Chitooligosaccharide sensing and downstream signaling: Contrasted outcomes in pathogenic and beneficial plant-microbe interactions

Planta

Volumn 232, Issue 4, 2010, Pages 787-806

  Hamel, Louis Philippe ^a   Beaudoin, Nathalie ^a  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

Author keywords

Chitin receptor; Chitooligosaccharide; Defense response; Nod factor receptor; Rhizobial symbiosis; Signal perception and transduction

Indexed keywords

CHITIN; OLIGOSACCHARIDE;

HOST PATHOGEN INTERACTION; METABOLISM; PHYSIOLOGY; REVIEW; RHIZOBIUM; SIGNAL TRANSDUCTION; SYMBIOSIS;

CHITIN; HOST-PATHOGEN INTERACTIONS; OLIGOSACCHARIDES; RHIZOBIUM; SIGNAL TRANSDUCTION; SYMBIOSIS;

RHIZOBIACEAE;

EID: 77955841193     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-010-1215-9     Document Type: Review

References (176)

1. Amborabé BE, Bonmort J, Fleurat-Lessard P, Roblin G (2008) Early events induced by chitosan on plant cells. J Exp Bot 59: 2317-2324.
2. Andriankaja A, Boisson-Dernier A, Frances L, Sauviac L, Jauneau A, Barker DG, de Carvalho-Niebel F (2007) AP2-ERF transcription factors mediate Nod factor dependent MtENOD11 activation in root hairs via a novel cis-regulatory motif. Plant Cell 19: 2866-2885.
3. Ané JM, Kiss GB, Riely BK, Penmetsa RV, Oldroyd GE, Ayax C, Lévy J, Debellé F, Baek JM, Kaló P, Rosenberg C, Roe BA, Long SR, Dénarié J, Cook DR (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303: 1364-1367.
4. Arlorio M, Ludwig A, Boller T, Bonafonte P (1992) Inhibition of fungal growth by plant chitinases and β-1, 3-glucanases. Protoplasma 171: 34-43.
5. Arrighi JF, Barre A, Ben Amor B, Bersoult A, Soriano LC, Mirabella R, de Carvalho-Niebel F, Journet EP, Gherardi M, Huguet T, Geurts R, Dénarié J, Rouge P, Gough C (2006) The Medicago truncatula lysin motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol 142: 265-279.
6. Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415: 977-983.
7. Asamizu E, Nakamura Y, Sato S, Tabata S (2005) Comparison of the transcript profiles from the root and the nodulating root of the model legume Lotus japonicus by serial analysis of gene expression. Mol Plant Microbe Interact 18: 487-498.
8. Aslam SN, Newman MA, Erbs G, Morrissey KL, Chinchilla D, Boller T, Jensen TT, De Castro C, Ierano T, Molinaro A, Jackson RW, Knight MR, Cooper RM (2008) Bacterial polysaccharides suppress induced innate immunity by calcium chelation. Curr Biol 18: 1078-1083.
9. Ausubel FM (2005) Are innate immune signaling pathways in plants and animals conserved? Nat Immunol 6: 973-979.
10. Barber MS, Bertram RE, Ride JP (1989) Chitin oligosaccharides elicit lignification in wounded wheat leaves. Physiol Mol Plant Pathol 34: 3-12.
11. Barnett MJ, Fisher RF (2006) Global gene expression in the rhizobial-legume symbiosis. Symbiosis 42: 1-24.
12. Barnett MJ, Toman CJ, Fisher RF, Long SR (2004) A dual-genome symbiosis chip for coordinate study of signal exchange and development in a prokaryote-host interaction. Proc Natl Acad Sci USA 101: 16636-16641.
13. Baureithel K, Felix G, Boller T (1994) Specific, high affinity binding of chitin fragments to tomato cells and membranes. Competitive inhibition of binding by derivatives of chitooligosaccharides and a Nod factor of Rhizobium. J Biol Chem 269: 17931-17938.
14. Bek AS, Sauer J, Thygesen MB, Duus JO, Petersen BO, Thirup S, James E, Jensen KJ, Stougaard J, Radutoiu S (2010) Improved characterization of Nod factors and genetically based variation in LysM Receptor domains identify amino acids expendable for nod factor recognition in Lotus spp. Mol Plant Microbe Interact 23: 58-66.
15. Ben Amor B, Shaw SL, Oldroyd GE, 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.
16. Benedito VA, Torres-Jerez I, Murray JD, Andriankaja A, Allen S, Kakar K, Wandrey M, Verdier J, Zuber H, Ott T, Moreau S, Niebel A, Frickey T, Weiller G, He J, Dai X, Zhao PX, Tang Y, Udvardi MK (2008) A gene expression atlas of the model legume Medicago truncatula. Plant J 55: 504-513.
