The role of the cell wall compartment in mutualistic symbioses of plants

Frontiers in Plant Science

Volumn 5, Issue JUN, 2014, Pages

  Rich, Mélanie K ^a   Schorderet, Martine ^a   Reinhardt, Didier ^a  

^a UNIVERSITY OF FRIBOURG   (Switzerland)

Author keywords

Arbuscular mycorrhiza; Cell wall; Nodulation; Petunia; Rhizobium; Rhizophagus; Symbiosis; Symbiotic interface

Indexed keywords

EID: 84979519620     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00238     Document Type: Review

References (169)

1. Abdel-Lateif, K., Bogusz, D., and Hocher, V. (2012). The role of flavonoids in the establishment of plant roots endosymbioses with arbuscular mycorrhiza fungi, rhizobia and Frankia bacteria. Plant Signal. Behav. 7, 636-641. doi: 10.4161/psb.20039
2. Akiyama, K., Matsuzaki, K., and Hayashi, H. (2005). Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435, 824-827. doi: 10.1038/nature03608
3. Alassimone, J., Naseer, S., and Geldner, N. (2010). A developmental framework for endodermal differentiation and polarity. Proc. Natl. Acad. Sci. U.S.A. 107, 5214-5219. doi: 10.1073/pnas.0910772107
4. Baier, M. C., Barsch, A., Küster, H., and Hohnjec, N. (2007). Antisense repression of the Medicago truncatula nodule-enhanced sucrose synthase leads to a handicapped nitrogen fixation mirrored by specific alterations in the symbiotic transcriptome and metabolome. Plant Physiol. 145, 1600-1618. doi: 10.1104/pp.107.106955
5. Baier, M. C., Keck, M., Godde, V., Niehaus, K., Küster, H., and Hohnjec, N. (2010). Knockdown of the symbiotic sucrose synthase MtSucS1 affects arbuscule maturation and maintenance in mycorrhizal roots of Medicago truncatula. Plant Physiol. 152, 1000-1014. doi: 10.1104/pp.109.149898
6. Balestrini, R., and Bonfante, P. (2005). The interface compartment in arbuscular mycorrhizae: a special type of plant cell wall? Plant Biosyst. 139, 8-15. doi: 10.1080/11263500500056799
7. Balestrini, R., Cosgrove, D. J., and Bonfante, P. (2005). Differential location of alpha-expansin proteins during the accommodation of root cells to an arbuscular mycorrhizal fungus. Planta 220, 889-899. doi: 10.1007/s00425-004-1431-2
8. Bapaume, L., and Reinhardt, D. (2012). How membranes shape symbioses: signaling and transport in nodulation and arbuscular mycorrhiza. Front. Plant Sci. 3:223. doi: 10.3389/fpls.2012.00223
9. Becker, A., Fraysse, N., and Sharypova, L. (2005). Recent advances in studies on structure and symbiosis-related function of rhizobial K-antigens and lipopolysaccharides. Mol. Plant Microbe Interact. 18, 899-905. doi: 10.1094/MPMI-18-0899
10. 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
11. Blee, K. A., and Anderson, A. J. (2000). “Defense responses in plants to arbuscular mycorrhizal fungi,” in Current Advances in Mycorrhizae Research, eds G. K. Podila and D. D. Douds (St. Paul: APS Press), 27-44.
12. Bohlool, B. B., and Schmidt, E. L. (1974). Lectins-possible basis for specificity in Rhizobium-legume root nodule symbiosis. Science 185, 269-271. doi: 10.1126/science.185.4147.269
13. Boller, T., and 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. doi: 10.1146/annurev.arplant.57.032905.105346
14. 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. doi: 10.1111/j.1365-313X.2010.04385.x
15. Brewin, N. J. (2004). Plant cell wall remodelling in the Rhizobium-legume symbiosis. Crit. Rev. Plant Sci. 23, 293-316. doi: 10.1080/07352680490480734
16. Brundrett, M. C. (2002). Coevolution of roots and mycorrhizas of land plants. New Phytol. 154, 275-304. doi: 10.1046/j.1469-8137.2002.00397.x
17. Buée, M., Rossignol, M., Jauneau, A., Ranjeva, R., and Bécard, G. (2000). The pre-symbiotic growth of arbuscular mycorrhizal fungi is induced by a branching factor partially purified from plant root exudates. Mol. Plant Microbe Interact. 13, 693-698. doi: 10.1094/MPMI.2000.13.6.693
18. Caffall, K. H., and Mohnen, D. (2009). The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr. Res. 344, 1879-1900. doi: 10.1016/j.carres.2009.05.021
19. Caspary, R. (1865). Bemerkungen über die Schutzscheide und die Bildung des Stammes und der Wurzel. Jahrb. Wiss. Bot. 4, 101-124.
20. Chaffey, N. (2013). “Secondary growth of tree roots,” in Plant Roots-The Hidden Half, Chap. 8, eds A. Eshel and T. Beeckman (Boca Raton: CRC Press), 1-24.
