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Original Articles

Plant Cell Wall Remodelling in the Rhizobium–Legume Symbiosis

Pages 293-316 | Published online: 10 Aug 2010

REFERENCES

  • Albrecht , C. , Geurts , R. , Lapeyrie , F. and Bisseling , T. 1998 . Endomycorrhizae and rhizobial Nod factors both require SYM8 to induce the expression of the early nodulin genes PsENOD5 and PsENOD12A . Plant J. , 15 : 605 – 614 .
  • Albus , U. , Baier , R. , Holst , O. , Puhler , A. and Niehaus , K. 2001 . Suppression of an elicitor-induced oxidative burst reaction in Medicago sativa cell cultures by Sinorhizobium meliloti lipopolysaccharides . New Phytologist , 151 : 597 – 606 .
  • Ampe , F. , Kiss , E. , Sabourdy , F. and Batut , J. 2003 . Transcriptome analysis of Sinorhizobium meliloti during symbiosis . Genome Biol. , 4 : art – R15 .
  • Andreeva , I. N. , Kozharinova , G. M. and Izmailov , S. F. 1998 . Senescence of legume nodules . Russ. J. Plant Physiol. , 45 : 101 – 112 .
  • Ane , H. M. , Kiss , G. B. , Denarie , J. and Cook , D. R. 2004 . Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes . Science , 303 : 1364 – 1367 .
  • Arsenijevic-Maksimovic , I. , Broughton , W. J. and Krause , A. 1997 . Rhizobia modulate root-hair-specific expression of extensin genes . Mol. Plant Microbe Interact. , 10 : 95 – 101 .
  • Baron , C. and Zambryski , P. C. 1995 . Notes from the underground—Highlights from plant-microbe interactions . Trends Biotechnol. , 13 : 356 – 362 .
  • Ben Amor , B. , Shaw , S. L. , Oldroyd , G. E. D. , Maillet , F. , Penmetsa , R. V. , Cook , D. , Long , S. R. , Denarie , J. and 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 .
  • Berg , R. H. 1999 . Frankia forms infection threads . Can. J. Botany-Revue Canadienne de Botanique , 77 : 1327 – 1333 .
  • Bolanos , L. , Brewin , N. J. and Bonilla , I. 1996 . Effects of boron on Rhizobium-legume cell-surface interactions and nodule development . Plant Physiol. , 110 : 1249 – 1256 .
  • Bolanos , L. , Redondo-Nieto , M. , Rivilla , R. , Brewin , N. J. and Bonilla , I. 2004 . Cell surface interactions of Rhizobium and other bacterial strains with symbiosomal and peribacteroid membrane components from pea nodules . Mol. Plant Microbe Interact. , 17 : 216 – 223 .
  • Bolte , S. , Schiene , K. and Dietz , K. J. 2000 . Characterization of a small GTP-binding protein of the rab 5 family in Mesembryanthemum crystallinum with increased level of expression during early salt stress . Plant Mol. Biol. , 42 : 923 – 936 .
  • Bond , L. 1948 . Origin and developmental morphology of root nodules of Pisum sativum . Bot. Gaz. , 109 : 411 – 434 .
  • Bradley , D. J. , Butcher , G. W. , Galfre , G. , Wood , E. A. and Brewin , N. J. 1986 . Physical association between the peribacteroid membrane and lipopolysaccharide from the bacteroid outer-membrane in Rhizobium-infected pea root nodule cells . J. Cell Sci. , 85 : 47 – 61 .
  • Bradley , D. J. , Wood , E. A. , Larkins , A. P. , Galfre , G. , Butcher , G. W. and Brewin , N. J. 1988 . Isolation of monoclonal antibodies reacting with peribacteroid membranes and other components of pea root nodules containg Rhizobium leguminosarum . Planta , 173 : 149 – 160 .
  • Brady , J. D. and Fry , S. C. 1997 . Formation of Di-isodityrosine and loss of isodityrosine in the cell walls of tomato cell-suspension cultures treated with fungal elicitors or H2O2 . Plant Physiol. , 115 : 87 – 92 .
  • Brenchley , W. E. and Thornton , H. G. 1925 . The relation between the development, structure and functioning of nodules on Vicia faba, as influenced by the presence or absence of boron in the nutrient medium . Proc. Roy. Soc. London Ser. B , 98 : 373 – 398 .
  • Brewin , N. J. 1991 . Development of the legume root nodule . Ann. Rev. Cell Biol. , 7 : 191 – 226 .
  • Brewin , N. J. 1998 . “ Tissue and cell invasion by Rhizobium: the structure and development of infection threads and symbiosomes. ” . In The Rhizoibaceae , Edited by: Spaink , H. P. , Kondorosi , A. and Hooykaas , P. J. J. 417 – 429 . Dordrecht : Kluwer .
  • Brewin , N. J. 2002 . Pods and nods: a new look at symbiotic nitrogen fixing bacteria . Biologist , 49 : 113 – 117 .
  • Brewin , N. J. and Kardailsky , I. V. 1997 . Legume lectins and nodulation by Rhizobium . Trends Plant Sci. , 2 : 92 – 98 .
  • Broughton , W. J. 2003 . Roses by other names: taxonomy of the Rhizobiaceae . J. Bacteriol. , 185 : 2975 – 2979 .
  • Brown , P. H. , Bellaloui , N. , Wimmer , M. A. , Bassil , E. S. , Ruiz , J. , Hu , H. , Pfeffer , H. , Dannel , F. and Romheld , V. 2002 . Boron in plant biology . Plant Biology , 4 : 205 – 223 .
  • Calvert , H. E. , Pence , M. K. , Pierce , M. , Malik , N. S. A. and Bauer , W. D. 1984 . Anatomical analysis of the development and distribution of Rhizobium infections in soybean roots . Can. J. Botany-Revue Canadienne de Botanique , 62 : 2375 – 2384 .
  • Campbell , G. R. O. , Sharypova , L. A. , Scheidle , H. , Jones , K. M. , Niehaus , K. , Becker , A. and Walker , G. C. 2003 . Striking complexity of lipopolysaccharide defects in a collection of Sinorhizobium meliloti mutants . J. Bacteriol. , 185 : 3853 – 3862 .
  • Cano-Delgado , A. , Penfield , S. , Smith , C. , Catley , M. and Bevan , M. 2003 . Reduced cellulose synthesis invokes lignification and defense responses in Arabidopsis thaliana . Plant J. , 34 : 351 – 362 .
  • Cardenas , L. , Vidali , L. , Dominguez , J. , Perez , H. , Sanchez , F. , Hepler , P. K. and Quinto , C. 1998 . Rearrangement of actin microfilaments in plant root hairs responding to Rhizobium etli nodulation signals . Plant Physiol. , 116 : 871 – 877 .
  • Carol , R. J. and Dolan , L. 2002 . Building a hair: tip growth in Arabidopsis thaliana root hairs . Philos. Transac. Roy. Soc. London Series B-Biol. Sci. , 357 : 815 – 821 .