17. Bittel P, Robatzek S (2007) Microbe-associated molecular patterns (MAMPs) probe plant immunity. Curr Opin Plant Biol 10: 335-341.
18. Bladergroen MR, Spaink HP (1998) Genes and signal molecules involved in the rhizobia-leguminoseae symbiosis. Curr Opin Plant Biol 1: 353-359.
19. Blair DE, Hekmat O, Schuttelkopf AW, Shrestha B, Tokuyasu K, Withers SG, van Aalten DM (2006) Structure and mechanism of chitin deacetylase from the fungal pathogen Colletotrichum lindemuthianum. Biochemistry 45: 9416-9426.
20. Block A, Li G, Fu ZQ, Alfano JR (2008) Phytopathogen type III effector weaponry and their plant targets. Curr Opin Plant Biol 11: 396-403.
21. Bolle C (2004) The role of GRAS proteins in plant signal transduction and development. Planta 218: 683-692.
22. Boller T (1995) Chemoperception of microbial signals in plant cells. Annu Rev Plant Physiol Plant Mol Biol 46: 189-214.
23. Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60: 379-406.
24. Boller T, He SY (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324: 742-744.
25. Bono JJ, Riond J, Nicolaou KC, Bockovich NJ, Estevez VA, Cullimore JV, Ranjeva R (1995) Characterization of a binding site for chemically synthesized lipo-oligosaccharidic NodRm factors in particulate fractions prepared from roots. Plant J 7: 253-260.
26. Borisov AY, Madsen LH, Tsyganov VE, Umehara Y, Voroshilova VA, Batagov AO, Sandal N, Mortensen A, Schauser L, Ellis N, Tikhonovich IA, Stougaard J (2003) The Sym35 gene required for root nodule development in pea is an ortholog of Nin from Lotus japonicus. Plant Physiol 131: 1009-1017.
27. Brechenmacher L, Kim MY, Benitez M, Li M, Joshi T, Calla B, Lee MP, Libault M, Vodkin LO, Xu D, Lee SH, Clough SJ, Stacey G (2008) Transcription profiling of soybean nodulation by Bradyrhizobium japonicum. Mol Plant Microbe Interact 21: 631-645.
28. Brogue K, Chet I, Holliday M, Cressman R, Biddle P, Knowlton S, Mauvais CJ, Broglie R (1991) Transgenic plants with enhanced resistance to the fungal pathogen Rhizoctonia solani. Science 254: 1194-1197.
29. Buist G, Steen A, Kok J, Kuipers OP (2008) LysM, a widely distributed protein motif for binding to (peptido)glycans. Mol Microbiol 68: 838-847.
30. Cabrera JC, Messiaen J, Cambier P, van Cutsem P (2006) Size, acetylation and concentration of chitooligosaccharide elicitors determine the switch from defense involving PAL activation to cell death and water peroxide production in Arabidopsis cell suspensions. Physiol Plant 127: 44-56.
31. Capela D, Carrere S, Batut J (2005) Transcriptome-based identification of the Sinorhizobium meliloti NodD1 regulon. Appl Environ Microbiol 71: 4910-4913.
32. Catoira R, Galera C, de Billy F, Penmetsa RV, Journet EP, Maillet F, Rosenberg C, Cook D, Gough C, Dénarié J (2000) Four genes of Medicago truncatula controlling components of a Nod factor transduction pathway. Plant Cell 12: 1647-1666.
33. Chang C, Damiani I, Puppo A, Frendo P (2009) Redox changes during the legume-rhizobium symbiosis. Mol Plant 2: 370-377.
34. 2+ spiking and specific ENOD gene expression. Plant Physiol 136: 3582-3593.
35. Chen HP, Xu LL (2005) Isolation and characterization of a novel chitosan-binding protein from non-heading Chinese cabbage leaves. J Integr Plant Biol 47: 452-456.
36. Chinchilla D, Shan L, He P, de Vries S, Kemmerling B (2009) One for all: the receptor-associated kinase BAK1. Trends Plant Sci 14: 535-541.
37. Chujo T, Takai R, Akimoto-Tomiyama C, Ando S, Minami E, Nagamura Y, Kaku H, Shibuya N, Yasuda M, Nakashita H, Umemura K, Okada A, Okada K, Nojiri H, Yamane H (2007) Involvement of the elicitor-induced gene OsWRKY53 in the expression of defense-related genes in rice. Biochim Biophys Acta 1769: 497-505.
