Policing the legume-Rhizobium symbiosis: A critical test of partner choice

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Westhoek, Annet ^a   Field, Elsa ^a   Rehling, Finn ^a,b   Mulley, Geraldine ^c   Webb, Isabel ^a   Poole, Philip S ^a   Turnbull, Lindsay A ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b PHILIPPS UNIVERSITY MARBURG   (Germany)

^c UNIVERSITY OF READING   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DIFFUSION; EXERCISE; LEGUME; MARKER GENE; NITROGEN FIXATION; NONHUMAN; RHIZOBIUM; SYMBIOSIS; MICROBIOLOGY; NODULATION; PEA; PHYSIOLOGY; RHIZOBIUM LEGUMINOSARUM;

NITROGEN FIXATION; PEAS; RHIZOBIUM LEGUMINOSARUM; ROOT NODULES, PLANT; SYMBIOSIS;

EID: 85018747635     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-01634-2     Document Type: Article

References (63)

1. Lebauer, D. S. & Treseder, K. K. Nitrogen limitation of net primary productivity in terrestrial ecosystems is globally distritubed. Ecology 89, 371-379, doi: 10.1890/06-2057.1 (2008).
2. Sprent, J. I. Evolving ideas of legume evolution and diversity: A taxonomic perspective on the occurrence of nodulation. New Phytol 174, 11-25, doi: 10.1111/j.1469-8137.2007.02015.x (2007).
3. Graham, P. H. & Vance, C. P. Legumes: importance and constraints to greater use. Plant Physiol 131, 872-877, doi: 10.1104/pp.017004 (2003).
4. Hafeez, F., Hameed, S., Ahmad, T. & Malik, K. A. Competition between effective and less effective strains of Bradyrhizobium spp. for nodulation on Vigna radiata. Biol. Fertil. Soils 33, 382-386, doi: 10.1007/s003740000337 (2001).
5. Kiers, E. T., Hutton, M. G. & Denison, R. F. Human selection and the relaxation of legume defences against ineffective rhizobia. Proc. R. Soc. B 274, 3119-26, doi: 10.1098/rspb.2007.1187 (2007).
6. Denison, R. F. Legume sanctions and the evolution of symbiotic cooperation by rhizobia. Am. Nat. 156, 567-576, doi: 10.1086/316994 (2000).
7. Heath, K. & Tiffin, P. Stabilizing mechanisms in a legume-rhizobium mutualism. Evolution (N. Y) 63, 652-662 (2009).
8. Udvardi, M. & Poole, P. S. Transport and metabolism in legume-rhizobia symbioses. Annu. Rev. Plant Biol. 64, 781-805, doi: 10.1146/annurev-Arplant-050312-120235 (2013).
9. Gage, D. J. Analysis of infection thread development using Gfp-and DsRed-expressing Sinorhizobium meliloti. J. Bacteriol. 184, 7042-7046, doi: 10.1128/JB.184.24.7042-7046.2002 (2002).
10. Oldroyd, G. E. D. & Downie, J. A. Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. 59, 519-46, doi: 10.1146/annurev.arplant.59.032607.092839 (2008).
11. Hagen, M. & Hamrick, J. Population level processes in Rhizobium leguminosarum bv.Trifolii: The role of founder effects. Mol. Ecol. 5, 707-714, doi: 10.1111/j.1365-294X.1996.tb00367.x (1996).
12. Silva, C., Eguiarte, L. E. & Souza, V. Reticulated and epidemic population genetic structure of Rhizobium etli biovar phaseoli in a traditionally managed locality in Mexico. Mol. Ecol 8, 277-287, doi: 10.1046/j.1365-294X.1999.00564.x (1999).
13. Kiers, E. T. & Denison, R. F. Sanctions, cooperation, and the stability of plant-rhizosphere mutualisms. Annu. Rev. Ecol. Evol. Syst. 39, 215-236, doi: 10.1146/annurev.ecolsys.39.110707.173423 (2008).
14. Gubry-Rangin, C., Garcia, M. & Béna, G. Partner choice in Medicago truncatula-Sinorhizobium symbiosis. Proc. Biol. Sci 277, 1947-51, doi: 10.1098/rspb.2009.2072 (2010).
15. Regus, J., Gano, K. A., Hollowell, A. C. & Sachs, J. L. Efficiency of partner choice and sanctions in Lotus is not altered by nitrogen fertilization. Proc. R. Soc. B 281, 20132587-20132587, doi: 10.1098/rspb.2013.2587 (2014).
16. West, S. A., Kiers, E. T., Pen, I. & Denison, R. F. Sanctions and mutualism stability: when should less beneficial mutualists be tolerated? J. Evol. Biol 15, 830-837, doi: 10.1046/j.1420-9101.2002.00441.x (2002).
17. Simms, E. & Taylor, D. Partner choice in nitrogen-fixation mutualisms of legumes and rhizobia. Integr. Comp. Biol. 42, 369-380, doi: 10.1093/icb/42.2.369 (2002).
18. Simms, E. L. et al. An empirical test of partner choice mechanisms in a wild legume-rhizobium interaction. Proc. Biol. Sci 273, 77-81, doi: 10.1098/rspb.2005.3292 (2006).