  • Carvalho-Niebel , F. , Timmers , A. C. J. , Chabaud , M. , Defaux-Petras , A. and Barker , D. G. 2002 . The Nod factor-elicited annexin MtAnn1 is preferentially localised at the nuclear periphery in symbiotically activated root tissues of Medicago truncatula . Plant J. , 32 : 343 – 352 .
  • Cassab , G. I. 1998 . Plant cell wall proteins . Ann. Rev. Plant Physiol. Plant Mol. Biol. , 49 : 281 – 309 .
  • Catoira , R. , Timmers , A. C. J. , Maillet , F. , Galera , C. , Penmetsa , R. V. , Cook , D. , Denarie , J. and Gough , C. 2001 . The HCL gene of Medicago truncatula controls Rhizobium-induced root hair curling . Development , 128 : 1507 – 1518 .
  • Cermola , M. , Fedorova , E. , Tate , R. , Riccio , A. , Favre , R. and Patriarca , E. J. 2000 . Nodule invasion and symbiosome differentiation during Rhizobium etli Phaseolus vulgaris symbiosis . Mol. Plant Microbe Interact. , 13 : 733 – 741 .
  • Chabaud , M. , Venard , C. , Defaux-Petras , A. , Becard , G. and Barker , D. G. 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 .
  • Chen , R. , Silver , D. L. and de Bruijn , F. J. 1998 . Nodule parenchyma-specific expression of the Sesbania rostrata early nodulin gene SrEnod2 is mediated by its 3 untranslated region . Plant Cell , 10 : 1585 – 1602 .
  • Cheng , H. P. and Walker , G. C. 1998 . Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti . J. Bacteriol. , 180 : 5183 – 5191 .
  • Colebatch , G. , Trevaskis , B. and Udvardi , M. 2002 . Symbiotic nitrogen fixation research in the postgenomics era . New Phytolo. , 153 : 37 – 42 .
  • Cooper , J. B. and Long , S. R. 1994 . Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-zeatin secretion . Plant Cell , 6 : 215 – 225 .
  • Csanadi , G. , Szecsi , J. , Kalo , P. , Kiss , P. , Endre , G. , Kondorosi , A. , Kondorosi , E. and Kiss , G. B. 1994 . ENOD12, an early nodulin gene, is not required for nodule formation and efficient nitrogen-fixation in alfalfa . Plant Cell , 6 : 201 – 213 .
  • D'Haeze , W. , De Rycke , R. , Mathis , R. , Goormachtig , S. , Pagnotta , S. , Verplancke , C. , Capoen , W. and Holsters , M. 2003 . Reactive oxygen species and ethylene play a positive role in lateral root base nodulation of a semiaquatic legume . Proc. Natl. Acad. Sci. USA , 100 : 11789 – 11794 .
  • D'Haeze , W. and Holsters , M. 2002 . Nod factor structures, responses, and perception during initiation of nodule development . Glycobiology , 12 : 79R – 105R .
  • Dahiya , P. and Brewin , N. J. 2000 . Immunogold localization of callose and other cell wall components in pea nodule transfer cells . Protoplasma , 214 : 210 – 218 .
  • Dahiya , P. , Sherrier , D. J. , Kardailsky , I. V. , Borisov , A. Y. and Brewin , N. J. 1998 . Symbiotic gene sym31 controls the presence of a lectinlike glycoprotein in the symbiosome compartment of nitrogen-fixing pea nodules . Mol. Plant Microbe Interact. , 11 : 915 – 923 .
  • Davidson , A. L. and Newcomb , W. 2001 . Changes in actin microfilament arrays in developing pea root nodule cells . Can. J. Botany-Revue Canadienne de Botanique , 79 : 767 – 776 .
  • de Faria , S. M. , McInroy , S. G. and Sprent , J. I. 1987 . The occurrence of infected cells with persistent infection threads in legume root nodules . Can. J. Bot. , 65 : 553 – 558 .
  • de Faria , S. M. 1999 . “ Nodulation of forest legumes ” . In Soil Fertility, Soil Biology and Plant Nutrition , Edited by: Sequira , J. O. 667 – 686 . Buenos Aires : Federal University of Brazil .
  • Dean , R. M. , Rivers , R. L. , Zeidel , M. L. and Roberts , D. M. 1999 . Purification and functional reconstitution of soybean nodulin 26. An aquaporin with water and glycerol transport properties . Biochemistry , 38 : 347 – 353 .
  • Diaz , C. L. , Spaink , H. P. and Kijne , J. W. 2000 . Heterologous rhizobial lipochitin oligosaccharides and chitin oligomers induce cortical cell divisions in red clover roots, transformed with the pea lectin gene . Mol. Plant Microbe Interact. , 13 : 268 – 276 .
  • Doblin , M. S. , Kurek , I. , Jacob-Wilk , D. and Delmer , D. P. 2002 . Cellulose biosynthesis in plants: from genes to rosettes . Plant Cell Physiol , 43 : 1407 – 1420 .
  • Downie , J. A. and Parniske , M. 2002 . Plant biology—fixation with regulation . Nature , 420 : 369 – 370 .
  • Doyle , J. J. 1998 . Phylogenetic perspectives on nodulation: evolving views of plants and symbiotic bacteria . Trends Plant Sci. , 3 : 473 – 478 .
  • Doyle , J. J. , Doyle , J. L. , Ballenger , J. A. , Dickson , E. E. , Kajita , T. and Ohashi , H. 1997 . A phylogeny of the chloroplast gene rbcL in theLeguminosae: taxonomic correlations and insights into the evolution of nodulation . Am. J. Botany , 84 : 541 – 554 .
  • Duc , G. , Trouvelot , A. and Sagan , M. 1989 . First report of non-mycorrhizal plant mutants obtained in pea and fababean . Plant Sci. , 60 : 215 – 222 .
  • Ellis , C. , Karafyllidis , I. , Wasternack , C. and Turner , J. G. 2002 . The Arabidopsis mutant cev1 links cell wall signaling to jasmonate and ethylene responses . Plant Cell , 14 : 1557 – 1566 .
  • Endre , G. , Kereszt , A. , Kevei , Z. , Mihacea , S. , Kalo , P. and Kiss , G. B. 2002 . A receptor kinase gene regulating symbiotic nodule development . Nature , 417 : 962 – 966 .
  • Esseling , J. J. , Lhuissier , F. G. P. and Emons , A. M. C. 2003 . Nod factor-induced root hair curling: continuous polar growth towards the point of nod factor application . Plant Physiol. , 132 : 1982 – 1988 .
  • Esseling , J. J. , Lhuissier , F. G. P. and Emons , A. M. C. 2004 . A non-symbiotic root hair growth tip phenotype in NORK-mutated legumes: implications for Nod factor-induced signalling and formation of multi-faceted root hair pockets for bacteria . Plant Cell , 16 : 933 – 966 .