38. Chye ML, Zhao KJ, He ZM, Ramalingam S, Fung KL (2005) An agglutinating chitinase with two chitin-binding domains confers fungal protection in transgenic potato. Planta 220: 717-730.
39. Colebatch G, Kloska S, Trevaskis B, Freund S, Altmann T, Udvardi MK (2002) Novel aspects of symbiotic nitrogen fixation uncovered by transcript profiling with cDNA arrays. Mol Plant Microbe Interact 15: 411-420.
40. Colebatch G, Desbrosses G, Ott T, Krusell L, Montanari O, Kloska S, Kopka J, Udvardi MK (2004) Global changes in transcription orchestrate metabolic differentiation during symbiotic nitrogen fixation in Lotus japonicus. Plant J 39: 487-512.
41. Cullimore J, Dénarié J (2003) Plant sciences. How legumes select their sweet talking symbionts. Science 302: 575-578.
42. D'Haeze W, Holsters M (2002) Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 12: 79R-105R.
43. Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411: 826-833.
44. Day RB, McAlvin CB, Loh JT, Denny RL, Wood TC, Young ND, Stacey G (2000) Differential expression of two soybean apyrases, one of which is an early nodulin. Mol Plant Microbe Interact 13: 1053-1070.
45. Day RB, Okada M, Ito Y, Tsukada K, Zaghouani H, Shibuya N, Stacey G (2001) Binding site for chitin oligosaccharides in the soybean plasma membrane. Plant Physiol 126: 1162-1173.
46. Day RB, Akimoto-Tomiyama C, Yazaki J, Nakamura K, Fujii F, Shimbo K, Yamamoto K, Sakata K, Sasaki T, Kishimoto N, Kikuchi S, Shibuya N, Minami E (2002) Large-scale identification of elicitor-responsive genes in suspension-cultured rice cells by DNA microarray. Plant Biotechnol 19: 153-155.
47. de Jonge R, Thomma BP (2009) Fungal LysM effectors: extinguishers of host immunity? Trends Microbiol 17: 151-157.
48. Dénarié J, Debellé F, Promé JC (1996) Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu Rev Biochem 65: 503-535.
49. Dodds PN, Lawrence GJ, Catanzariti AM, Teh T, Wang CI, Ayliffe MA, Kobe B, Ellis JG (2006) Direct protein interaction underlies gene-for-gene specificity and coevolution of the flax resistance genes and flax rust avirulence genes. Proc Natl Acad Sci USA 103: 8888-8893.
50. 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.
51. Ehrhardt DW, Wais R, Long SR (1996) Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85: 673-681.
52. El Yahyaoui F, Kuster H, Ben Amor B, Hohnjec N, Puhler A, Becker A, Gouzy J, Vernie 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.
53. Endre G, Kereszt A, Kevei Z, Mihacea S, Kaló P, Kiss GB (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417: 962-966.
54. 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.
55. Esseling JJ, Lhuissier FG, Emons AM (2003) Nod factor-induced root hair curling: continuous polar growth towards the point of Nod factor application. Plant Physiol 132: 1982-1988.
56. Etzler ME, Kalsi G, Ewing NN, Roberts NJ, Day RB, Murphy JB (1999) A nod factor binding lectin with apyrase activity from legume roots. Proc Natl Acad Sci USA 96: 5856-5861.
57. Eulgem T (2005) Regulation of the Arabidopsis defense transcriptome. Trends Plant Sci 10: 71-78.
58. Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10: 366-371.
59. Fauvart M, Michiels J (2008) Rhizobial secreted proteins as determinants of host specificity in the Rhizobium-legume symbiosis. FEMS Microbiol Lett 285: 1-9.
60. Felix G, Regenass M, Boller T (1993) Specific perception of subnanomolar concentrations of chitin fragments by tomato cells-induction of extracellular alkalinization, changes in protein-phosphorylation, and establishment of a refractory state. Plant J 4: 307-316.
61. Fiil BK, Petersen K, Petersen M, Mundy J (2009) Gene regulation by MAP kinase cascades. Curr Opin Plant Biol 12: 615-621.
62. Foucher F, Kondorosi E (2000) Cell cycle regulation in the course of nodule organogenesis in Medicago. Plant Mol Biol 43: 773-786.
63. Gage DJ (2002) Analysis of infection thread development using Gfp- and DsRed-expressing Sinorhizobium meliloti. J Bacteriol 184: 7042-7046.
64. 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.
65. Garvey KJ, Saedi MS, Ito J (1986) Nucleotide sequence of Bacillus phage phi 29 genes 14 and 15: homology of gene 15 with other phage lysozymes. Nucleic Acids Res 14: 10001-10008.
66. 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.
