Widespread fitness alignment in the legume-rhizobium symbiosis

New Phytologist

Volumn 194, Issue 4, 2012, Pages 1096-1111

  Friesen, Maren L ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Conflict; Legume rhizobium; Meta analysis; Mutualism; Pleiotropy; Symbiosis

Indexed keywords

ABOVEGROUND BIOMASS; FITNESS; HOST-SYMBIONT INTERACTION; LEGUME; META-ANALYSIS; NODULATION; PLEIOTROPY; RHIZOBACTERIUM; SYMBIOSIS;

ARTICLE; EVOLUTION; FABACEAE; GENETICS; MICROBIOLOGY; MUTATION; NODULATION; PLEIOTROPY; REPRODUCTIVE FITNESS; RHIZOBIUM; SYMBIOSIS;

BIOLOGICAL EVOLUTION; FABACEAE; GENETIC FITNESS; GENETIC PLEIOTROPY; MUTATION; PLANT ROOT NODULATION; RHIZOBIUM; SYMBIOSIS;

RHIZOBIACEAE; RHIZOBIUM;

EID: 84860497851     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2012.04099.x     Document Type: Article

References (156)

1. Amadou C, Pascal G, Mangenot S, Glew M, Bontemps C, Capela D, Carrère S, Cruveiller S, Dossat C, Lajus A et al. 2008. Genome sequence of the beta-rhizobium Cupriavidus taiwanensis and comparative genomics of rhizobia. Genome Research 18: 1472-1483.
2. Amarger N. 1981. Competition for nodule formation between effective and ineffective strains of Rhizobium meliloti. Soil Biology and Biochemistry 13: 475-480.
3. Amarger N, Lobreau J. 1982. Quantitative study of nodulation competitiveness in Rhizobium strains. Applied and Environmental Microbiology 44: 583-588.
4. Ames-Gottfred NP, Christie BR. 1989. Competition among strains of Rhizobium leguminosarum biovar trifolii and use of a diallel analysis in assessing competition. Applied and Environmental Microbiology 55: 1599-1604.
5. Ampe F, Kiss E, Sabourdy F, Batut J. 2003. Transcriptome analysis of Sinorhizobium meliloti during symbiosis. Genome Biology 4: R15.
6. Ampomah OY, Jensen JB, Bhuvaneswari TV. 2008. Lack of trehalose catabolism in Sinorhizobium species increases their nodulation competitiveness on certain host genotypes. New Phytologist 179: 495-504.
7. Ané J-M, Zhu H, Frugoli J. 2008. Recent advances in Medicago truncatula genomics. International Journal of Plant Genomics 2008: 1-12.
8. Archetti M, Scheuring I, Hoffman M, Frederickson ME, Pierce NE, Yu DW. 2011. Economic game theory for mutualism and cooperation. Ecology Letters 14: 1300-1312.
9. Barnett MJ, Toman CJ, Fisher RF, Long SR. 2004. A dual-genome Symbiosis Chip for coordinate study of signal exchange and development in a prokaryote-host interaction. Proceedings of the National Academy of Sciences, USA 101: 16636-16641.
10. Batut J, Mergaert P, Masson-Boivin C. 2011. Peptide signalling in the rhizobium-legume symbiosis. Current Opinion in Microbiology 14: 181-187.
11. Baudoin M. 1975. Host castration as a parasitic strategy. Evolution; International Journal of Organic Evolution 29: 335-352.
12. Bauer W. 1981. Infection of legumes by rhizobia. Annual Review of Plant Physiology 32: 407-449.
13. Bianco C, Defez R. 2009. Medicago truncatula improves salt tolerance when nodulated by an indole-3-acetic acid-overproducing Sinorhizobium meliloti strain. Journal of Experimental Botany 60: 3097-3107.
14. Boucher D, James S, Keeler K. 1982. The ecology of mutualism. Annual Review of Ecology and Systematics 13: 315-347.
15. Branca A, Paape TD, Zhou P, Briskine R, Farmer AD, Mudge J, Bharti AK, Woodward JE, May GD, Gentzbittel L et al. 2011. Whole-genome nucleotide diversity, recombination, and linkage disequilibrium in the model legume Medicago truncatula. Proceedings of the National Academy of Sciences, USA 108: E864-E870.
16. Brockman F, Forse L, Bezdicek D, Fredrickson J. 1991. Impairment of transposon-induced mutants of Rhizobium leguminosarum. Soil Biology and Biochemistry 23: 861-867.