  • Etzler , M. E. , Kalsi , G. , Ewing , N. N. , Roberts , N. J. , Day , R. B. and Murphy , J. B. 1999 . A nod factor binding lectin with apyrase activity from legume roots . Proc. Natl. Acad. Sci. USA , 96 : 5856 – 5861 .
  • Fedorova , E. , Thomson , R. , Whitehead , L. F. , Maudoux , O. , Udvardi , M. K. and Day , D. A. 1999 . Localization of H+ -ATPase in soybean root nodules . Planta , 209 : 25 – 32 .
  • Felle , H. H. , Kondorosi , E. , Kondorosi , A. and Schultze , M. 1999 . Elevation of the cytosolic free [Ca2+] is indispensable for the transduction of the nod factor signal in alfalfa . Plant Physiol. , 121 : 273 – 279 .
  • Ferguson , G. P. , Roop , R. M. and Walker , G. C. 2002 . Deficiency of a Sinorhizobium meliloti bacA mutant in alfalfa symbiosis correlates with alteration of the cell envelope . J. Bacteriol. , 184 : 5625 – 5632 .
  • Ferraioli , S. , Tate , R. , Cermola , M. , Favre , R. , Iaccarino , M. and Patriarca , E. J. 2002 . Auxotrophic mutant strains of Rhizobium etli reveal new nodule development phenotypes . Mol. Plant Microbe Interact. , 15 : 501 – 510 .
  • Foreman , J. , Demidchik , V. , Bothwell , J. H. F. , Mylona , P. , Miedema , H. , Torres , M. A. , Linstead , P. , Costa , S. , Brownlee , C. , Jones , J. D. G. , Davies , J. M. and Dolan , L. 2003 . Reactive oxygen species produced by NADPH oxidase regulate plant cell growth . Nature , 422 : 442 – 446 .
  • Fraysse , N. , Couderc , F. and Poinsot , V. 2003 . Surface polysaccharide involvement in establishing the rhizobium-legume symbiosis . Eur. J. Biochem. , 270 : 1365 – 1380 .
  • Frueauf , J. B. , Dolata , M. , Leykam , J. F. , Lloyd , E. A. , Gonzales , M. , Vandenbosch , K. and Kieliszewski , M. J. 2000 . Peptides isolated from cell walls of Medicago truncatula nodules and uninfected root . Phytochem. , 55 : 429 – 438 .
  • Fruhling , M. , Hohnjec , N. , Schroder , G. , Kuster , H. , Puhler , A. and Perlick , A. M. 2000 . Genomic organization and expression properties of the VfENOD5 gene from broad bean (Vicia faba L.) . Plant Sci. , 155 : 169 – 178 .
  • Fujie , M. , Nakanishi , Y. , Murooka , Y. and Yamada , T. 1998 . AsNODc22, a novel nodulin gene of Astragalus sinicus, encodes a protein that localizes along the cell wall of bacteria-infected cells in a nodule . Plant Cell Physiol. , 39 : 846 – 852 .
  • Gage , D. J. 2002 . Analysis of infection thread development using Gfp- and DsRed-expressing Sinorhizobium meliloti . J. Bacteriol. , 184 : 7042 – 7046 .
  • Gage , D. J. , Bobo , T. and Long , S. R. 1996 . Use of green fluorescent protein to visualize the early events of symbiosis between Rhizobium meliloti and alfalfa (Medicago sativa). . J. Bacteriol. , 178 : 178 – 7159 .
  • Gage , D. J. and Margolin , W. 2000 . Hanging by a thread: invasion of legume plants by rhizobia . Curr. Opin. Microbiol. , 3 : 613 – 617 .
  • Gamas , P. , Niebel , F. D. C. and Lescure , N. 1996 . Use of subtractive hybridisation to identify new Medicago truncatula genes induced during root nodule development . Mol. Plant Microbe Interact. , 9 : 233 – 242 .
  • Gaspar , Y. , Johnson , K. L. , McKenna , J. A. , Bacic , A. and Schultz , C. J. 2001 . The complex structures of arabinogalactan-proteins and the journey towards understanding function . Plant Mol. Biol. , 47 : 161 – 176 .
  • Giordano , W. and Hirsch , A. M. 2004 . The expression of MaEXP1, a Melilotus alba expansin gene is up-regulated during the sweetclover-Sinorhizobium meliloti interaction . Mol. Plant Microbe Interact. , 17 : 613 – 622 .
  • Goedhart , J. , Hink , M. A. , Visser , A. J. W. G. , Bisseling , T. and Gadella , T. W. J. 2000 . In vivo fluorescence correlation microscopy (FCM) reveals accumulation and immobilization of Nod factors in root hair cell walls . Plant J. , 21 : 109 – 119 .
  • Goodrum , L. J. , Patel , A. , Leykam , J. F. and Kieliszewski , M. J. 2000 . Gum arabic glycoprotein contains glycomodules of both extensin and arabinogalactan-glycoproteins . Phytochem. , 54 : 99 – 106 .
  • Greene , E. A. , Erard , M. , Dedieu , A. and Barker , D. G. 1998 . MtENOD16 and 20 are members of a family of phytocyanin-related early nodulins . Plant Mol. Biol. , 36 : 775 – 783 .
  • Gualtieri , G. and Bisseling , T. 2000 . The evolution of nodulation . Plant Mol. Biol. , 42 : 181 – 194 .
  • Guinel , F. C. and Geil , R. D. 2002 . A model for the development of the rhizobial and arbuscular mycorrhizal symbioses in legumes and its use to understand the roles of ethylene in the establishment of these two symbioses . Can. J. Botany-Revue Canadienne de Botanique , 80 : 695 – 720 .
  • Guinel , F. C. and Sloetjes , L. L. 2000 . Ethylene is involved in the nodulation phenotype of Pisum sativum R50 (sym 16), a pleiotropic mutant that nodulates poorly and has pale green leaves . J. Exper. Botany , 51 : 885 – 894 .
  • Gyorgyey , J. , Vaubert , D. , Jimenez-Zurdo , J. I. , Charon , C. , Troussard , L. , Kondorosi , A. and Kondorosi , E. 2000 . Analysis of Medicago truncatula nodule expressed sequence tags . Mol. Plant Microbe Interact. , 13 : 62 – 71 .
  • Hall , Q. and Cannon , M. C. 2002 . The cell wall hydroxyproline-rich glycoprotein RSH is essential for normal embryo development in Arabidopsis . Plant Cell , 14 : 1161 – 1172 .
  • Harrison , M. J. 1999 . Molecular and cellular aspects of the arbuscular mycorrhizal symbiosis . Ann. Rev. Plant Physiol. Plant Mol. Bio. , 50 : 361 – 389 .
  • Hayashi , M. , Imaizumi-Anraku , H. , Akao , S. and Kawaguchi , M. 2000 . Nodule organogenesis in Lotus japonicus . J. Plant Res. , 113 : 489 – 495 .
