Secretion systems and signal exchange between nitrogen-fixing rhizobia and legumes

Frontiers in Plant Science

Volumn 6, Issue JULY, 2015, Pages

  Nelson, Matthew S ^a   Sadowsky, Michael J ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Effector proteins; Nodulation; Rhizobia; Signal exchange; Symbiosis; Type III secretion system; Type IV secretion system; Type VI secretion system

Indexed keywords

FABACEAE;

EID: 84936946915     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.00491     Document Type: Review

References (113)

1. Angot, A., Peeters, N., Lechner, E., Vailleau, F., Baud, C., Gentzbittel, L., et al. (2006). Ralstonia solanacearum requires F-box-like domain-containing type III effectors to promote disease on several host plants. Proc. Natl. Acad. Sci. U. S. A. 103, 14620-14625. doi: 10. 1073/pnas. 0509393103.
2. Bartsev, A. V., Boukli, N. M., Deakin, W. J., Staehelin, C., and Broughton, W. J. (2003). Purification and phosphorylation of the effector protein NopL from Rhizobium sp. NGR234. FEBS Lett. 554, 271-274. doi: 10. 1016/S0014-5793(03)01145-1.
3. Bartsev, A. V., Deakin, W. J., Boukli, N. M., Mcalvin, C. B., Stacey, G., Broughton, W. J., et al. (2004). NopL, an effector protein of Rhizobium sp. NGR234, thwarts activation of plant defense reactions 1. Plant Physiol. 134, 871-879. doi: 10. 1104/pp. 103. 031740.
4. Belkhadir, Y., Subramaniam, R., and Dangl, J. L. (2004). Plant disease resistance protein signaling: NBS-LRR proteins and their partners. Curr. Opin. Plant Biol. 7, 391-399. doi: 10. 1016/j. pbi. 2004. 05. 009.
5. Bingle, L. E., Bailey, C. M., and Pallen, M. J. (2008). Type VI secretion: a beginner's guide. Curr. Opin. Microbiol. 11, 3-8. doi: 10. 1016/j. mib. 2008. 01. 006.
6. Bladergroen, M. R., Badelt, K., and Spaink, H. P. (2003). Infection-blocking genes of a symbioticRhizobium leguminosarum strain that are involved in temperature-dependent protein secretion. Mol. Plant Microbe Interact. 16, 53-64. doi: 10. 1094/MPMI. 2003. 16. 1. 53.
7. Broughton, W. J., Hanin, M., Relić, B., Kopciñska, J., Golinowski, W., Şimşek, Ş., et al. (2006). Flavonoid-inducible modifications to rhamnan O antigens are necessary for Rhizobium sp. strainNGR234-legume symbioses. J. Bacteriol. 188, 3654-3663. doi: 10. 1128/JB. 188. 10. 3654-3663. 2006.
8. Cascales, E., and Christie, P. J. (2003). The versatile bacterial type IV secretion systems. Nat. Rev. Microbiol. 1, 137-49. doi: 10. 1038/nrmicro753.
9. Dai, W. J., Zeng, Y., Xie, Z. P., and Staehelin, C. (2008). Symbiosis-promoting and deleterious effects of NopT, a novel type 3 effector of Rhizobium sp. strain NGR234. J. Bacteriol. 190, 5101-5110. doi: 10. 1128/JB. 00306-8.
10. Deakin, W. J., and Broughton, W. J. (2009). Symbiotic use of pathogenic strategies: rhizobial protein secretion systems. Nat. Rev. Microbiol. 7, 312-20. doi: 10. 1038/nrmicro2091.
11. Deakin, W. J., Marie, C., Saad, M. M., Krishnan, H. B., and Broughton, W. J. (2005). NopA is associated with cell surface appendages produced by the type III secretion system of Rhizobiumsp. strain NGR234. Mol. Plant Microbe Interact. 18, 499-507. doi: 10. 1094/MPMI-18-9.
