How membranes shape plant symbioses: Signaling and transport in nodulation and arbuscular mycorrhiza

Frontiers in Plant Science

Volumn 3, Issue OCT, 2012, Pages

  Bapaume, Laure ^a   Reinhardt, Didier ^a  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

Author keywords

Arbuscule; LysM receptor; Mycorrhiza; Rhizobium; Root nodules; Symbiosis; SYMRK; VAPYRIN

Indexed keywords

EID: 84881661846     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2012.00223     Document Type: Review

References (236)

1. Aguilar, O. M., Rival, O., and Peltzer, E. (2004). Analysis of Rhizobium etli and of its symbiosis with wild Phaseolus vulgaris supports coevolution in centers of host diversification. Proc. Natl. Acad. Sci. U.S.A. 101, 13548-13553.
2. Akiyama, K., Matsuzaki, K., and Hayashi, H. (2005). Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435, 824-827.
3. Allen, J. W., and Shachar-Hill, Y. (2009). Sulfur transfer through an arbuscular mycorrhiza. Plant Physiol. 149, 549-560.
4. Al-Yahya'ei, M., Oehl, F., Vallino, M., Lumini, E., Redecker, D., Wiemken, A., et al. (2011). Unique arbuscular mycorrhizal fungal communities uncovered in date palm plantations and surrounding desert habitats of Southern Arabia. Mycorrhiza 21, 195-209.
5. Anderberg, H. I., Kjellbom, P., and Johanson, U. (2012). Annotation of Selaginella moellendorffii major intrinsic protein and the evolution of the protein family in terrestrial plants. Front. Plant Sci. 3, 1-14.
6. Aroca, R., Porcel, R., and Ruiz-Lozano, J. M. (2007). How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses? New Phytol. 173, 808-816.
7. Arrighi, J. F., Barre, A., Ben Amor, B., Bersoult, A., Soriano, L. C., Mirabella, R., et al. (2006). The Medicago truncatula lysine motif-receptor-like kinase gene family includes NFP and new nodule-expressed genes. Plant Physiol. 142, 265-279.
8. Augé, R. M. (2001). Water relations, drought and vesicular-arbuscular mycorrhizal symbiosis. Mycorrhiza 11, 3-42.
9. Balestrini, R., Gomez-Ariza, J., Lanfranco, L., and Bonfante, P. (2007). Laser microdissection reveals that transcripts for five plant and one fungal phosphate transporter genes are contemporaneously present in arbusculated cells. Mol. Plant Microbe Interact. 20, 1055-1062.
10. Balestrini, R., and Lanfranco, L. (2007). Fungal and plant gene expression in arbuscular mycorrhizal symbiosis (vol 16, pg 509, 2006). Mycorrhiza 17, 153.
11. Balzergue, C., Puech-Pagès, V., Bécard, G., and Rochange, S. F. (2011). The regulation of arbuscular mycorrhizal symbiosis by phosphate in pea involves early and systemic signalling events. J. Exp. Bot. 62, 1049-1060.
12. Banning, A., Tomasovic, A., and Tikkanen, R. (2011). Functional aspects of membrane association of Reggie/Flotillin proteins. Curr. Protein Pept. Sci. 12, 725-735.
13. Ben Amor, B., Shaw, S. L., Oldroyd, G. E. D., Maillet, F., Penmetsa, R. V., Cook, D., et al. (2003). The NFP locus ofMedicago 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.
14. Benedetto, A., Magurno, F., Bonfante, P., and Lanfranco, L. (2005). Expression profiles of a phosphate transporter gene (GmosPT) from the endomycorrhizal fungus Glomus mosseae. Mycorrhiza 15, 620-627.
15. Bennett, V., and Baines, A. J. (2001). Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol. Rev. 81, 1353-1392.
16. Bensmihen, S., De Billy, F., and Gough, C. (2011). Contribution of NFP LysM domains to the recognition of nod factors during the Medicago truncatula/Sinorhizobium meliloti symbiosis. PLoS ONE 6:e26114. doi: 10.1371/journal.pone.0026114
17. Besserer, A., Puech-Pagès, V., Kiefer, P., Gomez-Roldan, V., Jauneau, A., Roy, S., et al. (2006). Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol. 4:e226. doi: 10.1371/journal.pbio.0040226
18. Bhat, R. A., Miklis, M., Schmelzer, E., Schulze-Lefert, P., and Panstruga, R. (2005). Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain. Proc. Natl. Acad. Sci. U.S.A. 102, 3135-3140.
19. Bidartondo, M. I., Read, D. J., Trappe, J. M., Merckx, V., Ligrone, R., and Duckett, J. G. (2011). The dawn of symbiosis between plants and fungi. Biol. Lett. 7, 574-577.
20. Bolton, M. D., Van Esse, H. P., Vossen, J. H., De Jonge, R., Stergiopoulos, I., Stulemeijer, I. J. E., et al. (2008). The novel Cladosporium fulvum lysin motif effector Ecp6 is a virulence factor with orthologues in other fungal species. Mol. Microbiol. 69, 119-136.
21. Bonfante-Fasolo, P. (1984). "Anatomy and morphology of VA mycorrhizae, " in VA Mycorrhizae, eds C. L. Powell and D. J. Bagyaraj (Boca Raton, FL, USA: CRC Press), 5-33.
22. Breuillin, F., Schramm, J., Hajirezaei, M., Ahkami, A., Favre, P., Druege, U., et al. (2010). Phosphate systemically inhibits development of arbuscular mycorrhiza in Petunia hybrida and represses genes involved in mycorrhizal functioning. Plant J. 64, 1002-1017.
23. Breuninger, M., and Requena, N. (2004). Recognition events in AM symbiosis: analysis of fungal gene expression at the early appressorium stage. Fungal Genet. Biol. 41, 794-804.
24. Broghammer, A., Krusell, L., Blaise, M., Sauer, J., Sullivan, J. T., Maolanon, N., et al. (2012). Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. Proc. Natl. Acad. Sci. U.S.A. 109, 13859-13864.
25. Brundrett, M. C. (2002). Coevolution of roots and mycorrhizas of land plants. New Phytol. 154, 275-304.
26. Buist, G., Steen, A., Kok, J., and Kuipers, O. R. (2008). LysM, a widely distributed protein motif for binding to (peptido)glycans. Mol. Microbiol. 68, 838-847.
27. Bunn, R., Lekberg, Y., and Zabinski, C. (2009). Arbuscular mycorrhizal fungi ameliorate temperature stress in thermophilic plants. Ecology 90, 1378-1388.
28. Capoen, W., Sun, J., Wysham, D., Otegui, M. S., Venkateshwaran, M., Hirsch, S., et al. (2011). Nuclear membranes control symbiotic calcium signaling of legumes. Proc. Natl. Acad. Sci. U.S.A. 108, 14348-14353.
29. Cappellazzo, G., Lanfranco, L., Fitz, M., Wipf, D., and Bonfante, P. (2008). Characterization of an amino acid permease from the endomycorrhizal fungus Glomus mosseae. Plant Physiol. 147, 429-437.