  • Heidstra , R. , Yang , W. C. , Yalcin , Y. , Peck , S. , Emons , A. M. , van Kammen , A. and Bisseling , T. 1997 . Ethylene provides positional information on cortical cell division but is not involved in Nod factor-induced root hair tip growth in Rhizobium-legume interaction . Development , 124 : 1781 – 1787 .
  • Herouart , D. , Baudouin , E. , Frendo , P. , Harrison , J. , Santos , R. , Jamet , A. , Van de Sype , G. , Touati , D. and Puppo , A. 2002 . Reactive oxygen species, nitric oxide and glutathione: a key role in the establishment of the legume-Rhizobium symbiosis? Plant Physiol . Biochem. , 40 : 619 – 624 .
  • Higashi , S. , Kushiyama , K. and Allan , D. 1987 . Electron-microscopic observations of infection threads in driselase-treated nodules of Astragalus sinicus . Can. J. Microbiol. , 32 : 947 – 952 .
  • Hirsch , A. M. , Fang , Y. , Asad , S. and Kapulnik , Y. 1997 . The role of phytohormones in plant-microbe symbioses . Plant and Soil , 194 : 171 – 184 .
  • Hirsch , A. M. and La Rue , T. A. 1997 . Is the legume nodule a modified root or stem or an Organ sui generis? Crit . Rev. Plant Sci. , 16 : 361 – 392 .
  • Imaizumi-Anraku , H. , Kouchi , H. , Syono , K. , Akao , S. and Kawaguchi , M. 2000 . Analysis of ENOD40 expression in alb1, a symbiotic mutant of Lotus japonicus that forms empty nodules with incompletely developed nodule vascular bundles . Mol. Gen. Genet. , 264 : 402 – 410 .
  • Jackson , P. , Paulo , S. , Brownleader , M. , Freire , P. O. and Ricardo , C. P. P. 1999 . An extensin peroxidase is associated with white-light inhibition of lupin (Lupinus albus) hypocotyl growth . Austr. J. Plant Physiol. , 26 : 29 – 36 .
  • Januschke , J. , Gervais , L. , Dass , S. , Kaltschmidt , J. A. , Lopez-Schier , H. , St Johnston , D. , Brand , A. H. , Roth , S. and Guichet , A. 2002 . Polar transport in the Drosophilia oocyte requires Dynein and Kinesin I cooperation . Curr. Biol. , 12 : 1971 – 1981 .
  • Johnson , K. L. , Jones , B. J. , Bacic , A. and Schultz , C. J. 2003 . The fasciclin-like arabinogalactan proteins of arabidopsis. A multigene family of putative cell adhesion molecules . Plant Physiol. , 133 : 1911 – 1925 .
  • Journet , E. P. , El Gachtouli , N. , Vernoud , V. , de Billy , F. , Pichon , M. , Dedieu , A. , Arnould , C. , Morandi , D. , Barker , D. G. and 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 .
  • Kannenberg , E. L. and Carlson , R. W. 2001 . Lipid A and O-chain modifications cause Rhizobium lipopolysaccharides to become hydrophobic during bacteroid development . Molecular Microbiol. , 39 : 379 – 391 .
  • Kapranov , P. , Routt , S. M. , Bankaitis , V. A. , de Bruijn , F. J. and Szczyglowski , K. 2001 . Nodule-specific regulation of phosphatidylinositol transfer protein expression in Lotus japonicus . Plant Cell , 13 : 1369 – 1382 .
  • Kato , T. , Kawashima , K. , Miwa , M. , Mimura , Y. , Tamaoki , M. , Kouchi , H. and Suganuma , N. 2002 . Expression of genes encoding late nodulins characterized by a putative signal peptide and conserved cysteine residues is reduced in ineffective pea nodules . Mol. Plant Microbe Interact. , 15 : 129 – 137 .
  • Keating , D. H. , Willits , M. G. and Long , S. R. 2002 . A Sinorhizobium meliloti lipopolysaccharide mutant altered in cell surface sulfation . J. Bacteriol. , 184 : 6681 – 6689 .
  • Kevei , Z. , Vinardell , J. M. , Kiss , G. B. , Kondorosi , A. and Kondorosi , E. 2002 . Glycine-rich proteins encoded by a nodule-specific gene family are implicated in different stages of symbiotic nodule development in Medicago spp . Mol. Plant Microbe Interact. , 15 : 922 – 931 .
  • Kieliszewski , M. J. 2001 . The latest hype on Hyp-O-glycosylation codes . Phytochem. , 57 : 319 – 323 .
  • Kieliszewski , M. J. and Shpak , E. 2001 . Synthetic genes for the elucidation of glycosylation codes for arabinogalactan-proteins and other hydroxyproline-rich glycoproteins . Cell. Mol. Life Sci. , 58 : 1386 – 1398 .
  • Kijne , J. W. , Bauchrowitz , M. A. and Diaz , C. L. 1997 . Root lectins and rhizobia . Plant Physiol. , 115 : 869 – 873 .
  • Kimura , S. and Kondo , T. 2002 . Recent progress in cellulose biosynthesis . J. Plant Res. , 115 : 297 – 302 .
  • Kistner , C. and Parniske , M. 2002 . Evolution of signal transduction in intracellular symbiosis . Trends Plant Sci. , 7 : 511 – 518 .
  • Kosuta , S. , Chabaud , M. , Lougnon , G. , Gough , C. , Denarie , J. , Barker , D. G. and Becard , G. 2003 . A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula . Plant Physiol. , 131 : 952 – 962 .
  • Krusell , L. , Madsen , L. H. , Sato , S. , Aubert , G. , Genua , A. , Szczyglowski , K. , Duc , G. , Kaneko , T. , Tabata , S. , de Bruijn , F. , Pajuelo , E. , Sandal , N. and Stougaard , J. 2002 . Shoot control of root development and nodulation is mediated by a receptor-like kinase . Nature , 420 : 422 – 426 .
  • Lamblin , A. F. J. , Crow , J. A. , Johnson , J. E. , Silverstein , K. A. T. , Kunau , T. M. , Kilian , A. , Benz , D. , Stromvik , M. , Endre , G. , Vandenbosch , K. A. , Cook , D. R. , Young , N. D. and Retzel , E. F. 2003 . MtDB: a database for personalized data mining of the model legume Medicago truncatula transcriptome . Nucleic Acids Res. , 31 : 196 – 201 .
  • Laurenzi , M. , Tipping , A. J. , Marcus , S. E. , Knox , J. P. , Federico , R. , Angelini , R. and McPherson , M. J. 2001 . Analysis of the distribution of copper amine oxidase in cell walls of legume seedlings . Planta , 214 : 37 – 45 .
  • Lerouge , P. , Roche , P. , Faucher , C. , Maillet , F. , Truchet , G. , Prome , C. and Denarie , J. 1990 . Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal . Nature , 344 : 781 – 784 .
