A Legume Genetic Framework Controls Infection of Nodules by Symbiotic and Endophytic Bacteria

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Plants have evolved elaborated mechanisms to monitor microbial presence and to control their infection, therefore only particular microbes, so called “endophytes,” are able to colonise the internal tissues with minimal or no host damage. The legume root nodule is a unique environmental niche induced by symbiotic bacteria, but where multiple species, symbiotic and endophytic co-exist. Genetic studies of the binary interaction legume-symbiont led to the discovery of key components evolved in the two partners allowing mutual recognition and nodule infection. In contrast, there is limited knowledge about the endophytic nodule infection, the role of the legume host, or the symbiont in the process of nodule colonisation by endophytes. Here we focus on the early stages of nodule infection in order to identify which molecular signatures and genetic components favour/allow endophyte accommodation, and multiple species co-existence inside nodules. We found that colonisation of Lotus japonicus nodules by endophytic bacteria is a selective process, that endophyte nodule occupancy is host-controlled, and that exopolysaccharides are key bacterial features for chronic infection of nodules. Our strategy based on model legume genetics and co-inoculation can thus be used for identifying mechanisms operating behind host-microbes compatibility in environments where multiple species co-exist.

Vyšlo v časopise: A Legume Genetic Framework Controls Infection of Nodules by Symbiotic and Endophytic Bacteria. PLoS Genet 11(6): e32767. doi:10.1371/journal.pgen.1005280
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005280

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Zdroje

1. Jones JD, Dangl JL. The plant immune system. Nature. 2006 Nov 16;444(7117):323–9. 17108957

2. Kiers ET, Denison RF. Sanctions, Cooperation, and the Stability of Plant-Rhizosphere Mutualisms. Annual Review of Ecology Evolution and Systematics. Palo Alto: Annual Reviews; 2008. p. 215–36.

3. Parniske M. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat Rev Microbiol. 2008 Oct;6(10):763–75. doi: 10.1038/nrmicro1987 18794914

4. Turner TR, Ramakrishnan K, Walshaw J, Heavens D, Alston M, Swarbreck D, et al. Comparative metatranscriptomics reveals kingdom level changes in the rhizosphere microbiome of plants. The ISME journal. 2013 Dec;7(12):2248–58. doi: 10.1038/ismej.2013.119 23864127

5. Bulgarelli D, Schlaeppi K, Spaepen S, Ver Loren van Themaat E, Schulze-Lefert P. Structure and functions of the bacterial microbiota of plants. Annual review of plant biology. 2013;64:807–38. doi: 10.1146/annurev-arplant-050312-120106 23373698

6. Sessitsch A, Hardoim P, Doring J, Weilharter A, Krause A, Woyke T, et al. Functional characteristics of an endophyte community colonizing rice roots as revealed by metagenomic analysis. Molecular plant-microbe interactions: MPMI. 2012 Jan;25(1):28–36. doi: 10.1094/MPMI-08-11-0204 21970692

7. Broghammer A, Krusell L, Blaise M, Sauer J, Sullivan JT, Maolanon N, et al. Legume receptors perceive the rhizobial lipochitin oligosaccharide signal molecules by direct binding. P Natl Acad Sci USA. 2012 Aug 21;109(34):13859–64. doi: 10.1073/pnas.1205171109 22859506

8. Radutoiu S, Madsen LH, Madsen EB, Felle HH, Umehara Y, Gronlund M, et al. Plant recognition of symbiotic bacteria requires two LysM receptor-like kinases. Nature. 2003 Oct 9;425(6958):585–92. 14534578

9. Radutoiu S, Madsen LH, Madsen EB, Jurkiewicz A, Fukai E, Quistgaard EM, et al. LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range. The EMBO journal. 2007 Sep 5;26(17):3923–35. 17690687

10. Charpentier M, Bredemeier R, Wanner G, Takeda N, Schleiff E, Parniske M. Lotus japonicus CASTOR and POLLUX are ion channels essential for perinuclear calcium spiking in legume root endosymbiosis. Plant Cell. 2008 Dec;20(12):3467–79. doi: 10.1105/tpc.108.063255 19106374

11. Groth M, Takeda N, Perry J, Uchida H, Draxl S, Brachmann A, et al. NENA, a Lotus japonicus homolog of Sec13, is required for rhizodermal infection by arbuscular mycorrhiza fungi and rhizobia but dispensable for cortical endosymbiotic development. Plant Cell. 2010 Jul;22(7):2509–26. doi: 10.1105/tpc.109.069807 20675572