21. Cosgrove, D. J. (2000a). Expansive growth of plant cell walls. Plant Physiol. Biochem. 38, 109-124. doi: 10.1016/S0981-9428(00)00164-9
22. Cosgrove, D. J. (2000b). Loosening of plant cell walls by expansins. Nature 407, 321-326. doi: 10.1038/35030000
23. De Hoff, P. L., Brill, L. M., and Hirsch, A. M. (2009). Plant lectins: the ties that bind in root symbiosis and plant defense. Mol. Genet. Genomics 282, 1-15. doi: 10.1007/s00438-009-0460-8
24. Deising, H. B., Werner, S., and Wernitz, M. (2000). The role of fungal appressoria in plant infection. Microbes Infect. 2, 1631-1641. doi: 10.1016/S1286-4579(00)01319-8
25. Demchenko, K., Winzer, T., Stougaard, J., Parniske, M., and Pawlowski, K. (2004). Distinct roles of Lotus japonicus SYMRK and SYM15 in root colonization and arbuscule formation. New Phytol. 163, 381-392. doi: 10.1111/j.1469-8137.2004.01123.x
26. Dermatsev, V., Weingarten-Baror, C., Resnick, N., Gadkar, V., Wininger, S., Kolotilin, I., et al. (2010). Microarray analysis and functional tests suggest the involvement of expansins in the early stages of symbiosis of the arbuscular mycorrhizal fungus Glomus intraradices on tomato (Solanum lycopersicum). Mol. Plant Pathol. 11, 121-135. doi: 10.1111/j.1364-3703.2009.00581.x
27. Deslandes, L., and Rivas, S. (2012). Catch me if you can: bacterial effectors and plant targets. Trends Plant Sci. 17, 644-655. doi: 10.1016/j.tplants.2012.06.011
28. Diaz, C. L., Logman, T. J. J., Stam, H. C., and Kijne, J. W. (1995). Sugar-binding activity of pea lectin expressed in white clover hairy roots. Plant Physiol. 109, 1167-1177.
29. Diaz, C. L., Melchers, L. S., Hooykaas, P. J. J., Lugtenberg, B. J. J., and Kijne, J. W. (1989). Root lectin as a determinant of host plant specificity in the Rhizobium-legume symbiosis. Nature 338, 579-581. doi: 10.1038/338579a0
30. Dolan, L., Janmaat, K., Willemsen, V., Linstead, P., Poethig, S., Roberts, K., et al. (1993). Cellular organization of the Arabidopsis thaliana root. Development 119, 71-84.
31. Douds, D. D., Pfeffer, P. E., and Shachar-Hill, Y. (2000). “Carbon partitioning, cost, and metabolism of arbuscular mycorrhizas,” in Arbuscular Mycorrhizas: Physiology and Function, eds Y. Kapulnik and D. D. Douds (Dordrecht: Kluwer Academic Publishers).
32. Elfstrand, M., Feddermann, N., Ineichen, K., Nagaraj, V. J., Wiemken, A., Boller, T., et al. (2005). Ectopic expression of the mycorrhiza-specific chitinase gene Mtchit 3-3 in Medicago truncatula root-organ cultures stimulates spore germination of glomalean fungi. New Phytol. 167, 557-570. doi: 10.1111/j.1469-8137.2005.01397.x
33. Enstone, D. E., Peterson, C. A., and Ma, F. S. (2002). Root endodermis and exodermis: structure, function, and responses to the environment. J. Plant Growth Regul. 21, 335-351. doi: 10.1007/s00344-003-0002-2
34. Feddermann, N., Duvvuru Muni, R. R., Zeier, T., Stuurman, J., Ercolin, F., Schorderet, M., et al. (2010). The PAM1 gene of petunia, required for intracellular accommodation and morphogenesis of arbuscular mycorrhizal fungi, encodes a homologue of VAPYRIN. Plant J. 64, 470-481. doi: 10.1111/j.1365-313X.2010.04341.x
35. 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. doi: 10.1104/pp.108.125674
36. Frenzel, A., Manthey, K., Perlick, A. M., Meyer, F., Puhler, A., Küster, H., et al. (2005). Combined transcriptome profiling reveals a novel family of arbuscular mycorrhizal-specific Medicago truncatula lectin genes. Mol. Plant Microbe Interact. 18, 771-782. doi: 10.1094/MPMI-18-0771
37. Gage, D. J., and Margolin, W. (2000). Hanging by a thread: invasion of legume plants by rhizobia. Curr. Opin. Microbiol. 3, 613-617. doi: 10.1016/S1369-5274(00)00149-1
38. Geldner, N. (2013a). Casparian strips. Curr. Biol. 23, R1025-R1026. doi: 10.1016/j.cub.2013.08.052
39. Geldner, N. (2013b). The endodermis. Annu. Rev. Plant Biol. 64, 531-558. doi: 10.1146/annurev-arplant-050312-120050
40. Genre, A., Chabaud, M., Balzergue, C., Puech-Pagès, V., Novero, M., Rey, T., et al. (2013). Short-chain chitin oligomers from arbuscular mycorrhizal fungi trigger nuclear Ca2+ spiking in Medicago truncatula roots and their production is enhanced by strigolactone. New Phytol. 198, 179-189. doi: 10.1111/nph.12146
41. 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 both Medicago truncatula and Daucus carota. Plant Cell 20, 1407-1420. doi: 10.1105/tpc.108.059014
42. 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. doi: 10.1105/tpc.105.035410
43. Gerats, T., and Vandenbussche, M. (2005). A model system for comparative research: Petunia. Trends Plant Sci. 10, 251-256. doi: 10.1016/j.tplants.2005.03.005
44. Gianinazzi-Pearson, V. (1996). Plant cell responses to arbuscular mycorrhizal fungi: getting to the roots of the symbiosis. Plant Cell 8, 1871-1883. doi: 10.1105/tpc.8.10.1871
45. 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. doi: 10.1007/s004250000323
46. Gianinazzi-Pearson, V., Branzanti, B., and Gianinazzi, S. (1989). In vitro enhancement of spore germination and early hyphal growth of a vesicular-arbuscular mycorrhizal fungus by host root exudates and plant flavonoids. Symbiosis 7, 243-255.