  • Levy , J. , Denarie , J. and Debelle , F. 2004 . A putative Ca- and calmodulin-dependent protein kinase required for bacterial and fungal symbioses . Science , 303 : 1361 – 1364 .
  • Lhuissier , F. G. P. , De Ruijter , N. C. A. , Sieberer , B. J. , Esseling , J. J. and Emons , A. M. C. 2001 . Time course of cell biological events evoked in legume root hairs by Rhizobium Nod factors: state of the art . Ann. Botany , 87 : 289 – 302 .
  • Limpens , E. and Bisseling , T. 2003 . Signaling in symbiosis . Curr. Opin. Plant Biol. , 6 : 343 – 350 .
  • Limpens , E. , Franken , C. , Smit , P. , Willemse , J. , Bisseling , T. and Geurts , R. 2003 . LysM domain receptor kinases regulating rhizobial Nod factor- induced infection . Science , 302 : 630 – 633 .
  • Löbler , M. and Hirsch , A. M. 1993 . A gene that encodes a proline-rich nodulin with limited homology to PsENOD12 is expressed in the invasion zone of Rhizobium-meliloti-induced alfalfa root nodules . Plant Physiol. , 103 : 21 – 30 .
  • Lodwig , E. and Poole , P. 2003 . Metabolism of Rhizobium bacteroids . Crit. Rev. Plant Sci. , 22 : 37 – 78 .
  • Long , S. R. 1996 . Rhizobium symbiosis: Nod factors in perspective . Plant Cell , 8 : 1885 – 1898 .
  • Loria , R. , Coombs , J. , Yoshida , M. , Kers , J. and Bukhalid , R. 2003 . A paucity of bacterial root diseases: Streptomyces succeeds where others fail . Physiol. Mole. Plant Pathol. , 62 : 65 – 72 .
  • Lotocka , B. , Kopcinska , J. and Golinowski , W. 1997 . Morphogenesis of root nodules in white clover. I. Effective root nodules induced by the wild type Rhizobium leguminosarum biovar. trifolii . Acta Societatis Botanicorum Poloniae , 66 : 273 – 292 .
  • Lotocka , B. , Kopcinska , J. , Gorecka , M. and Golinowski , W. 2000 . Formation and abortion of root nodule primordia in Lupinus luteus L . Acta Biologica Cracoviensia Series Botanica , 42 : 87 – 102 .
  • MacDougall , A. J. , Brett , G. M. , Morris , V. J. , Rigby , N. M. , Ridout , M. J. and Ring , S. G. 2001 . The effect of peptide behaviour–pectin interactions on the gelation of a plant cell wall pectin . Carbohyd. Res. , 335 : 115 – 126 .
  • Madsen , E. B. , Madsen , L. H. , Radutoiu , S. , Olbryt , M. , Rakwalska , M. , Szczyglowski , K. , Sato , S. , Kaneko , T. , Tabata , S. , Sandal , N. and Stougaard , J. 2003 . A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals . Nature , 425 : 637 – 640 .
  • Mathesius , U. , Bayliss , C. , Weinman , J. J. , Schlaman , H. R. M. , Spaink , H. P. , Rolfe , B. G. , McCully , M. E. and Djordjevic , M. A. 1998a . Flavonoids synthesized in cortical cells during nodule initiation are early developmental markers in white clover . Mol. Plant Microbe Interact. , 11 : 1223 – 1232 .
  • Mathesius , U. , Keijzers , G. , Natera , S. H. A. , Weinman , J. J. , Djordjevic , M. A. and Rolfe , B. G. 2001 . Establishment of a root proteome reference map for the model legume Medicago truncatula using the expressed sequence tag database for peptide mass fingerprinting . Proteomics , 1 : 1424 – 1440 .
  • Mathesius , U. , Schlaman , H. R. M. , Spaink , H. P. , Sautter , C. , Rolfe , B. G. and Djordjevic , M. A. 1998b . Auxin transport inhibition precedes root nodule formation in white clover roots and is regulated by flavonoids and derivatives of chitin oligosaccharides . Plant J. , 14 : 23 – 34 .
  • Mathesius , U. , Weinman , J. J. , Rolfe , B. G. and Djordjevic , M. A. 2000 . Rhizobia can induce nodules in white clover by “hijacking” mature cortical cells activated during lateral root development . Mol. Plant Microbe Interact. , 13 : 170 – 182 .
  • Mathis , R. , Grosjean , C. , de Billy , F. , Huguet , T. and Gamas , P. 1999 . The early nodulin gene MtN6 is a novel marker for events preceding infection of Medicago truncatula roots by Sinorhizobium meliloti . Mol. Plant Microbe Interact. , 12 : 544 – 555 .
  • Matthysse , A. G. and Kijne , J. W. 1998 . “ Attachment of Rhizobiaceae to plant cells. ” . In The Rhizobiaceae , Edited by: Spaink , H. P. , Kondorosi , A. and Hooykaas , P. J. J. 235 – 249 . Dordrecht : Kluwer .
  • Miklashevichs , E. , Rohrig , H. , Schell , J. and Schmidt , J. 2001 . Perception and signal transduction of rhizobial NOD factors . Crit. Rev. Plant Sci. , 20 : 373 – 394 .
  • Mitra , R. M. , Gleason , C. A. , Edwards , A. , Hadfield , J. , Downie , J. A. , Oldroyd , G. E. D. and Long , S. R. 2004 . A Ca/Calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcript-based cloning . Proc. Nat. Acad. Sci. USA , 101 : 4701 – 4705 .
  • Morzhina , E. V. , Tsyganov , V. E. , Borisov , A. Y. , Lebsky , V. K. and Tikhonovich , I. A. 2000 . Four developmental stages identified by genetic dissection of pea (Pisum sativum L.) root nodule morphogenesis . Plant Sci. , 155 : 75 – 83 .
  • Mulder , B. M. and Emons , A. M. C. 2001 . A dynamical model for plant cell wall architecture formation . J. Math. Biol. , 42 : 261 – 289 .
  • Munoz , J. A. , Coronado , C. , Perez-Hormaeche , J. , Kondorosi , A. , Ratet , P. and Palomares , A. J. 1998 . MsPG3, a Medicago sativa polygalacturonase gene expressed during the alfalfa Rhizobium meliloti interaction . Proc. Natl. Acad. Sci. USA , 95 : 9687 – 9692 .
  • Navarro-Gochicoa , M. T. , Camut , S. , Niebel , A. and Cullimore , J. V. 2003a . Expression of the apyrase-like APY1 genes in roots of Medicago truncatula is induced rapidly and transiently by stress and not by Sinorhizobium meliloti or Nod factors . Plant Physiol. , 131 : 1124 – 1136 .
  • Navarro-Gochicoa , M. T. , Camut , S. , Timmers , A. C. J. , Niebel , A. , Herve , C. , Boutet , E. , Bono , J. J. , Imberty , A. and Cullimore , J. V. 2003b . Characterization of four lectin-like receptor kinases expressed in roots of Medicago truncatula. Structure, location, regulation of expression, and potential role in the symbiosis with Sinorhizobium meliloti . Plant Physiol. , 133 : 1893 – 1910 .