30. Casieri, L., Gallardo, K., and Wipf, D. (2012). Transcriptional response of Medicago truncatula sulphate transporters to arbuscular mycorrhizal symbiosis with and without sulphur stress. Planta 235, 1431-1447.
31. Catalano, C. M., Czymmek, K. J., Gann, J. G., and Sherrier, D. J. (2007). Medicago truncatula syntaxin SYP132 defines the symbiosome membrane and infection droplet membrane in root nodules. Planta 225, 541-550.
32. Catalano, C. M., Lane, W. S., and Sherrier, D. J. (2004). Biochemical characterization of symbiosome membrane proteins from Medicago truncatula root nodules. Electrophoresis 25, 519-531.
33. Chabaud, M., Genre, A., Sieberer, B. J., Faccio, A., Fournier, J., Novero, M., et al. (2011). Arbuscular mycorrhizal hyphopodia and germinated spore exudates trigger Ca2+ spiking in the legume and nonlegume root epidermis. New Phytol. 189, 347-355.
34. Charpentier, M., Bredemeier, R., Wanner, G., Takeda, N., Schleiff, E., and Parniske, M. (2008). Lotus japonicusCASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume Root endosymbiosis. Plant Cell 20, 3467-3479.
35. Chen, A., Gu, M., Sun, S., Zhu, L., Hong, S., and Xu, G. (2011). Identification of two conserved cis-acting elements, MYCS and P1BS, involved in the regulation of mycorrhiza-activated phosphate transporters in eudicot species. New Phytol. 189, 1157-1169.
36. Chen, C. Y., Ane, J. M., and Zhu, H. Y. (2008). OsIPD3, an ortholog of the Medicago truncatula DMI3 interacting protein IPD3, is required for mycorrhizal symbiosis in rice. New Phytol. 180, 311-315.
37. Chen, C. Y., Gao, M. Q., Liu, J. Y., and Zhu, H. Y. (2007). Fungal symbiosis in rice requires an ortholog of a legume common symbiosis gene encoding a Ca2+/calmodulin-dependent protein kinase(1[OA]). Plant Physiol. 145, 1619-1628.
38. Chen, L.-Q., Hou, B.-H., Lalonde, S., Takanaga, H., Hartung, M. L., Qu, X.-Q., et al. (2010). Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468, 527-532.
39. Chen, T., Zhu, H., Ke, D., Cai, K., Wang, C., Gou, H., et al. (2012). A MAP kinase kinase interacts with SymRK and regulates nodule organogenesis in Lotus japonicus. Plant Cell 24, 823-838.
40. Clark, R. B., and Zeto, S. K. (2000). Mineral acquisition by arbuscular mycorrhizal plants. J. Plant Nutr. 23, 867-902.
41. Collins, N. C., Thordal-Christensen, H., Lipka, V., Bau, S., Kombrink, E., Qiu, J. L., et al. (2003). SNARE-protein-mediated disease resistance at the plant cell wall. Nature 425, 973-977.
42. Cox, G., and Sanders, F. (1974). Ultrastructure of the host-fungus interface in a vesicular-arbuscular mycorrhiza. New Phytol. 73, 901-912.
43. Danielson, J. A. H., and Johanson, U. (2010). "Phylogeny of major intrinsic proteins, " in Mips and Their Role in the Exchange of Metalloids, eds T. P. Jahn and G. P. Bienert (New York, NY: Springer), 19-32.
44. De Jonge, R., Van Esse, H. P., Kombrink, A., Shinya, T., Desaki, Y., Bours, R., et al. (2010). Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science 329, 953-955.
45. 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.
46. Den Herder, G., Yoshida, S., Antolin-Llovera, M., Ried, M. K., and Parniske, M. (2012). Lotus japonicus E3 ligase SEVEN IN ABSENTIA4 destabilizes the symbiosis receptor-like kinase SYMRK and negatively regulates rhizobial infection. Plant cell 24, 1691-1707.
47. Dénarié, J., Debellé, F., and Promé, J. C. (1996). Rhizobium lipo-chitooligosaccharide nodulation factors: signaling molecules mediating recognition and morphogenesis. Annu. Rev. Biochem. 65, 503-535.
48. Doidy, J., Grace, E., Kühn, C., Simon-Plas, F., Casieri, L., and Wipf, D. (2012). Sugar transporters in plants and in their interactions with fungi. Trends Plant Sci. 17, 413-422.
49. Dor, E., Joel, D. M., Kapulnik, Y., Koltai, H., and Hershenhorn, J. (2011). The synthetic strigolactone GR24 influences the growth pattern of phytopathogenic fungi. Planta 234, 419-427.
50. Egerton-Warburton, L. M., Querejeta, J. I., and Allen, M. F. (2007). Common mycorrhizal networks provide a potential pathway for the transfer of hydraulically lifted water between plants. J. Exp. Bot. 58, 1473-1483.
51. Endre, G., Kereszt, A., Kevei, Z., Mihacea, S., Kaló, P., and Kiss, G. B. (2002). A receptor kinase gene regulating symbiotic nodule development. Nature 417, 962-966.
52. Engel, A., Fujiyoshi, Y., Gonen, T., and Walz, T. (2008). Junction-forming aquaporins. Curr. Opin. Struct. Biol. 18, 229-235.
53. Fang, H., Mullins, C., and Green, N. (1997). In addition to SEC11, a newly identified gene, SPC3, is essential for signal peptidase activity in the yeast endoplasmic reticulum. J. Biol. Chem. 272, 13152-13158.
54. Feddermann, N., Duvvuru Muni, R. R., Zeier, T., Stuurman, J., Ercolin, F., Schorderet, M., et al. (2010). The PAM1gene of petunia, required for intracellular accommodation and morphogenesis of arbuscular mycorrhizal fungi, encodes a homologue of VAPYRIN. Plant J. 64, 470-481.
55. Feddermann, N., and Reinhardt, D. (2011). Conserved residues in the ankyrin domain of VAPYRIN indicate potential protein-protein interaction surfaces. Plant Signal. Behav. 6, 680-684.
56. 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.
57. Fellbaum, C. R., Gachomo, E. W., Beesetty, Y., Choudhari, S., Strahan, G. D., Pfeffer, P. E., et al. (2011). Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. U.S.A. 109, 2666-2671.
58. Ferrol, N., Gianinazzi, S., and Gianinazzi-Person, V. (2002). "Arbuscular mycorrhiza induced ATPases and membrane nutrient transport mechanisms, " in Mycorrhizal Technology in Agriculture: from Genes to Bioproducts, eds S. Gianinazzi, H. Schüepp, J. M. Barea, and K. Haselwandter (Basel: Birkhäuser), 113-122.
59. Flemetakis, E., Dimou, M., Cotzur, D., Efrose, R. C., Aivalakis, G., Colebatch, G., et al. (2003). A sucrose transporter, LjSUT4, is up-regulated during Lotus japonicus nodule development. J. Exp. Bot. 54, 1789-1791.