47. Gianinazzi-Pearson, V., Dumas-Gaudot, E., Gollotte, A., Tahiri-Alaoui, A., and Gianinazzi, S. (1996). Cellular and molecular defence-related root responses to invasion by arbuscular mycorrhizal fungi. New Phytol. 133, 45-57. doi: 10.1111/j.1469-8137.1996.tb04340.x
48. Gianinazzi-Pearson, V., and Smith, F. A. (2003). Mycorrhiza 2002-a productive year. Mycorrhiza 13, 1. doi: 10.1007/s00572-003-0230-0
49. Giordano, W., and Hirsch, A. M. (2004). The expression of MaEXP1, a Melilotus alba expansin gene, is upregulated during the sweetclover-Sinorhizobium meliloti interaction. Mol. Plant Microbe Interact. 17, 613-622. doi: 10.1094/MPMI.2004.17.6.613
50. Giovannetti, M., Avio, L., Sbrana, C., and Citernesi, A. S. (1993). Factors affecting appressorium development in the vesicular arbuscular mycorrhizal fungus Glomus mosseae (Nicol. & Gerd.) Gerd. & Trappe. New Phytol. 123, 115-122. doi: 10.1111/j.1469-8137.1993.tb04537.x
51. Giovannetti, M., Sbrana, C., Citernesi, A. S., and Avio, L. (1996). Analysis of factors involved in fungal recognition responses to host derived signals by arbuscular mycorrhizal fungi. New Phytol. 133, 65-71. doi: 10.1111/j.1469-8137.1996.tb04342.x
52. Giovannetti, M., Sbrana, C., and Logi, C. (1994). Early processes involved in host recognition by arbuscular mycorrhizal fungi. New Phytol. 127, 703-709. doi: 10.1111/j.1469-8137.1994.tb02973.x
53. Gobbato, E., Marsh, J. F., Vernie, T., Wang, E., Maillet, F., Kim, J., et al. (2012). A GRAS-type transcription factor with a specific function in mycorrhizal signaling. Curr. Biol. 22, 2236-2241. doi: 10.1016/j.cub.2012.09.044
54. Gollotte, A., Gianinazzi-Pearson, V., and Gianinazzi, S. (1994). Immunocytochemical study of plant-arbuscular mycorrhizal fungus interfaces in isogenic peas myc+ or mycorrhiza resistant (myc-). Acta Bot. Gall. 141, 449-454. doi: 10.1080/12538078.1994.10515182
55. Gollotte, A., Gianinazzi-Pearson, V., Giovannetti, M., Sbrana, C., Avio, L., and Gianinazzi, S. (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. doi: 10.1007/BF00240902
56. Gomez-Roldan, V., Fermas, S., Brewer, P. B., Puech-Pagès, V., Dun, E. A., Pillot, J. P., et al. (2008). Strigolactone inhibition of shoot branching. Nature 455, 189-194. doi: 10.1038/nature07271
57. Goormachtig, S., Lievens, S., Van de Velde, W., Van Montagu, M., and Holsters, M. (1998). Srchi13, a novel early nodulin from Sesbania rostrata, is related to acidic class III chitinases. Plant Cell 10, 905-915. doi: 10.1105/tpc.10.6.905
58. Grunwald, U., Guo, W. B., Fischer, K., Isayenkov, S., Ludwig-Müller, J., Hause, B., et al. (2009). Overlapping expression patterns and differential transcript levels of phosphate transporter genes in arbuscular mycorrhizal, Pi-fertilised and phytohormone-treated Medicgo truncatula roots. Planta 229, 1023-1034. doi: 10.1007/s00425-008-0877-z
59. 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 Phytol. 182, 200-212. doi: 10.1111/j.1469-8137.2008.02725.x
60. 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. doi: 10.1104/pp.109.136390
61. 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. doi: 10.1073/pnas.0502999102
62. Gutjahr, C., and Parniske, M. (2013). Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annu. Rev. Cell Dev. Biol. 29, 593-617. doi: 10.1146/annurev-cellbio-101512-122413
63. Gutjahr, C., and Paszkowski, U. (2013). Multiple control levels of root system remodeling in arbuscular mycorrhizal symbiosis. Front. Plant Sci. 4:204. doi: 10.3389/fpls.2013.00204
