Mutualistic Effectors: Architects of Symbiosis

Effectors in Plant-Microbe Interactions

Volumn , Issue , 2011, Pages 295-326

  Plett, Jonathan M ^a   Martin, Francis ^a  

^a UNIVERSITÉ DE LORRAINE   (France)

Author keywords

Arbuscular fungi; Auxin; Ectomycorrhizal fungi; Effectors; Elicitors; Ethylene; Hydrophobin; MiSSP7

Indexed keywords

EID: 84871691109     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9781119949138.ch12     Document Type: Chapter

References (162)

1. Albrecht, C., Burgess, T., Dell, B., et al. (1994) Chitinase and peroxidase activities are induced in eucalyptus roots according to aggressiveness of Australian ectomycorrhizal strains of Pisolithus sp. New Phytologist 127, 217-222.
2. Alexander, T., Toth, R., Meier, R., et al. (1989) Dynamics of arbuscule development and degeneration in onion, bean and tomato with reference to vesicular-arbuscular mycorrhiza with grasses. Canadian Journal of Botany 67, 2505-2513.
3. Aloui, A., Recorbet, G., Golotte, A., et al. (2009) On the mechanisms of cadmium stress alleviation in Medicago truncatula by arbuscular mycorrhizal symbiosis: a root proteomic study. Proteomics 9, 420-433.
4. Ané, J.M., Kiss, G.B., Riely, B.K. et al. (2004) Medicago truncatula DMI1 required for bacterial and fungal symbioses in legumes. Science 303, 1364-1367.
5. Arrighi, J.F., Barre, A., Ben Amor, B., et al. (2006) The Medicago truncatula lysine motif-receptorlike kinase gene family includes NFP and new nodule-expressed genes. Plant Physiology 142, 265-279.
6. Barker, S.J. & Tagu, D. (2000) The roles of auxins and cytokinins in mycorrhizal symbioses. Journal of Plant Growth Regulation 19, 144-154.
7. Baylis, G.T.S. (1972) Fungi, phosphorus and the evolution of the root system. Search 3, 257-258.
8. Béguiristain, T. & Lapeyrie, F. (1997) Host plant stimulates hypaphorine accumulation in Pisolithus tinctorius hyphae during ectomycorrhizal infection while excreted fungal hypaphorine controls root hair development. New Phytologist 136, 525-532.
9. Béguiristain, T., Côté, R., Rubini, P., et al. (1995) Hypaphorine accumulation in hyphae of the ectomycorrhizal fungus. Phytochemistry 40, 1089-1091.
10. Ben Amor, B., Shaw, S.L., Oldroyd, G.E.D., et al. (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 Journal 34, 495-506.
11. Birch, P.R., Rehmany, A.P., Pritchard, L., et al. (2006) Trafficking arms: oomycete effectors enter host plant cells. Trends in Microbiology 14, 8-11.
12. Bowles, D.J. (1990) Defense-related proteins in higher plants. Annual Reviews in Biochemistry 59, 873-907.
13. Brownleader, M.D., Ahmed, N., Traevan, M., et al. (1995) Purification and partial characterization of tomato extension peroxidase. Plant Physiology 109, 1115-1123.
14. Brundrett, M.C. (2002) Coevolution of roots and mycorrhizas of land plants. New Phytologist 154, 275-304.
15. Burgess, T., Laurent, P., Dell, B., et al. (1995) Effect of the fungal isolate aggressivity on the biosynthesis of symbiosis-related polypeptides in differentiating eucalypt ectomycorrhiza. Planta 195, 408-417.
16. Camehl, I., Sherameti, I., Venus, Y., et al. (2009) Ethylene signalling and ethylene-targeted transcription factors are required to balance beneficial and nonbeneficial traits in the symbiosis between the endophytic fungus Piriformospora indica and Arabidopsis thaliana. New Phytologist 185, 1062-1073.
17. Carnero Diaz, E., Martin, F., Tagu, D. (1996) Eucalypt _-tubulin:cDNA cloning and increased level of transcripts in ectomycorrhizal root systems. Plant Molecular Biology 31, 905-910.
18. Catoira, R., Galera, C., de Billy, F., et al. (2000) Four genes of Medicago truncatula controlling components of a nod factor transduction pathway. Plant Cell 12, 1647-1665.
19. Chabaud, M., Genre, A., Sieberer, B.J., et al. (2011) Arbuscular mycorrhizal hyphopodia and germinated spore exudates trigger Ca2+spiking in the legume and nonlegume root epidermis. New Phytologist 189, 347-355.
