Cell autonomous sanctions in legumes target ineffective rhizobia in nodules with mixed infections

American Journal of Botany

Volumn 104, Issue 9, 2017, Pages 1299-1312

  Regus, John U ^a   Quides, Kenjiro W ^a   O’Neill, Matthew R ^a   Suzuki, Rina ^a   Savory, Elizabeth A ^b   Chang, Jeff H ^b   Sachs, Joel L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b OREGON STATE UNIVERSITY   (United States)

Author keywords

Bradyrhizobium; Coinfection; Fabaceae; Host control; Induced nodule senescence; Legume rhizobium mutualism; Mesorhizobium; Nitrogen fixation; Programmed cell death; Symbiont cheating

Indexed keywords

CELLS AND CELL COMPONENTS; FITNESS; INFECTIVITY; LEGUME; MUTUALISM; NITROGEN FIXATION; RHIZOBACTERIUM; SENESCENCE; SURVIVAL; SYMBIONT;

BRADYRHIZOBIUM; FABACEAE; LOTUS CORNICULATUS VAR. JAPONICUS; MESORHIZOBIUM; RHIZOBIUM;

BIOLOGICAL MODEL; BRADYRHIZOBIUM; GROWTH, DEVELOPMENT AND AGING; LOTUS (GENUS); MICROBIOLOGY; NODULATION; PHYSIOLOGY; ULTRASTRUCTURE;

BRADYRHIZOBIUM; LOTUS; MODELS, BIOLOGICAL; ROOT NODULES, PLANT;

EID: 85030688977     PISSN: 00029122     EISSN: None     Source Type: Journal    
DOI: 10.3732/ajb.1700165     Document Type: Article

References (86)