67. Gibson KE, Kobayashi H, Walker GC (2008) Molecular determinants of a symbiotic chronic infection. Annu Rev Genet 42: 413-441.
68. Gimenez-Ibanez S, Hann DR, Ntoukakis V, Petutschnig E, Lipka V, Rathjen JP (2009a) AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr Biol 19: 423-429.
69. Gimenez-Ibanez S, Ntoukakis V, Rathjen JP (2009b) The LysM receptor kinase CERK1 mediates bacterial perception in Arabidopsis. Plant Signal Behav 4: 539-541.
70. Giraud E, Moulin L, Vallenet D, Barbe V, Cytryn E, Avarre JC, Jaubert M, Simon D, Cartieaux F, Prin Y, Bena G, Hannibal L, Fardoux J, Kojadinovic M, Vuillet L, Lajus A, Cruveiller S, Rouy Z, Mangenot S, Segurens B, Dossat C, Franck WL, Chang WS, Saunders E, Bruce D, Richardson P, Normand P, Dreyfus B, Pignol D, Stacey G, Emerich D, Vermeglio A, Medigue C, Sadowsky M (2007) Legumes symbioses: absence of Nod genes in photosynthetic bradyrhizobia. Science 316: 1307-1312.
71. Gleason C, Chaudhuri S, Yang T, Muñoz A, Poovaiah BW, Oldroyd GE (2006) Nodulation independent of rhizobia induced by a calcium-activated kinase lacking autoinhibition. Nature 441: 1149-1152.
72. Goedhart J, Bono JJ, Bisseling T, Gadella TW Jr (2003) Identical accumulation and immobilization of sulfated and nonsulfated Nod factors in host and nonhost root hair cell walls. Mol Plant Microbe Interact 16: 884-892.
73. Govindarajulu M, Kim SY, Libault M, Berg RH, Tanaka K, Stacey G, Taylor CG (2009) GS52 ecto-apyrase plays a critical role during soybean nodulation. Plant Physiol 149: 994-1004.
74. Grant SR, Fisher EJ, Chang JH, Mole BM, Dangl JL (2006) Subterfuge and manipulation: type III effector proteins of phytopathogenic bacteria. Annu Rev Microbiol 60: 425-449.
75. Gressent F, Drouillard S, Mantegazza N, Samain E, Geremia RA, Canut H, Niebel A, Driguez H, Ranjeva R, Cullimore J, Bono JJ (1999) Ligand specificity of a high-affinity binding site for lipo-chitooligosaccharidic Nod factors in Medicago cell suspension cultures. Proc Natl Acad Sci USA 96: 4704-4709.
76. Gressent F, Mantegazza N, Cullimore JV, Driguez H, Ranjeva R, Bono JJ (2002) High-affinity nod factor binding site from Phaseolus vulgaris cell suspension cultures. Mol Plant Microbe Interact 15: 834-839.
77. Hamel LP, Miles GP, Samuel MA, Ellis BE, Séguin A, Beaudoin N (2005) Activation of stress-responsive mitogen-activated protein kinase pathways in hybrid poplar (Populus trichocarpa x Populus deltoides). Tree Physiol 25: 277-288.
78. Heckmann AB, Lombardo F, Miwa H, Perry JA, Bunnewell S, Parniske M, Wang TL, Downie JA (2006) Lotus japonicus nodulation requires two GRAS domain regulators, one of which is functionally conserved in a non-legume. Plant Physiol 142: 1739-1750.
79. Hirsch S, Kim J, Muñoz A, Heckmann AB, Downie JA, Oldroyd GE (2009) GRAS proteins form a DNA binding complex to induce gene expression during nodulation signaling in Medicago truncatula. Plant Cell 21: 545-557.
80. Hogg BV, Cullimore JV, Ranjeva R, Bono JJ (2006) The DMI1 and DMI2 early symbiotic genes of medicago truncatula are required for a high-affinity nodulation factor-binding site associated to a particulate fraction of roots. Plant Physiol 140: 365-373.
81. Høgslund N, Radutoiu S, Krusell L, Voroshilova V, Hannah MA, Goffard N, Sanchez DH, Lippold F, Ott T, Sato S, Tabata S, Liboriussen P, Lohmann GV, Schauser L, Weiller GF, Udvardi MK, Stougaard J (2009) Dissection of symbiosis and organ development by integrated transcriptome analysis of Lotus japonicus mutant and wild-type plants. PLoS One 4: e6556.
82. Holley SR, Yalamanchili RD, Moura DS, Ryan CA, Stratmann JW (2003) Convergence of signaling pathways induced by systemin, oligosaccharide elicitors, and ultraviolet-B radiation at the level of mitogen-activated protein kinases in Lycopersicon peruvianum suspension-cultured cells. Plant Physiol 132: 1728-1738.