20. Chang, M., Chou, J.-C., Chen, C.-P., et al. (2007) Noncovalent protein transduction in plant cells by macropinocytosis. New Phytologist 174, 46-56.
21. Chang, M., Chou, J.-C., Lee, H.-J. (2005) Cellular internalization of fluorescent proteins via argininerich intracellular delivery peptide in plant cells. Plant Cell Physiology 46, 484-488.
22. Chao, Q., Rothenberg, M., Solano, R., et al. (1997) Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENE-INSENSITIVE3 and related proteins. Cell 89, 1133-1144.
23. Chen, L.-Q., Hou, B.-H., Lalonde, S., et al. (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468, 527-532.
24. Corner, E.J.H. (1972) Boletus in Malaysia. Botanic gardens, Singapore.
25. D'Heaze, W. & Holsters, M. (2002) Nod factor structures, responses and perception during initiation of nodule development. Glycobiology 12, 79R-105R.
26. Dauphin, A., Gerard, J., Lapeyrie, F., et al. (2007) Fungal hypaphorine reduces growth and induces cytosolic calcium increase in root hairs of Eucalyptus globulus. Protoplasma 231, 83-88.
27. De Carvalho, D. (1994) Contribution 'a l'étude des protéines régulées par la symbiose ectomycorhizienne. Ph.D. Thesis, Ecole Nationale du Génie Rural et Forestier, Nancy, France.
28. de Jonge, R., van Esse, H.P., Kombrink, A., et al. (2010) Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329, 953-955.
29. Denarie, J., Debelle, F.,&Prome, J.-C. (1996) Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annual Review of Biochemistry 65, 503-535.
30. Deng, J. & Dean, R.A. (2008) Characterization of adenylate cyclase interacting protein ACI1 in the rice blast fungus, Magnaporthe oryzae. The Open Mycology Journal 2, 74-81.
31. Dexheimer, J. & Pargney, J.C. (1991) Comparative anatomy of the host-fungus interface in mycorrhizas. Experientia 47, 312-320.
32. DiMichele, W.A. & Hook, R.W. (1992) Paleozoic terrestrial ecosystems. In: A.K. Behrensmeyer, J.D. Damuth, W.A. DiMichele, R. Potts, H.-D. Sues, and S.L. Wing (eds.). University of Chicago Press, Chicago, pp. 205-325.
33. Ditengou, F.A. & Lapeyrie, F. (2000) Hypaphorine from the ectomycorrhizal fungus Pisolithus tinctorius counteracts activities of indole-3-acetic acid and ethylene but not synthetic auxins in eucalypt seedlings. Molecular Plant-Microbe Interactions 13, 151-158.
34. Dou, D., Kale, S.D., Wang, X., et al. (2008) RXLR-mediated entry of Phytophthora sojae effectorAvr1b into soybean cells does not require pathogen-encoded machinery. Plant Cell 20, 1930-1947.
35. Doyle, R.J. & Rosenberg, M. (1990) Microbial Cell Surface Hydrophobicity. American Society of Microbiology, Washington, D.C.
36. Dumas-Gaudot, E., Valot, B., Bestel-Corre, G., et al. (2004) Proteomics as a way to identify extraradicular fungal proteins from Glomus intraradices-RiT-DNA carrot root mycorrhizas. FEMS Microbiology Ecology 48, 401-411.
37. Endre, G., Kereszt, A., Kevei, Z., et al. (2002) A receptor kinase gene regulating symbiotic nodule development. Nature 417, 962-966.
38. Ezawa, T., Hayatsu, M., & Saito, M. (2005) A new hypothesis on the strategy for acquisition of phosphorus in arbuscular mycorrhiza: up-regulation of secreted acid phosphatase gene in the host plant. Molecular Plant-Microbe Interactions 18, 1046-1053.
39. Felten, J., Kohler, A., Morin, E., et al. (2009) The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signaling. Plant Physiology 151, 1991-2005.
40. Finlay, R.D. & Söderström, B. (1992) Mycorrhiza and carbon flow to the soil. In: M. Allen (ed) Mycorrhiza Functioning. Chapman and Hall, London, UK, pp. 134-160.
41. Floerl, S., Druebert, C., Majcherczyk, A., et al. (2008) Defence reactions in the apoplastic proteome of oilseed rape (Brassica napus var. napus) attenuate Verticillium longisporum growth but not disease symptoms. BMC Plant Biology 8, 129.