60. Fliegmann, J., Uhlenbroich, S., Shinya, T., Martinez, Y., Lefebvre, B., Shibuya, N., et al. (2011). Biochemical and phylogenetic analysis of CEBiP-like LysM domain-containing extracellular proteins in higher plants. Plant Physiol. Biochem. 49, 709-720.
61. Fournier, J., Timmers, A. C. J., Sieberer, B. J., Jauneau, A., Chabaud, M., and Barker, D. G. (2008). Mechanism of infection thread elongation in root hairs of Medicago truncatula and dynamic interplay with associated rhizobial colonization. Plant Physiol. 148, 1985-1995.
62. García-Garrido, J. M., and Ocampo, J. A. (2002). Regulation of the plant defence response in arbuscular mycorrhizal symbiosis. J. Exp. Bot. 53, 1377-1386.
63. Gaude, N., Bortfeld, S., Duensing, N., Lohse, M., and Krajinski, F. (2012). Arbuscule-containing and non-colonized cortical cells of mycorrhizal roots undergo extensive and specific reprogramming during arbuscular mycorrhizal development. Plant J. 69, 510-528.
64. Genre, A., Chabaud, M., Faccio, A., Barker, D. G., and Bonfante, P. (2008). Prepenetration apparatus assembly precedes and predicts the colonization patterns of arbuscular mycorrhizal fungi within the root cortex of bothMedicago truncatula and Daucus carota. Plant Cell 20, 1407-1420.
65. Genre, A., Chabaud, M., Timmers, T., Bonfante, P., and Barker, D. G. (2005). Arbuscular mycorrhizal fungi elicit a novel intracellular apparatus in Medicago truncatula root epidermal cells before infection. Plant Cell 17, 3489-3499.
66. Genre, A., Ivanov, S., Fendrych, M., Faccio, A., Zarsky, V., Bisseling, T., et al. (2012). Multiple exocytotic markers accumulate at the sites of perifungal membrane biogenesis in arbuscular mycorrhizas. Plant Cell Physiol. 53, 244-255.
67. Gherbi, H., Markmann, K., Svistoonoff, S., Estevan, J., Autran, D., Giczey, G., et al. (2008). SymRK defines a common genetic basis for plant root endosymbioses with arbuscular mycorrhiza fungi, rhizobia, and Frankia bacteria. Proc. Natl. Acad. Sci. U.S.A. 105, 4928-4932.
68. Gianinazzi-Pearson, V., Arnould, C., Oufattole, M., Arango, M., and Gianinazzi, S. (2000). Differential activation of H+-ATPase genes by an arbuscular mycorrhizal fungus in root cells of transgenic tobacco. Planta 211, 609-613.
69. Gimenez-Ibanez, S., Hann, D. R., Ntoukakls, V., Petutschnig, E., Lipka, V., and Rathjen, J. P. (2009). AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Curr. Biol. 19, 423-429.
70. Gomez, S. K., Javot, H., Deewatthanawong, P., Torres-Jerez, I., Tang, Y. H., Blancaflor, E. B., et al. (2009). Medicago truncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizal symbiosis. BMC Plant Biol. 9. doi: 10.1186/1471-2229-9-10
71. Gough, C., and Cullimore, J. (2011). Lipo-chitooligosaccharide signaling in endosymbiotic plant-microbe interactions. Mol. Plant Microbe Interact. 24, 867-878.
72. Govindarajulu, M., Pfeffer, P. E., Jin, H. R., Abubaker, J., Douds, D. D., Allen, J. W., et al. (2005). Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 435, 819-823.
73. Groth, M., Takeda, N., Perry, J., Uchida, H., Draexl, S., Brachmann, A., et al. (2010). NENA, a Lotus japonicushomolog of Sec13, is required for rhizodermal infection by arbuscular mycorrhiza fungi and rhizobia but dispensable for cortical endosymbiotic development. Plant Cell 22, 2509-2526.
74. Guether, M., Balestrini, R., Hannah, M., He, J., Udvardi, M., and Bonfante, P. (2009a). Genome-wide reprogramming of regulatory networks, cell wall and membrane biogenesis during arbuscular-mycorrhizal symbiosis in Lotus japonicus. New Phytologist 182, 200-212.
75. Guether, M., Neuhauser, B., Balestrini, R., Dynowski, M., Ludewig, U., and Bonfante, P. (2009b). A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiol. 150, 73-83.
76. Güimil, S., Chang, H. S., Zhu, T., Sesma, A., Osbourn, A., Roux, C., et al. (2005). Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization. Proc. Natl. Acad. Sci. U.S.A. 102, 8066-8070.
77. Gust, A. A., Willmann, R., Desaki, Y., Grabherr, H. M., and Nürnberger, T. (2012). Plant LysM proteins: modules mediating symbiosis and immunity. Trends Plant Sci. 17, 495-502.
78. Gutjahr, C., Banba, M., Croset, V., An, K., Miyao, A., An, G., et al. (2008). Arbuscular mycorrhiza-specific signaling in rice transcends the common symbiosis signaling pathway. Plant Cell 20, 2989-3005.
79. Gutjahr, C., Radovanovic, D., Geoffroy, J., Zhang, Q., Siegler, H., Chiapello, M., et al. (2012). The half-size ABC transporters STR1 and STR2 are indispensable for mycorrhizal arbuscule formation in rice. Plant J. 69, 906-920.
80. Guttenberger, M. (2000). Arbuscules of vesicular-arbuscular mycorrhizal fungi inhabit an acidic compartment within plant roots. Planta 211, 299-304.
81. Hakoyama, T., Niimi, K., Yamamoto, T., Isobe, S., Sato, S., Nakamura, Y., et al. (2012). The integral membrane protein SEN1 is required for symbiotic nitrogen fixation in Lotus japonicus nodules. Plant Cell Physiol. 53, 225-236.
82. Hammer, E. C., Pallon, J., Wallander, H., and Olsson, P. A. (2011). Tit for tat? A mycorrhizal fungus accumulates phosphorus under low plant carbon availability. FEMS Microbiol. Ecol. 76, 236-244.
83. Haney, C. H., and Long, S. R. (2010). Plant flotillins are required for infection by nitrogen-fixing bacteria. Proc. Natl. Acad. Sci. U.S.A. 107, 478-483.
84. Haney, C. H., Riely, B. K., Tricoli, D. M., Cook, D. R., Ehrhardt, D. W., and Long, S. R. (2011). Symbiotic rhizobia bacteria trigger a change in localization and dynamics of the Medicago truncatula receptor kinase LYK3. Plant Cell23, 2774-2787.
85. Harrison, M. J. (1996). A sugar transporter from Medicago truncatula: altered expression pattern in roots during vesicular-arbuscular (VA) mycorrhizal associations. Plant J. 9, 491-503.
