jansa J, Laloi M, Leggewie G, Amrhein N, Bucher M (2001) A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414:462–466

    Article  PubMed  Google Scholar 

  84. Relić B, Perret X, Estrada-García MT, Kopcinska J, Golinowski W, Krishnan HB, Pueppke SG, Broughton WJ (1994) Nod factors of Rhizobium are a key to the legume door. Mol Microbiol 13:171–178

    PubMed  Google Scholar 

  85. Remy W, Taylor TN, Hass H, Kerp H (1994) Four hundred-million-year-old vesicular arbuscular mycorrhizae. Proc Natl Acad Sci USA 91:11841–11843

    PubMed  Google Scholar 

  86. Riely BK, Ané J-M, Penmetsa RV, Cook DR (2004) Genetic and genomic analysis in model legumes bring Nod-factor signaling to center stage. Curr Opin Plant Biol 7:408–413

    Article  PubMed  Google Scholar 

  87. Romanenko AS, Rifel' AA, Salyaev RK (2002) Endocytosis of exopolysaccharides of the potato ring rot causal agent by host-plant cells. Dokl Biol Sci 386:451–453

    Article  PubMed  Google Scholar 

  88. Roth LE, Stacey G (1989) Bacterium release into host cells of nitrogen-fixing soybean nodules: the symbiosome membrane comes from three sources. Eur J Cell Biol 49:13–23

    PubMed  Google Scholar 

  89. Šamaj J, Baluška F, Voigt B, Schlicht M, Volkmann D, Menzel D (2004) Endocytosis, actin cytoskeleton and signaling. Plant Physiol 135:1150–1161

    Article  PubMed  Google Scholar 

  90. Sanders IR (2003) Preference, specificity and cheating in the arbuscular mycorrhizal symbiosis. Trends Plant Sci 8:143–145

    Article  PubMed  Google Scholar 

  91. Scheres B, van Engelen F, van der Knaap E, van de Wiel C, van Kammen A, Bisseling T (1990) Sequential induction of nodulin gene expression in the developing pea nodule. Plant Cell 2:687–700

    Article  PubMed  Google Scholar 

  92. Schiene K, Donath S, Brecht M, Pühler A, Niehaus K (2004) A Rab-related small GTP binding protein is predominantly expressed in root nodules of Medicago sativa. Mol Gen Genomics 272:57–66

    Article  Google Scholar 

  93. Schultze M, Kondorosi A (1998) Regulation of symbiotic root nodule development. Annu Rev Genet 32:33–57

    Article  PubMed  Google Scholar 

  94. Schulze-Lefert P (2004) Knocking on the heaven's wall: pathogenesis of and resistance to biotrophic fungi at the cell wall. Curr Opin Plant Biol 7:377–383

    Article  PubMed  Google Scholar 

  95. Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421

    Google Scholar 

  96. Son O, Yang H-S, Lee H-J, Lee M-Y, Shin K-H, Jeon S-L, Lee M-S, Choi S-Y, Chun J-Y, Kim H, An C-S, Hong S-K, Kim N-S, Koh S-K, Cho MJ, Kim S, Verma DPS, Cheon C-I (2003) Expression of srab7 and SCaM genes required for endocytosis of Rhizobium in root nodules. Plant Sci 165:1239-1244

    Article  Google Scholar 

  97. Sprent JI (2002) Nodulation in legumes. Royal Botanical Gardens, Kew

    Google Scholar 

  98. Strack D, Fester T, Hause B, Schliemann W, Walter MH (2003) Arbuscular mycorrhiza: biological, chemical, and molecular aspects. J Chem Ecol 29:1955–1979

    Article  PubMed  Google Scholar 

  99. Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J, Szczyglowski K, Parniske M (2002) A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417:959–962

    Article  PubMed  Google Scholar 

  100. Tansengco ML, Hayashi M, Kawaguchi M, Imaizumi-Anraku H, Murooka Y (2003) crinkle, a novel symbiotic mutant that affects the infection thread growth and alters the root hair trichome and seed development in Lotus japonicus. Plant Physiol 131:1054–1063

    Article  PubMed  Google Scholar 

  101. Timmers ACJ, Auriac M-C, de Billy F, Truchet G (1998) Nod factor internalization and microtubular cytoskeleton changes occur concomitantly during nodule differentiation in alfalfa. Development 125:339–349

    PubMed  Google Scholar 

  102. Timmers ACJ, Auriac M-C, Truchet G (1999) Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements. Development 126:3617–3628

    PubMed  Google Scholar 

  103. Tsyganov VE, Borisov AY, Rozov SM, Tikhonovich IA (1994) New symbiotic mutants of pea obtained after mutagenesis of laboratory line SGE. Pisum Genet 26:36–37