42. Garcerá, A., Martinez, A.I., Castillo, L., et al. (2003) Identification and study of a Candida albicans protein homologs to Saccharomyces cerevisiae Ssr1p, an internal cell-wall protein. Microbiology 149, 2137-2145.
43. Gay, G., Normand, L., Marmeisse, R., et al. (1994) Auxin overproducer mutants of Hebeloma cylindrosporum Romagnési have increased mycorrhizal activity. New Phytologist 128, 645- 657.
44. Gehrig, H., Schußler, A., & Kluge, M. (1996) Geosiphon pyriforme, a fungus forming endocytobiosis with Nostoc (Cyanobacteria), is an ancestral member of the glomales: evidence by SSU rRNA analysis. Journal of Molecular Evolution 43, 71-81.
45. Gollotte, A., Gianinazzi-Pearson, V., Giovanetti, M., et al. (1993) Cellular localization and cytochemical probing of resistance reactions to arbuscular mycorrhizal fungi in a "locus a" myc- mutant of Pisum sativum L. Planta 191, 112-122.
46. Graham, J.H. & Linderman, R.G. (1980) Ethylene production by ectomycorrhizal fungi, Fusarium oxysporum f. sp. Pini, and by aseptically synthesized ectomycorrhizae and Fusarium-infected Douglas-fir roots. Canadian Journal of Microbiology 26, 1340-1347.
47. Grell, M.N., Mouritzen, P., & Giese, H. (2003) A Blumeria graminis gene family encoding proteins with a C-terminal variable region with homologs in pathogenic fungi. Gene 311, 181-192.
48. Grouffaud, S., vanWest, P., Avrova, A.O., et al. (2008) Plasmodium falciparum and Hyaloperonospora parasitica effector translocation motifs are functional in Phytophthora infestans. Microbiology 154, 3743-3751.
49. Hanlon, M.T. & Coenen, C. (2011) Genetic evidence for auxin involvement in arbuscular mycorrhiza initiation. New Phytologist 189, 701-709.
50. Hazledine, S., Sun, J., Wysham, D., et al. (2009) Nonlinear time series analysis of nodulation factor induced calcium oscillations: evidence for deterministic chaos? PLoS One 4, e6637.
51. Hibbett, D.S. &Matheny, P.B. (2009) The relative ages of ectomycorrhizal mushrooms and their plant hosts estimated using Bayesian relaxed molecular clock analyses. BMC Biology 7, 13.
52. Hilbert, J.L., Costa, G.,&Martin, F. (1991) Ectomycorrhizal synthesis and polypeptide changes during the early stage of eucalypt mycorrhiza development. Plant Physiology 97, 977-984.
53. Högberg, P., Hordgre, A., Buchmann, N., et al. (2001) Large-scale forest girdling shows that current photosynthesis drives soil respiration. Nature 411, 789-792.
54. Hogenhout, S.A., van der Hoorn, R.A., Terauchi, R., et al. (2009) Emerging concepts in effector biology of plant-associated organisms. Molecular Plant-Microbe Interactions 22, 115-122.
55. Honegger, R. (1993) Developmental biology of lichens. New Phytologist 125, 659-677.
56. Ibeas, J.I., Lee, H., Damsz, B., et al. (2000) Fungal cell wall phosphomannans facilitate the toxic activity of a plant PR-5 protein. Plant Journal 23, 375-383.
57. Jambois, A., Daupin, A., Kawano, T., et al. (2005) Competitve anagonism between IAA and indole alkaloid hypaphorine must contribute to regulate ontogenesis. Physiologia Plantarum 123, 120-129.
58. Jentchel, K., Theil, D., Rehn, F., et al. (2007) Arbuscular mycorrhiza enhances auxin levels and alters auxin biosynthesis in Tropaeolum majus during early stages of colonization. Physiologia Plantarum 129, 320-333.
59. Joly, D.L., Feau, N., Tanguay, P., et al. (2010) Comparative analysis of secreted protein evolution using expressed sequence tags from four poplar leaf rusts (Melampsora spp.). BMC Genomics 11, 422.
60. Kaku, H., Nishizawa, Y., Ishii-Minami, N., et al. (2006) Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. PNAS 103, 11086-11091.
61. Kale, S.D., Gu, B., Capelluto, D.G.S., et al. (2010) External phosphatidylinositol-3-phosphate mediates host cell entry by eukaryotic pathogen effectors. Cell 142, 284-295.