17. Bromfield E, Jones DG. 1979. Competitive ability and symbiotic effectiveness of doubly labeled antibiotic resistant mutants of Rhizobium trifolii. Annals of Applied Biology 91: 211-219.
18. Brown P, Ahmad M. 1996. Competitive interaction among strains of Rhizobium leguminosarum bv phaseoli in the nodulation of kidney beans (Phaseolus vulgaris L). Biology and Fertility of Soils 21: 7-9.
19. Bull JJ, Rice WR. 1991. Distinguishing mechanisms for the evolution of co-operation. Journal of Theoretical Biology 149: 63-74.
20. Burdon J, Gibson A, Searle S, Woods M, Brockwell J. 1999. Variation in the effectiveness of symbiotic associations between native rhizobia and temperate Australian Acacia: within-species interactions. Journal of Applied Ecology 36: 398-408.
21. Camerini S, Senatore B, Lonardo E, Imperlini E, Bianco C, Moschetti G, Rotino GL, Campion B, Defez R. 2008. Introduction of a novel pathway for IAA biosynthesis to rhizobia alters vetch root nodule development. Archives of Microbiology 190: 67-77.
22. Cevallos MA, Encarnacion S, Leija A, Mora Y, Mora J. 1996. Genetic and physiological characterization of a Rhizobium etli mutant strain unable to synthesize poly-beta-hydroxybutyrate. Journal of Bacteriology 178: 1646-1654.
23. Chandra R, Pareek R. 1985. Role of host genotype in effectiveness and competitiveness of chickpea (Cicer arietinum L.) rhizobium. Tropical Agriculture 62: 90-94.
24. Chen L, Figueredo A, Villani H, Michajluk J, Hungria M. 2002. Diversity and symbiotic effectiveness of rhizobia isolated from field-grown soybean nodules in Paraguay. Biology and Fertility of Soils 35: 448-457.
25. Cheng HP, Walker GC. 1998. Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti. Journal of Bacteriology 180: 5183-5191.
26. Clay K. 1991. Parasitic castration of plants by fungi. Trends in Ecology and Evolution 6: 162-166.
27. Date R, Hurse L. 1992. Growth, competitiveness and effectiveness of spontaneous antibiotic-resistant strains of Bradyrhizobium for Desmodium intortum cv Greenleaf. Soil Biology and Biochemistry 24: 33-39.
28. Dazzo FB, Truchet GL, Hollingsworth RI, Hrabak EM, Pankratz HS, Philip-Hollingsworth S, Salzwedel JL, Chapman K, Appenzeller L, Squartini A. 1991. Rhizobium lipopolysaccharide modulates infection thread development in white clover root hairs. Journal of Bacteriology 173: 5371-5384.
29. De Mita S, Santoni S, Ronfort J, Bataillon T. 2007. Adaptive evolution of the symbiotic gene NORK is not correlated with shifts of rhizobial specificity in the genus Medicago. BMC Evolutionary Biology 7: 210.
30. Denison RF. 2000. Legume sanctions and the evolution of symbiotic cooperation by rhizobia. American Naturalist 156: 567-576.
31. Denison RF, Bledsoe C, Kahn M, O'Gara F, Simms E, Thomashow L. 2003. Cooperation in the rhizosphere and the "free rider" problem. Ecology 84: 838-845.
32. DerSimonian R, Laird N. 1986. Meta-analysis in clinical trials. Controlled Clinical Trials 7: 177-188.
33. Ding Y, Kalo P, Yendrek C, Sun J, Liang Y, Marsh JF, Harris JM, Oldroyd GED. 2008. Abscisic acid coordinates nod factor and cytokinin signaling during the regulation of nodulation in Medicago truncatula. The Plant Cell 20: 2681-2695.
34. Fagard R, Staessen JA, Thijs L. 1995. The relationships between left ventricular mass and daytime and night-time blood pressures: a meta-analysis of comparative studies. Journal of Hypertension 13: 823-829.
35. Ferguson BJ, Indrasumunar A, Hayashi S, Lin M-H, Lin Y-H, Reid DE, Gresshoff PM. 2010. Molecular analysis of legume nodule development and autoregulation. Journal of Integrative Plant Biology 52: 61-76.
36. Filzmoser P, Hron K, Reimann C. 2012. Interpretation of multivariate outliers for compositional data. Computers and Geosciences. 39: 77-85.