    Google Scholar 

  104. Tsyganov VE, Morzhina EV, Stefanov SY, Borisov AY, Lebsky VK, Tikhonovich IA (1998) The pea (Pisum sativum L.) genes sym33 and sym40 control infection thread formation and root nodule function. Mol Gen Genet 259:491–503

    Article  PubMed  Google Scholar 

  105. Tsyganov VE, Voroshilova VA, Priefer UB, Borisov AY, Tikhonovich IA (2002) Genetic dissection of the initiation of the infection process and nodule tissue development in the Rhizobium–pea (Pisum sativum L.) symbiosis. Ann Bot 89:357–366

    Google Scholar 

  106. van Spronsen PC, Bakhuizen R, van Brussel AAN, Kijne JW (1994) Cell wall degradation during infection thread formation by the root nodule bacterium Rhizobium leguminosarum is a two-step process. Eur J Cell Biol 64:88–94

    PubMed  Google Scholar 

  107. Vasse J, de Billy F, Camut S, Truchet G (1990) Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. J Bacteriol 172:4295–4306

    PubMed  Google Scholar 

  108. Veereshlingam H, Haynes JG, Penmetsa RV, Cook DR, Sherrier DJ, Dickstein R (2004) nip, a symbiotic mutant that forms root nodules with aberrant infection threads and plant defense-like response. Plant Physiol 136:3692–3702

    Article  PubMed  Google Scholar 

  109. Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman DG (1997) Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–750

    Google Scholar 

  110. Voigt B, Timmers ACJ, Šamaj J, Hlavacka A, Ueda T, Preuss M, Nielsen E, Mathur J, Emans N, Stenmark H, Nakano A, Baluška F, Menzel D (2005) Actin-based motility of endosomes is linked to the polar tip growth of root hairs. Eur J Cell Biol 84:609-621

    Article  PubMed  Google Scholar 

  111. Walker SA, Downie JA (2000) Entry of Rhizobium leguminosarum bv. viciae into root hairs requires minimal Nod factor specificity, but subsequent infection thread growth requires nodO or nodE. Mol Plant-Microbe Interact 13:754–762

    PubMed  Google Scholar 

  112. Weidmann S, Sanchez L, Descombin J, Chatagnier O, Gianinazzi S, Gianinazzi-Pearson V (2004) Fungal elicitation of signal transduction-related plant genes precedes mycorrhiza establishment and requires the dmi3 gene in Medicago truncatula. Mol Plant-Microbe Interact 17:1385–1393

    PubMed  Google Scholar 

  113. Whitehead LF, Day DA (1997) The peribacteroid membrane. Physiol Plant 100:30–44

    Article  Google Scholar 

  114. Wick P, Gansel X, Oulevey C, Page V, Studer I, Dürst M, Sticher L (2003) The expression of the t-SNARE AtSNAP33 is induced by pathogens and mechanical stimulation. Plant Physiol 132:343–351

    Article  PubMed  Google Scholar 

  115. Wisniewski J-P, Rathbun EA, Knox JP, Brewin NJ (2000) Involvement of diamine oxidase and peroxidase in insolubilization of the extracellular matrix: implications for pea nodule initiation by Rhizobium leguminosarum. Mol Plant-Microbe Interact 13:413–420

    PubMed  Google Scholar 

  116. Yang W-C, de Blank C, Meskiene I, Hirt H, Bakker J, van Kammen A, Franssen H, Bisseling T (1994) Rhizobium Nod factors reactivate the cell cycle during infection and nodule primordium formation, but the cycle is only completed in primordium formation. Plant Cell 6:1415–1426

    Article  PubMed  Google Scholar 

  117. Yu Q, Hlavacka A, Matoh T, Volkmann D, Menzel D, Goldbach HE, Baluška F (2002) Short-term boron deprivation inhibits endocytosis of cell wall pectins in meristematic cells of maize and wheat root apices. Plant Physiol 130:415–421

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Laboratoire Interactions Plantes Micro-organismes, Unité Mixte de Recherche 441--2594, B.P. 52627, Chemin de Borde Rouge-Auzeville, 31326, Castanet Tolosan, France

    Antonius C. J. Timmers

  2. Department of Plant Systems Biology, Flanders Interuniversity Institute for Biotechnology (VIB), Ghent University, Technologiepark 927, 9052, Gent, Belgium

    Marcelle Holsters & Sofie Goormachtig

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  1. Antonius C. J. Timmers
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  2. Marcelle Holsters
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  3. Sofie Goormachtig
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Correspondence to Marcelle Holsters .

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Jozef Šamaj František Baluška Diedrik Menzel

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Timmers, A.C.J., Holsters, M., Goormachtig, S. Endocytosis and Endosymbiosis. In: Šamaj, J., Baluška, F., Menzel, D. (eds) Plant Endocytosis. Plant Cell Monographs, vol 1. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7089_015

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