62. Kaló, P., Gleason, C., Edwards, A., et al. (2005) Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 308, 1786-1789.
63. Kamoun, S. (2007) Groovy times: filamentous pathogen effectors revealed. Current Opinion in Plant Biology 10, 358-365.
64. Kanamori, N., Madsen, L.H., Radutoiu, S., et al. (2006) A nucleoporin is required for induction of Ca2+spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proceedings of the National Academy of Science USA 103, 359-364.
65. Kidston, R. & Lang, W.H. (1921) Old red sandstone plants showing structure, from the Rhynie Chert bed, Aberdeenshire. Part 5. The thallophyta occurring in the peat-bed; the succession of the plants throughout a vertical section of the bed, and the conditions of accumulation and preservation of the deposit. Transactions of the Royal Society of Edinburgh 52, 855-902.
66. Kloppholz, S., Kuhn, H., & Requena, N. (2011) A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr Biol 21, 1204-1209.
67. Kondoh, O., Muto, A., Kajiwara, S., et al. (1995) Fruiting body-specific cDNA mfbAc, from the mushroom Lentinus edodes encodes a high-molecular-weight cell-adhesion protein containing an Arg-Gly-Asp motif. Gene 154, 31-37.
68. Kosuta, S., Chabaud, M., Lougnon, G., et al. (2003) A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiology 131, 952-962.
69. Kosuta, S., Hazledine, S., Sun, J., et al. (2008) Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proceedings of the National Academy of Sciences USA 105, 9823-9828.
70. Kulkarni, R.D., Kelkar, H.S.,&Dean, R.A. (2003) An eight-cysteine-containing CFEM domain unique to a group of fungal membrane proteins. Trends in Biochemical Sciences 28, 118-121.
71. Lamarre, C., Deslauriers, N., & Bourbonnais, Y. (2000) Expression cloning of the Candida albicans CSA1 gene encoding a mycelial surface antigen by sorting of Saccharomyces cerevisiae transformants with monoclonal antibody-coated magnetic beads. Molecular Microbiology 35, 444-453.
72. Lambais, M.R. & Mehdy, M.C. (1993) Suppression of endochitinase, _-1,3-endoglucanase, and chalcone isomerase expression in bean vesicular-arbuscular mycorrhizal roots under different soil phosphate conditions. Molecular Plant-Microbe Interactions 6, 75-83.
73. Lapeyrie, F., Lei, J., Malajczuk, M., et al. (1989) Ultra-structural and biochemical changes at the pre-infection stage of mycorrhizal formation by two isolates of Pisolithus tinctorius. Annales des Sciences Foresti'eres 46s, 754s-757s.
74. Laurans, F., Pepin, R.,&Gay, G. (2001) Fungal auxin overproduction affects the anatomy of Hebeloma cylindrosporum-Pinus pinaster ectomycorrhizas. Tree Physiology 21, 533-540.
75. Laurent, P. (1995) Contribution 'a l'étude des protéines régulées par la symbiose chez l'ectomycorhize d'Eucalyptus-Pisolithus. Caractérisation de mannoprotéines pariétales chez le basidiomycete Pisolithus tinctorius. Ph.D. Thesis, University Henri Poincaré - Nancy 1, France.
76. Laurent, P., Tagu, D., De Carvalho, D., et al. (1999) Cell wall acidic polypeptides in Pisolithus tinctorius are up-regulated during the development of Eucalyptus globulus ectomycorrhiza. Molecular Plant-Microbe Interactions, 12, 862-871.
77. Leake, J.R., Johnson, D., Donnelly, D.P., et al. (2004) Networks of power and influence: the role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Canadian Journal of Botany 82, 1016-1045.
78. Lei, J., Lapeyrie, F., Malajczuk, N., et al. (1990) Infectivity of pine and eucalypt isolates of Pisolithus tinctorius on roots of Eucalyptus urophylla in vitro. II. Ultrastructural and biochemical changes at the early stage of mycorrhiza formation. New Phytologist 116, 115-122.
79. Limpens, E., Franken, C., Smit, P., et al. (2003) LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science 302, 630-633.
80. Linder, S. & Axelsson, B. (1982) Changes in carbon uptake and allocation patterns as a result of irrigation and fertilization in a young Pinus sylvestris stand. In: R.H.Waring (ed) Carbon Uptake and Allocation in Subalpine Ecosystems as a Key to Management. Forest Research Laboratory, Oregon State University, pp 38-44.