12. De Lyra, M. D. C. C. P., López-Baena, F. J., Madinabeitia, N., Vinardell, J. M., Espuny, M. D. R., Cubo, M. T., et al. (2006). Inactivation of the Sinorhizobium fredii HH103 rhcJ gene abolishes nodulation outer proteins (Nops) secretion and decreases the symbiotic capacity with soybean. Int. Microbiol. 9, 125-133.
13. 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. doi: 10. 1146/annurev. biochem. 65. 1. 503.
14. de Souza, J. A. M., Tieppo, E., de Souza Magnani, G., Alves, L. M. C., Cardoso, R. L., Cruz, L. M., et al. (2012). Draft genome sequence of the nitrogen-fixing symbiotic bacterium Bradyrhizobium elkanii 587. J. Bacteriol. 194, 3547-3548. doi: 10. 1128/JB. 00563-2.
15. Dodds, P. N., and Rathjen, J. P. (2010). Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11, 539-548. doi: 10. 1038/nrg2812.
16. Endre, G., Kereszt, A., Kevei, Z., Mihacea, S., Kalo, P., and Kiss, G. B. (2002). A receptor kinase gene regulating symbiotic nodule development. Nature 417, 962-966. doi: 10. 1038/nature00842.
17. Esseling, J. J., Lhuissier, F. G. P., and Emons, A. M. C. (2003). Nod factor-induced root hair curling: continuous polar growth towards the point of nod factor application. Plant Physiol. 132, 1982-1988. doi: 10. 1104/pp. 103. 021634.
18. Fauvart, M., and Michiels, J. (2008). Rhizobial secreted proteins as determinants of host specificity in the Rhizobium-legume symbiosis. FEMS Microbiol. Lett. 285, 1-9. doi: 10. 1111/j. 1574-6968. 2008. 01254. x.
19. Ferguson, B. J., Indrasumunar, A., Hayashi, S., Lin, M. H., Lin, Y. H., Reid, D. E., et al. (2010). Molecular analysis of legume nodule development and autoregulation. J. Integr. Plant Biol. 52, 61-76. doi: 10. 1111/j. 1744-7909. 2010. 00899. x.
20. Fotiadis, C. T., Dimou, M., Georgakopoulos, D. G., Katinakis, P., and Tampakaki, A. P. (2012). Functional characterization of NopT1 and NopT2, two type III effectors of Bradyrhizobium japonicum. FEMS Microbiol. Lett. 327, 66-77. doi: 10. 1111/j. 1574-6968. 2011. 02466. x.
21. Fournier, J., Teillet, A., Chabaud, M., Ivanov, S., Genre, A., Limpens, E., et al. (2015). Remodeling of the infection chamber prior to infection thread formation reveals a two-step mechanism for rhizobial entry into the host legume root hair. Plant Physiol. 167, 1233-12342. doi: 10. 1104/pp. 114. 253302.
22. Gage, D. J. (2004). Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol. Mol. Biol. Rev. 68, 280-300. doi: 10. 1128/MMBR. 68. 2. 280-300. 2004.
23. Gazi, A. D., Sarris, P. F., Fadouloglou, V. E., Charova, S. N., Mathioudakis, N., Panopoulos, N. J., et al. (2012). Phylogenetic analysis of a gene cluster encoding an additional, rhizobial-like type III secretion system that is narrowly distributed among Pseudomonas syringae strains. BMC Microbiol. 12: 188. doi: 10. 1186/1471-2180-12-188.
24. Ghosh, P. (2004). Process of protein transport by the type III secretion system. Society 68, 771-795. doi: 10. 1128/MMBR. 68. 4. 771.
25. Giraud, E., Moulin, L., Vallenet, D., Barbe, V., Cytryn, E., Avarre, J.-C., et al. (2007). Legumes symbioses: absence of Nod genes in photosynthetic bradyrhizobia. Science 316, 1307-1312. doi: 10. 1126/science. 1139548.
26. Göhre, V., Spallek, T., Häweker, H., Mersmann, S., Mentzel, T., Boller, T., et al. (2008). Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr. Biol. 18, 1824-1832. doi: 10. 1016/j. cub. 2008. 10. 063.