19. Kiers, E. T., Rousseau, R. A., West, S. A. & Denison, R. F. Host sanctions and the legume-rhizobium mutualism. Nature 425, 78-81, doi: 10.1038/nature01931 (2003).
20. Kiers, T. E., Rousseau, R. A. & Denison, R. F. Measured sanctions: legume hosts detect quantitative variation in rhizobium cooperation and punish accordingly. Evol. Ecol. Res. 8, 1077-1086 (2006).
21. Oono, R., Anderson, C. G. & Denison, R. F. Failure to fix nitrogen by non-reproductive symbiotic rhizobia triggers host sanctions that reduce fitness of their reproductive clonemates. Proc. R. Soc. B 278, 2698-703, doi: 10.1098/rspb.2010.2193 (2011).
22. Malek, W. The role of motility in the efficiency of nodulation by Rhizobium meliloti. Arch. Microbiol. 158, 26-28, doi: 10.1007/BF00249061 (1992).
23. Robleto, E. A., Kmiecik, K., Oplinger, E. S., Nienhuis, J. & Triplett, E. W. Trifolitoxin production increases nodulation competitiveness of Rhizobium etli CE3 under agricultural conditions. Appl. Environ. Microbiol. 64, 2630-2633 (1998).
24. Frederix, M. et al. Mutation of praR in Rhizobium leguminosarum enhances root biofilms, improving nodulation competitiveness by increased expression of attachment proteins. Mol. Microbiol. 93, 464-478, doi: 10.1111/mmi.12670 (2014).
25. Triplett, E. W. & Sadowsky, M. Genetics of competition for nodulation of legumes. Annu. Rev. Microbiol. 46, 399-428, doi: 10.1146/annurev.mi.46.100192.002151 (1992).
26. Friesen, M. L. Widespread fitness alignment in the legume-rhizobium symbiosis. New Phytol 194, 1096-1111, doi: 10.1111/nph.2012.194.issue-4 (2012).
27. Hahn, M. & Studer, D. Competitiveness of a nif-Bradyrhizobium japonicum mutant against the wild-Type strain. FEMS Microbiol. Lett. 33, 143-148 (1986).
28. Gordon, B. R. et al. Decoupled genomic elements and the evolution of partner quality in nitrogen-fixing rhizobia. Ecol. Evol 6(5), 1317-1327, doi: 10.1002/ece3.2016.6.issue-5 (2016).
29. West, S. A., Kiers, E. T., Simms, E. L. & Denison, R. F. Sanctions and mutualism stability: why do rhizobia fix nitrogen? Proc. R. Soc. B 269, 685-94, doi: 10.1098/rspb.2001.1878 (2002).
30. Oono, R., Denison, R. & Kiers, E. Controlling the reproductive fate of rhizobia: how universal are legume sanctions? New Phytol 183, 967-979, doi: 10.1111/nph.2009.183.issue-4 (2009).
31. Marco, D. E. et al. An experimental and modelling exploration of the host-sanction hypothesis in legume-rhizobia mutualism. J. Theor. Biol. 259, 423-33, doi: 10.1016/j.jtbi.2009.03.033 (2009).
32. Bshary, R. & Schäffer, D. Choosy reef fish select cleaner fish that provide high-quality service. Anim. Behav. 63, 557-564, doi: 10.1006/anbe.2001.1923 (2002).
33. Pellmyr, O. & Huth, C. J. Evolutionary stability of mutualism between yuccas and yucca moths. Nature 372, 257-260, doi: 10.1038/372257a0 (1994).
34. Tarachai, Y., Compton, S. G. & Trisonthi, C. The benefits of pollination for a fig wasp. Symbiosis 45, 29-32 (2008).
35. Oldroyd, G. E. D. & Downie, J. A. Calcium, kinases and nodulation signalling in legumes. Nat. Rev. Mol. Cell Biol. 5, 566-576, doi: 10.1038/nrm1424 (2004).
36. Garg, N. Symbiotic nitrogen fixation in legume nodules: process and signaling. A review. Agron. Sustain. Dev. 27, 59-68, doi: 10.1051/agro:2006030 (2007).
37. Murray, J. D. Invasion by invitation: rhizobial infection in legumes. Mol. Plant. Microbe. Interact. 24, 631-639, doi: 10.1094/MPMI-08-10-0181 (2011).
38. Yang, S., Tang, F., Gao, M., Krishnan, H. B. & Zhu, H. R gene-controlled host specificity in the legume-rhizobia symbiosis. Proc. Natl. Acad. Sci. USA. 107, 18735-18740, doi: 10.1073/pnas.1011957107 (2010).
39. Lira, M. A., Nascimento, L. R. S. & Fracetto, G. G. M. Legume-rhizobia signal exchange: Promiscuity and environmental effects. Front. Microbiol 6, 1-9 (2015).
40. Jones, K. M. et al. Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti or an exopolysaccharide-deficient mutant. Proc. Natl. Acad. Sci. U. S. A. 105, 704-709, doi: 10.1073/pnas.0709338105 (2008).
41. Via, V. D., Zanetti, M. E. & Blanco, F. How legumes recognize rhizobia. Plant Signal. Behav 11, e1120396, doi: 10.1080/15592324.2015.1120396 (2015).