81. Lugones, L.G., Bosscher, J.S., Scholtmeijer, K., et al. (1996) An abundant hydrophobin (ABH11) forms hydrophobic rodlet layers in Agaricus bisporus fruiting bodies. Microbiology 142, 1321- 1329.
82. Madsen, E.B., Madsen, L.H., Radutoiu, S., et al. (2003) A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425, 637-640.
83. Maillet, F., Poinsot, V., Andre, O., et al. (2011) Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469, 58-63.
84. Martin, F. & Selosse, M.-A. (2008) The Laccaria genome: a symbiont blueprint decoded. New Phytologist 180, 296-310.
85. Martin, F., Aerts, A., Ahrén, D., et al. (2008a) The genome sequence of the basidiomycete fungus Laccaria bicolor provides insights into the mycorrhizal symbiosis. Nature 452, 88-92.
86. Martin, F., Gianinazzi-Pearson, V., Hijri, M., et al. (2008b) The long hard road to a completed Glomus intraradices genome. New Phytologist 180, 747-750.
87. Martin, F., Kohler, A., Murat, C., et al. (2010) Périgord black truffle genome uncovers evolutionary origins and mechanisms of symbiosis. Nature 464, 1033-1038.
88. Martin, F., Laurent, P., de Cavalho, D., et al. (1995) Fungal gene expression during ectomycorrhiza formation. Canadian Journal of Botany 73, S541-S547.
89. Martin, F., Laurent, P., de Carvalho, D., et al. (1999) Cell wall proteins of the ectomycorrhizal basidiomycete Pisolithus tinctorius: identification, function and expression in symbiosis. Fungal Genetics and Biology 27, 161-174.
90. Meixner, C., Ludwig-Muller, J., Miersch, O., et al. (2005) Lack of mycorrhizal autoregulation and phytohormonal changes in the supernodulating soybean mutant nts1007. Planta 222, 709-715.
91. Mensen, R., Hager, A., & Salzer, P. (1998) Elicitor-induced changes of wall-bound and secreted peroxidase activities in suspension-cultured spruce (Picea abies) cells are attenuated by auxins. Physiologia Plantarum 102, 539-546.
92. Mitra, R.M., Gleason, C.A., Edwards, A., et al. (2004) A Ca2+/calmodulin-dependent protein kinase required for symbiotic nodule development: gene identification by transcript-based cloning. Proceedings of the National Academy of Science USA 101, 4701-4705.
93. Moyersoen, B. (2006) Pakaraimaea dipterocarpacea is ectomycorrhizal, indicating an ancient Gondwanaland origin for the ectomycorrhizal habit in Dipterocarpaceae. New Phytologist 172,753-762.
94. Moyersoen, B., Becker, P., & Alexander, I.J. (2001) Are ectomycorrhizas more abundant than arbuscular mycorrhizas in tropical heath forests? New Phytologist 150, 591-599.
95. Mukherjee, A. & Ané, J.-M. (2011) Germinating spore exudates from arbuscular mycorrhizal fungi: molecular and developmental responses in plants and their regulation by ethylene. Molecular Plant-Microbe Interactions 24, 260-270.
96. Nagendran, S., Hallen-Adams, H.E., Paper, J.M., et al. (2009) Reduced potential for secreted plant cell-wall-degrading enzymes in the ectomycorrhizal fungus Amanita bisporigera, based on the secretome of Trichoderma reesei. Fungal Genetics and Biology 46, 427-435.
97. Navazio, L., Moscatiello, R., Genre, A., et al. (2007) A diffusible signal from arbuscular mycorrhizal fungi elicits a transient cytosolic calcium elevation in host plant cells. Plant Physiology 144, 673-681.
98. Nehls, U., Béguiristain, T., Ditengou, F., et al. (1998) The expression of a symbiosis-regulated gene in eucalypt roots is regulated by auxins and hypaphorine, the tryptophan betaine of the ectomycorrhizal basidiomycete Pisolithus tinctorius. Planta 207, 296-302.
99. Oldroyd, G.E.D. & Downie, J.A. (2004) Calcium, kinases and nodulation signalling in legumes. National Review of Molecular Cell Biology 5, 566-576.
100. Oldroyd, G.E.D. & Long, S.R. (2003) Identification and characterization of nodulation-signaling pathway 2, a gene of Medicago truncatula involved in Nod factor signaling. Plant Physiology 131, 1027-1032.