27. González, E. M., Aparicio-tejo, P. M., Gordon, A. J., Minchin, F. R., Royuela, M., and Arrese-igor, C. (1998). Water-deficit effects on carbon and nitrogen metabolism of pea nodules. J. Exp. Bot. 49, 1705-1714. doi: 10. 1093/jxb/49. 327. 1705.
28. Goormachtig, S., Capoen, W., and Holsters, M. (2004). Rhizobium infection: lessons from the versatile nodulation behaviour of water-tolerant legumes. Trends Plant Sci. 9, 518-522. doi: 10. 1016/j. tplants. 2004. 09. 005.
29. Hansen, G., Das, A., and Chilton, M. D. (1994). Constitutive expression of the virulence genes improves the efficiency of plant transformation by Agrobacterium. Proc. Natl. Acad. Sci. U. S. A. 91, 7603-7607. doi: 10. 1073/pnas. 91. 16. 7603.
30. 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, 3429-44. doi: 10. 1093/jxb/err430.
31. Hernández-Jiménez, M. J., Mercedes Lucas, M., and de Felipe, M. R. (2002). Antioxidant defence and damage in senescing lupin nodules. Plant Physiol. Biochem. 40, 645-657. doi: 10. 1016/S0981-9428(02)01422-5.
32. Herridge, D., and Rose, I. (2000). Breeding for enhanced nitrogen fixation in crop legumes. F. Crop. Res. 65, 229-248. doi: 10. 1016/S0378-4290(99)00089-1.
33. Hotson, A., Chosed, R., Shu, H., Orth, K., and Mudgett, M. B. (2003). Xanthomonas type III effector XopD targets SUMO-conjugated proteins in planta. Mol. Microbiol. 50, 377-389. doi: 10. 1046/j. 1365-2958. 2003. 03730. x.
34. Howieson, J. G. (1995). Rhizobial persistence and its role in the development of sustainable agricultural systems in Mediterranean environments. Soil Biol. Biochem. 27, 603-610. doi: 10. 1016/0038-0717(95)98638-5.
35. Hubber, A. M., Sullivan, J. T., and Ronson, C. W. (2007). Symbiosis-induced cascade regulation of the Mesorhizobium loti R7A VirB/D4 type IV secretion system. Mol. Plant Microbe Interact. 20, 255-261. doi: 10. 1094/MPMI-20-3-0255.
36. Hubber, A., Vergunst, A. C., Sullivan, J. T., Hooykaas, P. J. J., and Ronson, C. W. (2004). Symbiotic phenotypes and translocated effector proteins of the Mesorhizobium loti strain R7A VirB/D4 type IV secretion system. Mol. Microbiol. 54, 561-574. doi: 10. 1111/j. 1365-2958. 2004. 04292. x.
37. Jones, J. D. G., and Dangl, J. L. (2006). The plant immune system. Nature 444, 323-329. doi: 10. 1038/nature05286.
38. 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. doi: 10. 1038/nrmicro1705.
39. 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. doi: 10. 1111/j. 1365-2958. 2008. 06507. x.
40. Kiers, E. T., Rousseau, R. A., West, S. A., and Denison, R. F. (2003). Host sanctions and the legume-Rhizobium mutualism. Nature 425, 78-81. doi: 10. 1038/nature01931.
41. Kimbrel, J. A., Thomas, W. J., Jiang, Y., Creason, A. L., Thireault, C. A., Sachs, J. L., et al. (2013). Mutualistic co-evolution of type III effector genes in Sinorhizobium fredii and Bradyrhizobium japonicum. PLoS Pathog. 9: e1003204. doi: 10. 1371/journal. ppat. 1003204.
42. Kobayashi, H., Naciri-Graven, Y., Broughton, W. J., and Perret, X. (2004). Flavonoids induce temporal shifts in gene-expression of nod-box controlled loci in Rhizobium sp. NGR234. Mol. Microbiol. 51, 335-347. doi: 10. 1046/j. 1365-2958. 2003. 03841. x.