86. Harrison, M. J., Dewbre, G. R., and Liu, J. Y. (2002). A phosphate transporter from Medicago truncatula involved in the acquisiton of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14, 2413-2429.
87. Harrison, M. J., and Van Buuren, M. L. (1995). A phosphate transporter from the mycorrhizal fungus Glomus versiforme. Nature 378, 626-629.
88. Hassan, S., and Mathesius, U. (2012). The role of flavonoids in root-rhizosphere signalling: opportunities and challenges for improving plant-microbe interactions. J. Exp. Bot. 63, 3429-3444.
89. Hause, B., and Fester, T. (2005). Molecular and cell biology of arbuscular mycorrhizal symbiosis. Planta 221, 184-196.
90. Heckman, D. S., Geiser, D. M., Eidell, B. R., Stauffer, R. L., Kardos, N. L., and Hedges, S. B. (2001). Molecular evidence for the early colonization of land by fungi and plants. Science 293, 1129-1133.
91. Helber, N., Wippel, K., Sauer, N., Schaarschmidt, S., Hause, B., and Requena, N. (2011). A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp is crucial for the symbiotic relationship with plants. Plant Cell 23, 3812-3823.
92. Hijikata, N., Murase, M., Tani, C., Ohtomo, R., Osaki, M., and Ezawa, T. (2010). Polyphosphate has a central role in the rapid and massive accumulation of phosphorus in extraradical mycelium of an arbuscular mycorrhizal fungus. New Phytol. 186, 285-289.
93. Hill, A. E., Shachar-Hill, B., and Shachar-Hill, Y. (2004). What are aquaporins for? J. Membr. Biol. 197, 1-32.
94. Hocher, V., Alloisio, N., Auguy, F., Fournier, P., Doumas, P., Pujic, P., et al. (2011). Transcriptomics of actinorhizal symbioses reveals homologs of the whole common symbiotic signaling cascade. Plant Physiol. 156, 700-711.
95. Hohnjec, N., Vieweg, M. E., Puhler, A., Becker, A., and Kuster, H. (2005). Overlaps in the transcriptional profiles ofMedicago truncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiol. 137, 1283-1301.
96. Horvath, B., Yeun, L. H., Domonkos, A., Halasz, G., Gobbato, E., Ayaydin, F., et al. (2011). Medicago truncatulaIPD3 Is a member of the common symbiotic signaling pathway required for rhizobial and mycorrhizal symbioses. Mol. Plant Microbe Interact. 24, 1345-1358.
97. Hwang, J. H., Ellingson, S. R., and Roberts, D. M. (2010). Ammonia permeability of the soybean nodulin 26 channel. FEBS Lett. 584, 4339-4343.
98. Ivanov, S., Fedorova, E. E., Limpens, E., De Mita, S., Genre, A., Bonfante, P., et al. (2012). Rhizobium-legume symbiosis shares an exocytotic pathway required for arbuscule formation. Proc. Natl. Acad. Sci. U.S.A. 109, 8316-8321.
99. Jahn, R., and Scheller, R. H. (2006). SNAREs-engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 7, 631-643.
100. Jarsch, I. K., and Ott, T. (2011). Perspectives on remorin proteins, membrane rafts, and their role during plant-microbe interactions. Mol. Plant Microbe Interact. 24, 7-12.
101. Javot, H., Penmetsa, R. V., Terzaghi, N., Cook, D. R., and Harrison, M. J. (2007). A Medicago truncatula phosphate transporter indispensable for the arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. U.S.A. 104, 1720-1725.
102. Jones, K. M., Kobayashi, H., Davies, B. W., Taga, M. E., and Walker, G. C. (2007). How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat. Rev. Microbiol. 5, 619-633.
103. Kaiser, B. N., Finnegan, P. M., Tyerman, S. D., Whitehead, L. F., Bergersen, F. J., Day, D. A., et al. (1998). Characterization of an ammonium transport protein from the peribacteroid membrane of soybean nodules. Science281, 1202-1206.
104. Kaku, H., Nishizawa, Y., Ishii-Minami, N., Akimoto-Tomiyama, C., Dohmae, N., Takio, K., et al. (2006). Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc. Natl. Acad. Sci. U.S.A. 103, 11086-11091.
105. Kalde, M., Nuhse, T. S., Findlay, K., and Peck, S. C. (2007). The syntaxin SYP132 contributes to plant resistance against bacteria and secretion of pathogenesis-related protein 1. Proc. Natl. Acad. Sci. U.S.A. 104, 11850-11855.
106. Kambara, K., Ardissone, S., Kobayashi, H., Saad, M. M., Schumpp, O., Broughton, W. J., et al. (2009). Rhizobia utilize pathogen-like effector proteins during symbiosis. Mol. Microbiol. 71, 92-106.
107. Kanamori, N., Madsen, L. H., Radutoiu, S., Frantescu, M., Quistgaard, E. M. H., Miwa, H., et al. (2006). A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc. Natl. Acad. Sci. U.S.A. 103, 359-364.
108. Karandashov, V., and Bucher, M. (2005). Symbiotic phosphate transport in arbuscular mycorrhizas. Trends Plant Sci. 10, 22-29.
109. Keinath, N. F., Kierszniowska, S., Lorek, J., Bourdais, G., Kessler, S. A., Shimosato-Asano, H., et al. (2010). PAMP (Pathogen-associated Molecular Pattern)-induced changes in plasma membrane compartmentalization reveal novel components of plant immunity. J. Biol. Chem. 285, 39140-39149.
110. Kevei, Z., Lougnon, G., Mergaert, P., Horvath, G. V., Kereszt, A., Jayaraman, D., et al. (2007). 3-hydroxy-3-methylglutaryl coenzyme A reductase1 interacts with NORK and is crucial for nodulation in Medicago truncatula. Plant Cell 19, 3974-3989.
111. Khan, W., Costa, C., Souleimanov, A., Prithiviraj, B., and Smith, D. L. (2011). Response of Arabidopsis thalianaroots to lipo-chitooligosaccharide from Bradyrhizobium japonicum and other chitin-like compounds. Plant Growth Regul. 63, 243-249.
112. Kiers, E. T., Duhamel, M., Beesetty, Y., Mensah, J. A., Franken, O., Verbruggen, E., et al. (2011). Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333, 880-882.
113. Kistner, C., and Parniske, M. (2002). Evolution of signal transduction in intracellular symbiosis. Trends Plant Sci. 7, 511-518.
114. Kloppholz, S., Kuhn, H., and Requena, N. (2011). A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr. Biol. 21, 1204-1209.
115. Kobae, Y., and Hata, S. (2010). Dynamics of periarbuscular membranes visualized with a fluorescent phosphate transporter in arbuscular mycorrhizal roots of rice. Plant Cell Physiol. 51, 341-353.
116. Kobae, Y., Tamura, Y., Takai, S., Banba, M., and Hata, S. (2010). Localized expression of arbuscular mycorrhiza-inducible ammonium transporters in soybean. Plant Cell Physiol. 51, 1411-1415.