12. Kanamori N, Madsen LH, Radutoiu S, Frantescu M, Quistgaard EM, Miwa H, et al. A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. P Natl Acad Sci USA. 2006 Jan 10;103(2):359–64. 16407163

13. Saito K, Yoshikawa M, Yano K, Miwa H, Uchida H, Asamizu E, et al. NUCLEOPORIN85 is required for calcium spiking, fungal and bacterial symbioses, and seed production in Lotus japonicus. Plant Cell. 2007 Feb;19(2):610–24. 17307929

14. Stracke S, Kistner C, Yoshida S, Mulder L, Sato S, Kaneko T, et al. A plant receptor-like kinase required for both bacterial and fungal symbiosis. Nature. 2002 Jun 27;417(6892):959–62. 12087405

15. Madsen LH, Tirichine L, Jurkiewicz A, Sullivan JT, Heckmann AB, Bek AS, et al. The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nature communications. 2010;1:10. doi: 10.1038/ncomms1009 20975672

16. Miller JB, Pratap A, Miyahara A, Zhou L, Bornemann S, Morris RJ, et al. Calcium/Calmodulin-dependent protein kinase is negatively and positively regulated by calcium, providing a mechanism for decoding calcium responses during symbiosis signaling. Plant Cell. 2013 Dec;25(12):5053–66. doi: 10.1105/tpc.113.116921 24368786

17. Singh S, Katzer K, Lambert J, Cerri M, Parniske M. CYCLOPS, A DNA-Binding Transcriptional Activator, Orchestrates Symbiotic Root Nodule Development. Cell Host Microbe. 2014 Feb 12;15(2):139–52. doi: 10.1016/j.chom.2014.01.011 24528861

18. Desbrosses GJ, Stougaard J. Root nodulation: a paradigm for how plant-microbe symbiosis influences host developmental pathways. Cell Host Microbe. 2011 Oct 20;10(4):348–58. doi: 10.1016/j.chom.2011.09.005 22018235

19. Heckmann AB, Lombardo F, Miwa H, Perry JA, Bunnewell S, Parniske M, et al. Lotus japonicus nodulation requires two GRAS domain regulators, one of which is functionally conserved in a non-legume. Plant Physiol. 2006 Dec;142(4):1739–50. 17071642

20. Murray JD, Karas BJ, Sato S, Tabata S, Amyot L, Szczyglowski K. A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science. 2007 Jan 5;315(5808):101–4. 17110535

21. Tirichine L, Sandal N, Madsen LH, Radutoiu S, Albrektsen AS, Sato S, et al. A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science. 2007 Jan 5;315(5808):104–7. 17110537

22. Hossain MS, Liao J, James EK, Sato S, Tabata S, Jurkiewicz A, et al. Lotus japonicus ARPC1 is required for rhizobial infection. Plant Physiol. 2012 Oct;160(2):917–28. doi: 10.1104/pp.112.202572 22864583

23. Tansengco ML, Hayashi M, Kawaguchi M, Imaizumi-Anraku H, Murooka Y. crinkle, a novel symbiotic mutant that affects the infection thread growth and alters the root hair, trichome, and seed development in Lotus japonicus. Plant Physiol. 2003 Mar;131(3):1054–63. 12644658

24. Xie F, Murray JD, Kim J, Heckmann AB, Edwards A, Oldroyd GE, et al. Legume pectate lyase required for root infection by rhizobia. P Natl Acad Sci USA. 2012 Jan 10;109(2):633–8. doi: 10.1073/pnas.1113992109 22203959

25. Yano K, Shibata S, Chen WL, Sato S, Kaneko T, Jurkiewicz A, et al. CERBERUS, a novel U-box protein containing WD-40 repeats, is required for formation of the infection thread and nodule development in the legume-Rhizobium symbiosis. The Plant journal: for cell and molecular biology. 2009 Oct;60(1):168–80. doi: 10.1111/j.1365-313X.2009.03943.x 19508425

26. Yano K, Tansengco ML, Hio T, Higashi K, Murooka Y, Imaizumi-Anraku H, et al. New nodulation mutants responsible for infection thread development in Lotus japonicus. Molecular plant-microbe interactions: MPMI. 2006 Jul;19(7):801–10. 16838792