83. Iizasa E, Mitsutomi M, Nagano Y (2010) Direct binding of a plant LysM receptor-like kinase, LysM RLK1/CERK1, to chitin in vitro. J Biol Chem 285: 2996-3004.
84. Imaizumi-Anraku H, Takeda N, Charpentier M, Perry J, Miwa H, Umehara Y, Kouchi H, Murakami Y, Mulder L, Vickers K, Pike J, Downie JA, Wang T, Sato S, Asamizu E, Tabata S, Yoshikawa M, Murooka Y, Wu GJ, Kawaguchi M, Kawasaki S, Parniske M, Hayashi M (2005) Plastid proteins crucial for symbiotic fungal and bacterial entry into plant roots. Nature 433: 527-531.
85. Iriti M, Faoro F (2009) Chitosan as a MAMP, searching for a PRR. Plant Signal Behav 4: 66-68.
86. Ito Y, Kaku H, Shibuya N (1997) Identification of a high-affinity binding protein for N-acetylchitooligosaccharide elicitor in the plasma membrane of suspension-cultured rice cells by affinity labeling. Plant J 12: 347-356.
87. Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B (2000) Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J 19: 4004-4014.
88. Jones JD, Dangl JL (2006) The plant immune system. Nature 444: 323-329.
89. Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat Rev Microbiol 5: 619-633.
90. Joris B, Englebert S, Chu CP, Kariyama R, Daneo-Moore L, Shockman GD, Ghuysen JM (1992) Modular design of the Enterococcus hirae muramidase-2 and Streptococcus faecalis autolysin. FEMS Microbiol Lett 91: 257-264.
91. Kaku H, Nishizawa Y, Ishii-Minami N, Akimoto-Tomiyama C, Dohmae N, Takio K, Minami E, Shibuya N (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc Natl Acad Sci USA 103: 11086-11091.
92. Kaló P, Gleason C, Edwards A, Marsh J, Mitra RM, Hirsch S, Jakab J, Sims S, Long SR, Rogers J, Kiss GB, Downie JA, Oldroyd GE (2005) Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308: 1786-1789.
93. Kalsi G, Etzler ME (2000) Localization of a Nod factor-binding protein in legume roots and factors influencing its distribution and expression. Plant Physiol 124: 1039-1048.
94. 2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc Natl Acad Sci USA 103: 359-364.
95. Knogge W, Scheel D (2006) LysM receptors recognize friend and foe. Proc Natl Acad Sci USA 103: 10829-10830.
96. Kouchi H, Hata S (1995) GmN56, a novel nodule-specific cDNA from soybean root nodules encodes a protein homologous to isopropylmalate synthase and homocitrate synthase. Mol Plant Microbe Interact 8: 172-176.
97. Lee H, Hur CG, Oh CJ, Kim HB, Pakr SY, An CS (2004) Analysis of the root nodule-enhanced transcriptome in soybean. Mol Cells 18: 53-62.
98. 2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 303: 1361-1364.
99. Libault M, Wan J, Czechowski T, Udvardi M, Stacey G (2007) Identification of 118 Arabidopsis transcription factor and 30 ubiquitin-ligase genes responding to chitin, a plant-defense elicitor. Mol Plant Microbe Interact 20: 900-911.
100. Libault M, Joshi T, Takahashi K, Hurley-Sommer A, Puricelli K, Blake S, Finger RE, Taylor CG, Xu D, Nguyen HT, Stacey G (2009) Large-scale analysis of putative soybean regulatory gene expression identifies a Myb gene involved in soybean nodule development. Plant Physiol 151: 1207-1220.
101. Libault M, Farmer A, Brechenmacher L, Drnevich J, Langley RJ, Bilgin DD, Radwan O, Neece DJ, Clough SJ, May GD, Stacey G (2010) Complete transcriptome of the soybean root hair cell, a single-cell model, and its alteration in response to Bradyrhizobium japonicum infection. Plant Physiol 152: 541-552.
102. 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.
103. Lin W, Hu X, Zhang W, Rogers WJ, Cai W (2005) Hydrogen peroxide mediates defence responses induced by chitosans of different molecular weights in rice. J Plant Physiol 162: 937-944.
104. Lohar DP, Sharopova N, Endre G, Penuela S, Samac D, Town C, Silverstein KA, VandenBosch KA (2006) Transcript analysis of early nodulation events in Medicago truncatula. Plant Physiol 140: 221-234.