43. Krause, A., Doerfel, A., and Göttfert, M. (2002). Mutational and transcriptional analysis of the type III secretion system of Bradyrhizobium japonicum. Mol. Plant Microbe Interact. 15, 1228-1235. doi: 10. 1094/MPMI. 2002. 15. 12. 1228.
44. Krishnan, H. B., Lorio, J., Kim, W. S., Jiang, G., Kim, K. Y., DeBoer, M., et al. (2003). Extracellular proteins involved in soybean cultivar-specific nodulation are associated with pilus-like surface appendages and exported by a type III protein secretion system in Sinorhizobium frediiUSDA257. Mol. Plant Microbe Interact. 16, 617-625. doi: 10. 1094/MPMI. 2003. 16. 7. 617.
45. Krusell, L., Madsen, L. H., Sato, S., Aubert, G., Genua, A., Szczyglowski, K., et al. (2002). Shoot control of root development and nodulation is mediated by a receptor-like kinase. Nature 420, 422-426. doi: 10. 1038/nature01207.
46. Kuldau, G. A., De Vos, G., Owen, J., McCaffrey, G., and Zambryski, P. (1990). The virB operon ofAgrobacterium tumefaciens pTiC58 encodes 11 open reading frames. Mol. Gen. Genet. 221, 256-266. doi: 10. 1007/BF00261729.
47. Lindeberg, M., Myers, C. R., Collmer, A., and Schneider, D. J. (2008). Roadmap to new virulence determinants in Pseudomonas syringae: insights from comparative genomics and genome organization. Mol. Plant Microbe Interact. 21, 685-700. doi: 10. 1094/MPMI-21-6-0685.
48. Lodwig, E. M., Hosie, A. H. F., Bourdes, A., Findlay, K., Allaway, D., Karunakaran, R., et al. (2006). Amino-acid cycling drives nitrogen fixation in the legume-Rhizobium symbiosis. Nature422, 722-726. doi: 10. 1038/nature01549. 1.
49. Long, S. R. (1996). Rhizobium symbiosis: nod factors in perspective. Plant Cell 8, 1885-1898. doi: 10. 1105/tpc. 8. 10. 1885.
50. López-Baena, F. J., Vinardell, J. M., Pérez-Montaño, F., Crespo-Rivas, J. C., Bellogín, R. A., Espuny, M. D. R., et al. (2008). Regulation and symbiotic significance of nodulation outer proteins secretion in Sinorhizobium fredii HH103. Microbiology 154, 1825-1836. doi: 10. 1099/mic. 0. 2007/016337-16330.
51. Lorio, J. C., Kim, W. S., and Krishnan, H. B. (2004). NopB, a soybean cultivar-specificity protein from Sinorhizobium fredii USDA257, is a type III secreted protein. Mol. Plant Microbe Interact. 17, 1259-1268. doi: 10. 1094/MPMI. 2004. 17. 11. 1259.
52. Macho, A. P., and Zipfel, C. (2015). Science direct targeting of plant pattern recognition receptor-triggered immunity by bacterial type-III secretion system effectors. Curr. Opin. Microbiol. 23, 14-22. doi: 10. 1016/j. mib. 2014. 10. 009.
53. Marchetti, M., Capela, D., Glew, M., Cruveiller, S., Chane-Woon-Ming, B., Gris, C., et al. (2010). Experimental evolution of a plant pathogen into a legume symbiont. PLoS Biol. 8: e1000280. doi: 10. 1371/journal. pbio. 1000280.
54. Marie, C., Deakin, W. J., Ojanen-Reuhs, T., Diallo, E., Reuhs, B., Broughton, W. J., et al. (2004). TtsI, a key regulator of Rhizobium species NGR234 is required for type III-dependent protein secretion and synthesis of rhamnose-rich polysaccharides. Mol. Plant Microbe Interact. 17, 958-966. doi: 10. 1094/MPMI. 2004. 17. 9. 958.
55. Masson-Boivin, C., Giraud, E., Perret, X., and Batut, J. (2009). Establishing nitrogen-fixing symbiosis with legumes: how many Rhizobium recipes? Trends Microbiol. 17, 458-466. doi: 10. 1016/j. tim. 2009. 07. 004.