117. Kosuta, S., Hazledine, S., Sun, J., Miwa, H., Morris, R. J., Downie, J. A., et al. (2008). Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proc. Natl. Acad. Sci. U.S.A. 105, 9823-9828.
118. Krajinski, F., Hause, B., Gianinazzi-Pearson, V., and Franken, P. (2002). Mtha1, a plasma membrane H+-ATPase gene from Medicago truncatula, shows arbuscule-specific induced expression in mycorrhizal tissue. Plant Biol. 4, 754-761.
119. Kretzschmar, T., Kohlen, W., Sasse, J., Borghi, L., Schlegel, M., Bachelier, J. B., et al. (2012). A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature 483, 341-346.
120. Kuga, Y., Saito, K., Nayuki, K., Peterson, R. L., and Saito, M. (2008). Ultrastructure of rapidly frozen and freeze-substituted germ tubes of an arbuscular mycorrhizal fungus and localization of polyphosphate. New Phytol. 178, 189-200.
121. Kuhn, H., Kuster, H., and Requena, N. (2010). Membrane steroid-binding protein 1 induced by a diffusible fungal signal is critical for mycorrhization in Medicago truncatula. New Phytol. 185, 716-733.
122. Kwon, C., Neu, C., Pajonk, S., Yun, H. S., Lipka, U., Humphry, M., et al. (2008). Co-option of a default secretory pathway for plant immune responses. Nature 451, 835-840.
123. Lefebvre, B., Timmers, T., Mbengue, M., Moreau, S., Herve, C., Toth, K., et al. (2010). A remorin protein interacts with symbiotic receptors and regulates bacterial infection. Proc. Natl. Acad. Sci. U.S.A. 107, 2343-2348.
124. Lev, S., Ben Halevy, D., Peretti, D., and Dahan, N. (2008). The VAP protein family: from cellular functions to motor neuron disease. Trends Cell Biol. 18, 282-290.
125. Lewis, J. D., Lee, A., Ma, W. B., Zhou, H. B., Guttman, D. S., and Desveaux, D. (2011). The YopJ superfamily in plant-associated bacteria. Mol. Plant Pathol. 12, 928-937.
126. Leyman, B., Geelen, D., Quintero, F. J., and Blatt, M. R. (1999). A tobacco syntaxin with a role in hormonal control of guard cell ion channels. Science 283, 537-540.
127. Li, H. Y., Smith, F. A., Dickson, S., Holloway, R. E., and Smith, S. E. (2008). Plant growth depressions in arbuscular mycorrhizal symbioses: not just caused by carbon drain? New Phytol. 178, 852-862.
128. Ligrone, R., Duckett, J. G., and Renzaglia, K. S. (2012). Major transitions in the evolution of early land plants: a bryological perspective. Ann. Bot. 109, 851-871.
129. Limpens, E., Ivanov, S., Van Esse, W., Voets, G., Fedorova, E., and Bisseling, T. (2009). Medicago N-2-fixing symbiosomes acquire the endocytic identity marker Rab7 but delay the acquisition of vacuolar identity. Plant Cell21, 2811-2828.
130. Limpens, E., Mirabella, R., Fedorova, E., Franken, C., Franssen, H., Bisseling, T., et al. (2005). Formation of organelle-like N-2-fixing symbiosomes in legume root nodules is controlled by DMI2. Proc. Natl. Acad. Sci. U.S.A. 102, 10375-10380.
131. Liu, T. T., Liu, Z. X., Song, C. J., Hu, Y. F., Han, Z. F., She, J., et al. (2012). Chitin-induced dimerization activates a plant immune receptor. Science 336, 1160-1164.
132. Lohmann, G. V., Shimoda, Y., Nielsen, M. W., Jorgensen, F. G., Grossmann, C., Sandal, N., et al. (2010). Evolution and regulation of the Lotus japonicus LysM receptor gene family. Mol. Plant Microbe Interact. 23, 510-521.
133. Lohse, S., Hause, B., Hause, G., and Fester, T. (2006). FtsZ characterization and immunolocalization in the two phases of plastid reorganization in arbuscular mycorrhizal roots of Medicago truncatula. Plant Cell Physiol. 47, 1124-1134.
134. Lohse, S., Schliemann, W., Ammer, C., Kopka, J., Strack, D., and Fester, T. (2005). Organization and metabolism of plastids and mitochondria in arbuscular mycorrhizal roots of Medicago truncatula. Plant Physiol. 139, 329-340.
135. Long, S. R. (1989). Rhizobium-legume nodulation-life together in the underground. Cell 56, 203-214.
136. Lopez-Pedrosa, A., Gonzalez-Guerrero, M., Valderas, A., Azcon-Aguilar, C., and Ferrol, N. (2006). GintAMT1 encodes a functional high-affinity ammonium transporter that is expressed in the extraradical mycelium of Glomus intraradices. Fungal Genet. Biol. 43, 102-110.
137. Lovering, A. L., Safadi, S. S., and Strynadka, N. C. J. (2012). Structural perspective of peptidoglycan biosynthesis and assembly. Annu. Rev. Biochem. 81, 451-478.
138. Madsen, E. B., AntolíN-Llovera, M., Grossmann, G., Ye, J., Vieweg, S., Broghammer, A., et al. (2011). Autophosphorylation is essential for the in vivo function of the Lotus japonicus Nod factor receptor 1 and receptor-mediated signalling in cooperation with Nod factor receptor 5. Plant J. 65, 404-417.
139. Madsen, E. B., Madsen, L. H., Radutoiu, S., Olbryt, M., Rakwalska, M., Szczyglowski, K., et al. (2003). A receptor kinase gene of the LysM type is involved in legume perception of rhizobial signals. Nature 425, 637-640.
140. Maeda, D., Ashida, K., Iguchi, K., Chechetka, S. A., Hijikata, A., Okusako, Y., et al. (2006). Knockdown of an arbuscular mycorrhiza-inducible phosphate transporter gene of Lotus japonicus suppresses mutualistic symbiosis. Plant Cell Physiol. 47, 807-817.
141. Maillet, F., Poinsot, V., André, O., Puech-Pagès, V., Haouy, A., Gueunier, M., et al. (2011). Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 469, 58-64.
142. Maldonado-Mendoza, I. E., Dewbre, G. R., and Harrison, M. J. (2001). A phosphate transporter gene from the extra-radical mycelium of an arbuscular mycorrhizal fungus Glomus intraradices is regulated in response to phosphate in the environment. Mol. Plant Microbe Interact. 14, 1140-1148.
143. Markmann, K., Giczey, G., and Parniske, M. (2008). Functional adaptation of a plant receptor-kinase paved the way for the evolution of intracellular root symbioses with bacteria. PLoS Biol. 6:e68. doi: 10.1371/journal.pbio.0060068
144. Martinez-Romero, E. (2009). Coevolution in rhizobium-legume symbiosis? DNA Cell Biol. 28, 361-370.
145. Marulanda, A., Azcon, R., and Ruiz-Lozano, J. M. (2003). Contribution of six arbuscular mycorrhizal fungal isolates to water uptake by Lactuca sativa plants under drought stress. Physiologia Plantarum 119, 526-533.