105. Lohmann GV, Shimoda Y, Nielsen MW, Jorgensen FG, Grossmann C, Sandal N, Sorensen K, Thirup S, Madsen LH, Tabata S, Sato S, Stougaard J, Radutoiu S (2010) Evolution and regulation of the Lotus japonicus LysM receptor gene family. Mol Plant Microbe Interact 23: 510-521.
106. Long SR (1996) Rhizobium symbiosis: Nod factors in perspective. Plant Cell 8: 1885-1898.
107. Madsen EB, Madsen LH, Radutoiu S, Olbryt M, Rakwalska M, Szczyglowski K, Sato S, Kaneko T, Tabata S, Sandal N, Stougaard J (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425: 637-640.
108. Maleck K, Levine A, Eulgem T, Morgan A, Schmid J, Lawton KA, Dangl JL, Dietrich RA (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26: 403-410.
109. Marsh JF, Rakocevic A, Mitra RM, Brocard L, Sun J, Eschstruth A, Long SR, Schultze M, Ratet P, Oldroyd GE (2007) Medicago truncatula NIN is essential for rhizobial-independent nodule organogenesis induced by autoactive calcium/calmodulin-dependent protein kinase. Plant Physiol 144: 324-335.
110. Mathesius U (2003) Conservation and divergence of signalling pathways between roots and soil microbes: the Rhizobium-legume symbiosis compared to the development of lateral roots, mycorrhizal interactions and nematode-induced galls. Plant Soil 255: 105-119.
111. McAlvin CB, Stacey G (2005) Transgenic expression of the soybean apyrase in Lotus japonicus enhances nodulation. Plant Physiol 137: 1456-1462.
112. Messinese E, Mun JH, Yeun LH, Jayaraman D, Rouge P, Barre A, Lougnon G, Schornack S, Bono JJ, Cook DR, Ané JM (2007) A novel nuclear protein interacts with the symbiotic DMI3 calcium- and calmodulin-dependent protein kinase of Medicago truncatula. Mol Plant Microbe Interact 20: 912-921.
113. Mészáros T, Helfer A, Hatzimasoura E, Magyar Z, Serazetdinova L, Rios G, Bardóczy V, Teige M, Koncz C, Peck S, Bögre L (2006) The Arabidopsis MAP kinase kinase MKK1 participates in defence responses to the bacterial elicitor flagellin. Plant J 48: 485-498.
114. Middleton PH, Jakab J, Penmetsa RV, Starker CG, Doll J, Kaló P, Prabhu R, Marsh JF, Mitra RM, Kereszt A, Dudas B, VandenBosch K, Long SR, Cook DR, Kiss GB, Oldroyd GE (2007) An ERF transcription factor in Medicago truncatula that is essential for Nod factor signal transduction. Plant Cell 19: 1221-1234.
115. 2+/calmodulin-dependent protein kinase required for symbiotic nodule development: Gene identification by transcript-based cloning. Proc Natl Acad Sci USA 101: 4701-4705.
116. Mitra RM, Shaw SL, Long SR (2004b) 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.
117. Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci USA 104: 19613-19618.
118. Murakami Y, Miwa H, Imaizumi-Anraku H, Kouchi H, Downie JA, Kawaguchi M, Kawasaki S (2006) Positional cloning identifies Lotus japonicus NSP2, a putative transcription factor of the GRAS family, required for NIN and ENOD40 gene expression in nodule initiation. DNA Res 13: 255-265.
119. Navarro L, Zipfel C, Rowland O, Keller I, Robatzek S, Boller T, Jones JD (2004) The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiol 135: 1113-1128.
120. Ohnuma T, Onaga S, Murata K, Taira T, Katoh E (2008) LysM domains from Pteris ryukyuensis chitinase-A: a stability study and characterization of the chitin-binding site. J Biol Chem 283: 5178-5187.
121. Okada M, Matsumura M, Ito Y, Shibuya N (2002) High-affinity binding proteins for N-acetylchitooligosaccharide elicitor in the plasma membranes from wheat, barley and carrot cells: conserved presence and correlation with the responsiveness to the elicitor. Plant Cell Physiol 43: 505-512.
122. Okada A, Okada K, Miyamoto K, Koga J, Shibuya N, Nojiri H, Yamane H (2009) OsTGAP1, a bZIP transcription factor, coordinately regulates the inductive production of diterpenoid phytoalexins in rice. J Biol Chem 284: 26510-26518.
123. Oldroyd GE, Downie JA (2008) Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 59: 519-546.
124. Oldroyd GE, Long SR (2003) Identification and characterization of nodulation-signaling pathway 2, a gene of Medicago truncatula involved in Nod actor signaling. Plant Physiol 131: 1027-1032.