1. Allan, G. J., and J. M. Porter. 2000. Tribal delimitation and phylogenetic relationships of Loteae and Coronilleae (Faboideae: Fabaceae) with special reference to Lotus: Evidence from nuclear ribosomal ITS sequences. American Journal of Botany 87: 1871–1881.
2. Amarger, N. 1981. Competition for nodule formation between effective and ineffective strains of Rhizobium meliloti. Soil Biology & Biochemistry 13: 475–480.
3. Banba, M., A. B. M. Siddique, H. Kouchi, K. Izui, and S. Hata. 2001. Lotus japonicus forms early senescent root nodules with Rhizobium etli. Molecular Plant-Microbe Interactions 14: 173–180.
4. Brockwell, J., E. A. Schwinghamer, and R. R. Gault. 1977. Ecological studies of root-nodule bacteria introduced into field environments. V. A critical examination of stability of antigenic and streptomycin-resistance markers for identification of strains of Rhizobium trifolii. Soil Biology & Biochemistry 9: 19–24.
5. Bromfield, E. S. P., and D. G. Jones. 1980. A strain marker in Rhizobium trifolii based on the absorption of congo red. Zentralblatt fur Bakteriologie, Parasitenkunde, Infektionskrankheiten und Hygiene. Zweite Naturwissenschaftliche Abteilung: Mikrobiologie der Landwirtschaft der Technologie und des Umweltschutzes 135: 290–295.
6. Burdon, J. J., A. H. Gibson, S. D. Searle, M. J. Woods, and J. Brockwell. 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.
7. Chang, J. H., J. M. Urbach, T. F. Law, L. W. Arnold, A. Hu, S. Gombar, S. R. Grant, et al. 2005. A high-throughput, near-saturating screen for type III effector genes from Pseudomonas syringae. Proceedings of the National Academy of Sciences, USA 102: 2549–2554.
8. Checcucci, A., E. Azzarello, M. Bazzicalupo, M. Galardini, A. Lagomarsino, S. Mancuso, L. Marti, et al. 2016. Mixed nodule infection in Sinorhizobium meliloti–Medicago sativa symbiosis suggests the presence of cheating behavior. Frontiers in Plant Science 7: 835.
9. Chua, K. Y., C. E. Pankhurst, P. E. MacDonald, D. H. Hopcroft, B. D. W. Jarvis, and D. B. Scott. 1985. Isolation and characterization of transposon Tn5-induced symbiotic mutants of Rhizobium loti. Journal of Bacteriology 162: 335–343.
10. Chungopast, S., P. Thapanapongworakul, H. Matsuura, D. Tan Van, T. Asahi, K. Tada, S. Tajima, and M. Nomura. 2014. Glutamine synthetase I-deficiency in Mesorhizobium loti differentially affects nodule development and activity in Lotus japonicus. Journal of Plant Physiology 171: 104–108.
11. Collins, M. T., J. E. Thies, and L. K. Abbott. 2002. Diversity and symbiotic effectiveness of Rhizobium leguminosarum bv. trifolii isolates from pasture soils in south-western Australia. Australian Journal of Soil Research 40: 1319–1329.
12. Degtjareva, G. V., T. E. Kramina, D. D. Sokoloff, T. H. Samigullin, C. M. Valiejo-Roman, and A. S. Antonov. 2006. Phylogeny of the genus Lotus (Leguminosae, Loteae): Evidence from nrITS sequences and morphology. Canadian Journal of Botany 84: 813–830.
13. Denison, R. F. 2000. Legume sanctions and the evolution of symbiotic cooperation by rhizobia. American Naturalist 156: 567–576.
14. Denison, R. F., and E. T. Kiers. 2004. Lifestyle alternatives for rhizobia: Mutualism, parasitism, and forgoing symbiosis. FEMS Microbiology Letters 237: 187–193.
15. Denton, M. D., D. R. Coventry, W. D. Bellotti, and J. G. Howieson. 2000. Distribution, abundance and symbiotic effectiveness of Rhizobium leguminosarum bv. trifolii from alkaline pasture soils in South Australia. Australian Journal of Experimental Agriculture 40: 25–35.
16. Devine, T. E., and L. D. Kuykendall. 1996. Host genetic control of symbiosis in soybean (Glycine max L.). Plant and Soil 186: 173–187.
17. Devine, T. E., L. D. Kuykendall, and J. J. O’Neill. 1990. The Rj4 allele in soybean represses nodulation by chlorosis-inducing bradyrhizobia classified as DNA homology group II by antibiotic resistance profiles. Theoretical and Applied Genetics 80: 33–37.
18. Frederickson, M. E. 2013. Rethinking mutualism stability: Cheaters and the evolution of sanctions. Quarterly Review of Biology 88: 269–295.
19. Friesen, M. L. 2012. Widespread fitness alignment in the legume–Rhizobium symbiosis. New Phytologist 194: 1096–1111.