27. Yokota K, Fukai E, Madsen LH, Jurkiewicz A, Rueda P, Radutoiu S, et al. Rearrangement of actin cytoskeleton mediates invasion of Lotus japonicus roots by Mesorhizobium loti. Plant Cell. 2009 Jan;21(1):267–84. doi: 10.1105/tpc.108.063693 19136645

28. Krusell L, Krause K, Ott T, Desbrosses G, Kramer U, Sato S, et al. The sulfate transporter SST1 is crucial for symbiotic nitrogen fixation in Lotus japonicus root nodules. Plant Cell. 2005 May;17(5):1625–36. 15805486

29. Van de Velde W, Zehirov G, Szatmari A, Debreczeny M, Ishihara H, Kevei Z, et al. Plant peptides govern terminal differentiation of bacteria in symbiosis. Science. [Research Support, Non-U.S. Gov't]. 2010 Feb 26;327(5969):1122–6. doi: 10.1126/science.1184057 20185722

30. D'antuono AL, Casabuono A, Couto A, Ugalde RA, Lepek VC. Nodule development induced by Mesorhizobium loti mutant strains affected in polysaccharide synthesis. Mol Plant Microbe In. 2005 May;18(5):446–57. 15915643

31. Downie JA. The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS microbiology reviews. 2010 Mar;34(2):150–70. doi: 10.1111/j.1574-6976.2009.00205.x 20070373

32. Kelly SJ, Muszynski A, Kawaharada Y, Hubber AM, Sullivan JT, Sandal N, et al. Conditional requirement for exopolysaccharide in the Mesorhizobium-Lotus symbiosis. Molecular plant-microbe interactions: MPMI. 2013 Mar;26(3):319–29. doi: 10.1094/MPMI-09-12-0227-R 23134480

33. Marchetti M, Capela D, Glew M, Cruveiller S, Chane-Woon-Ming B, Gris C, et al. Experimental evolution of a plant pathogen into a legume symbiont. PLoS Biol. [Research Support, Non-U.S. Gov't]. 2010 Jan;8(1):e1000280. doi: 10.1371/journal.pbio.1000280 20084095

34. Okazaki S, Kaneko T, Sato S, Saeki K. Hijacking of leguminous nodulation signaling by the rhizobial type III secretion system. P Natl Acad Sci USA. 2013 Oct 15;110(42):17131–6. doi: 10.1073/pnas.1302360110 24082124

35. Okazaki S, Okabe S, Higashi M, Shimoda Y, Sato S, Tabata S, et al. Identification and functional analysis of type III effector proteins in Mesorhizobium loti. Molecular plant-microbe interactions: MPMI. 2010 Feb;23(2):223–34. doi: 10.1094/MPMI-23-2-0223 20064065

36. Gibson KE, Kobayashi H, Walker GC. Molecular determinants of a symbiotic chronic infection. Annu Rev Genet. [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Review]. 2008;42:413–41. doi: 10.1146/annurev.genet.42.110807.091427 18983260

37. Jones KM, Sharopova N, Lohar DP, Zhang JQ, VandenBosch KA, Walker GC. Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti or an exopolysaccharide-deficient mutant. P Natl Acad Sci USA. 2008 Jan 15;105(2):704–9. doi: 10.1073/pnas.0709338105 18184805

38. Lerouge P, Roche P, Faucher C, Maillet F, Truchet G, Prome JC, et al. Symbiotic host-specificity of Rhizobium meliloti is determined by a sulphated and acylated glucosamine oligosaccharide signal. Nature. 1990 Apr 19;344(6268):781–4. 2330031

39. Spaink HP, Sheeley DM, van Brussel AA, Glushka J, York WS, Tak T, et al. A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature. [Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.]. 1991 Nov 14;354(6349):125–30. 1944592

40. Gyaneshwar P, Hirsch AM, Moulin L, Chen WM, Elliott GN, Bontemps C, et al. Legume-nodulating betaproteobacteria: diversity, host range, and future prospects. Molecular plant-microbe interactions: MPMI. 2011 Nov;24(11):1276–88. doi: 10.1094/MPMI-06-11-0172 21830951