56. Matamoros, M. A., Baird, L. M., Escuredo, P. R., Dalton, D. A., Minchin, F. R., Iturbe-Ormaetxe, I., et al. (1999). Stress-induced legume root nodule senescence. Physiological, biochemical, and structural alterations. Plant Physiol. 121, 97-112. doi: 10. 1104/pp. 121. 1. 97.
57. Matsunami, T., Kaihatsu, A., Maekawa, T., Takahashi, M., and Kokubun, M. (2004). Characterization of vegetative growth of a supernodulating soybean genotype, sakukei 4. Plant Prod. Sci. 7, 165-171. doi: 10. 1626/pps. 7. 165.
58. Mergaert, P., Uchiumi, T., Alunni, B., Evanno, G., Cheron, A., Catrice, O., et al. (2006). Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium-legume symbiosis. Proc. Natl. Acad. Sci. U. S. A. 103, 5230-5235. doi: 10. 1073/pnas. 0600912103.
59. Michiels, J., Pelemans, H., Vlassak, K., Verreth, C., and Vanderleyden, J. (1995). Identification and characterization of a Rhizobium leguminosarum bv. phaseoli gene that is important for nodulation competitiveness and shows structural homology to a Rhizobium fredii host-inducible gene. Mol. Plant Microbe Interact. 8, 468-472. doi: 10. 1094/MPMI-8-0468.
60. Mortier, V., Holsters, M., and Goormachtig, S. (2012). Never too many? How legumes control nodule numbers. Plant Cell Environ. 35, 245-258. doi: 10. 1111/j. 1365-3040. 2011. 02406. x.
61. Nimchuk, Z., Marois, E., Kjemtrup, S., Leister, R. T., Katagiri, F., and Dangl, J. L. (2000). Eukaryotic fatty acylation drives plasma membrane targeting and enhances function of several type III effector proteins from Pseudomonas syringae. Cell 101, 353-363. doi: 10. 1016/S0092-8674(00)80846-6.
62. Nishimura, R., Hayashi, M., Wu, G.-J., Kouchi, H., Imaizumi-Anraku, H., Murakami, Y., et al. (2002). HAR1 mediates systemic regulation of symbiotic organ development. Nature 420, 426-429. doi: 10. 1038/nature01231.
63. Okamoto, S., Shinohara, H., Mori, T., Matsubayashi, Y., and Kawaguchi, M. (2013). Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase. Nat. Commun. 4: 2191. doi: 10. 1038/ncomms3191.
64. 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.
65. Okazaki, S., Okabe, S., Higashi, M., Shimoda, Y., Sato, S., Tabata, S., et al. (2010). Identification and functional analysis of type III effector proteins in Mesorhizobium loti. Mol. Plant Microbe Interact. 23, 223-234. doi: 10. 1094/MPMI-23-2-0223.
66. Okazaki, S., Zehner, S., Hempel, J., Lang, K., and Göttfert, M. (2009). Genetic organization and functional analysis of the type III secretion system of Bradyrhizobium elkanii. FEMS Microbiol. Lett. 295, 88-95. doi: 10. 1111/j. 1574-6968. 2009. 01593. x.
67. Oldroyd, G. E. D., and Downie, J. A. (2008). Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. 59, 519-546. doi: 10. 1146/annurev. arplant. 59. 032607. 092839.
68. 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-110410-9.
69. Pedley, K. F., and Martin, G. B. (2005). Role of mitogen-activated protein kinases in plant immunity. Curr. Opin. Plant Biol. 8, 541-547. doi: 10. 1016/j. pbi. 2005. 07. 006.
70. Perret, X., Staehelin, C., and Broughton, W. J. (2000). Molecular basis of symbiotic promiscuity. Microbiol. Mol. Biol. Rev. 64, 180-201. doi: 10. 1128/MMBR. 64. 1. 180-201. 2000.