20. Friesen, M. L., and A. Mathias. 2010. Mixed infections may promote diversification of mutualistic symbionts: Why are there ineffective rhizobia? Journal of Evolutionary Biology 23: 323–334.
21. Gage, D. J. 2002. Analysis of infection thread development using GFP- and DsRed-expressing Sinorhizobium meliloti. Journal of Bacteriology 184: 7042–7046.
22. 2 fixation, carbon metabolism, and oxidative damage in nodules of dark-stressed common bean plants. Plant Physiology 113: 1193–1201.
23. González, E. M., P. M. Aparicio-Tejo, A. J. Gordon, F. R. Minchin, M. Royuela, and C. Arrese-Igor. 1998. Water-deficit effects on carbon and nitrogen metabolism of pea nodules. Journal of Experimental Botany 49: 1705–1714.
24. Grillo, M. A., J. R. Stinchcombe, and K. D. Heath. 2016. Nitrogen addition does not influence pre-infection partner choice in the legume–rhizobium symbiosis. American Journal of Botany 103: 1763–1770.
25. Gubry-Rangin, C., M. Garcia, and G. Béna. 2010. Partner choice in Medicago truncatula–Sinorhizobium symbiosis. Proceedings of the Royal Society, B, Biological Sciences 277: 1947–1951.
26. Haag, A. F., M. Baloban, M. Sani, B. Kerscher, O. Pierre, A. Farkas, R. Longhi, et al. 2011. Protection of Sinorhizobium against host cysteine-rich antimicro-bial peptides is critical for symbiosis. PLoS Biology 9: e1001169.
27. − Bradyrhizobium japonicum mutant against the wild-type strain. FEMS Microbiology Letters 33: 143–148.
28. Handberg, K., and J. Stougaard. 1992. Lotus japonicus, an autogamous, diploid legume species for classical and molecular genetics. Plant Journal 2: 487–496.
29. Heath, K. D., and P. Tiffin. 2009. Stabilizing mechanisms in a legume–rhizobium mutualism. Evolution 63: 652–662.
30. Johnston, A. W. B., and J. E. Beringer. 1975. Identification of rhizobium strains in pea root nodules using genetic markers. Journal of General Microbiology 87: 343–350.
31. Jones, K. M., H. Kobayashi, B. W. Davies, M. E. Taga, and G. C. Walker. 2007. How rhizobial symbionts invade plants: The Sinorhizobium–Medicago model. Nature Reviews. Microbiology 5: 619–633.
32. Kawaguchi, M. 2000. Lotus japonicus ‘Miyakojima’ MG-20: An early-flowering accession suitable for indoor handling. Journal of Plant Research 113: 507–509.
33. Kembel, S. W., and J. F. Cahill Jr. 2005. Plant phenotypic plasticity below-ground: A phylogenetic perspective on root foraging trade-offs. American Naturalist 166: 216–230.
34. Kiers, E. T., R. F. Denison, A. Kawakita, and E. A. Herre. 2011. The biological reality of host sanctions and partner fidelity. Proceedings of the National Academy of Sciences, USA 108: E7.
35. Kiers, E. T., R. A. Rousseau, and R. F. Denison. 2006. Measured sanctions: Legume hosts detect quantitative variation in rhizobium cooperation and punish accordingly. Evolutionary Ecology Research 8: 1077–1086.
36. Kiers, E. T., R. A. Rousseau, S. A. West, and R. F. Denison. 2003. Host sanctions and the legume–rhizobium mutualism. Nature 425: 78–81.
37. Labandera, C. A., and J. M. Vincent. 1975. Competition between an introduced strain and native Uruguayan strains of Rhizobium trifolii. Plant and Soil 42: 327–347.
38. Maekawa, T., M. Maekawa-Yoshikawa, N. Takeda, H. Imaizumi-Anraku, Y. Murooka, and M. Hayashi. 2009. Gibberellin controls the nodulation signaling pathway in Lotus japonicus. Plant Journal 58: 183–194.
39. Marco, D. E., J. P. Carbajal, S. Cannas, R. Pérez-Arnedo, A. Hildalgo-Perea, J. Olivares, J. E. Ruiz-Sainz, and J. Sanjuán. 2009. An experimental and modelling exploration of the host-sanction hypothesis in legume–rhizobia mutualism. Journal of Theoretical Biology 259: 423–433.
40. Maruya, J., and K. Saeki. 2010. The bacA gene homolog, mlr7400, in Mesorhizobium loti MAFF303099 is dispensable for symbiosis with Lotus japonicus but partially capable of supporting the symbiotic function of bacA in Sinorhizobium meliloti. Plant & Cell Physiology 51: 1443–1452.
41. Mathu, S., L. Herrmann, P. Pypers, V. Matiru, R. Mwirichia, and D. Lesueur. 2012. Potential of indigenous bradyrhizobia versus commercial inoculants to improve cowpea (Vigna unguiculata L. Walp.) [sic] and green gram (Vigna radiata L. Wilczek.) [sic] yields in Kenya. Soil Science and Plant Nutrition 58: 750–763.