64. 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. doi: 10.1111/j.1365-313X.2011.04842.x
65. Guttenberger, M. (2000). Arbuscules of vesicular-arbuscular mycorrhizal fungi inhabit an acidic compartment within plant roots. Planta 211, 299-304. doi: 10.1007/s004250000324
66. Harrison, M. J., Dewbre, G. R., and Liu, J. Y. (2002). A phosphate transporter from Medicago truncatula involved in the acquisition of phosphate released by arbuscular mycorrhizal fungi. Plant Cell 14, 2413-2429. doi: 10.1105/tpc.004861
67. Helber, N., and Requena, N. (2008). Expression of the fluorescence markers DsRed and GFP fused to a nuclear localization signal in the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol. 177, 537-548. doi: 10.1111/j.1469-8137.2007.02257.x
68. 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. doi: 10.1105/tpc.111.089813
69. Hohnjec, N., Vieweg, M. E., Puhler, A., Becker, A., and Küster, H. (2005). Overlaps in the transcriptional profiles of Medicago truncatula roots inoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza. Plant Physiol. 137, 1283-1301. doi: 10.1104/pp.104.056572
70. 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. doi: 10.1073/pnas.1200407109
71. Jones, J. D. G., and Dangl, J. L. (2006). The plant immune system. Nature 444, 323-329. doi: 10.1038/nature05286
72. Journet, E. P., El-Gachtouli, N., Vernoud, V., de Billy, F., Pichon, M., Dedieu, A., et al. (2001). Medicago truncatula ENOD11: a novel RPRP-encoding early nodulin gene expressed during mycorrhization in arbuscule-containing cells. Mol. Plant Microbe Interact. 14, 737-748. doi: 10.1094/MPMI.2001.14.6.737
73. Kardailsky, I. V., Sherrier, D. J., and Brewin, N. J. (1996). Identification of a new pea gene, PsNlec1, encoding a lectin-like glycoprotein isolated from the symbiosomes of root nodules. Plant Physiol. 111, 49-60. doi: 10.1104/pp.111.1.49
74. Kereszt, A., Mergaert, P., and Kondorosi, E. (2011). Bacteroid development in legume nodules: evolution of mutual benefit or of sacrificial victims? Mol. Plant Microbe Interact. 24, 1300-1309. doi: 10.1094/MPMI-06-11-0152
75. Ketelaar, T. (2013). The actin cytoskeleton in root hairs: all is fine at the tip. Curr. Opin. Plant Biol. 16, 749-756. doi: 10.1016/j.pbi.2013.10.003
76. Kim, H. K., Park, J., and Hwang, I. (2014). Investigating water transport through the xylem network in vascular plants. J. Exp. Bot. 65, 1895-1904. doi: 10.1093/jxb/eru075
77. Kloppholz, S., Kuhn, H., and Requena, N. (2011). A secreted fungal effector of Glomus intraradices promotes symbiotic biotrophy. Curr. Biol. 21, 1204-1209. doi: 10.1016/j.cub.2011.06.044
78. 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. doi: 10.1093/pcp/pcq099
79. Koegel, S., Lahmidi, N. A., Arnould, C., Chatagnier, O., Walder, F., Ineichen, K., et al. (2013). The family of ammonium transporters (AMT) in Sorghum bicolor: two AMT members are induced locally, but not systemically in roots colonized by arbuscular mycorrhizal fungi. New Phytol. 198, 853-865. doi: 10.1111/nph.12199
80. 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. doi: 10.1038/nature10873
81. Lambais, M. R. (2000). “Regulation of plant defense-related genes in arbuscular mycorrhizae,” in Current Advances in Mycorrhizae Research, eds G. K. Podila and D. D. Douds (St. Paul: APS Press), 45-60.
