Rhizobium-legume symbiosis in the absence of Nod factors: Two possible scenarios with or without the T3SS

ISME Journal

Volumn 10, Issue 1, 2016, Pages 64-74

  Okazaki, Shin ^a   Tittabutr, Panlada ^b   Teulet, Albin ^c   Thouin, Julien ^c   Fardoux, Joel ^c   Chaintreuil, Clemence ^c   Gully, Djamel ^c   Arrighi, Jean François ^c   Furuta, Noriyuki ^a   Miwa, Hiroki ^a   Yasuda, Michiko ^a   Nouwen, Nico ^c   Teaumroong, Neung ^b   Giraud, Eric ^c  

^a TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

^b SURANAREE UNIVERSITY OF TECHNOLOGY   (Thailand)

^c LABORATOIRE DES SYMBIOSES TROPICALES ET MÉDITERRANÉENNES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLOGY; INTERSPECIFIC INTERACTION; LEGUME; NITROGEN FIXATION; NODULATION; PHOTOSYNTHESIS; RHIZOBACTERIUM; SYMBIOSIS;

AESCHYNOMENE INDICA; BRADYRHIZOBIUM; BRADYRHIZOBIUM ELKANII; PHOTORHIZOBIUM; RHIZOBIUM;

BACTERIAL DNA; NITROGENASE; RNA 16S;

BACTERIAL GENOME; BRADYRHIZOBIUM; CLASSIFICATION; DNA SEQUENCE; EVOLUTION; FABACEAE; GENETICS; METABOLISM; MICROBIOLOGY; PHYLOGENY; POLYMERASE CHAIN REACTION; SYMBIOSIS;

BIOLOGICAL EVOLUTION; BRADYRHIZOBIUM; DNA, BACTERIAL; FABACEAE; GENOME, BACTERIAL; NITROGENASE; PHYLOGENY; POLYMERASE CHAIN REACTION; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SYMBIOSIS;

EID: 84936972674     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2015.103     Document Type: Article

References (36)