41. Lei X, Wang ET, Chen WF, Sui XH, Chen WX. Diverse bacteria isolated from root nodules of wild Vicia species grown in temperate region of China. Arch Microbiol. 2008 Dec;190(6):657–71. doi: 10.1007/s00203-008-0418-y 18704366

42. Li L, Sinkko H, Montonen L, Wei G, Lindstrom K, Rasanen LA. Biogeography of symbiotic and other endophytic bacteria isolated from medicinal Glycyrrhiza species in China. FEMS Microbiol Ecol. [Research Support, Non-U.S. Gov't]. 2012 Jan;79(1):46–68. doi: 10.1111/j.1574-6941.2011.01198.x 22066910

43. Lorite MJ, Donate-Correa J, del Arco-Aguilar M, Perez Galdona R, Sanjuan J, Leon-Barrios M. Lotus endemic to the Canary Islands are nodulated by diverse and novel rhizobial species and symbiotypes. Systematic and applied microbiology. 2010 Aug;33(5):282–90. doi: 10.1016/j.syapm.2010.03.006 20447791

44. Martinez-Romero E. Diversity of Rhizobium-Phaseolus vulgaris symbiosis: overview and perspectives. Plant Soil. 2003 May;252(1):11–23.

45. Muresu R, Polone E, Sulas L, Baldan B, Tondello A, Delogu G, et al. Coexistence of predominantly nonculturable rhizobia with diverse, endophytic bacterial taxa within nodules of wild legumes. FEMS Microbiol Ecol. 2008 Mar;63(3):383–400. doi: 10.1111/j.1574-6941.2007.00424.x 18194345

46. Saidi S, Mnasri B, Mhamdi R. Diversity of nodule-endophytic agrobacteria-like strains associated with different grain legumes in Tunisia. Systematic and applied microbiology. 2011 Nov;34(7):524–30. doi: 10.1016/j.syapm.2011.01.009 21621936

47. Kiers ET, Hutton MG, Denison RF. Human selection and the relaxation of legume defences against ineffective rhizobia. Proceedings Biological sciences / The Royal Society. 2007 Dec 22;274(1629):3119–26. 17939985

48. Terpolilli JJ, Hood GA, Poole PS. What Determines the Efficiency of N-2-Fixing Rhizobium-Legume Symbioses? Adv Microb Physiol. 2012;60:325–89. doi: 10.1016/B978-0-12-398264-3.00005-X 22633062

49. Sullivan JT, Ronson CW. Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene (vol 95, pg 5145, 1998). P Natl Acad Sci USA. 1998 Jul 21;95(15):9059-.

50. Remigi P, Capela D, Clerissi C, Tasse L, Torchet R, Bouchez O, et al. Transient Hypermutagenesis Accelerates the Evolution of Legume Endosymbionts following Horizontal Gene Transfer. PLoS Biol. 2014 Sep;12(9):e1001942. doi: 10.1371/journal.pbio.1001942 25181317

51. Elbeltagy A, Nishioka K, Sato T, Suzuki H, Ye B, Hamada T, et al. Endophytic colonization and in planta nitrogen fixation by a Herbaspirillum sp isolated from wild rice species. Appl Environ Microb. 2001 Nov;67(11):5285–93. 11679357

52. Rothballer M, Eckert B, Schmid M, Fekete A, Schloter M, Lehner A, et al. Endophytic root colonization of gramineous plants by Herbaspirillum frisingense. FEMS Microbiol Ecol. 2008 Oct;66(1):85–95. doi: 10.1111/j.1574-6941.2008.00582.x 18761671

53. Bulgarelli D, Rott M, Schlaeppi K, Ver Loren van Themaat E, Ahmadinejad N, Assenza F, et al. Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature. 2012 Aug 2;488(7409):91–5. doi: 10.1038/nature11336 22859207

54. Den Herder J, Vanhee C, De Rycke R, Corich V, Holsters M, Goormachtig S. Nod factor perception during infection thread growth fine-tunes nodulation. Mol Plant Microbe In. 2007 Feb;20(2):129–37. 17313164

55. Rodpothong P, Sullivan JT, Songsrirote K, Sumpton D, Cheung KW, Thomas-Oates J, et al. Nodulation gene mutants of Mesorhizobium loti R7A-nodZ and nolL mutants have host-specific phenotypes on Lotus spp. Molecular plant-microbe interactions: MPMI. 2009 Dec;22(12):1546–54. doi: 10.1094/MPMI-22-12-1546 19888820

56. Lehman AP, Long SR. Exopolysaccharides from Sinorhizobium meliloti Can Protect against H2O2-Dependent Damage. J Bacteriol. 2013 Dec;195(23):5362–9. doi: 10.1128/JB.00681-13 24078609

57. Reeve WG, Tiwari RP, Worsley PS, Dilworth MJ, Glenn AR, Howieson JG. Constructs for insertional mutagenesis, transcriptional signal localization and gene regulation studies in root nodule and other bacteria. Microbiol-Uk. 1999 Jun;145:1307–16.