37. Firmin JL, Wilson KE, Carlson RW, Davies AE, Downie JA. 1993. Resistance to nodulation of cv. Afghanistan peas is overcome by nodX, which mediates an O-acetylation of the Rhizobium leguminosarum lipo-oligosaccharide nodulation factor. Molecular Microbiology 10: 351-360.
38. Frean MR, Abraham ER. 2004. Adaptation and enslavement in endosymbiont-host associations. Physical Review E 69: 051913.
39. Friesen ML, Mathias A. 2010. Mixed infections may promote diversification of mutualistic symbionts: why are there ineffective rhizobia? Journal of Evolutionary Biology 23: 323-334.
40. Friesen ML, Porter SS, Stark SC, von Wettberg EJ, Sachs J, Martínez-Romero E. 2011. Microbially mediated plant functional traits. Annual Review of Ecology Evolution and Systematics 42: 23-46.
41. Friesen ML, von Wettberg EJ. 2010. Adapting genomics to study the evolution and ecology of agricultural systems. Current Opinion in Plant Biology 13: 119-125.
42. Fuhrmann J, Wollum A. 1989. Symbiotic interactions between soybean and competing strains of Bradyrhizobium japonicum. Plant and Soil 119: 139-145.
43. Gage D. 2004. Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiology and Molecular Biology Reviews 68: 280-300.
44. Galardini M, Mengoni A, Brilli M, Pini F, Fioravanti A, Lucas S, Lapidus A, Cheng J-F, Goodwin L, Pitluck S et al. 2011. Exploring the symbiotic pangenome of the nitrogen-fixing bacterium Sinorhizobium meliloti. BMC Genomics 12: 235.
45. Gaudet CL, Keddy PA. 1988. A comparative approach to predicting competitive ability from plant traits. Nature 334: 242-243.
46. Glick BR, Cheng Z, Czarny J, Duan J. 2007. Promotion of plant growth by ACC deaminase-producing soil bacteria. European Journal of Plant Pathology 119: 329.
47. Gould S, Vrba E. 1982. Exaptation-a missing term in the science of form. Paleobiology 8: 4-15.
48. Graham PH, Vance CP. 2003. Legumes: importance and constraints to greater use. Plant Physiology 131: 872-877.
49. Gubry-Rangin C, Garcia M, Béna G. 2010. Partner choice in Medicago truncatula-Sinorhizobium symbiosis. Proceedings of the Royal Society of London B 277: 1947-1951.
50. Hafeez F, Hameed S, Ahmad T, Malik K. 2001. Competition between effective and less effective strains of Bradyrhizobium spp. for nodulation on Vigna radiata. Biology and Fertility of Soils 33: 382-386.
51. Heath KD. 2008. The coevolutionary genetics of plant-microbe interactions. New Phytologist 180: 268-270.
52. Heath KD. 2010. Intergenomic epistasis and coevolutionary constraint in plants and rhizobia. Evolution 64: 1446-1458.
53. Heath KD, Tiffin P. 2007. Context dependence in the coevolution of plant and rhizobial mutualists. Proceedings of the Royal Society of London B 274: 1905-1912.
54. Heath KD, Tiffin P. 2009. Stabilizing mechanisms in a legume-rhizobium mutualism. Evolution 63: 652-662.
55. Hoeksema J, Chaudhary V, Gehring C, Johnson N, Karst J, Koide R, Pringle A, Zabinski C, Bever J, Moore J et al. 2010. A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecology Letters 13: 394-407.
56. Hungria M, Andrade D, Chueire L, Probanza A, Guttierrez-Manero F, Megias M. 2000. Isolation and characterization of new efficient and competitive bean (Phaseolus vulgaris L.) rhizobia from Brazil. Soil Biology and Biochemistry 32: 1515-1528.
57. Hungria M, Boddey L, Santos M, Vargas M. 1998. Nitrogen fixation capacity and nodule occupancy by Bradyrhizobium japonicum and B. elkanii strains. Biology and Fertility of Soils 27: 393-399.
58. Hungria M, Campo R, Chueire L, Grange L, Megias M. 2001. Symbiotic effectiveness of fast-growing rhizobial strains isolated from soybean nodules in Brazil. Biology and Fertility of Soils 33: 387-394.