82. Lee, Y., Rubio, M. C., Alassimone, J., and Geldner, N. (2013). A mechanism for localized lignin deposition in the endodermis. Cell 153, 402-412. doi: 10.1016/j.cell.2013.02.045
83. Liang, Y., Cao, Y. R., Tanaka, K., Thibivilliers, S., Wan, J. R., Choi, J., et al. (2013). Nonlegumes respond to rhizobial Nod factors by suppressing the innate immune response. Science 341, 1384-1387. doi: 10.1126/science.1242736
84. Liu, J. Y., Blaylock, L. A., Endre, G., Cho, J., Town, C. D., VandenBosch, K. A., et al. (2003). Transcript profiling coupled with spatial expression analyses reveals genes involved in distinct developmental stages of an arbuscular mycorrhizal symbiosis. Plant Cell 15, 2106-2123. doi: 10.1105/tpc.014183
85. Lopez-Gomez, M., Sandal, N., Stougaard, J., and Boller, T. (2012). Interplay of flg22-induced defence responses and nodulation in Lotus japonicus. J. Exp. Bot. 63, 393-401. doi: 10.1093/jxb/err291
86. Lucas, W. J., Ham, L. K., and Kim, J. Y. (2009). Plasmodesmata-bridging the gap between neighboring plant cells. Trends Cell Biol. 19, 495-503. doi: 10.1016/j.tcb.2009.07.003
87. Ma, J. F., Yamaji, N., Mitani, N., Tamai, K., Konishi, S., Fujiwara, T., et al. (2007). An efflux transporter of silicon in rice. Nature 448, 209-212. doi: 10.1038/nature05964
88. 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. doi: 10.1038/nature09622
89. Manthey, K., Krajinski, F., Hohnjec, N., Firnhaber, C., Puhler, A., Perlick, A. M., et al. (2004). Transcriptome profiling in root nodules and arbuscular mycorrhiza identifies a collection of novel genes induced during Medicago truncatula root endosymbioses. Mol. Plant Microbe Interact. 17, 1063-1077. doi: 10.1094/MPMI.2004.17.10.1063
90. Margaret, I., Lucas, M. M., Acosta-Jurado, S., Buendia-Claveria, A. M., Fedorova, E., Hidalgo, A., et al. (2013). The Sinorhizobium fredii HH103 lipopolysaccharide is not only relevant at early soybean nodulation stages but also for symbiosome stability in mature nodules. PLoS ONE 8:e74717. doi: 10.1371/journal.pone.0074717
91. Martin, F., Aerts, A., Ahren, D., Brun, A., Danchin, E. G. J., Duchaussoy, F., et al. (2008). The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452, 88-92. doi: 10.1038/nature06556
92. Martin, F., and Selosse, M. A. (2008). The Laccaria genome: a symbiont blueprint decoded. New Phytol. 180, 296-310. doi: 10.1111/j.1469-8137.2008.02613.x
93. 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. doi: 10.1111/j.1469-8137.1982.tb03238.x
94. Mathis, R., Van Gijsegem, F., De Rycke, R., D'Haeze, W., Van Maelsaeke, E., Anthonio, E., et al. (2005). Lipopolysaccharides as a communication signal for progression of legume endosymbiosis. Proc. Natl. Acad. Sci. U.S.A. 102, 2655-2660. doi: 10.1073/pnas.0409816102
95. McFarlane, H., Döring, A., and Persson, S. (2014). The cell biology of cellulose synthesis. Annu. Rev. Plant Biol. 65, 69-94. doi: 10.1146/annurev-arplant-050213-040240
96. Meckfessel, M. H., Blancaflor, E. B., Plunkett, M., Dong, Q. F., and Dickstein, R. (2012). Multiple domains in MtENOD8 protein including the signal peptide target it to the symbiosome. Plant Physiol. 159, 299-310. doi: 10.1104/pp.111.191403
97. Meyer, C. J., and Peterson, C. A. (2013). “Structure and function of three suberized cell layers: epidermis, exodermis, and endodermis,” in Plant Roots-The Hidden Half, Chap. 5, eds A. Eshel and T. Beeckman (Boca Raton, FL: CRC Press), 1-20.
98. Nagahashi, G., and Douds, D. D. (1997). Appressorium formation by AM fungi on isolated cell walls of carrot roots. New Phytol. 136, 299-304. doi: 10.1046/j.1469-8137.1997.00739.x
99. Nagahashi, G., and Douds, D. D. (2011). The effects of hydroxy fatty acids on the hyphal branching of germinated spores of AM fungi. Fungal Biol. 115, 351-358. doi: 10.1016/j.funbio.2011.01.006
100. Nagendran, S., Hallen-Adams, H. E., Paper, J. M., Aslam, N., and Walton, J. D. (2009). Reduced genomic potential for secreted plant cell-wall-degrading enzymes in the ectomycorrhizal fungus Amanita bisporigera, based on the secretome of Trichoderma reesei. Fungal Genet. Biol. 46, 427-435. doi: 10.1016/j.fgb.2009.02.001
101. Neumann, G., and Martinoia, E. (2002). Cluster roots-an underground adaptation for survival in extreme environments. Trends Plant Sci. 7, 162-167. doi: 10.1016/S1360-1385(02)02241-0
102. Niehaus, K., and Becker, A. (1998). The role of microbial surface polysaccharides in the Rhizobium-legume interaction. Subcell. Biochem. 29, 73-116. doi: 10.1007/978-1-4899-1707-2_3
103. Nouri, E., Breuillin-Sessoms, F., Feller, U., and Reinhardt, D. (2014). Phosphorus and nitrogen regulate arbuscular mycorrhizal symbiosis in Petunia hybrida. PLoS ONE 9:e90841. doi: 10.1371/journal.pone.0090841
104. Novero, M., Faccio, A., Genre, A., Stougaard, J., Webb, K. J., Mulder, L., et al. (2002). Dual requirement of the LjSym4 gene for mycorrhizal development in epidermal and cortical cells of Lotus japonicus roots. New Phytol. 154, 741-749. doi: 10.1046/j.1469-8137.2002.00424.x
105. Okazaki, S., Kaneko, T., Sato, S., and Saeki, K. (2013). Hijacking of leguminous nodulation signaling by the rhizobial type III secretion system. Proc. Natl. Acad. Sci. U.S.A. 110, 17131-17136. doi: 10.1073/pnas.1302360110