  • Niehaus , K. , Lagares , A. and Puhler , 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 .
  • Noreen , S. , Schlaman , H. R. M. , Bellogin , R. A. , Buendia-Claveria , A. M. , Espuny , M. R. , Harteveld , M. , Medina , C. , Ollero , F. J. , Olsthoorn , M. M. A. , Soria-Diaz , M. E. , Spaink , H. P. , Temprano , F. , Thomas-Oates , J. , Vinardell , J. M. , Yang , S. S. , Zhang , H. Y. and Ruiz-Sainz , J. E. 2003 . Alfalfa nodulation by Sinorhizobium fredii does not require sulfated Nod-factors . Func. Plant Biol. , 30 : 1219 – 1232 .
  • Novero , M. , Faccio , A. , Genre , A. , Stougaard , J. , Webb , K. J. , Mulder , L. , Parniske , M. and Bonfante , P. 2002 . Dual requirement of the LjSym4gene for mycorrhizal development in epidermal and cortical cells of Lotus japonicus roots . New Phytol. , 154 : 741 – 749 .
  • Nuc , K. , Nuc , P. and Slomski , R. 2001 . Yellow lupine cyclophilin transcripts are highly accumulated in the nodule meristem zone . Mol. Plant Microbe Interact. , 14 : 1384 – 1394 .
  • Oke , V. and Long , S. R. 1999 . Bacterial genes induced within the nodule during the Rhizobium-legume symbiosis . Mol. Microbiol. , 32 : 837 – 849 .
  • Oldroyd , G. E. D. and Long , S. R. 2003 . Identification and characterization of nodulation-signaling pathway 2, a gene of Medicago truncatula involved in Nod factor signaling . Plant Physiol. , 131 : 1027 – 1032 .
  • Panstruga , R. and Schulze-Lefert , P. 2002 . Live and let live: insights into powdery mildew disease and resistance . Mole. Plant Pathol. , 3 : 495 – 502 .
  • Parniske , M. 2000 . Intracellular accommodation of microbes by plants: a common developmental program for symbiosis and disease? Curr . Opin. Plant Biol. , 3 : 320 – 328 .
  • Pawlowski , K. and Bisseling , T. 1996 . Rhizobial and actinorhizal symbioses: what are the shared features . Plant Cell , 8 : 1899 – 1913 .
  • Pawlowski , K. , Swensen , S. , Guan , C. H. , Hadri , A. E. , Berry , A. M. and Bisseling , T. 2003 . Distinct patterns of symbiosis-related gene expression in actinorhizal nodules from different plant families . Mol. Plant Microbe Interact. , 16 : 796 – 807 .
  • Pellock , B. J. , Cheng , H. P. and Walker , G. C. 2000 . Alfalfa root nodule invasion efficiency is dependent on Sinorhizobium meliloti polysaccharides . J. Bacteriol. , 182 : 4310 – 4318 .
  • Perotto , S. , Brewin , N. J. and Kannenberg , E. L. 1994 . Cytological evidence for a host-defense response that reduces cell and tissue invasion in pea nodules by lipopolysaccharide-defective mutants of Rhizobium leguminosarum strain 3841 . Mol. Plant Microbe Interact. , 7 : 99 – 112 .
  • Perotto , S. , Vandenbosch , K. A. , Butcher , G. W. and Brewin , N. J. 1991 . Molecular composition and development of the plant glycocalyx associated with the peribacteroid membrane of pea root-nodules . Development , 112 : 763 – 773 .
  • Perret , X. , Staehelin , C. and Broughton , W. J. 2000 . Molecular basis of symbiotic promiscuity . Microbiol. and Mol. Biol. Rev. , 64 : 180 – 195 .
  • Peters , N. K. and Verma , D. P. S. 1990 . Phenolic compounds as regulators of gene expression in plant-microbe relations . Mol. Plant Microbe Interact. , 3 : 4 – 8 .
  • Pichon , M. , Journet , E. P. and Dedieu , A. 1992 . Rhizobium meliloti induces transient expression of the early nodulin gene ENOD12 in the differentiating root epidermis of transgenic alfalfa . Plant Cell , 10 : 1199 – 1211 .
  • Pingret , J. L. , Journet , E. P. and Barker , D. G. 1998 . Rhizobium nod factor signaling: evidence for a G protein-mediated transduction mechanism . Plant Cell , 10 : 659 – 671 .
  • Price , N. J. , Pinheiro , C. , Soares , C. M. , Ashford , D. A. , Ricardo , C. P. and Jackson , P. A. 2003 . A biochemical and molecular characterization of LEP1, an extensin peroxidase from lupin . J. Biol. Chem. , 278 : 41389 – 41399 .
  • Quispel , A. 1988 . “ Hellriegel and Wilfarth's discovery of symbiotic nitrogen fixation one hundred years ago ” . In Nitrogen Fixation: Hundred Years After , Edited by: Bothe , H. , de Bruijn , F. and Newton , W. 3 – 12 . Stuttgart : Gustav Fischer .
  • Radutoiu , S. , Madsen , L. H. , Madsen , E. B. , Felle , H. H. , Umehara , Y. , Gronlund , M. , Sato , S. , Nakamura , Y. , Tabata , S. , Sandal , N. and Stougaard , J. 2003 . Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases . Nature , 425 : 585 – 592 .
  • Rae , A. L. , Bonfantefasolo , P. and Brewin , N. J. 1992 . Structure and growth of infection threads in the legume symbiosis with Rhizobium-leguminosarum . Plant J. , 2 : 385 – 395 .
  • Rae , A. L. , Perotto , S. , Knox , J. P. , Kannenberg , E. L. and Brewin , N. J. 1991 . Expression of extracellular glycoproteins in the uninfected cells of developing pea nodule tissue . Mol. Plant Microbe Interact. , 4 : 563 – 570 .
  • Ramu , S. K. , Peng , H. M. and Cook , D. R. 2002 . Nod factor induction of reactive oxygen species production is correlated with expression of the early nodulin gene rip1 in Medicago truncatula . Mol. Plant Microbe Interact. , 15 : 522 – 528 .
  • Rathbun , E. A. , Naldrett , M. J. and Brewin , N. J. 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 .
  • Relic , B. , Perret , X. , Estradagarcia , M. T. , Kopcinska , J. , Golinowski , W. , Krishnan , H. B. , Pueppke , S. G. and Broughton , W. J. 1994 . Nod factors of Rhizobium are a key to the legume door . Mol. Microb. , 13 : 171 – 178 .
  • Rodriguez-Carvajal , M. A. , du Penhoat , C. H. , Mazeau , K. , Doco , T. and Perez , S. 2003 . The three-dimensional structure of the mega-oligosaccharide rhamnogalacturonan II monomer: a combined molecular modeling and NMR investigation . Carbohyd. Res. , 338 : 651 – 671 .