101. Parniske, M. & Downie, J.A. (2003) Plant biology-locks, keys and symbioses. Nature 425, 569-570.
102. Perez, A, Pedros, B., Murgui, A., et al. (2006) Biofilm formation by Candida albicans mutants for genes coding fungal proteins exhibiting the eight-cysteine-containing CFEM domain. FEMS Yeast Research 6, 1074-1084.
103. Perret, X., Staehelin, C., & Broughton, W.J. (2000) Molecular basis of symbiotic promiscuity. Microbiology and Molecular Biology Reviews 64, 180-201.
104. Pierchbacher, M.D. & Ruoslahti, E. (1984) Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature 309, 30-33.
105. Pirozynski, K.A. & Malloch, D.W. (1975) The origin of land plants: a matter of mycotrophism. Biosystems 6, 153-164.
106. Plett, J.M. & Martin, F. (2011) Blurred boundaries: lifestyle lessons from fungal ectomycorrhizal genomes. Trends in Genetics 27, 14-22.
107. Plett, J.M., Kemppainen, M., Kale, S.D., Kohler, A., Legué, V., Brun, A., Tyler, B.M., Pardo, A.G. & Martin F. (2011) A secreted effector protein of Laccaria bicolor is required for symbiosis development. Current Biology 21, 1197-1203.
108. Radutoiu, S., Madsen, L.H., Madsen, E.B., et al. (2003) Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425, 585-592.
109. Read, D.J. & Perez-Moreno, J. (2003) Mycorrhizas and nutrient cycling in ecosystems-a journey towards relevance? New Phytologist 157, 475-492.
110. Reboutier, D., Bianchi, M., Brault, M., et al. (2002) The indolic compound hypaphorine produced by ectomycorrhizal fungus interferes with auxin action and evokes early responses in nonhost Arabidopsis thaliana. Molecular Plant-Microbe Interactions 15, 932-938.
111. Recorbet, G., Rogniaux, H., Gianinazzi-Pearson, V., et al. (2009) Fungal proteins in the extra-radical phase of mycorrhiza: a shotgun proteomic picture. New Phytologist 181, 248-260.
112. Recorbet, G., Valot, B., Robert, F., et al. (2010) Identification of in planta-expressed arbuscular mycorrhizal fungal proteins upon comparison of the root proteomes of Medicago truncatula colonized with two Glomus species. Fungal Genetics and Biology 47, 608-618.
113. Redecker, D., Kodner, R., & Graham, L.E. (2000) Glomalean fungi from the Ordovician. Science 289, 1920-1921.
114. Roby, D., Gadelle, A., & Toppan, A. (1987) Chitin oligosaccharides as elicitors of chitinase activity in melon plants. Biochemical and Biophysical Research Communications 143, 885-892.
115. Rohe, M., Gierlich, A., Hermann, H., et al. (1995) The race-specific elicitor, NIP1, from the barley pathogen, Rhynchosporium secalis, determines avirulence on host plants of the Rrs1 resistance genotype. EMBO Journal 14, 4168-4177.
116. Ruoslahti, E. (1996) RGD and other recognition sequences for integrins. Annual Reviews in Cell Developmental Biology 12, 697-715.
117. Rupp, L.A. & Mudge, K.W. (1985) Ethephon and auxin induce mycorrhiza-like changes in the morphology of root organ cultures of mugo pine. Physiologia Plantarum 64, 316-322.
118. Rupp, L.A., Mudge, K.W., & Negm, F.B. (1989) Involvement of ethylene in ectomycorrhiza formation and dichotomous branching of roots of mugo pine seedlings. Canadian Journal of Botany 67, 477-482.
119. Ryu, C.-M., Farag, M.A., Hu, C.-H., et al. (2003) Bacterial volatiles promote growth in Arabidopsis. Proceedings of the National Academy of Sciences USA 100, 4927-4932.
120. Saito, K., Yoshikawa, M., Yano, Y., et al. (2007) NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell 19, 610-624.
121. Salzer, P. & Hager, A. (1993) Effect of auxins and ectomycorrhizal elicitors on wall-bound proteins and enzymes of spruce (Picea abies [L.] Karst.) cells. Trees 8, 49-55.
122. Salzer, P., Hebe, G., Reith, A., Zitterell-Haid, B., et al. (1996) Rapid reactions of spruce cells to elicitors released from the ectomycorrhizal fungus Hebeloma crustulinforme, and inactivation of these elicitors by extracellular spruce cell enzymes. Planta 198, 118-126.