1. Aslam SN, Newman MA, Erbs G, Morrissey KL, Chinchilla D, Boller T et al. (2008). Bacterial polysaccharides suppress induced innate immunity by calcium chelation. Curr Biol 18: 1078-1083.
2. Bonaldi K, Gargani D, Prin Y, Fardoux J, Gully D, Nouwen N et al. (2011). Nodulation of Aeschynomene afraspera and A. indica by photosynthetic Bradyrhizobium sp. strain ORS285: The Nod-dependent versus the Nod-independent symbiotic interaction. Mol Plant Microbe Interact 24: 1359-1371.
3. Bonaldi K, Gourion B, Fardoux J, Hannibal L, Cartieaux F et al. (2010). Large-scale transposon mutagenesis of photosynthetic Bradyrhizobium sp. strain ORS278 reveals new genetic loci putatively important for Nod-independent symbiosis with Aeschynomene indica. Mol Plant Microbe Interact 23: 760-770.
4. Chaintreuil C, Arrighi JF, Giraud E, Miché L, Moulin L, Dreyfus B et al. (2013). Evolution of symbiosis in the legume genus Aeschynomene. New Phytol 200: 1247-1259.
5. D'Haeze W, Holsters M. (2004). Surface polysaccharides enable bacteria to evade plant immunity. Trends Microbiol 12: 555-561.
6. Dodds PN, Rathjen JP. (2010). Plant immunity: Towards an integrated view of plant-pathogen interactions. Nat Rev Genet 11: 539-548.
7. Felsenstein J. (1985). Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 424-429.
8. Fraysse N, Couderc F, Poinsot V. (2003). Surface polysaccharide involvement in establishing the rhizobiumlegume symbiosis. Eur J Biochem 270: 1365-1380.
9. Gage DJ. (2002). Analysis of infection thread development using Gfp-and DsRed-expressing Sinorhizobium meliloti. J Bacteriol 184: 7042-7046.
10. Giraud E, Moulin L, Vallenet D, Barbe V, Cytryn E, Avarre JC et al. (2007). Legumes symbioses: Absence of Nod genes in photosynthetic bradyrhizobia. Science 316: 1307-1312.
11. Gourion B, Berrabah F, Ratet P, Stacey G. (2014). Rhizobiumlegume symbioses: The crucial role of plant immunity. Trends Plant Sci pii: S1360-S1385 (14)00297-0.
12. Gueye F, Moulin L, Sylla S, Ndoye I, Béna G. (2009). Genetic diversity and distribution of Bradyrhizobium and Azorhizobium strains associated with the herb legume Zornia glochidiata sampled from across Senegal. Syst Appl Microbiol 32: 387-399.
13. Haag AF, Baloban M, Sani M, Kerscher B, Pierre O, Farkas A et al. (2011). Protection of Sinorhizobium against host cysteine-rich antimicrobial peptides is critical for symbiosis. PLoS Biol 9: E1001169.
14. Hueck CJ. (1998). Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62: 379-433.
15. Kelly SJ, Muszyski A, Kawaharada Y, Hubber AM, Sullivan JT, Sandal N et al. (2013). Conditional requirement for exopolysaccharide in the Mesorhizobium-Lotus symbiosis. Mol Plant Microbe Interact 26: 319-329.
16. Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Promé JC et al. (1990). Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature 344: 781-784.
17. Liang Y, Tóth K, Cao Y, Tanaka K, Espinoza C, Stacey G. (2014). Lipochitooligosaccharide recognition: An ancient story. New Phytol 204: 289-296.
18. Lorquin J, Molouba F, Dupuy N, Ndiaye S, Alazard D, Gillis M et al. Diversity of photosynthetic Bradyrhizobium strains from stem nodules of Aeschynomene species. In Palacios R, Mora J, Newton WE(Eds) (1993). New Horizons in Nitrogen Fixation. Boston: Kluwer, 17: 683-689.
19. Madsen LH, Tirichine L, Jurkiewicz A, Sullivan JT, Heckmann AB, Bek AS et al. (2010). The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat Commun 1: 10.
20. Miché L, Moulin L, Chaintreuil C, Contreras-Jimenez JL, Munive-Hernández JA, Del Carmen Villegas-Hernandez M et al. (2010). Diversity analyses of Aeschynomene symbionts in Tropical Africa and Central America reveal that Nod-independent stem nodulation is not restricted to photosynthetic bradyrhizobia. Environ Microbiol 12: 2152-2164.
21. Molouba F, Lorquin J, Willems A, Hoste B, Giraud E, Dreyfus B et al. (1999). Photosynthetic bradyrhizobia from Aeschynomene spp. are specific to stemnodulated species and form a separate 16 S ribosomal DNA restriction fragment length polymorphism group. Appl Environ Microbiol 65: 3084-3094.
22. Montecchia MS, Kerber NL, Pucheu NL, Perticari A, Garciá AF. (2002). Analysis of genomic diversity among photosynthetic stem-nodulating rhizobial strains from northeast Argentina. Syst Appl Microbiol 25: 423-433.
23. Mornico D, Miché L, Béna G, Nouwen N, Verméglio A, Vallenet D et al. (2011). Comparative genomics of Aeschynomene symbionts: Insights into the ecological lifestyle of Nod-independent photosynthetic bradyrhizobia. Genes 3: 35-61.
24. Nagata T, Takebe L. (1970). Cell wall regeneration and cell division in isolated tobacco mesophyll protoplasts. Planta 92: 301-308.
25. Okazaki S, Kaneko T, Sato S, Saeki K. (2013). Hijacking of leguminous nodulation signaling by the rhizobial type III secretion system. Proc Natl Acad Sci USA 110: 17131-17136.
26. Oldroyd GE, Murray JD, Poole PS, Downie JA. (2011). The rules of engagement in the legume-rhizobial symbiosis. Annu Rev Genet 45: 119-144.
27. Oldroyd GE. (2013). Speak, friend, and enter: Signalling systems that promote beneficial symbiotic associations in plants. Nat Rev Microbiol 11: 252-263.
28. Saitou RR, Nei M. (1987). A neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 44: 406-425.
29. Tampakaki AP. (2014). Commonalities and differences of T3SSs in rhizobia and plant pathogenic bacteria. Front Plant Sci 5: 114.
30. Thompson JD, Gibson TJ, Higgins DG (2002). Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinformatics. Chapter 2: Unit 2.3
31. . 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.
32. Vincent JM. (1970). A Manual for the Practical Study of Root-Nodule Bacteria. Blackwell Scientific Publications: Oxford, United Kingdom.
33. Wang D, Yang S, Tang F, Zhu H. (2012). Symbiosis specificity in the legume: Rhizobial mutualism. Cell Microbiol 14: 334-342.
34. Wassem R, Kobayashi H, Kambara K, Le Quéré A, Walker GC, Broughton WJ et al. (2008). TtsI regulates symbiotic genes in Rhizobium species NGR-234 by binding to tts boxes. Mol Microbiol 68: 736-748.
35. Wilson KJ, Sessitsch A, Corbo JC, Giller KE, Akkermans AD, Jefferson RA. (1995).-Glucuronidase (GUS) transposons for ecological and genetic studies of rhizobia and other Gram-negative bacteria. Microbiology 141: 1691-1705.
36. Zehner S, Schober G, Wenzel M, Lang K, Göttfert M. (2008). Expression of the Bradyrhizobium japonicum type III secretion system in legume nodules and analysis of the associated tts box promoter. Mol Plant Microbe Interact 21: 1087-1093.