42. Young, J. P. & Johnston, A. W. The evolution of specificity in the legume-rhizobium symbiosis. Trends Ecol. Evol. 4, 341-349, doi: 10.1016/0169-5347(89)90089-X (1989).
43. Barrett, L. G., Zee, P. C., Bever, J. D., Miller, J. T. & Thrall, P. H. Evolutionary history shapes patterns of mutualistic benefit in Acacia-rhizobial interactions. Evolution (N. Y). (pp. 1473-1485 (2016).
44. Terpolilli, J. J., Hood, G. A. & Poole, P. S. What determines the efficiency of N2-fixing Rhizobium-legume symbioses? Adv. Microb. Physiol 60, 325-89, doi: 10.1016/B978-0-12-398264-3.00005-X (2012).
45. Downie, J. A. The roles of extracellular proteins, polysaccharides and signals in the interactions of rhizobia with legume roots. FEMS Microbiol. Rev. 34, 150-170, doi: 10.1111/j.1574-6976.2009.00205.x (2010).
46. Batstone, R. T., Dutton, E. M., Wang, D., Yang, M. & Frederickson, M. E. The evolution of symbiont preference traits in the model legume Medicago truncatula. New Phytol. 213, 1850-1861, doi: 10.1111/nph.14308 (2016).
47. Grillo, M. A., Mita, S., De, Burke, P. V., Sol, K. L. S. & Heath, K. D. Intrapopulation genomics in a model mutualist: Population structure and candidate symbiosis genes under selection in Medicago truncatula. Evolution (N. Y) 70, 2704-2717 (2016).
48. Yoder, J. B. Understanding the coevolutionary dynamics of mutualism with population genomics. Am. J. Bot. 103, 1742-1752, doi: 10.3732/ajb.1600154 (2016).
49. Steidinger, B. S. & Bever, J. D. Host discrimination in modular mutualisms: A theoretical framework for meta-populations of mutualists and exploiters. Proc. R. Soc. B 283, 20152428, doi: 10.1098/rspb.2015.2428 (2016).
50. Zgadzaj, R., James, E. K., Kelly, S., Kawaharada, Y. & De, N. Infection of Nodules by Symbiotic and Endophytic Bacteria. PLoS Genet. 11, 1-21, doi: 10.1371/journal.pgen.1005280 (2015).
51. Moawad, H. A., Ellis, W. R. & Schmidt, E. L. Rhizosphere response as a factor in competition among three serogroups of indigenous Rhizobium japonicum for nodulation of field-grown soybeans. Appl. Environ. Microbiol. 47, 607-612 (1984).
52. Sánchez-Cañizares, C. & Palacios, J. Construction of a marker system for the evaluation of competitiveness for legume nodulation in Rhizobium strains. J. Microbiol. Methods 92, 246-249, doi: 10.1016/j.mimet.2012.12.022 (2013).
53. Young, J. P. W. et al. The genome of Rhizobium leguminosarum has recognizable core and accessory components. Genome Biol. 7, R34, doi: 10.1186/gb-2006-7-4-r34 (2006).
54. Fischer, H. M. Genetic regulation of nitrogen fixation in rhizobia. Microbiol. Rev. 58, 352-386 (1994).
55. Buchanan-Wollaston, V. Generalized transduction in Rhizobium meliloti. J. Gen. Microbiol. 112, 135-142, doi: 10.1099/00221287-112-1-135 (1979).
56. Beringer, J. E. R factor transfer in Rhizobium leguminosarum. J. Gen. Microbiol 84, 188-198, doi: 10.1099/00221287-84-1-188 (1974).
57. Poole, P. S., Blyth, A., Reid, C. J. & Walters, K. Myo-inositol catabolism and catabolite regulation in Rhizobium leguminosarum bv. viciae. Microbiology 140, 2787-2795, doi: 10.1099/00221287-140-10-2787 (1994).
58. Sessitsch, A., Wilson, K. J., Akkermans, A. D. L. & De Vos, W. M. Simultaneous detection of different Rhizobium strains marked with either the Escherichia coli gusA gene or the Pyrococcus furiosus celB gene. Appl. Environ. Microbiol. 62, 4191-4194 (1996).
59. Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675, doi: 10.1038/nmeth.2089 (2012).
60. R Core Team. R: A language and environment for statistical computing (2013).
61. Johnston, A. W. & Beringer, J. E. Identification of the rhizobium strains in pea root nodules using genetic markers. J. Gen. Microbiol. 87, 343-350, doi: 10.1099/00221287-87-2-343 (1975).
62. Prentki, P. & Krisch, H. M. In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29, 303-313, doi: 10.1016/0378-1119(84)90059-3 (1984).
63. Quandt, J. & Hynes, M. F. Versatile suicide vectors which allow direct selection for gene replacement in Gram-negative bacteria. Gene 127, 15-21, doi: 10.1016/0378-1119(93)90611-6 (1993).