123. Salzer, P., Hübner, B., Sirrenberg, A., & Hagen, A. (1997) Differential effect of purified spruce chitinases and _-1,3-glucanases on the activity of elicitors from ectomycorrhizal fungi. Plant Physiology 114, 957-968.
124. Sauter, M. & Hager, A. (1989) The mycorrhizal fungus Amanita muscaria induces chitinase activity in roots and in suspension-cultured cells of its host Picea abies. Planta 179, 61-66.
125. Scagel, C.F. & Linderman, R.G. (1998) Influence of ectomycorrhizal fungal inoculation on growth and root IAA concentrations of transplanted conifers. Tree Physiology 18, 739-747.
126. Sharp, J.A., McNeil, M., & Albersheim, P. (1984a) The primary structure of one elicitor active and seven elicitor-inactive hexa (ß-D-glucopyranolsyl)-D-glucitols isolated from the mycelia walls of Phytophthora megasperma f.sp. glycinea. Journal of Biological Chemistry 25, 11321-11326.
127. Sharp, J.A., Valent, B.,&Albersheim, P. (1984b) Purification and partial characterization of a ß-glucan fragment that elicits phytoalexin accumulation in soybean. Journal of Biological Chemistry 25, 11312-11320.
128. Shaul-Keinan, O., Gadkar, V., Ginzberg, I., et al. (2002) Hormone concentrations in tobacco roots change during arbuscular mycorrhizal colonization with Glomus intraradices. New Phytologist 154, 501-507.
129. Sirrenberg, A., Salzer, P., Hager, A. (1995) Induction of mycorrhiza-like structures and defence reactions in dual cultures of spruce callus and ectomycorrhizal fungi. New Phytologist 130, 149-156.
130. Smit, P., Raedts, J., Portyanko, V., Debelle, F., et al. (2005) NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 308, 1789-1791.
131. Smith, S.E. & Read, D.J. (2008) Mycorrhizal Symbiosis, 3rd ed. Academic Press, London, UK.
132. Song, J., Win, J., Tian, M., Schornack, S., et al. (2009) Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease Rcr3. Proceedings of the National Academy of Science USA 106, 1654-1659.
133. Soragni, E., Bolchi, A., Balestrini, R., et al. (2001)Anutrient-regulated, dual localization phospholipase A2 in the symbiotic fungus Tuber borchii. EMBO Journal 20, 5079-5090.
134. Spanu, P., Boller, T., Ludwig, A., Wiemken, A., et al. (1989) Chitinase in roots of mycorrhizal Allium porrum: regulation and localization. Planta 177, 447-455.
135. Spanu, P. & Bonfante-Fasolo, P. (1988) Cell wall-bound peroxidase activity in roots of mycorrhizal Allium porrum. New Phytologist 109, 119-124.
136. Splivallo, R., Fischer, U., Gobel, C., et al. (2009) Truffles regulate plant root morphogenesis via the production of auxin and ethylene. Plant Physiology 150, 2018-2029.
137. Stevenson, K.J., Slater, J.A., & Takai, S. (1979) Cerato-ulmin, a wilting toxin of Dutch elm disease fungus. Phytochemistry 18, 235-238.
138. Stracke, S., Kistner, C., Yoshida, S., et al. (2002)Aplant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417, 959-962.
139. Tagu, D. & Martin, F. (1996) Molecular analysis of cell wall proteins expressed during the early steps of ectomycorrhiza development. New Phytologist 133, 73-85.
140. Tagu, D., Nasse, B.,&Martin, F. (1996) Cloning and characterization of hydrophobin-encoding cDNAs from the ectomycorrhizal basidiomycete Pisolithus tinctorius. Gene 168, 93-97.
141. Talbot, N.J., Ebbole, D.J., & Hamer, J.E. 1993. Identification and characterization ofMPG1, a gene involved in pathogenicity from the rice blast fungus Magnaporthe grisea. Plant Cell 5, 1575-1590.
142. Talbot, N.J., Kershaw, M.J., Wakley, G.E., et al. 1996. MPG1 encodes a fungal hydrophobin involved in surface interactions during infection-related development by the rice blast fungusMagnaporthe grisea. Plant Cell 8, 985-999.
143. Tedersoo, L., May, T.W., & Smith, M.E. 2010. Ectomycorrhizal lifestyle in fungi: global diversity, distribution, and evolution of phylogenetic lineages. Mycorrhiza 20, 217-263.