59. Hungria M, Campo R, Mendes I. 2003. Benefits of inoculation of the common bean (Phaseolus vulgaris) crop with efficient and competitive Rhizobium tropici strains. Biology and Fertility of Soils 39: 88-93.
60. Hunter W, Kuykendall L. 1990. Enhanced nodulation and nitrogen fixation by a revertant of a nodulation-defective Bradyrhizobium japonicum tryptophan auxotroph. Applied and Environmental Microbiology 56: 2399-2403.
61. Jensen J, Ampomah O, Darrah R, Peters N, Bhuvaneswari T. 2005. Role of trehalose transport and utilization in Sinorhizobium meliloti-Alfalfa interactions. Molecular Plant-Microbe Interactions 18: 694-702.
62. Jensen JB, Peters NK, Bhuvaneswari TV. 2002. Redundancy in periplasmic binding protein-dependent transport systems for trehalose, sucrose, and maltose in Sinorhizobium meliloti. Journal of Bacteriology 184: 2978-2986.
63. Jiang G, Krishnan AH, Kim YW, Wacek TJ, Krishnan HB. 2001. A functional myo-inositol dehydrogenase gene is required for efficient nitrogen fixation and competitiveness of Sinorhizobium fredii USDA191 to nodulate soybean (Glycine max L. Merr.). Journal of Bacteriology 183: 2595-2604.
64. Jiménez-Zurdo JI, van Dillewijn P, Soto MJ, de Felipe MR, Olivares J, Toro N. 1995. Characterization of a Rhizobium meliloti proline dehydrogenase mutant altered in nodulation efficiency and competitiveness on alfalfa roots. Molecular Plant-Microbe Interactions 8: 492-498.
65. Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC. 2007. How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nature Reviews Microbiology 5: 619-633.
66. Jones KM, Sharopova N, Lohar DP, Zhang JQ, VandenBosch KA, Walker GC. 2008. Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti or an exopolysaccharide-deficient mutant. Proceedings of the National Academy of Sciences, USA 105: 704-709.
67. Kaschuk G, Leffelaar PA, Giller KE, Alberton O, Hungria M, Kuyper TW. 2010. Responses of legumes to rhizobia and arbuscular mycorrhizal fungi: a meta-analysis of potential photosynthate limitation of symbioses. Soil Biology and Biochemistry 42: 125-127.
68. Kiers ET, Denison RF. 2008. Sanctions, cooperation, and the stability of plant-rhizosphere mutualisms. Annual Review of Ecology Evolution and Systematics 39: 215-236.
69. Kiers ET, Hutton MG, Denison RF. 2007. Human selection and the relaxation of legume defences against ineffective rhizobia. Proceedings of the Royal Society of London B 274: 3119-3126.
70. Kiers ET, Palmer TM, Ives AR, Bruno JF, Bronstein JL. 2010. Mutualisms in a changing world: an evolutionary perspective. Ecology Letters 13: 1459-1474.
71. Kiers ET, Rousseau RA, Denison RF. 2006. Measured sanctions: legume hosts detect quantitative variation in rhizobium cooperation and punish accordingly. Evolutionary Ecology Research 8: 1077-1086.
72. Kiers ET, Rousseau RA, West SA, Denison RF. 2003. Host sanctions and the legume-rhizobium mutualism. Nature 425: 78-81.
73. Kundu S, Dudeja SS. 2008. Molecular diversity, effectiveness and competitiveness of indigenous rhizobial population infecting mungbean Vigna radiata (L. Wilczek) under semi-arid conditions. Indian Journal of Microbiology 48: 445-452.
74. Kuykendall L. 1989. Influence of Glycine max nodulation on the persistence in soil of a genetically marked Bradyrhizobium japonicum strain. Plant and Soil 116: 275-277.
75. Kuykendall L, Hashem F, Hunter W. 1996. Enhanced competitiveness of a Bradyrhizobium japonicum mutant strain improved for nodulation and nitrogen fixation. Plant and Soil 186: 121-125.
76. Lagares A, Caetano-Anollés G, Niehaus K, Lorenzen J, Ljunggren HD, Pühler A, Favelukes G. 1992. A Rhizobium meliloti lipopolysaccharide mutant altered in competitiveness for nodulation of alfalfa. Journal of Bacteriology 174: 5941-5952.
77. Laguerre G, Depret G, Bourion V, Duc G. 2007. Rhizobium leguminosarum bv. viciae genotypes interact with pea plants in developmental responses of nodules, roots and shoots. New Phytologist 176: 680-690.