42. Maunoury, N., M. Redondo-Nieto, M. Bourcy, W. Van de Velde, B. Alunni, P. Laporte, P. Durand, et al. 2010. Differentiation of symbiotic cells and endosymbionts in Medicago truncatula nodulation are coupled to two tran-scriptome-switches. PLoS One 5: e0009519.
43. Mergaert, P., T. Uchiumi, B. Alunni, G. Evanno, A. Cheron, O. Catrice, A.-E. Mausset, et al. 2006. Eukaryotic control on bacterial cell cycle and differentiation in the Rhizobium–legume symbiosis. Proceedings of the National Academy of Sciences, USA 103: 5230–5235.
44. Moawad, M., and E. L. Schmidt. 1987. Occurrence and nature of mixed infections in nodules of field-grown soybeans (Glycine max). Biology and Fertility of Soils 5: 112–114.
45. Mueller, U. G., and J. L. Sachs. 2015. Engineering microbiomes to improve plant and animal health. Trends in Microbiology 23: 606–617.
46. Oono, R., C. G. Anderson, and R. F. Denison. 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, B, Biological Sciences 278: 2698–2703.
47. Oono, R., R. F. Denison, and E. T. Kiers. 2009. Controlling the reproductive fate of rhizobia: How universal are legume sanctions? New Phytologist 183: 967–979.
48. Paau, A. S., C. B. Bloch, and W. J. Brill. 1980. Developmental fate of Rhizobium meliloti bacteroids in alfalfa nodules. Journal of Bacteriology 143: 1480–1490.
49. Pérez Guerra, J. C., G. Coussens, A. De Keyser, R. De Rycke, S. De Bodt, W. Van De Velde, S. Goormachtig, and M. Holsters. 2010. Comparison of developmental and stress-induced nodule senescence in Medicago truncatula. Plant Physiology 152: 1574–1584.
50. Porter, S. S., and E. L. Simms. 2014. Selection for cheating across disparate environments in the legume–rhizobium mutualism. Ecology Letters 17: 1121–1129.
51. Prell, J., J. P. White, A. Bourdes, S. Bunnewell, R. J. Bongaerts, and P. S. Poole. 2009. Legumes regulate Rhizobium bacteroid development and persistence by the supply of branched-chain amino acids. Proceedings of the National Academy of Sciences, USA 106: 12477–12482.
52. Puppo, A., K. Groten, F. Bastian, R. Carzaniga, M. Soussi, M. M. Lucas, M. R. de Felipe, et al. 2005. Legume nodule senescence: Roles for redox and hormone signalling in the orchestration of the natural aging process. New Phytologist 165: 683–701.
53. Quigley, P. E., P. J. Cunningham, M. Hannah, G. N. Ward, and T. Morgan. 1997. Symbiotic effectiveness of Rhizobium leguminosarum bv. trifolii collected from pastures in south-western Victoria. Australian Journal of Experimental Agriculture 37: 623–630.
54. Ratcliff, W. C., and R. F. Denison. 2008. Poly-3-hydroxybutyrate (PHB) supports survival and reproduction in starving rhizobia. FEMS Microbiology Letters 65: 391–399.
55. Regus, J. U., K. A. Gano, A. C. Hollowell, and J. L. Sachs. 2014. Efficiency of partner choice and sanctions in Lotus is not altered by nitrogen fertilization. Proceedings of the Royal Society, B, Biological Sciences 281: 20132587.
56. Regus, J. U., K. A. Gano, A. C. Hollowell, V. Sofish, and J. L. Sachs. 2015. Lotus hosts delimit the mutualism–parasitism continuum of Bradyrhizobium. Journal of Evolutionary Biology 28: 447–456.
57. Reid, D. E., B. J. Ferguson, S. Hayashi, Y.-H. Lin, and P. M. Gresshoff. 2011. Molecular mechanisms controlling legume autoregulation of nodulation. Annals of Botany 108: 789–795.
58. Sachs, J. L., M. O. Ehinger, and E. L. Simms. 2010a. Origins of cheating and loss of symbiosis in wild Bradyrhizobium. Journal of Evolutionary Biology 23: 1075–1089.
59. Sachs, J. L., S. W. Kembel, A. H. Lau, and E. L. Simms. 2009. In situ phylogenetic structure and diversity of wild Bradyrhizobium communities. Applied and Environmental Microbiology 75: 4727–4735.
60. Sachs, J. L., U. G. Mueller, T. P. Wilcox, and J. J. Bull. 2004. The evolution of cooperation. Quarterly Review of Biology 79: 135–160.
61. Sachs, J. L., J. E. Russell, and A. C. Hollowell. 2011a. Evolutionary instability of symbiotic function in Bradyrhizobium japonicum. PLoS One 6: e26370.
62. Sachs, J. L., J. E. Russell, Y. E. Lii, K. C. Black, G. Lopez, and A. S. Patil. 2010b. Host control over infection and proliferation of a cheater symbiont. Journal of Evolutionary Biology 23: 1919–1927.
63. Sachs, J. L., R. G. Skophammer, and J. U. Regus. 2011b. Evolutionary transitions in bacterial symbiosis. Proceedings of the National Academy of Sciences, USA 108: 10800–10807.