71. Prell, J., White, J. P., Bourdes, A., Bunnewell, S., Bongaerts, R. J., and Poole, P. S. (2009). Legumes regulate Rhizobium bacteroid development and persistence by the supply of branched-chain amino acids. Proc. Natl. Acad. Sci. U. S. A. 106, 12477-12482. doi: 10. 1073/pnas. 0903653106.
72. Puppo, A., Groten, K., Bastian, F., Carzaniga, R., Soussi, M., Lucas, M. M., et al. (2005). Legume nodule senescence: roles for redox and hormone signalling in the orchestration of the natural aging process. New Phytol. 165, 683-701. doi: 10. 1111/j. 1469-8137. 2004. 01285. x.
73. Puri, N., Jenner, C., Bennett, M., Stewart, R., Mansfield, J., Lyons, N., et al. (1997). Expression of avrPphB, an avirulence gene from Pseudomonas syringae pv. phaseolicola, and the delivery of signals causing the hypersensitive reaction in bean. Mol. Plant Microbe Interact. 10, 247-256. doi: 10. 1094/MPMI. 1997. 10. 2. 247.
74. 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. doi: 10. 1038/sj. emboj. 7601826.
75. Reid, D. E., Ferguson, B. J., and Gresshoff, P. M. (2011). Inoculation-and nitrate-induced CLE peptides of soybean control NARK-dependent nodule formation. Mol. Plant Microbe Interact. 24, 606-618. doi: 10. 1094/MPMI-09-10-0207.
76. Reid, D. E., Li, D., Ferguson, B. J., and Gresshoff, P. M. (2013). Structure-function analysis of the GmRIC1 signal peptide and CLE domain required for nodulation control in soybean. J. Exp. Bot. 64, 1575-1585. doi: 10. 1093/jxb/ert008.
77. Rodrigues, J. A., López-Baena, F. J., Ollero, F. J., Vinardell, J. M., Espuny, M. D. R., Bellogín, R. A., et al. (2007). NopM and NopD are rhizobial nodulation outer proteins: identification using LC-MALDI and LC-ESI with a monolithic capillary column. J. Proteome Res. 6, 1029-1037. doi: 10. 1021/pr060519f.
78. Saad, M. M., Crèvecoeur, M., Masson-Boivin, C., and Perret, X. (2012). The type 3 protein secretion system of Cupriavidus taiwanensis strain LMG19424 compromises symbiosis withLeucaena leucocephala. Appl. Environ. Microbiol. 78, 7476-7479. doi: 10. 1128/AEM. 01691-2.
79. Saad, M. M., Kobayashi, H., Marie, C., Brown, I. R., Mansfield, J. W., Broughton, W. J., et al. (2005). NopB, a type III secreted protein of Rhizobium sp. strain NGR234, is associated with pilus-like surface appendages. Society 187, 1173-1181. doi: 10. 1128/JB. 187. 3. 1173.
80. Saad, M. M., Staehelin, C., Broughton, W. J., and Deakin, W. J. (2008). Protein-protein interactions within type III secretion system-dependent pili of Rhizobium sp. strain NGR234. J. Bacteriol. 190, 750-754. doi: 10. 1128/JB. 01116-7.
81. Saeki, K. (2011). Rhizobial measures to evade host defense strategies and endogenous threats to persistent symbiotic nitrogen fixation: a focus on two legume-Rhizobium model systems. Cell. Mol. Life Sci. 68, 1327-1339. doi: 10. 1007/s00018-011-0650-5.
82. Sánchez, C., Iannino, F., Deakin, W. J., Ugalde, R. A., and Lepek, V. C. (2009). Characterization of the Mesorhizobium loti MAFF303099 type-three protein secretion system. Mol. Plant Microbe Interact. 22, 519-528. doi: 10. 1094/MPMI-22-5-0519.
83. Sánchez, C., Mercante, V., Babuin, M. F., and Lepek, V. C. (2012). Dual effect of Mesorhizobium loti T3SS functionality on the symbiotic process. FEMS Microbiol. Lett. 330, 148-156. doi: 10. 1111/j. 1574-6968. 2012. 02545. x.