78. Law R. 1985. Evolution in a mutualistic environment. In: Boucher D, ed. The biology of mutualism: ecology and evolution. New York, NY, USA: Oxford University Press, 145-170.
79. Lodeiro AR, López-García SL, Vázquez TE, Favelukes G. 2000. Stimulation of adhesiveness, infectivity, and competitiveness for nodulation of Bradyrhizobium japonicum by its pretreatment with soybean seed lectin. FEMS Microbiology Letters 188: 177-184.
80. Long SR. 1996. Rhizobium symbiosis: nod factors in perspective. The Plant Cell 8: 1885-1898.
81. Lynch M, Blanchard J, Houle D, Kibota T, Schultz S, Vassilieva L, Willis J. 1999. Perspective: spontaneous deleterious mutation. Evolution 53: 645-663.
82. Ma WR, Charles TC, Glick BR. 2004. Expression of an exogenous 1-aminocyclopropane-1-carboxylate deaminase gene in Sinorhizobium meliloti increases its ability to nodulate alfalfa. Applied and Environmental Microbiology 70: 5891-5897.
83. Ma WB, Penrose D, Glick BR. 2002. Strategies used by rhizobia to lower plant ethylene levels and increase nodulation. Canadian Journal of Microbiology 48: 947-954.
84. Malek W. 1992. The role of motility in the efficiency of nodulation by Rhizobium meliloti. Archives of Microbiology 158: 26-28.
85. Marroqui S, Zorreguieta A, Santamaría C, Temprano F, Soberon M, Megias M, Downie JA. 2001. Enhanced symbiotic performance by Rhizobium tropici glycogen synthase mutants. Journal of Bacteriology 183: 854-864.
86. Mavingui P, Flores M, Guo X, Dávila G, Perret X, Broughton WJ, Palacios R. 2002. Dynamics of genome architecture in Rhizobium sp. strain NGR234. Journal of Bacteriology 184: 171-176.
87. Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. 2005. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122: 107-118.
88. McInnes A, Thies J, Abbott L, Howieson J. 2004. Structure and diversity among rhizobial strains, populations and communities - a review. Soil Biology and Biochemistry 36: 1295-1308.
89. Moher D, Cook DJ, Eastwood S, Olkin I, Rennie D, Stroup DF. 2000. Improving the quality of reports of meta-analyses of randomised controlled trials: the QUOROM statement. Onkologie 23: 597-602.
90. Mortier V, Herder Den G, Whitford R, Van de Velde W, Rombauts S, D'haeseleer K, Holsters M, Goormachtig S. 2010. CLE peptides control Medicago truncatula nodulation locally and systemically. Plant Physiology 153: 222-237.
91. Murphy P, Wexler W, Grzemski W, Rao J, Gordon D. 1995. Rhizopines - their role in symbiosis and competition. Soil Biology and Biochemistry 27: 525-529.
92. Mytton L. 1975. Plant genotype×rhizobium strain interactions in white clover. Annals of Applied Biology 80: 103-107.
93. Noë R, Hammerstein P. 1994. Biological markets - supply-and-demand determine the effect of partner choice in cooperation, mutualism and mating. Behavioral Ecology and Sociobiology 35: 1-11.
94. Nurhayati D, Diatloff A, Hoult E. 1988. The effectiveness of some Indonesian strains of Rhizobium on four tropical legumes. Plant and Soil 108: 171-177.
95. Nurhayati D, Ivory D, Stur W. 1989. The effectiveness and competitiveness of some Indonesian Rhizobium strains on tropical legumes grown in four soil types of Java. Plant and Soil 117: 146-150.
96. Olah B, Kiss E, Gyorgypal Z, Borzi J, Cinege G, Csanadi G, Batut J, Kondorosi A, Dusha I. 2001. Mutation in the ntrR gene, a member of the vap gene family, increases the symbiotic efficiency of Sinorhizobium meliloti. Molecular Plant-Microbe Interactions 14: 887-894.
97. Oldroyd GED, Downie JA. 2008. Coordinating nodule morphogenesis with rhizobial infection in legumes. Annual Review of Plant Biology 59: 519-546.
98. Onishchuk OP, Kurchak ON, Sharypova LA, Provorov NA, Simarov BV. 2001. Analysis of various types of competition in Tn5-mutants of alfalfa rhizobium bacteria (Sinorhizobium meliloti). Genetika 37: 1507-1512.