146. Marx, C., Dexheimer, J., Gianinazzi-Pearson, V., and Gianinazzi, S. (1982). Enzymatic studies on the metabolism of vesicular-arbuscular mycorrhizas. 4. Ultracytoenzymological evidence (ATPase) for active transfer processes in the host-arbuscule interface. New Phytol. 90, 37-43.
147. Maurel, C., Santoni, V., Luu, D. T., Wudick, M. M., and Verdoucq, L. (2009). The cellular dynamics of plant aquaporin expression and functions. Curr. Opin. Plant Biol. 12, 690-698.
148. Mbengue, M., Camut, S., De Carvalho-Niebel, F., Deslandes, L., Froidure, S., Klaus-Heisen, D., et al. (2010). TheMedicago truncatula E3 ubiquitin ligase PUB1 interacts with the LYK3 symbiotic receptor and negatively regulates infection and nodulation. Plant Cell 22, 3474-3488.
149. Mellor, R. B. (1989). Bacteroids in the Rhizobium-legume symbiosis inhabit a plant internal lytic compartment-implications for other microbial endosymbioses. J. Exp. Bot. 40, 831-839.
150. Merckx, V. S. F. T., Janssens, J. B., Hynson, N. A., Specht, C. D., Bruns, T. D., and Smets, E. F. (2012). Mycoheterotrophic interactions are not limited to a narrow phylogenetic range of arbuscular mycorrhizal fungi. Mol. Ecol. 21, 1524-1532.
151. Messinese, E., Mun, J. H., Yeun, L. H., Jayaraman, D., Rouge, P., Barre, A., et al. (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.
152. Miya, A., Albert, P., Shinya, T., Desaki, Y., Ichimura, K., Shirasu, K., et al. (2007). CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 104, 19613-19618.
153. Mosavi, L. K., Cammett, T. J., Desrosiers, D. C., and Peng, Z. Y. (2004). The ankyrin repeat as molecular architecture for protein recognition. Protein Sci. 13, 1435-1448.
154. Murray, J. D., Duvvuru Muni, R., Torres-Jerez, I., Tang, Y., Allen, S., Andriankaja, M., et al. (2011). Vapyrin, a gene essential for intracellular progression of arbuscular mycorrhizal symbiosis, is also essential for infection by rhizobia in the nodule symbiosis of Medicago truncatula. Plant J. 65, 244-252.
155. Nagy, R., Drissner, D., Amrhein, N., Jakobsen, I., and Bucher, M. (2009). Mycorrhizal phosphate uptake pathway in tomato is phosphorus-repressible and transcriptionally regulated. New Phytol. 181, 950-959.
156. Naisbitt, T., James, E. K., and Sprent, J. I. (1992). The evolutionary significance of the legume genus Chamaecrista, as determined by nodule structure. New Phytol. 122, 487-492.
157. Nakagawa, T., Kaku, H., Shimoda, Y., Sugiyama, A., Shimamura, M., Takanashi, K., et al. (2011). From defense to symbiosis: limited alterations in the kinase domain of LysM receptor-like kinases are crucial for evolution of legume-Rhizobium symbiosis. Plant J. 65, 169-180.
158. Oldroyd, G. E. D., and Downie, J. A. (2006). Nuclear calcium changes at the core of symbiosis signalling. Curr. Opin. Plant Biol. 9, 351-357.
159. Oldroyd, G. E. D., and Downie, J. A. (2008). Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. 59, 519-546.
160. Oldroyd, G. E. D., Murray, J. D., Poole, P. S., and Downie, J. A. (2011). The rules of engagement in the legume-rhizobial symbiosis. Ann. Rev. Genet. 45, 119-144.
161. Olsson, P. A., Hammer, E. C., Pallon, J., Van Aarle, I. M., and Wallander, H. (2011). Elemental composition in vesicles of an arbuscular mycorrhizal fungus, as revealed by PIXE analysis. Fungal Biol. 115, 643-648.
162. Olsson, P. A., Rahm, J., and Aliasgharzad, N. (2010). Carbon dynamics in mycorrhizal symbioses is linked to carbon costs and phosphorus benefits. FEMS Microbiol. Ecol. 72, 123-131.
163. Op Den Camp, R., Streng, A., De Mita, S., Cao, Q., Polone, E., Liu, W., et al. (2011). LysM-type mycorrhizal receptor recruited for Rhizobium symbiosis in nonlegume Parasponia. Science 331, 909-912.
164. Ovchinnikova, E., Journet, E. P., Chabaud, M., Cosson, V., Ratet, P., Duc, G., et al. (2011). IPD3 controls the formation of nitrogen-fixing symbiosomes in pea and Medicago Spp. Mol. Plant Microbe Interact. 24, 1333-1344.
165. Parniske, M. (2008). Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 6, 763-775.
166. Paszkowski, U., Kroken, S., Roux, C., and Briggs, S. P. (2002). Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis. Proc. Natl. Acad. Sci. U.S.A. 99, 13324-13329.
167. Pawlowski, K., and Demchenko, K. N. (2012). The diversity of actinorhizal symbiosis. Protoplasma. doi: 10.1007/s00709-012-0388-4. [Epub ahead of print].
168. Peiter, E., Sun, J., Heckmann, A. B., Venkateshwaran, M., Riely, B. K., Otegui, M. S., et al. (2007). The Medicago truncatula DMI1 protein modulates cytosolic calcium signaling. Plant Physiol. 145, 192-203.
169. Perez-Tienda, J., Testillano, P. S., Balestrini, R., Fiorilli, V., Azcon-Aguilar, C., and Ferrol, N. (2011). GintAMT2, a new member of the ammonium transporter family in the arbuscular mycorrhizal fungus Glomus intraradices. Fungal Genet. Biol. 48, 1044-1055.
170. Petutschnig, E. K., Jones, A. M. E., Serazetdinova, L., Lipka, U., and Lipka, V. (2010). The lysin motif receptor-like kinase (LysM-RLK) CERK1 Is a major chitin-binding protein in Arabidopsis thaliana and subject to chitin-induced phosphorylation. J. Biol. Chem. 285, 28902-28911.
171. Pfeffer, P. E., Douds, D. D., Becard, G., and Shachar-Hill, Y. (1999). Carbon uptake and the metabolism and transport of lipids in an arbuscular mycorrhiza. Plant Physiol. 120, 587-598.
172. Pini, F., Frascella, A., Santopolo, L., Bazzicalupo, M., Biondi, E. G., Scotti, C., et al. (2012). Exploring the plant-associated bacterial communities in Medicago sativa L. BMC Microbiology 12, 78.