84. Sasaki, T., Suzaki, T., Soyano, T., Kojima, M., Sakakibara, H., and Kawaguchi, M. (2014). Shoot-derived cytokinins systemically regulate root nodulation. Nat. Commun. 5, 1-9. doi: 10. 1038/ncomms5983.
85. Schell, M. A., Ulrich, R. L., Ribot, W. J., Brueggemann, E. E., Hines, H. B., Chen, D., et al. (2007). Type VI secretion is a major virulence determinant in Burkholderia mallei. Mol. Microbiol. 64, 1466-1485. doi: 10. 1111/j. 1365-2958. 2007. 05734. x.
86. Schrammeijer, B., Risseeuw, E., Pansegrau, W., Regensburg-Tuïnk, T. J., Crosby, W. L., and Hooykaas, P. J. (2001). Interaction of the virulence protein VirF of Agrobacterium tumefacienswith plant homologs of the yeast Skp1 protein. Curr. Biol. 11, 258-262. doi: 10. 1016/S0960-9822(01)00069-0.
87. Shames, S. R., and Finlay, B. B. (2012). Bacterial effector interplay: a new way to view effector function. Trends Microbiol. 20, 214-219. doi: 10. 1016/j. tim. 2012. 02. 007.
88. Shan, L., He, P., Li, J., Heese, A., Peck, S. C., Nürnberger, T., et al. (2008). Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4, 17-27. doi: 10. 1016/j. chom. 2008. 05. 017.
89. Shao, F., Merritt, P. M., Bao, Z., Innes, R. W., and Dixon, J. E. (2002). A Yersinia effector and aPseudomonas avirulence protein define a family of cysteine proteases functioning in bacterial pathogenesis. Cell 109, 575-588. doi: 10. 1016/S0092-8674(02)00766-3.
90. Skorpil, P., Saad, M. M., Boukli, N. M., Kobayashi, H., Ares-Orpel, F., Broughton, W. J., et al. (2005). NopP, a phosphorylated effector of Rhizobium sp. strain NGR234, is a major determinant of nodulation of the tropical legumes Flemingia congesta and Tephrosia vogelii. Mol. Microbiol. 57, 1304-1317. doi: 10. 1111/j. 1365-2958. 2005. 04768. x.
91. Stachel, S. E., and Zambryski, P. C. (1986). virA and virG control the plant-induced activation of the T-DNA transfer process of A. tumefaciens. Cell 46, 325-333. doi: 10. 1016/0092-8674(86)90653-7.
92. Sugawara, M., Epstein, B., Badgley, B., Unno, T., Xu, L., Reese, J., et al. (2013). Comparative genomics of the core and accessory genomes of 48 Sinorhizobium strains comprising five genospecies. Genome Biol. 14: R17. doi: 10. 1186/gb-2013-14-2-r17.
93. Suzaki, T., Yoro, E., and Kawaguchi, M. (2015). Leguminous plants: inventors of root Nodules to accommodate symbiotic bacteria. Int. Rev. Cell Mol. Biol. 316, 111-158. doi: 10. 1016/bs. ircmb. 2015. 01. 004.
94. Takahara, M., Magori, S., Soyano, T., Okamoto, S., Yoshida, C., Yano, K., et al. (2013). TOO MUCH LOVE, a novel kelch repeat-containing F-box protein, functions in the long-distance regulation of the Legume-Rhizobium symbiosis. Plant Cell Physiol. 54, 433-447. doi: 10. 1093/pcp/pct022.
95. Takahashi, M., Arihara, J., Nakayama, N., and Kokubun, M. (2003). Characteristics of growth and yield formation in the improved genotype of supernodulating soybean (Glycine max L. Merr.). Plant Prod. Sci. 6, 112-118. doi: 10. 1626/pps. 6. 112.
96. Tampakaki, A. P. (2014). Commonalities and differences of T3SSs in rhizobia and plant pathogenic bacteria. Front. Plant Sci. 5: 114. doi: 10. 3389/fpls. 2014. 00114.
97. Trese, A. (1995). A single dominant gene in McCall soybean prevents effective nodulation withRhizobium fredii USDA257. Euphytica 81, 279-282. doi: 10. 1007/BF00025618.