106. Olah, B., Briere, C., Bécard, G., Dénarié, J., and Gough, C. (2005). Nod factors and a diffusible factor from arbuscular mycorrhizal fungi stimulate lateral root formation in Medicago truncatula via the DMI1/DMI2 signalling pathway. Plant J. 44, 195-207. doi: 10.1111/j.1365-313X.2005.02522.x
107. Oldroyd, G. E. D. (2013). Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat. Rev. Microbiol. 11, 252-263. doi: 10.1038/nrmicro2990
108. Oldroyd, G. E. D., Murray, J. D., Poole, P. S., and Downie, J. A. (2011). The rules of engagement in the legume-rhizobial symbiosis. Annu. Rev. Genet. 45, 119-144. doi: 10.1146/annurev-genet-110410-132549
109. Panstruga, R. (2003). Establishing compatibility between plants and obligate biotrophic pathogens. Curr. Opin. Plant Biol. 6, 320-326. doi: 10.1016/S1369-5266(03)00043-8
110. Parniske, M. (2000). Intracellular accommodation of microbes by plants: a common developmental program for symbiosis and disease? Curr. Opin. Plant Biol. 3, 320-328. doi: 10.1016/S1369-5266(00)00088-1
111. Parniske, M. (2008). Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 6, 763-775. doi: 10.1038/nrmicro1987
112. Petricka, J. J., Winter, C. M., and Benfey, P. N. (2012). Control of Arabidopsis root development. Annu. Rev. Plant Biol. 63, 563-590. doi: 10.1146/annurev-arplant-042811-105501
113. 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. doi: 10.1104/pp.120.2.587
114. Pierre, O., Engler, G., Hopkins, J., Brau, F., Boncompagni, E., and Hérouart, D. (2013). Peribacteroid space acidification: a marker of mature bacteroid functioning in Medicago truncatula nodules. Plant Cell Environ. 36, 2059-2070. doi: 10.1111/pce.12116
115. Plett, J. M., Kemppainen, M., Kale, S. D., Kohler, A., Legue, V., Brun, A., et al. (2011). A secreted effector protein of Laccaria bicolor is required for symbiosis development. Curr. Biol. 21, 1197-1203. doi: 10.1016/j.cub.2011.05.033
116. Pollard, M., Beisson, F., Li, Y. H., and Ohlrogge, J. B. (2008). Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci. 13, 236-246. doi: 10.1016/j.tplants.2008.03.003
117. Pozo, M. J., and Azcon-Aguilar, C. (2007). Unraveling mycorrhiza-induced resistance. Curr. Opin. Plant Biol. 10, 393-398. doi: 10.1016/j.pbi.2007.05.004
118. 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. doi: 10.1104/pp.109.141879
119. 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. doi: 10.1073/pnas.1110215109
120. 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. doi: 10.1038/35106601
121. Rival, P., de Billy, F., Bono, J. J., Gough, C., Rosenberg, C., and Bensmihen, S. (2012). Epidermal and cortical roles of NFP and DMI3 in coordinating early steps of nodulation in Medicago truncatula. Development 139, 3383-3391. doi: 10.1242/dev.081620
122. Robledo, M., Jimenez-Zurdo, J. I., Velazquez, E., Trujillo, M. E., Zurdo-Pineiro, J. L., Ramirez-Bahena, M. H., et al. (2008). Rhizobium cellulase CelC2 is essential for primary symbiotic infection of legume host roots. Proc. Natl. Acad. Sci. U.S.A. 105, 7064-7069. doi: 10.1073/pnas.0802547105
123. Roppolo, D., De Rybel, B., Tendon, V. D., Pfister, A., Alassimone, J., Vermeer, J. E. M., et al. (2011). A novel protein family mediates Casparian strip formation in the endodermis. Nature 473, 380-383. doi: 10.1038/nature10070
124. 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. doi: 10.1002/1615-9861(200203)2:3<325::AID-PROT325>3.0.CO;2-W
125. Salzer, P., and Boller, T. (2000). “Elicitor-induced reactions in mycorrhizae and their suppression,” in Current Advances in Mycorrhizae Research, eds G. K. Podila and D. D. Douds (St. Paul: APS Press), 1-10.
126. Salzer, P., Bonanomi, A., Beyer, K., Vögeli-Lange, R., Aeschbacher, R. A., Lange, J., et al. (2000). Differential expression of eight chitinase genes in Medicago truncatula roots during mycorrhiza formation, nodulation, and pathogen infection. Mol. Plant Microbe Interact. 13, 763-777. doi: 10.1094/MPMI.2000.13.7.763
127. Sbrana, C., and Giovannetti, M. (2005). Chemotropism in the arbuscular mycorrhizal fungus Glomus mosseae. Mycorrhiza 15, 539-545. doi: 10.1007/s00572-005-0362-5
128. Schaarschmidt, S., Gonzalez, M. C., Roitsch, T., Strack, D., Sonnewald, U., and Hause, B. (2007). Regulation of arbuscular mycorrhization by carbon. The symbiotic interaction cannot be improved by increased carbon availability accomplished by root-specifically enhanced invertase activity. Plant Physiol. 143, 1827-1840. doi: 10.1104/pp.107.096446
129. Schaarschmidt, S., Roitsch, T., and Hause, B. (2006). Arbuscular mycorrhiza induces gene expression of the apoplastic invertase LIN6 in tomato (Lycopersicon esculentum) roots. J. Exp. Bot. 57, 4015-4023. doi: 10.1093/jxb/erl172
130. Scheller, H. V., and Ulvskov, P. (2010). Hemicelluloses. Annu. Rev. Plant Biol. 61, 263-289. doi: 10.1146/annurev-arplant-042809-112315
131. Schreiber, L. (2010). Transport barriers made of cutin, suberin and associated waxes. Trends Plant Sci. 15, 546-553. doi: 10.1016/j.tplants.2010.06.004
132. Sharda, J. N., and Koide, R. T. (2008). Can hypodermal passage cell distribution limit root penetration by mycorrhizal fungi? New Phytol. 180, 696-701. doi: 10.1111/j.1469-8137.2008.02600.x
133. Shaul, O., David, R., Sinvani, G., Ginzberg, I., Ganon, D., Wininger, S., et al. (2000). “Plant defense responses during arbuscular mycorrhizal symbiosis,” in Current Advances in Mycorrhizae Research, eds G. K. Podila and D. D. Douds (St. Paul: APS Press), 61-68.