125. Onaga S, Taira T (2008) A new type of plant chitinase containing LysM domains from a fern (Pteris ryukyuensis): roles of LysM domains in chitin binding and antifungal activity. Glycobiology 18: 414-423.
126. Osbourn AE (1996) Preformed antimicrobial compounds and plant defense against fungal attack. Plant Cell 8: 1821-1831.
127. Passarinho PA, de Vries SC (2002) Arabidopsis chitinases: a genomic survey. In: The Arabidopsis book. American Society of Plant Biologists, Rockville. doi: 10. 1199/tab. 0023.
128. Peck MC, Fisher RF, Long SR (2006) Diverse flavonoids stimulate NodD1 binding to nod gene promoters in Sinorhizobium meliloti. J Bacteriol 188: 5417-5427.
129. 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, Ané JM (2007) The Medicago truncatula DMI1 protein modulates cytosolic calcium signaling. Plant Physiol 145: 192-203.
130. Perret X, Staehelin C, Broughton WJ (2000) Molecular basis of symbiotic promiscuity. Microbiol Mol Biol Rev 64: 180-201.
131. Peters JW, Szilagyi RK (2006) Exploring new frontiers of nitrogenase structure and mechanism. Curr Opin Chem Biol 10: 101-108.
132. Pichon M, Journet EP, Dedieu A, de Billy F, Truchet G, Barker DG (1992) Rhizobium meliloti elicits transient expression of the early nodulin gene ENOD12 in the differentiating root epidermis of transgenic alfalfa. Plant Cell 4: 1199-1211.
133. Popescu SC, Popescu GV, Bachan S, Zhang Z, Gerstein M, Snyder M, Dinesh-Kumar SP (2009) MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes Dev 23: 80-92.
134. Raafat D, von Bargen K, Haas A, Sahl HG (2008) Insights into the mode of action of chitosan as an antibacterial compound. Appl Environ Microbiol 74: 3764-3773.
135. Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y, Gronlund M, Sato S, Nakamura Y, Tabata S, Sandal N, Stougaard J (2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425: 585-592.
136. 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.
137. Ramonell KM, Zhang B, Ewing RM, Chen Y, Xu D, Stacey G, Somerville S (2002) Microarray analysis of chitin elicitation in Arabidopsis thaliana. Mol Plant Pathol 3: 301-311.
138. Ramonell K, Berrocal-Lobo M, Koh S, Wan J, Edwards H, Stacey G, Somerville S (2005) Loss-of-function mutations in chitin responsive genes show increased susceptibility to the powdery mildew pathogen Erysiphe cichoracearum. Plant Physiol 138: 1027-1036.
139. Raymond J, Siefert JL, Staples CR, Blankenship RE (2004) The natural history of nitrogen fixation. Mol Biol Evol 21: 541-554.
140. Riely BK, Ané JM, 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.
141. Riely BK, Lougnon G, 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.
142. Roby D, Broglie K, Cressman R, Biddle P, Chet IL, Broglie R (1990) Activation of a bean chitinase promoter in transgenic tobacco plants by phytopathogenic fungi. Plant Cell 2: 999-1007.
143. Roche P, Maillet F, Plazanet C, Debellé F, Ferro M, Truchet G, Promé JC, Dénarié J (1996) The common nodABC genes of Rhizobium meliloti are host-range determinants. Proc Natl Acad Sci USA 93: 15305-15310.
144. Saito K, Yoshikawa M, Yano K, Miwa H, Uchida H, Asamizu E, Sato S, Tabata S, Imaizumi-Anraku H, Umehara Y, Kouchi H, Murooka Y, Szczyglowski K, Downie JA, Parniske M, Hayashi M, Kawaguchi M (2007) NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell 19: 610-624.
145. Samac DA, Shah DM (1991) Developmental and pathogen-induced activation of the Arabidopsis acidic chitinase promoter. Plant Cell 3: 1063-1072.
146. Schauser L, Roussis A, Stiller J, Stougaard J (1999) A plant regulator controlling development of symbiotic root nodules. Nature 402: 191-195.
147. Scheres B, van De Wiel C, Zalensky A, Horvath B, Spaink H, van Eck H, Zwartkruis F, Wolters AM, Gloudemans T, van Kammen A et al (1990) The ENOD12 gene product is involved in the infection process during the pea-Rhizobium interaction. Cell 60: 281-294.
148. Schulze B, Mentzel T, Jehle A, Mueller K, Beeler S, Boller T, Felix G, Chinchilla D (2010) Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J Biol Chem 26: 9444-9451.
149. Shibuya N, Minami E (2001) Oligosaccharide signalling for defense responses in plant. Physiol Mol Plant Pathol 59: 223-233.