58. Mazur A, Krol JE, Skorupska A. Isolation and sequencing of Rhizobium leguminosarum bv. Trifolii PssN, PssO and PssP genes encoding the proteins involved in polymerization and translocation of exopolysaccharide. DNA Sequence. 2001;12(1):1–12. 11697141

59. Skorupska A, Janczarek M, Marczak M, Mazur A, Krol J. Rhizobial exopolysaccharides: genetic control and symbiotic functions. Microbial cell factories. 2006 Feb 16;5.

60. vanWorkum WAT, Cremers HCJC, Wijfjes AHM, vanderKolk C, Wijffelman CA, Kijne JW. Cloning and characterization of four genes of Rhizobium leguminosarum bv trifolii involved in exopolysaccharide production and nodulation. Mol Plant Microbe In. 1997 Mar;10(2):290–301. 9057334

61. James EK, Sprent JI. Development of N2-fixing nodules on the wetland legume Lotus uliginosus exposed to conditions of flooding. New Phytologist. 1999;142(2):219–31.

62. Geddes BA, Oresnik IJ. Inability To Catabolize Galactose Leads to Increased Ability To Compete for Nodule Occupancy in Sinorhizobium meliloti. J Bacteriol. 2012 Sep;194(18):5044–53. doi: 10.1128/JB.00982-12 22797764

63. Hibbing ME, Fuqua C, Parsek MR, Peterson SB. Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol. 2010 Jan;8(1):15–25. doi: 10.1038/nrmicro2259 19946288

64. Ma LS, Hachani A, Lin JS, Filloux A, Lai EM. Agrobacterium tumefaciens Deploys a Superfamily of Type VI Secretion DNase Effectors as Weapons for Interbacterial Competition In Planta. Cell Host Microbe. 2014 Jul 9;16(1):94–104. doi: 10.1016/j.chom.2014.06.002 24981331

65. Vorholt JA. Microbial life in the phyllosphere. Nat Rev Microbiol. 2012 Dec;10(12):828–40. doi: 10.1038/nrmicro2910 23154261

66. Kiers ET, Rousseau RA, West SA, Denison RF. Host sanctions and the legume-rhizobium mutualism. Nature. 2003 Sep 4;425(6953):78–81. 12955144

67. Relic B, Perret X, Estradagarcia MT, Kopcinska J, Golinowski W, Krishnan HB, et al. Nod Factors of Rhizobium Are a Key to the Legume Door. Mol Microbiol. 1994 Jul;13(1):171–8. 7984092

68. Friesen ML, Mathias A. Mixed infections may promote diversification of mutualistic symbionts: why are there ineffective rhizobia? J Evolution Biol. 2010 Feb;23(2):323–34. doi: 10.1111/j.1420-9101.2009.01902.x 20002933

69. Fujita H, Aoki S, Kawaguchi M. Evolutionary Dynamics of Nitrogen Fixation in the Legume-Rhizobia Symbiosis. PloS one. 2014 Apr 1;9(4).

70. Weyl EG, Frederickson ME, Yu DW, Pierce NE. Economic contract theory tests models of mutualism. P Natl Acad Sci USA. 2010 Sep 7;107(36):15712–6. doi: 10.1073/pnas.1005294107 20733067

71. Brown SD, Utturkar SM, Klingeman DM, Johnson CM, Martin SL, Land ML, et al. Twenty-one genome sequences from Pseudomonas species and 19 genome sequences from diverse bacteria isolated from the rhizosphere and endosphere of Populus deltoides. J Bacteriol. 2012 Nov;194(21):5991–3. doi: 10.1128/JB.01243-12 23045501

72. Hardoim PR, Andreote FD, Reinhold-Hurek B, Sessitsch A, van Overbeek LS, van Elsas JD. Rice root-associated bacteria: insights into community structures across 10 cultivars. FEMS Microbiol Ecol. 2011 Jul;77(1):154–64. doi: 10.1111/j.1574-6941.2011.01092.x 21426364

73. Ikeda S, Okubo T, Anda M, Nakashita H, Yasuda M, Sato S, et al. Community- and genome-based views of plant-associated bacteria: plant-bacterial interactions in soybean and rice. Plant & cell physiology. 2010 Sep;51(9):1398–410.

74. Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, et al. Defining the core Arabidopsis thaliana root microbiome. Nature. 2012 Aug 2;488(7409):86–90. doi: 10.1038/nature11237 22859206

75. Tan Z, Hurek T, Vinuesa P, Muller P, Ladha JK, Reinhold-Hurek B. Specific detection of Bradyrhizobium and Rhizobium strains colonizing rice (Oryza sativa) roots by 16S-23S ribosomal DNA intergenic spacer-targeted PCR. Applied and environmental microbiology. 2001 Aug;67(8):3655–64. 11472944

76. Schlaman HRM, Horvath B, Vijgenboom E, Okker RJH, Lugtenberg BJJ. Suppression of Nodulation Gene-Expression in Bacteroids of Rhizobium-Leguminosarum Biovar Viciae. J Bacteriol. 1991 Jul;173(14):4277–87. 1712355

77. Timmers ACJ, Auriac MC, de Billy F, Truchet G. Nod factor internalization and microtubular cytoskeleton changes occur concomitantly during nodule differentiation in alfalfa. Development. 1998 Feb;125(3):339–49. 9425130

78. Epstein B, Branca A, Mudge J, Bharti AK, Briskine R, Farmer AD, et al. Population Genomics of the Facultatively Mutualistic Bacteria Sinorhizobium meliloti and S. medicae. PLoS genetics. 2012 Aug;8(8).

79. Den Herder G, Parniske M. The unbearable naivety of legumes in symbiosis. Curr Opin Plant Biol. 2009 Aug;12(4):491–9. doi: 10.1016/j.pbi.2009.05.010 19632141

80. Schumpp O, Deakin WJ. How inefficient rhizobia prolong their existence within nodules. Trends Plant Sci. 2010 Apr;15(4):189–95. doi: 10.1016/j.tplants.2010.01.001 20117958

81. Triplett EW, Sadowsky MJ. Genetics of Competition for Nodulation of Legumes. Annu Rev Microbiol. 1992;46:399–428. 1444262

82. Yates RJ, Howieson JG, Reeve WG, O'Hara GW. A re-appraisal of the biology and terminology describing rhizobial strain success in nodule occupancy of legumes in agriculture. Plant Soil. 2011 Nov;348(1–2):255–67.

83. Howieson J, Ballard R. Optimising the legume symbiosis in stressful and competitive environments within southern Australia—some contemporary thoughts. Soil Biol Biochem. 2004 Aug;36(8):1261–73.

84. Botha WJ, Jaftha JB, Bloem JF, Habig JH, Law IJ. Effect of soil bradyrhizobia on the success of soybean inoculant strain CB 1809. Microbiol Res. 2004;159(3):219–31. 15462522

85. Streeter JG. Failure of Inoculant Rhizobia to Overcome the Dominance of Indigenous Strains for Nodule Formation. Can J Microbiol. 1994 Jul;40(7):513–22.

86. Vlassak KM, Vanderleyden J. Factors influencing nodule occupancy by inoculant rhizobia. Crit Rev Plant Sci. 1997;16(2):163–229.

87. Alves BJR, Boddey RM, Urquiaga S. The success of BNF in soybean in Brazil. Plant Soil. 2003 May;252(1):1–9.

88. Angus AA, Agapakis CM, Fong S, Yerrapragada S, Estrada-de los Santos P, Yang P, et al. Plant-Associated Symbiotic Burkholderia Species Lack Hallmark Strategies Required in Mammalian Pathogenesis. PloS one. 2014 Jan 8;9(1).

89. Chen WM, James EK, Prescott AR, Kierans M, Sprent JI. Nodulation of Mimosa spp. by the beta-proteobacterium Ralstonia taiwanensis. Molecular plant-microbe interactions: MPMI. 2003 Dec;16(12):1051–61. 14651338