98. Tseng, T.-T., Tyler, B. M., and Setubal, J. C. (2009). Protein secretion systems in bacterial-host associations, and their description in the Gene Ontology. BMC Microbiol. 9(Suppl. 1): S2. doi: 10. 1186/1471-2180-9-S1-S2.
99. Tzfira, T., Vaidya, M., and Citovsky, V. (2004). Involvement of targeted proteolysis in plant genetic transformation by Agrobacterium. Nature 431, 6-11. doi: 10. 1038/nature02837. 1.
100. Udvardi, M., and Poole, P. S. (2013). Transport and metabolism in legume-rhizobia symbioses. Annu. Rev. Plant Biol. 64, 781-805. doi: 10. 1146/annurev-arplant-050312-120235.
101. Vasse, J., Billy, F., and Truchet, G. (1993). Abortion of infection during the Rhizobium meliloti-alfalfa symbiotic interaction is accompanied by a hypersensitive reaction. Plant J. 4, 555-566. doi: 10. 1046/j. 1365-313X. 1993. 04030555. x.
102. 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.
103. Vergunst, A. C., Schrammeijer, B., den Dulk-Ras, A., de Vlaam, C. M. T., Regensburg-Tuïnk, T. J. G., and Hooykaas, P. J. J. (2000). VirB/D4-dependent protein translocation from Agrobacteriuminto plant cells. Science 290, 979-982. doi: 10. 1126/science. 290. 5493. 979.
104. Vergunst, A. C., van Lier, M. C. M., den Dulk-Ras, A., Stüve, T. A. G., Ouwehand, A., and Hooykaas, P. J. J. (2005). Positive charge is an important feature of the C-terminal transport signal of the VirB/D4-translocated proteins of Agrobacterium. Proc. Natl. Acad. Sci. U. S. A. 102, 832-837. doi: 10. 1073/pnas. 0406241102.
105. Viprey, V., Del Greco, A., Golinowski, W., Broughton, W. J., and Perret, X. (1998). Symbiotic implications of type III protein secretion machinery in Rhizobium. Mol. Microbiol. 28, 1381-1389. doi: 10. 1046/j. 1365-2958. 1998. 00920. x.
106. Wang, D., Yang, S., Tang, F., and Zhu, H. (2012). Symbiosis specificity in the legume-rhizobial mutualism. Cell. Microbiol. 14, 334-342. doi: 10. 1111/j. 1462-5822. 2011. 01736. x.
107. Wassem, R., Kobayashi, H., Kambara, K., Le Quéré, A., Walker, G. C., Broughton, W. J., et al. (2008). TtsI regulates symbiotic genes in Rhizobium species NGR234 by binding to tts boxes. Mol. Microbiol. 68, 736-748. doi: 10. 1111/j. 1365-2958. 2008. 06187. x.
108. Wenzel, M., Friedrich, L., Göttfert, M., and Zehner, S. (2010). The type III-secreted protein NopE1 affects symbiosis and exhibits a calcium-dependent autocleavage activity. Mol. Plant Microbe Interact. 23, 124-129. doi: 10. 1094/MPMI-23-1-0124.
109. Wooldridge, K. (2009). Bacterial Secreted Proteins: Secretory Mechanisms and Role in Pathogenesis. Poole: Caister Academic Press.
110. 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.
111. Yang, S., Tang, F., Gao, M., Krishnan, H. B., and Zhu, H. (2010). R gene-controlled host specificity in the legume-rhizobia symbiosis. Proc. Natl. Acad. Sci. U. S. A. 107, 18735-18740. doi: 10. 1073/pnas. 1011957107.
112. 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: symbiotic effects, phosphorylation, and interference with mitogen-activated protein kinase signaling. J. Biol. Chem. 286, 32178-32187. doi: 10. 1074/jbc. M111. 265942.
113. Zupan, J. R., and Zambryski, P. (1995). Transfer of T-DNA from Agrobacterium to the plant cell. Plant Physiol. 107, 1041-1047. doi: 10. 1104/pp. 107. 4. 1041.