  • Rodriguez-Llorente , I. D. , Perez–Hormaeche , J. , Dary , M. , Caviedes , M. A. , Kondorosi , A. , Ratet , P. and Palomares , A. J. 2003 . Expression of MsPG3-GFP fusions in Medicago truncatula ‘hairy roots’ reveals preferential tip localization of the protein in root hairs . Eur. J. Biochem. , 270 : 261 – 269 .
  • Roth , L. E. and 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 .
  • Saalbach , G. , Erik , P. and Wienkoop , S. 2002 . Characterisation by proteomics of peribacteroid space and peribacteroid membrane preparations from pea (Pisum sativum) symbiosomes . Proteomics , 2 : 325 – 337 .
  • Santi , C. , von Groll , U. , Ribeiro , A. , Chiurazzi , M. , Auguy , F. , Bogusz , D. , Franche , C. and Pawlowski , K. 2003 . Comparison of nodule induction in legume and actinorhizal symbioses: the induction of actinorhizal nodules does not involve ENOD40 . Mol. Plant Microbe Interact. , 16 : 808 – 816 .
  • Santos , R. , Herouart , D. , Puppo , A. and Touati , D. 2000 . Critical protective role of bacterial superoxide dismutase in Rhizobium-legume symbiosis . Mol. Microbiol. , 38 : 750 – 759 .
  • Scheible , W. R. , Fry , B. , Kochevenko , A. , Schindelasch , D. , Zimmerli , L. , Somerville , S. , Loria , R. and Somerville , C. R. 2003 . An Arabidopsis mutant resistant to thaxtomin A, a cellulose synthesis inhibitor from Streptomyces species . Plant Cell , 15 : 1781 – 1794 .
  • Scheres , B. , van Engelen , F. , van der Knap , E. , van de Wiel , C. , van Kammen , A. and Bisseling , T. 1990 . Sequential induction of nodulin gene expression in the developing pea nodule . Plant Cell , 2 : 687 – 700 .
  • Schultz , C. J. , Johnson , K. L. , Currie , G. and Bacic , A. 2000 . The classical arabinogalactan protein gene family of arabidopsis . Plant Cell , 12 : 1751 – 1767 .
  • Schultze , M. and Kondorosi , A. 1998 . Regulation of symbiotic root nodule development . Annu. Rev. Genet. , 32 : 33 – 57 .
  • Sharypova , L. A. , Niehaus , K. , Scheidle , H. , Holst , O. and Becker , A. 2003 . Sinorhizobium meliloti acpXL mutant lacks the C28 hydroxylated fatty acid moiety of lipid A and does not express a slow migrating form of lipopolysaccharide . J. Biol. Chem. , 278 : 12946 – 12954 .
  • Shaw , S. L. and Long , S. R. 2003a . Nod factor elicits two separable calcium responses in Medicago truncatula root hair cells . Plant Physiol. , 131 : 976 – 984 .
  • Shaw , S. L. and Long , S. R. 2003b . Nod factor inhibition of reactive oxygen efflux in a host legume . Plant Physiol. , 132 : 2196 – 2204 .
  • Sherrier , D. J. , Prime , T. A. and Dupree , P. 1999 . Glycosylphosphatidylinositol-anchored cell-surface proteins from Arabidopsis . Electrophoresis , 20 : 2027 – 2035 .
  • Shimada , N. , Aoki , T. , Sato , S. , Nakamura , Y. , Tabata , S. and Ayabe , S. 2003 . A cluster of genes encodes the two types of chalcone isomerase involved in the biosynthesis of general flavonoids and legume-specific 5-deoxy(iso)flavonoids in Lotus japonicus . Plant Physiol. , 131 : 941 – 951 .
  • Showalter , A. M. 2001 . Arabinogalactan-proteins: structure, expression and function . Cell. Mol. Life Sci. , 58 : 1399 – 1417 .
  • Sieberer , B. and Emons , A. M. C. 2000 . Cytoarchitecture and pattern of cytoplasmic streaming in root hairs of Medicago truncatula during development and deformation by nodulation factors . Protoplasma , 214 : 118 – 127 .
  • Sieberer , B. J. , Timmers , A. C. J. , Lhuissier , F. G. P. and Emons , A. M. C. 2002 . Endoplasmic microtubules configure the subapical cytoplasm and are required for fast growth of Medicago truncatula root hairs . Plant Physiol. , 130 : 977 – 988 .
  • Soltis , D. E. , Soltis , P. S. , Morgan , D. R. , Swensen , S. M. , Mullin , B. C. , Dowd , J. M. and Martin , P. G. 1995 . Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen-fixation in angiosperms . Proc. Natl. Acad. Sci. USA , 92 : 2647 – 2651 .
  • Spaink , H. P. , Kondorosi , A. and Hooykaas , P. J. J. 1998 . The Rhizobiaceae , Dordrecht : Kluwer .
  • Sprent , J. I. 2001 . Nodulation in Legumes , Kew, London : Royal Botanical Gardens .
  • Stougaard , J. 2001 . Genetics and genomics of root symbiosis . Curr. Opin. Plant Biol. , 4 : 328 – 335 .
  • Stracke , S. , Kistner , C. , Yoshida , S. , Mulder , L. , Sato , S. , Kaneko , T. , Tabata , S. , Sandal , N. , Stougaard , J. , Szczyglowski , K. and Parniske , M. 2002 . A plant receptor-like kinase required for both bacterial and fungal symbiosis . Nature , 417 : 959 – 962 .
  • Stuurman , N. , Bras , C. P. , Schlaman , H. R. M. , Wijfjes , A. H. M. , Bloemberg , G. and Spaink , H. P. 2000 . Use of green fluorescent protein color variants expressed on stable broad-host-range vectors to visualize rhizobia interacting with plants . Mol. Plant Microbe Interact. , 13 : 1163 – 1169 .
  • Szczyglowski , K. and Amyot , L. 2003 . Symbiosis, inventiveness by recruitment? . Plant Physiol. , 131 : 131 – 935 .
  • Szczyglowski , K. , Shaw , R. S. , Wopereis , J. , Copeland , S. , Hamburger , D. , Kasiborski , B. , Dazzo , F. B. and de Bruijn , F. J. 1998 . Nodule organogenesis and symbiotic mutants of the model legume Lotus japonicus . Mol. Plant Microbe Interact. , 11 : 684 – 697 .
  • Tan , L. , Qiu , F. , Lamport , D. T. A. and Kieliszewski , M. J. 2004 . Structure of a hydroxyproline (Hyp)-arabinogalactan polysaccharide from repetitive Ala-Hyp expressed in transgenic Nicotiana tabacum . J. Biol. Chem. , 279 : 13156 – 13165 .
  • Tansengco , M. L. , Hayashi , M. , Kawaguchi , M. , Imaizumi-Anraku , H. and 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 .