64. Sato, S., Y. Nakamura, T. Kaneko, E. Asamizu, T. Kato, M. Nakao, S. Sasamoto, et al. 2008. Genome structure of the legume, Lotus japonicus. DNA Research 15: 227–239.
65. Schneider, C. A., W. S. Rasband, and K. W. Eliceiri. 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9: 671–675.
66. Schumpp, O., and W. J. Deakin. 2010. How inefficient rhizobia prolong their existence within nodules. Trends in Plant Science 15: 189–195.
67. Sheehy, J. E., F. R. Minchin, and J. F. Witty. 1983. Biological control of the resistance to oxygen flux in nodules. Annals of Botany 52: 565–571.
68. Shimoda, Y., H. Mitsui, H. Kamimatsuse, K. Minamisawa, E. Nishiyama, Y. Ohtsubo, Y. Nagata, et al. 2008. Construction of signature-tagged mutant library in Mesorhizobium loti as a powerful tool for functional genomics. DNA Research 15: 297–308.
69. Simms, E. L., D. L. Taylor, J. Povich, R. P. Shefferson, J. L. Sachs, M. Urbina, and Y. Tausczik. 2006. An empirical test of partner choice mechanisms in a wild legume–rhizobium interaction. Proceedings of the Royal Society, B, Biological Sciences 273: 77–81.
70. Singleton, P. W., and K. R. Stockinger. 1983. Compensation against ineffective nodulation in soybean. Crop Science 23: 69–72.
71. Soltis, D. E., P. S. Soltis, D. R. Morgan, S. M. Swensen, B. C. Mullin, J. M. Dowd, and P. G. Martin. 1995. Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proceedings of the National Academy of Sciences, USA 92: 2647–2651.
72. Somasegaran, P., and J. Hoben. 1994. Handbook for rhizobia. Springer-Verlag, New York, New York, USA.
73. Tang, J., E. S. P. Bromfield, N. Rodrigue, S. Cloutier, and J. T. Tambong. 2012. Microevolution of symbiotic Bradyrhizobium populations associated with soybeans in east North America. Ecology and Evolution 2: 2943–2961.
74. +-malic enzyme affects nitrogenase activity of Mesorhizobium loti bacteroids in Lotus japonicus nodules. Plant Biotechnology 27: 311–316.
75. Thomas, H. 2013. Senescence, ageing and death of the whole plant. New Phytologist 197: 696–711.
76. Trainer, M. A., and T. C. Charles. 2006. The role of PHB metabolism in the symbiosis of rhizobia with legumes. Applied Microbiology and Biotechnology 71: 377–386.
77. van Berkum, P., P. Elia, Q. Song, and B. D. Eardly. 2012. Development and application of a multilocus sequence analysis method for the identification of genotypes within genus Bradyrhizobium and for establishing nodule occupancy of soybean (Glycine max L. Merr). Molecular Plant-Microbe Interactions 25: 321–330.
78. Van de Velde, W., J. C. Pérez Guerra, A. De Keyser, R. De Rycke, S. Rombauts, N. Maunoury, P. Mergaert, et al. 2006. Aging in legume symbiosis. A molecular view on nodule senescence in Medicago truncatula. Plant Physiology 141: 711–720.
79. Van de Velde, W., G. Zehirov, A. Szatmari, M. Debreczeny, H. Ishihara, Z. Kevei, A. Farkas, et al. 2010. Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327: 1122–1126.
80. van Doorn, W. G. 2011. Classes of programmed cell death in plants, compared to those in animals. Journal of Experimental Botany 62: 4749–4761.
81. Vance, C. P. 2008. Carbon and nitrogen metabolism in legume nodules. In M. J. Dilworth, E. K. James, J. I. Sprent, and W. W. Newton [eds.], Nitrogen-fixing leguminous symbiosis, vol. 7, 293–320. Springer, Dordrecht, Netherlands.
82. Wang, D., J. Griffitts, C. Starker, E. Fedorova, E. Limpens, S. Ivanov, T. Bisseling, and S. Long. 2010. A nodule-specific protein secretory pathway required for nitrogen-fixing symbiosis. Science 327: 1126–1129.
83. West, S. A., E. T. Kiers, I. Pen, and R. F. Denison. 2002a. Sanctions and mutualism stability: When should less beneficial mutualists be tolerated? Journal of Evolutionary Biology 15: 830–837.
84. West, S. A., E. T. Kiers, E. L. Simms, and R. F. Denison. 2002b. Sanctions and mutualism stability: Why do rhizobia fix nitrogen? Proceedings of the Royal Society, B, Biological Sciences 269: 685–694.
85. Weyl, E. G., M. E. Frederickson, D. W. Yu, and N. E. Pierce. 2010. Economic contract theory tests models of mutualism. Proceedings of the National Academy of Sciences, USA 107: 15712–15716.
86. White, J., J. Prell, E. K. James, and P. Poole. 2007. Nutrient sharing between symbionts. Plant Physiology 144: 604–614.