173. Pratelli, J., Sutter, J. U., and Blatt, M. R. (2004). A new catch in the SNARE. Trends Plant Sci. 9, 187-195.
174. Prell, J., and Poole, P. (2006). Metabolic changes of rhizobia in legume nodules. Trends Microbiol. 14, 161-168.
175. Pumplin, N., and Harrison, M. J. (2009). Live-cell imaging reveals periarbuscular membrane domains and organelle location in Medicago truncatula roots during arbuscular mycorrhizal symbiosis. Plant Physiol. 151, 809-819.
176. Pumplin, N., Mondo, S. J., Topp, S., Starker, C. G., Gantt, J. S., and Harrison, M. J. (2010). Medicago truncatulaVapyrin is a novel protein required for arbuscular mycorrhizal symbiosis. Plant J. 61, 482-494.
177. Pumplin, N., Zhang, X., Noar, R. D., and Harrison, M. J. (2012). Polar localization of a symbiosis-specific phosphate transporter is mediated by a transient reorientation of secretion. Proc. Natl. Acad. Sci. U.S.A. 109, E665-E672.
178. Radutoiu, S., Madsen, L. H., Madsen, E. B., Felle, H. H., Umehara, Y., Gronlund, M., et al. (2003). Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature 425, 585-592.
179. Radutoiu, S., Madsen, L. H., Madsen, E. B., Jurkiewicz, A., Fukai, E., Quistgaard, E. M. H., et al. (2007). LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO J. 26, 3923-3935.
180. Ramos, A. C., Martins, M. A., Okorokova-Facanha, A. L., Olivares, F. L., Okorokov, L. A., Sepulveda, N., et al. (2009). Arbuscular mycorrhizal fungi induce differential activation of the plasma membrane and vacuolar H+ pumps in maize roots. Mycorrhiza 19, 69-80.
181. Rausch, C., Daram, P., Brunner, S., Jansa, J., Laloi, M., Leggewie, G., et al. (2001). A phosphate transporter expressed in arbuscule-containing cells in potato. Nature 414, 462-466.
182. Redecker, D., Kodner, R., and Graham, L. E. (2000). Glomalean fungi from the Ordovician. Science 289, 1920-1921.
183. Requena, N., Breuninger, M., Franken, P., and Ocón, A. (2003). Symbiotic status, phosphate, and sucrose regulate the expression of two plasma membrane H+-ATPase genes from the mycorrhizal fungus Glomus mosseae. Plant Physiol. 132, 1540-1549.
184. Riely, B. K., Lougnon, G., Ané, J. M., and Cook, D. R. (2007). The symbiotic ion channel homolog DMI1 is localized in the nuclear membrane of Medicago truncatula roots. Plant J. 49, 208-216.
185. Rivers, R. L., Dean, R. M., Chandy, G., Hall, J. E., Roberts, D. M., and Zeidel, M. L. (1997). Functional analysis of nodulin 26, an aquaporin in soybean root nodule symbiosomes. J. Biol. Chem. 272, 16256-16261.
186. Robertson, J. G., and Lyttleton, P. (1982). Coated and smooth vesicles in the biogenesis of cell walls, plasma membranes, infection threads and peribacteroid membranes in root hairs and nodules of white clover. J. Cell. Sci. 58, 63-78.
187. Rogato, A., D'Apuzzo, E., Barbulova, A., Omrane, S., Stedel, C., Simon-Rosin, U., et al. (2008). Tissue-specific down-regulation of LjAMT1;1 compromises nodule function and enhances nodulation in Lotus japonicus. Plant Mol. Biol. 68, 585-595.
188. 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.
189. Saito, C., Ueda, T., Abe, H., Wada, Y., Kuroiwa, T., Hisada, A., et al. (2002). A complex and mobile structure forms a distinct subregion within the continuous vacuolar membrane in young cotyledons of Arabidopsis. Plant J. 29, 245-255.
190. Saito, K., Yoshikawa, M., Yano, K., Miwa, H., Uchida, H., Asamizu, E., et al. (2007). NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell 19, 610-624.
191. Sekhara Reddy, D. M. R., Schorderet, M., Feller, U., and Reinhardt, D. (2007). A petunia mutant affected in intracellular accommodation and morphogenesis of arbuscular mycorrhizal fungi. Plant J. 51, 739-750.
192. Sharda, J. N., and Koide, R. T. (2008). Can hypodermal passage cell distribution limit root penetration by mycorrhizal fungi? New Phytol. 180, 696-701.
193. Shimizu, T., Nakano, T., Takamizawa, D., Desaki, Y., Ishii-Minami, N., Nishizawa, Y., et al. (2010). Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J. 64, 204-214.
194. Shinya, T., Motoyama, N., Ikeda, A., Wada, M., Kamiya, K., Hayafune, M., et al. (2012). Functional characterization of CEBiP and CERK1 homologs in Arabidopsis and rice reveals the presence of different chitin receptor systems in plants. Plant Cell Physiol. doi: 10.1093/pcp/pcs113. [Epub ahead of print].
195. Simon-Plas, F., Perraki, A., Bayer, E., Gerbeau-Pissot, P., and Mongrand, S. (2011). An update on plant membrane rafts. Curr. Opin. Plant Biol. 14, 642-649.
196. Simons, K., and Ikonen, E. (1997). Functional rafts in cell membranes. Nature 387, 569-572.
197. Singer, S. J., and Nicolson, G. L. (1972). Fluid mosaic model of structure of cell membranes. Science 175, 720-731.
198. Singh, S., and Parniske, M. (2012). Activation of calcium-and calmodulin-dependent protein kinase (CCaMK), the central regulator of plant root endosymbiosis. Curr. Opin. Plant Biol. 15, 444-453.
199. Smit, P., Limpens, E., Geurts, R., Fedorova, E., Dolgikh, E., Gough, C., et al. (2007). Medicago LYK3, an entry receptor in rhizobial nodulation factor signaling. Plant Physiol. 145, 183-191.
200. Smith, S., and Read, D. (2008). Mycorrhizal Symbiosis. New York, NY: Academic Press.
201. Smith, S. E., and Smith, F. A. (2011). Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu. Rev. Plant Biol. 62, 227-250.
202. Soltis, D. E., Soltis, P. S., Morgan, D. R., Swensen, S. M., Mullin, B. C., Dowd, J. M., et al. (1995). Chloroplast gene sequence data suggest a single origin of predisposition for symbiotic nitrogen fixation in angiosperms. Proc. Natl. Acad. Sci. U.S.A. 92, 2647-2651.
203. Soto, M. J., Nogales, J., Perez-Mendoza, D., Gallegos, M. T., Olivares, J., and Sanjuan, J. (2011). Pathogenic and mutualistic plant-bacteria interactions: ever increasing similarities. Central Eur. J. Biol. 6, 911-917.
204. Spaink, H. P. (1995). The molecular basis of infection and nodulation by rhizobia-the ins and outs of sympathogenesis. Annu. Rev. Phytopathol. 33, 345-368.
205. Starker, C. G., Parra-Colmenares, A. L., Smith, L., Mitra, R. M., and Long, S. R. (2006). Nitrogen fixation mutants ofMedicago truncatula fail to support plant and bacterial symbiotic gene expression. Plant Physiol. 140, 671-680.