99. Oono R, Anderson CG, Denison R. 2011. Failure to fix nitrogen by non-reproductive symbiotic rhizobia triggers host sanctions that reduce fitness of their reproductive clonemates. Proceedings of the Royal Society of London B 278: 2698-2703.
100. Oono R, Denison R, Kiers E. 2009. Controlling the reproductive fate of rhizobia: how universal are legume sanctions? New Phytologist 183: 967-979.
101. Pankhurst C. 1981. Effect of plant nutrient supply on nodule effectiveness and rhizobium strain competition for nodulation of Lotus pedunculatus. Plant and Soil 60: 325-339.
102. Pankhurst C, Jones WT. 1979. Effectiveness of Lotus root nodules III. Effect of combined nitrogen on nodule effectiveness and flavolan synthesis in plant roots. Journal of Experimental Botany 30: 1109-1118.
103. Pankhurst C, Macdonald P, Reeves J. 1986. Enhanced nitrogen fixation and competitiveness for nodulation of Lotus pedunculatus by a plasmid-cured derivative of Rhizobium loti. Journal of General Microbiology 132: 2321-2328.
104. Parniske M, Kosch K, Werner D, Muller P. 1993. exoB mutants of Bradyrhizobium japonicum with reduced competitiveness for nodulation of Glycine max. Molecular Plant-Microbe Interactions 6: 99-106.
105. Parniske M, Zimmermann C, Cregan P, Werner D. 1990. Hypersensitive reaction of nodule cells in the Glycine sp.-Bradyrhizobium japonicum symbiosis occurs at the genotype-specific level. Botanica Acta 103: 143-148.
106. Patten CL, Glick BR. 1996. Bacterial biosynthesis of indole-3-acetic acid. Canadian Journal of Microbiology 42: 207-220.
107. Penmetsa RV, Cook DR. 1997. A legume ethylene-insensitive mutant hyperinfected by its rhizobial symbiont. Science 275: 527-530.
108. Penmetsa RV, Frugoli J, Smith L, Long S, Cook DR. 2003. Dual genetic pathways controlling nodule number in Medicago truncatula. Plant Physiology 131: 998-1008.
109. Popp C, Ott T. 2011. Regulation of signal transduction and bacterial infection during root nodule symbiosis. Current Opinion in Plant Biology 14: 458-467.
110. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE. 2010. Global pollinator declines: trends, impacts and drivers. Trends in Ecology and Evolution 25: 345-353.
111. Prell J, Poole P. 2006. Metabolic changes of rhizobia in legume nodules. Trends in Microbiology 14: 161-168.
112. Ratcliff WC, Denison RF. 2009. Rhizobitoxine producers gain more poly-3-hydroxybutyrate in symbiosis than do competing rhizobia, but reduce plant growth. ISME Journal 3: 870-872.
113. Ratcliff WC, Kadam S, Denison RF. 2008. Poly-3-hydroxybutyrate (PHB) supports survival and reproduction in starving rhizobia. FEMS Microbiology Ecology 65: 391-399.
114. R Development Core Team. 2011. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. URL [accessed on 8 July 2011].
115. Reid DE, Ferguson BJ, Hayashi S, Lin Y-H, Gresshoff PM. 2011. Molecular mechanisms controlling legume autoregulation of nodulation. Annals of Botany 108: 789-795.
116. Rice W, Olsen P, Collins M. 1995. Symbiotic effectiveness of Rhizobium meliloti at low root temperature. Plant and Soil 170: 351-358.
117. Robinson A. 1969. Competition between effective and ineffective strains of Rhizobium trifolii in nodulation of Trifolium subterraneum. Australian Journal of Agricultural Research 20: 827-841.
118. Robleto E, Kmiecik K, Oplinger E, Nienhuis J, Triplett E. 1998. Trifolitoxin production increases nodulation competitiveness of Rhizobium etli CE3 under agricultural conditions. Applied and Environmental Microbiology 64: 2630-2633.
119. Rodriguez-Navarro D, Santamaria C, Temprano F, Leidi E. 1999. Interaction effects between Rhizobium strain and bean cultivar on nodulation, plant growth, biomass partitioning and xylem sap composition. European Journal of Agronomy 11: 131-143.