150. Shibuya N, Kaku H, Kuchitsu K, Maliarik M (1993) Identification of a novel high-affinity binding site for N-acetylchitooligosaccharide elicitor in membrane fraction from suspension-cultured rice cells. FEBS Lett 329: 75-78.
151. Smit G, Swart S, Lugtenberg BJJ, Kijne JW (1992) Molecular mechanisms of attachment of Rhizobium bacteria to plant roots. Mol Microbiol 6: 2897-2903.
152. Smit P, Raedts J, Portyanko V, Debellé F, Gough C, Bisseling T, Geurts R (2005) NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308: 1789-1791.
153. 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.
154. Soto MJ, Dominguez-Ferreras A, Perez-Mendoza D, Sanjuan J, Olivares J (2009) Mutualism versus pathogenesis: the give-and-take in plant-bacteria interactions. Cell Microbiol 11: 381-388.
155. Stacey G, Libault M, Brechenmacher L, Wan J, May GD (2006) Genetics and functional genomics of legume nodulation. Curr Opin Plant Biol 9: 110-121.
156. Starker CG, Parra-Colmenares AL, Smith L, Mitra RM, Long SR (2006) Nitrogen fixation mutants of Medicago truncatula fail to support plant and bacterial symbiotic gene expression. Plant Physiol 140: 671-680.
157. 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.
158. Takezawa D, Ramachandiran S, Paranjape V, Poovaiah BW (1996) Dual regulation of a chimeric plant serine/threonine kinase by calcium and calcium/calmodulin. J Biol Chem 271: 8126-8132.
159. Tao Y, Xie Z, Chen W, Glazebrook J, Chang HS, Han B, Zhu T, Zou G, Katagiri F (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15: 317-330.
160. Tellström V, Usadel B, Thimm O, Stitt M, Küster H, Niehaus K (2007) The lipopolysaccharide of Sinorhizobium meliloti suppresses defense-associated gene expression in cell cultures of the host plant Medicago truncatula. Plant Physiol 143: 825-837.
161. 2+/calmodulin-dependent kinase leads to spontaneous nodule development. Nature 441: 1153-1156.
162. van den Burg HA, Harrison SJ, Joosten MH, Vervoort J, de Wit PJ (2006) Cladosporium fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol Plant Microbe Interact 19: 1420-1430.
163. van der Biezen EA, Jones JD (1998) Plant disease-resistance proteins and the gene-for-gene concept. Trends Biochem Sci 23: 454-456.
164. van der Hoorn RA, Kamoun S (2008) From guard to decoy: a new model for perception of plant pathogen effectors. Plant Cell 20: 2009-2017.
165. van Loon LC, Rep M, Pieterse CM (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44: 135-162.
166. Wan J, Zhang S, Stacey G (2004) Activation of a mitogen-activated protein kinase pahway in Arabidopsis by chitin. Mol Plant Pathol 5: 125-135.
167. Wan J, Zhang XC, Neece D, Ramonell KM, Clough S, Kim SY, Stacey MG, Stacey G (2008) A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20: 471-481.
168. Wubben JP, Joosten MHAJ, van Kan JAL, De Wit PJGM (1992) Subcellular localization of plant chitinases and 1, 3-β-glucanases in Cladosporium fulvum (syn. Fulvia fluva)-infected tomato leaves. Physiol Mol Plant Pathol 41: 23-32.
169. Yamada A, Shibuya N, Kodama O, Akatsuka T (1993) Induction of phytoalexin formation in suspension-cultured rice cells by N-acetyl-chitooligosaccharides. Biosci Biotechnol Biochem 57: 405-409.
170. Yang T, Poovaiah BW (2003) Calcium/calmodulin-mediated signal network in plants. Trends Plant Sci 8: 505-512.
171. Young DH, Kohle H, Kauss H (1982) Effect of chitosan on membrane permeability of suspension-cultured Glycine max and Phaseolus vulgaris cells. Plant Physiol 70: 1449-1454.
172. Zhang B, Ramonell K, Somerville S, Stacey G (2002) Characterization of early, chitin-induced gene expression in Arabidopsis. Mol Plant Microbe Interact 15: 963-970.
173. Zhang T, Liu Y, Yang T, Zhang L, Xu S, Xue L, An L (2006) Diverse signals converge at MAPK cascades in plant. Plant Physiol Biochem 44: 274-283.
174. Zhang XC, Wu X, Findley S, Wan J, Libault M, Nguyen HT, Cannon SB, Stacey G (2007) Molecular evolution of lysin motif-type receptor-like kinases in plants. Plant Physiol 144: 623-636.
175. Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JD, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428: 764-767.
176. Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125: 749-760.