  • Tate , R. , Patriarca , E. J. , Riccio , A. , Defez , R. and Iaccarino , M. 1994 . Development of Phaseolus vulgaris root nodules . Mol. Plant Microbe Interact. , 7 : 582 – 589 .
  • Timmers , A. C. J. , Auriac , M. C. and Truchet , G. 1999 . Refined analysis of early symbiotic steps of the Rhizobium-Medicago interaction in relationship with microtubular cytoskeleton rearrangements . Devel. , 126 : 3617 – 3628 .
  • Trevaskis , B. , Wandrey , M. , Colebatch , G. and Udvardi , M. K. 2002 . The soybean GmN6L gene encodes a late nodulin expressed in the infected zone of nitrogen-fixing nodules . Mol. Plant Microbe Interact. , 15 : 630 – 636 .
  • Tsyganov , V. E. , Voroshilova , V. A. , Priefer , U. B. , Borisov , A. Y. and Tikhonovich , I. A. 2002 . Genetic dissection of the initiation of the infection process and nodule tissue development in the Rhizobium-pea (Pisum sativum L.) symbiosis . Ann. Botany , 89 : 357 – 366 .
  • Uheda , E. , Daimon , H. and Yoshizako , F. 2001 . Colonization and invasion of peanut (Arachis hypogaea L.) roots by gusA-marked Bradyrhizobium sp . Can. J. Botany-Revue Canadienne de Botanique , 79 : 733 – 738 .
  • Uheda , E. and Silvester , W. B. 2001 . The role of papillae during the infection process in the Gunnera-Nostoc symbiosis . Plant and Cell Physiol. , 42 : 780 – 783 .
  • van Brussel , A. A. N. , Bakhuizen , R. , van Spronsen , P. C. , Spaink , H. P. , Tak , T. K. , Lugtenberg , B. J. J. and Kijne , J. W. 1992 . Induction of pre-infection thread structures in the leguminous host plant by mitogenic lipo-oligosaccharides of Rhizobium . Science , 257 : 70 – 72 .
  • van Rhijn , P. , Fujishige , N. A. , Lim , P. O. and Hirsch , A. M. 2001 . Sugar-binding activity of pea lectin enhances heterologous infection of transgenic alfalfa plants by Rhizobium leguminosarum biovar viciae . Plant Physiol. , 126 : 133 – 144 .
  • van Rhijn , P. , Goldberg , R. B. and Hirsch , A. M. 1998 . Lotus corniculatus nodulation specificity is changed by the presence of a soybean lectin gene . Plant Cell , 10 : 1233 – 1249 .
  • van Spronsen , P. C. , Bakhuizen , R. , van Brussel , A. A. N. and Kijne , J. W. 1994 . Cell-wall degradation during infection thread formation by the root- nodule bacterium Rhizobium leguminosarum is a 2-step process . Eur. J. Cell Biol. , 64 : 88 – 94 .
  • van Spronsen , P. C. , Gronlund , M. , Bras , C. P. , Spaink , H. P. and Kijne , J. W. 2001 . Cell biological changes of outer cortical root cells in early determinate nodulation . Mol. Plant Microbe Interact. , 14 : 839 – 847 .
  • van Spronsen , P. C. , Tak , T. , Rood , A. M. M. , van Brussel , A. A. N. , Kijne , J. W. and Boot , K. J. M. 2003 . Salicylic acid inhibits indeterminate-type nodulation but not determinate-type nodulation . Mol. Plant Microbe Interact. , 16 : 83 – 91 .
  • Vanden Bosch , K. A. , Bradley , D. J. , Knox , J. P. , Perotto , S. , Butcher , G. W. and Brewin , N. J. 1989 . Common components of the infection thread matrix and the intercellular space identified by immunocytochemical analysis of pea nodules and uninfected roots . EMBO J. , 8 : 335 – 341 .
  • Vernoud , V. , Journet , E. P. and Barker , D. G. 1999 . MtENOD20, a Nod factor-inducible molecular marker for root cortical cell activation . Mol. Plant Microbe Interact. , 12 : 604 – 614 .
  • Vincent , J. L. and Brewin , N. J. 2000 . Immunolocalization of a cysteine protease in vacuoles, vesicles, and symbiosomes of pea nodule cells . Plant Physiol. , 123 : 521 – 530 .
  • Vincent , J. L. , Dahiya , P. and Brewin , N. J. 2000 . Localized expression of cathepsin B-like sequences from root nodules of pea (Pisum sativum) . Mol. Plant Microbe Interact. , 13 : 778 – 780 .
  • Voroshilova , V. A. , Boesten , B. , Tsyganov , V. E. , Borisov , A. Y. , Tikhonovich , I. A. and Priefer , U. B. 2001 . Effect of mutations in Pisum sativum L. genes blocking different stages of nodule development on the expression of late symbiotic genes in Rhizobium leguminosarum bv. viciae . Mol. Plant Microbe Interact. , 14 : 471 – 476 .
  • Walker , S. A. and Downie , J. A. 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 .
  • Wang , L. X. , Wang , Y. , Pellock , B. and Walker , G. C. 1999 . Structural characterization of the symbiotically important low-molecular-weight succinoglycan of Sinorhizobium meliloti . J. Bacteriology , 181 : 6788 – 6796 .
  • Wilson , R. C. , Long , S. R. , Maruoka , E. M. and Cooper , J. B. 1994 . A new proline-rich early nodulin from Medicago truncatula is highly expressed in nodule meristematic cells . Plant Cell , 6 : 1265 – 1275 .
  • Wisniewski-Dye , F. and Downie , J. A. 2002 . Quorum-sensing in Rhizobium . Antonie Van Leeuwenhoek Int. J. General Mole. Microbiol. , 81 : 397 – 407 .
  • Wisniewski , J. P. , Gardner , C. D. and Brewin , N. J. 1999 . Isolation of lipoxygenase cDNA clones from pea nodule mRNA . Plant Mol. Biol. , 39 : 775 – 783 .
  • Wisniewski , J. P. , Rathbun , E. A. , Knox , J. P. and Brewin , N. J. 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 .
  • Wycoff , K. L. , Hunt , S. , Gonzales , M. B. , Vandenbosch , K. A. , Layzell , D. B. and Hirsch , A. M. 1998 . Effects of oxygen on nodule physiology and expression of nodulins in alfalfa . Plant Physiol. , 117 : 385 – 395 .
  • Yang , W. C. , de Blank , C. , Franssen , H. and Bisseling , T. 1994 . Rhizobium nod factors reactivate the cell cycle during infection and nodule primordium formation, but the cell cycle is only completed in primordium formation . Plant Cell , 6 : 1415 – 1426 .
  • Zhao , Z. D. , Tan , L. , Showalter , A. M. , Lamport , D. T. A. and Kieliszewski , M. J. 2002 . Tomato LeAGP-1 arabinogalactan-protein purified from transgenic tobacco corroborates the Hyp contiguity hypothesis . Plant J. , 31 : 431 – 444 .

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