206. Strack, D., and Fester, T. (2006). Isoprenoid metabolism and plastid reorganization in arbuscular mycorrhizal roots. New Phytol. 172, 22-34.
207. Stracke, S., Kistner, C., Yoshida, S., Mulder, L., Sato, S., Kaneko, T., et al. (2002). A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature 417, 959-962.
208. Tanner, W., Malinsky, J., and Opekarova, M. (2011). In plant and animal cells, detergent-resistant membranes do not define functional membrane rafts. Plant Cell 23, 1191-1193.
209. Tena, G., Boudsocq, M., and Sheen, J. (2011). Protein kinase signaling networks in plant innate immunity. Curr. Opin. Plant Biol. 14, 519-529.
210. Tian, C. J., Kasiborski, B., Koul, R., Lammers, P. J., Bucking, H., and Shachar-Hill, Y. (2010). Regulation of the nitrogen transfer pathway in the arbuscular mycorrhizal symbiosis: gene characterization and the coordination of expression with nitrogen flux. Plant Physiol. 153, 1175-1187.
211. Timmers, A. C. J., Auriac, M. C., De Billy, F., and Truchet, G. (1998). Nod factor internalization and microtubular cytoskeleton changes occur concomitantly during nodule differentiation in alfalfa. Development 125, 339-349.
212. Toth, K., Stratil, T. F., Madsen, E. B., Ye, J. Y., Popp, C., Antolin-Llovera, M., et al. (2012). Functional domain analysis of the remorin protein LjSYMREM1 in Lotus japonicus. PLoS ONE 7:e30817. doi: 10.1371/journal.pone.0030817
213. Tyerman, S. D., Whitehead, L. F., and Day, D. A. (1995). A channel-like transporter for NH4+ on the symbiotic interface of N2-fixing plants. Nature 378, 629-632.
214. Uehlein, N., Otto, B., Hanson, D. T., Fischer, M., McDowell, N., and Kaldenhoff, R. (2008). Function of Nicotiana tabacum aquaporins as chloroplast gas pores challenges the concept of membrane CO2 permeability. Plant Cell 20, 648-657.
215. Uetake, Y., Kojima, T., Ezawa, T., and Saito, M. (2002). Extensive tubular vacuole system in an arbuscular mycorrhizal fungus, Gigaspora margarita. New Phytol. 154, 761-768.
216. Van Brussel, A. A. N., Bakhuizen, R., Vanspronsen, P. C., Spaink, H. P., Tak, T., Lugtenberg, B. J. J., et al. (1992). Induction of preinfection thread structures in the leguminous host plant by mitogenic lipooligosaccharides of Rhizobium. Science 257, 70-72.
217. Van De Velde, W., Zehirov, G., Szatmari, A., Debreczeny, M., Ishihara, H., Kevei, Z., et al. (2010). Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327, 1122-1126.
218. Verma, D. P. S., Kazazian, V., Zogbi, V., and Bal, A. K. (1978). Isolation and characterization of membrane envelope enclosing bacteroids in soybean root-nodules. J. Cell Biol. 78, 919-936.
219. Walter, M. H., Floss, D. S., and Strack, D. (2010). Apocarotenoids: hormones, mycorrhizal metabolites and aroma volatiles. Planta 232, 1-17.
220. Wan, J., Tanaka, K., Zhang, X.-C., Son, G. H., Brechenmacher, L., Nguyen, T. H. N., et al. (2012). LYK4, a LysM receptor-like kinase, is important for chitin signaling and plant innate immunity in Arabidopsis. Plant Physiol. 160, 396-406.
221. Wan, J. R., Zhang, X. C., Neece, D., Ramonell, K. M., Clough, S., Kim, S. Y., et al. (2008). A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20, 471-481.
222. Wang, B., and Qiu, Y. L. (2006). Phylogenetic distribution and evolution of mycorrhizas in land plants. Mycorrhiza16, 299-363.
223. Wang, B., Yeun, L. H., Xue, J. Y., Liu, Y., Ane, J. M., and Qiu, Y. L. (2010a). Presence of three mycorrhizal genes in the common ancestor of land plants suggests a key role of mycorrhizas in the colonization of land by plants. New Phytol. 186, 514-525.
224. Wang, D., Griffitts, J., Starker, C., Fedorova, E., Limpens, E., Ivanov, S., et al. (2010b). A nodule-specific protein secretory pathway required for nitrogen-fixing symbiosis. Science 327, 1126-1129.
225. Wang, D., and Dong, X. N. (2011). A highway for war and peace: the secretory pathway in plant-microbe interactions. Mol. Plant 4, 581-587.
226. Wang, D., Yang, S. M., Tang, F., and Zhu, H. Y. (2012). Symbiosis specificity in the legume-rhizobial mutualism. Cell. Microbiol. 14, 334-342.
227. Wegmüller, S., Svistoonoff, S., Reinhardt, D., Stuurman, J., Amrhein, N., and Bucher, M. (2008). A transgenic dTph1 insertional mutagenesis system for forward genetics in mycorrhizal phosphate transport of Petunia. Plant J. 54, 1115-1127.
228. Willmann, R., Lajunen, H. M., Erbs, G., Newman, M.-A., Kolb, D., Tsuda, K., et al. (2011). Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection. Proc. Natl. Acad. Sci. U.S.A. 108, 19824-19829.
229. Yano, K., Yoshida, S., Muller, J., Singh, S., Banba, M., Vickers, K., et al. (2008). CYCLOPS, a mediator of symbiotic intracellular accommodation. Proc. Natl. Acad. Sci. U.S.A. 105, 20540-20545.
230. Yun, H. S., and Kwon, C. (2012). Trafficking at the host cell surface during plant immune responses. J. Plant Biol. 55, 185-190.
231. Yurgel, S. N., and Kahn, M. L. (2005). Sinorhizobium meliloti dctA mutants with partial ability to transport dicarboxylic acids. J. Bacteriol. 187, 1161-1172.
232. Zamioudis, C., and Pieterse, C. M. J. (2012). Modulation of host immunity by beneficial microbes. Mol. Plant Microbe Interact. 25, 139-150.
233. Zeng, L., Velasquez, A. C., Munkvold, K. R., Zhang, J., and Martin, G. B. (2012). A tomato LysM receptor-like kinase promotes immunity and its kinase activity is inhibited by AvrPtoB. Plant J. 69, 92-103.
234. Zeuthen, T. (2010). Water-transporting proteins. J. Membr. Biol. 234, 57-73.
235. Zhang, Q., Blaylock, L. A., and Harrison, M. J. (2010). Two Medicago truncatula half-ABC transporters are essential for arbuscule development in arbuscular mycorrhizal symbiosis. Plant Cell 22, 1483-1497.
236. Zhang, X. C., Cannon, S. B., and Stacey, G. (2009). Evolutionary genomics of LysM genes in land plants. BMC Evol. Biol. 9, 183.