144. Tedersoo, L., Sadam, A., Zambrano, M., Valencia, R.,&Bahram, M. 2009. Low diversity and high host preference of ectomycorrhizal fungi in Western Amazonia, a neotropical biodiversity hotspot. The ISME Journal 4, 465-471.
145. Templeton, M.D., Rikkerink, E.H.A., Beever, R.E. 1994. Small, cysteine-rich proteins and recognition in fungal-plant interactions. Molecular Plant-Microbe Interactions 7, 320-325.
146. Timonen, S. & Sen, R. (1998) Heterogeneity of fungal and plant enzyme expression in intact Scots pine - Suillus bovinus and - Paxillus involutus mycorrhizospheres developed in natural forest humus. New Phytologist 138, 355-366.
147. Torelli, A., Trotta, A., Acerbi, L., et al. (2000) IAA and ZR content in leek (Allium porrum L.), as influenced by P nutrition and arbuscular mycorrhizae, in relation to plant development. Plant and Soil 226 29-35.
148. van West, P., De Bruijin, I., Minor, K.L., et al. (2010) The putative RxLR effector protein SpHtp1 from the fish pathogenic oomycete Saprolegnia parasitica is translocated into fish cells. FEMS Microbiology Letters 310, 127-137.
149. Vogt, K.A., Grier, C.C., Meirer, C.E., & Edmonds, R.L. 1982. Mycorrhizal role in net primary production and nutrient cycling in Abies amabilis ecosystems in western Washington. Ecology 63, 370-380.
150. Volpin, H., Phillips, D.A., Okon, Y., & Kapulnik, Y. 1995. Suppression of an isoflavanoid phytoalexin defense response in mycorrhizal alfalfa roots. Plant Physiology 108, 1449-1454.
151. Wais, R.J., Galera, C., Oldroyd, G., et al. (2000) Genetic analysis of calcium spiking responses in nodulation mutants of Medicago truncatula. Proceedings of the National Academy of Sciences USA 97, 13407-13412.
152. Wan, J., Zhang, X.-C., Neece, D., et al. (2008) A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. The Plant Cell 20, 471-481.
153. Wessels, J.G.H. (1993) Tansley review no. 45. Wall growth, protein excretion and morphogenesis in fungi. New Phytologist 123, 397-413.
154. Wessels, J.G.H. (1994) Developmental regulation of fungal cell wall formation. Annual Reviews in Phytopathology 32, 413-437.
155. Wessels, J.G.H., Asgeirsdottir, S.A., Birkenkamp, K.U., et al. (1995) Genetic regulation of emergent growth in Schizophyllum commune. Canadian Journal of Botany 73, S273-S281.
156. Wosten, H.A.B., de Vries, O.M.H., & Wessels, J.G.H. (1993) Interfacial self-assembly of a fungal hydrophobin into a rodlet layer. Plant Cell 5, 1567-1574.
157. Wosten, H.A.B., Ruardy, T.G., van der Mei, H.C., Busscher, H.J., & Wessels, J.G.H. (1995) Interfacial self-assembly of a Schizophyllum commune hydrophobin into an insoluble amphipathic membrane depends on surgace hydrophobicity. Colliod Surfaces B: Biointerfaces 5, 189-195.
158. Wosten, H.A.B., Schuren, F.H.J., &Wessels, J.G.H. (1994) Interfacial self-assembly of a hydrophobin into an amphipathic membrane mediates fungal attachment to hydrophobic surfaces. EMBO Journal 13, 5848-5854.
159. Wosten, H.A.B.&Wessels, J.G.H. 1997. Hydrophorins, frommolecular structure to multiple functions in fungal development. Mycoscience 38, 363-374.
160. Xue, C., Park, G., Choi, W., et al. (2002) Two novel fungal virulence genes specifically expressed in appressoria of the rice blast fungus. Plant Cell 14, 2107-2119.
161. Yasuda, T., Ishihara, H., Amano, H., & Shishido, K. (1997) Generation of basidiomycetous hyphal cell-aggregates by addition of the Arg-Gly-Asp motif-containing fragment of high-molecularweight cell-adhesion protein MFBA derived from the basiomycete Lentinus edodes. Bioscience, Biotechnology and Biochemistry 61, 1587-1589.
162. Zsögön, A., Lambais, M.R., Benedito, V.A., et al. (2008) Reduced arbuscular mycorrhizal colonization in tomato ethylene mutants. Scientia Agricola 65, 259-267.