134. Shishkoff, N. (1987). Distribution of the dimorphic hypodermis of roots in angiosperm families. Ann. Bot. 60, 1-15.
135. Siciliano, V., Genre, A., Balestrini, R., Cappellazzo, G., deWit, P., and Bonfante, P. (2007). Transcriptome analysis of arbuscular mycorrhizal roots during development of the prepenetration apparatus. Plant Physiol. 144, 1455-1466. doi: 10.1104/pp.107.097980
136. Smith, S. E., and Read, D. J. (2008). Mycorrhizal Symbiosis. New York: Academic Press.
137. Solaiman, M. D. Z., and Saito, M. (1997). Use of sugars by intraradical hyphae of arbuscular mycorrhizal fungi revealed by radiorespirometry. New Phytol. 136, 533-538. doi: 10.1046/j.1469-8137.1997.00757.x
138. Spanu, P. D., Abbott, J. C., Amselem, J., Burgis, T. A., Soanes, D. M., Stuber, K., et al. (2010). Genome expansion and gene loss in powdery mildew fungi reveal tradeoffs in extreme parasitism. Science 330, 1543-1546. doi: 10.1126/science.1194573
139. Stergiopoulos, I., and de Wit, P. J. G. M. (2009). Fungal effector proteins, Annu. Rev. Phytopathol. 47, 233-263. doi: 10.1146/annurev.phyto.112408.132637
140. Takano, J., Tanaka, M., Toyoda, A., Miwa, K., Kasai, K., Fuji, K., et al. (2010). Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways. Proc. Natl. Acad. Sci. U.S.A. 107, 5220-5225. doi: 10.1073/pnas.0910744107
141. Takeda, N., Kistner, C., Kosuta, S., Winzer, T., Pitzschke, A., Groth, M., et al. (2007). Proteases in plant root symbiosis. Phytochemistry 68, 111-121. doi: 10.1016/j.phytochem.2006.09.022
142. Takeda, N., Sato, S., Asamizu, E., Tabata, S., and Parniske, M. (2009). Apoplastic plant subtilases support arbuscular mycorrhiza development in Lotus japonicus. Plant J. 58, 766-777. doi: 10.1111/j.1365-313X.2009.03824.x
143. Tian, Y., Liu, W., Cai, J., Zhang, L. Y., Wong, K. B., Feddermann, N., et al. (2013). The nodulation factor hydrolase of Medicago truncatula: characterization of an enzyme specifically cleaving rhizobial nodulation signals. Plant Physiol. 163, 1179-1190. doi: 10.1104/pp.113.223966
144. Tisserant, E., Kohler, A., Dozolme-Seddas, P., Balestrini, R., Benabdellah, K., Colard, A., et al. (2012). The transcriptome of the arbuscular mycorrhizal fungus Glomus intraradices (DAOM 197198) reveals functional tradeoffs in an obligate symbiont. New Phytol. 193, 755-769. doi: 10.1111/j.1469-8137.2011.03948.x
145. Tisserant, E., Malbreil, M., Kuo, A., Kohler, A., Symeonidi, A., Balestrini, R., et al. (2013). Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc. Natl. Acad. Sci. U.S.A. 110, 20117-20122. doi: 10.1073/pnas.1313452110
146. Umehara, M., Hanada, A., Yoshida, S., Akiyama, K., Arite, T., Takeda-Kamiya, N., et al. (2008). Inhibition of shoot branching by new terpenoid plant hormones. Nature 455, 195-200. doi: 10.1038/nature07272
147. Valot, B., Dieu, M., Recorbet, G., Raes, M., Gianinazzi, S., and Dumas-Gaudot, E. (2005). Identification of membrane-associated proteins regulated by the arbuscular mycorrhizal symbiosis. Plant Mol. Biol. 59, 565-580. doi: 10.1007/s11103-005-8269-2
148. 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. doi: 10.1126/science.257.5066.70
149. van Buuren, M. L., Maldonado-Mendoza, I. E., Trieu, A. T., Blaylock, L. A., and Harrison, M. J. (1999). Novel genes induced during an arbuscular mycorrhizal (AM) symbiosis formed between Medicago truncatula and Glomus versiforme. Mol. Plant Microbe Interact. 12, 171-181. doi: 10.1094/MPMI.1999.12.3.171
150. 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. doi: 10.1126/science.1184057
151. van Loon, L. C., Rep, M., and Pieterse, C. M. J. (2006). Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44, 135-162. doi: 10.1146/annurev.phyto.44.070505.143425
152. van Rhijn, P., Goldberg, R. B., and Hirsch, A. M. (1998). Lotus corniculatus nodulation specificity is changed by the presence of a soybean lectin gene. Plant Cell 10, 1233-1249. doi: 10.1105/tpc.10.8.1233
153. van Spronsen, P. C., Bakhuizen, R., van Brussel, A. A., and Kijne, J. W. (1994). Cell wall degradation during infection thread formation by the root nodule bacterium Rhizobium leguminosarum is a two-step process. Eur. J. Cell Biol. 64, 88-94.