120. Rojas-Jiménez K, Sohlenkamp C, Geiger O, Martínez-Romero E, Werner D, Vinuesa P. 2005. A ClC chloride channel homolog and ornithine-containing membrane lipids of Rhizobium tropici CIAT899 are involved in symbiotic efficiency and acid tolerance. Molecular Plant-Microbe Interactions 18: 1175-1185.
121. Sachs JL, Ehinger M, Simms E. 2010a. Origins of cheating and loss of symbiosis in wild Bradyrhizobium. Journal of Evolutionary Biology 23: 1075-1089.
122. Sachs JL, Mueller U, Wilcox T, Bull J. 2004. The evolution of cooperation. Quarterly Review of Biology 79: 135-160.
123. Sachs JL, Russell JE, Lii YE, Black KC, Lopez G, Patil AS. 2010b. Host control over infection and proliferation of a cheater symbiont. Journal of Evolutionary Biology 23: 1919-1927.
124. Sato S, Nakamura Y, Kaneko T, Asamizu E, Kato T, Nakao M, Sasamoto S, Watanabe A, Ono A, Kawashima K et al. 2008. Genome structure of the legume, Lotus japonicus. DNA Research 15: 227-239.
125. Savka MA, Dessaux Y, Oger P, Rossbach S. 2002. Engineering bacterial competitiveness and persistence in the phytosphere. Molecular Plant-Microbe Interactions 15: 866-874.
126. Saxena AK, Mittal S, Dwivedi A, Shashikala, Tilak KVBR. 1996. Competitiveness and symbiotic efficiency of potential inoculant strains of Bradyrhizobium sp. (Vigna). Microbiological Research 151: 219-224.
127. Schmutz J, Cannon SB, Schlueter J, Ma J, Mitros T, Nelson W, Hyten DL, Song Q, Thelen JJ, Cheng J et al. 2010. Genome sequence of the palaeopolyploid soybean. Nature 463: 178-183.
128. Segura D, Espin G. 1998. Mutational inactivation of a gene homologous to Escherichia coli ptsP affects poly-beta-hydroxybutyrate accumulation and nitrogen fixation in Azotobacter vinelandii. Journal of Bacteriology 180: 4790-4798.
129. Sen D, Weaver R. 1981. A comparision of nitrogen-fixing ability of peanut, cowpea and siratro plants nodulated by different strains of rhizobium. Plant and Soil 60: 317-319.
130. Sessitsch A, Jjemba P, Hardarson G, Akkermans A, Wilson K. 1997. Measurement of the competitiveness index of Rhizobium tropici strain CIAT899 derivatives marked with the gusA gene. Soil Biology and Biochemistry 29: 1099-1110.
131. Somasegaran P, Hoben H, Lewinson L. 1991. Symbiotic interactions of Phaseolus acutifolius and Phaseolus acutifolius×Phaseolus vulgaris hybrid progeny in symbiosis with Bradyrhizobium spp. and Rhizobium leguminosarum bv. phaseoli. Canadian Journal of Microbiology 37: 497-503.
132. Sugawara M, Okazaki S, Nukui N, Ezura H, Mitsui H, Minamisawa K. 2006. Rhizobitoxine modulates plant-microbe interactions by ethylene inhibition. Biotechnology Advances 24: 382-388.
133. Sullivan JT, Ronson CW. 1998. Evolution of rhizobia by acquisition of a 500-kb symbiosis island that integrates into a phe-tRNA gene. Proceedings of the National Academy of Sciences, USA 95: 5145-5149.
134. Tamimi S. 2002. Genetic diversity and symbiotic effectiveness of rhizobia isolated from root nodules of common bean (Phaseolus vulgaris L.) grown in the soils of the Jordan valley. Applied Soil Ecology 19: 183-190.
135. Thiao M, Neyra M, Isidore E, Sylla S, Lesueur D. 2004. Diversity and effectiveness of rhizobial strains from Gliricidia sepium native to Reunion Island, Kenya and New Caledonia. World Journal of Microbiology and Biotechnology 20: 703-709.
136. Thrall P, Burdon J, Woods M. 2000. Variation in the effectiveness of symbiotic associations between native rhizobia and temperate Australian legumes: interactions within and between genera. Journal of Applied Ecology 37: 52-65.
137. Thrall P, Slattery J, Broadhurst L, Bickford S. 2007. Geographic patterns of symbiont abundance and adaptation in native Australian Acacia-rhizobia interactions. Journal of Ecology 95: 1110-1122.