154. Veiga, R. S. L., Faccio, A., Genre, A., Pieterse, C. M. J., Bonfante, P., and van der Heijden, M. G. A. (2013). Arbuscular mycorrhizal fungi reduce growth and infect roots of the non-host plant Arabidopsis thaliana. Plant Cell Environ. 36, 1926-1937. doi: 10.1111/pce.12102
155. Vierheilig, H., Alt, M., Neuhaus, J. M., Boller, T., and Wiemken, A. (1993). Colonization of transgenic Nicotiana sylvestris plants, expressing different forms of Nicotiana tabacum chitinase, by the root pathogen Rhizoctonia solani and by the mycorrhizal symbiont Glomus mosseae. Mol. Plant Microbe Interact. 6, 261-264. doi: 10.1094/MPMI-6-261
156. Wang, D., Yang, S. M., Tang, F., and Zhu, H. Y. (2012a). Symbiosis specificity in the legume-rhizobial mutualism. Cell. Microbiol. 14, 334-342. doi: 10.1111/j.1462-5822.2011.01736.x
157. Wang, E. T., Schornack, S., Marsh, J. F., Gobbato, E., Schwessinger, B., Eastmond, P., et al. (2012b). A common signaling process that promotes mycorrhizal and oomycete colonization of plants. Curr. Biol. 22, 2242-2246. doi: 10.1016/j.cub.2012.09.043
158. Xie, F., Murray, J. D., Kim, J., Heckmann, A. B., Edwards, A., Oldroyd, G. E. D., et al. (2012). Legume pectate lyase required for root infection by rhizobia. Proc. Natl. Acad. Sci. U.S.A. 109, 633-638. doi: 10.1073/pnas.1113992109
159. Xie, X. N., Yoneyama, K., and Yoneyama, K. (2010). The strigolactone story. Annu. Rev. Phytopathol. 48, 93-117. doi: 10.1146/annurev-phyto-073009-114453
160. Xin, D. W., Liao, S., Xie, Z. P., Hann, D. R., Steinle, L., Boller, T., et al. (2012). Functional analysis of NopM, a novel E3 ubiquitin ligase (NEL) domain effector of Rhizobium sp strain NGR234. PLoS Pathog. 8:e1002707. doi: 10.1371/journal.ppat.1002707
161. Yamauchi, T., Shimamura, S., Nakazono, M., and Mochizuki, T. (2013). Aerenchyma formation in crop species: a review. Field Crops Res. 152, 8-16. doi: 10.1016/j.fcr.2012.12.008
162. Yang, S. Y., Gronlund, M., Jakobsen, I., Grotemeyer, M. S., Rentsch, D., Miyao, A., et al. (2012). Nonredundant regulation of rice arbuscular mycorrhizal symbiosis by two members of the PHOSPHATE TRANSPORTER1 gene family. Plant Cell 24, 4236-4251. doi: 10.1105/tpc.112.104901
163. Yeats, T. H., and Rose, J. K. C. (2013). The formation and function of plant cuticles. Plant Physiol. 163, 5-20. doi: 10.1104/pp.113.222737
164. Yi, M., and Valent, B. (2013). Communication between filamentous pathogens and plants at the biotrophic interface. Annu. Rev. Phytopathol. 51, 587-611. doi: 10.1146/annurev-phyto-081211-172916
165. Yurgel, S. N., and Kahn, M. L. (2004). Dicarboxylate transport by Rhizobia. FEMS Microbiol. Rev. 28, 489-501. doi: 10.1016/j.femsre.2004.04.002
166. Zamioudis, C., and Pieterse, C. M. J. (2012). Modulation of host immunity by beneficial microbes. Mol. Plant Microbe Interact. 25, 139-150. doi: 10.1094/MPMI-06-11-0179
167. Zhang, L., Chen, X. J., Lu, H. B., Xie, Z. P., and Staehelin, C. (2011). Functional analysis of the type 3 effector nodulation outer protein L (NopL) from Rhizobium sp NGR234. J. Biol. Chem. 286, 32178-32187. doi: 10.1074/jbc.M111.265942
168. 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. doi: 10.1105/tpc.110.074955
169. Zonia, L., and Munnik, T. (2007). Life under pressure: hydrostatic pressure in cell growth and function. Trends Plant Sci. 12, 90-97. doi: 10.1016/j.tplants.2007.01.006