138. Toro A. 1996. Nodulation competitiveness in the rhizobium-legume symbiosis. World Journal of Microbiology and Biotechnology 12: 157-162.
139. Trinick M, Hadobas P. 1989. Effectiveness and competition for nodulation of Vigna unguiculata and Macroptilium atropurpureum with Bradyrhizobium from Parasponia. Canadian Journal of Microbiology 35: 1156-1163.
140. Trinick M, Hadobas P. 1990. Symbiotic effectiveness of Bradyrhizobium strains isolated from Parasponia and tropical legumes on Parasponia host species. Plant and Soil 124: 117-126.
141. Triplett EW. 1990. Construction of a symbiotically effective strain of Rhizobium leguminosarum bv. trifolii with increased nodulation competitiveness. Applied and Environmental Microbiology 56: 98-103.
142. Triplett EW, Sadowsky M. 1992. Genetics of competition for nodulation of legumes. Annual Review of Microbiology 46: 399-428.
143. Tummers B. 2006. DataThief III v.1.1. URL [accessed on 1 July 2008].
144. Turco R, Moorman T, Bezdicek D. 1986. Effectiveness and competitiveness of spontaneous antibiotic-resistant mutants of Rhizobium leguminosarum and Rhizobium japonicum. Soil Biology and Biochemistry 18: 259-262.
145. Vargas L, Lisboa B, Scholles D, Pfeifer Silveira J, Jung G, Granada C, Neves A, Braga M, Negreiros T. 2007. Genetic diversity and symbiotic efficiency of black wattle-nodulating rhizobia in soils of Rio Grande do Sul State, Brazil. Revista Brasileira de Ciencia do Solo 31: 647-654.
146. Velázquez E, García-Fraile P, Ramírez-Bahena MH, Rivas R, Martínez-Molina E. 2010. Bacteria involved in nitrogen-fixing legume symbiosis: current taxonomic perspective. In: Khan MS, Musarrat J, Zaidi A, eds. Microbes for legume improvements. Vienna, Austria: Springer, 1-25.
147. Walker SA, Downie JA. 2000. Entry of Rhizobium leguminosarum bv. viciae into root hairs requires minimal nod factor specificity, but subsequent infection thread growth requires nodO or nodE. Molecular Plant-Microbe Interactions 13: 754-762.
148. West SA, Kiers ET, Pen I, Denison RF. 2002. Sanctions and mutualism stability: when should less beneficial mutualists be tolerated? Journal of Evolutionary Biology 15: 830-837.
149. Weyl EG, Frederickson ME, Yu DW, Pierce NE. 2010. Economic contract theory tests models of mutualism. Proceedings of the National Academy of Sciences, USA 107: 15712-15716.
150. Wielbo J, Marek-Kozaczuk M, Kubik-Komar A, Skorupska A. 2007. Increased metabolic potential of Rhizobium spp. is associated with bacterial competitiveness. Canadian Journal of Microbiology 53: 957-967.
151. Wilkinson H, Spoerke J, Parker M. 1996. Divergence in symbiotic compatibility in a legume-Bradyrhizobium mutualism. Evolution 50: 1470-1477.
152. Willems A, Fernández-López M, Muñoz-Adelantado E, Goris J, De Vos P, Martínez-Romero E, Toro N, Gillis M. 2003. Description of new Ensifer strains from nodules and proposal to transfer Ensifer adhaerens Casida 1982 to Sinorhizobium as Sinorhizobium adhaerens comb. nov. Request for an opinion. International Journal of Systematic and Evolutionary Microbiology 53: 1207-1217.
153. Wood S, Layzell D, Newcomb W, Pankhurst C. 1985. A morphometric study of effective nodules induced by Rhizobium loti and Bradyrhizobium sp. (Lotus) on Lotus pedunculatus. Canadian Journal of Botany 63: 43-53.
154. Young JPW, Crossman LC, Johnston AWB, Thomson NR, Ghazoui ZF, Hull KH, Wexler M, Curson ARJ, Todd JD, Poole PS et al. 2006. The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biology 7: R34.
155. Young ND, Debellé F, Oldroyd GED, Geurts R, Cannon SB, Udvardi MK, Benedito VA, Mayer KF, Gouzy J, Schoof H et al. 2011. The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480: 520-524.
156. Young ND, Udvardi M. 2009. Translating Medicago truncatula genomics to crop legumes. Current Opinion in Plant Biology 12: 193-201.