Evolution of bradyrhizobium-aeschynomene mutualism: Living testimony of the ancient world or highly evolved state?

Plant and Cell Physiology

Volumn 53, Issue 12, 2012, Pages 2000-2007

  Okubo, Takashi ^a   Fukushima, Shohei ^a   Minamisawa, Kiwamu ^a  

^a TOHOKU UNIVERSITY   (Japan)

Author keywords

Aeschynomene; Bradyrhizobium; Co evolution; Endophyte; Nod factors; Nodulation

Indexed keywords

BIOLOGICAL MODEL; BRADYRHIZOBIUM; CYTOLOGY; ENDOPHYTE; EVOLUTION; FABACEAE; GENETICS; MICROBIOLOGY; NITROGEN FIXATION; NODULATION; PHOTOSYNTHESIS; PHYLOGENY; PHYSIOLOGY; REVIEW; SYMBIOSIS;

BIOLOGICAL EVOLUTION; BRADYRHIZOBIUM; ENDOPHYTES; FABACEAE; MODELS, BIOLOGICAL; NITROGEN FIXATION; PHOTOSYNTHESIS; PHYLOGENY; PLANT ROOT NODULATION; ROOT NODULES, PLANT; SYMBIOSIS;

AESCHYNOMENE INDICA; BACTERIA (MICROORGANISMS); BRADYRHIZOBIACEAE; BRADYRHIZOBIUM; RHIZOBIACEAE;

EID: 84870837361     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcs150     Document Type: Review

References (52)

1. Akiyama, K., Ogasawara, S., Ito, S. and Hayashi, H. (2010) Structural requirements of strigolactones for hyphal branching in AM fungi. Plant Cell Physiol. 51: 1104-1117.
2. Anda, M., Ikeda, S., Eda, S., Okubo, T., Sato, S., Tabata, S. et al. (2011) Isolation and genetic characterization of Aurantimonas and Methylobacterium strains from stems of hypernodulated soybeans. Microbes Environ. 26: 172-180.
3. Arrighi, J.F., Cartieaux, F., Brown, S.C., Rodier-Goud, M., Boursot, M., Fardoux, J. et al. (2012) Aeschynomene evenia, a model plant for studying the molecular genetics of the nod-independent rhizobium-legume symbiosis. Mol. Plant Microbe Interact. 25: 851-861.
4. Boogerd, F.C. and van Rossum, D. (1997) Nodulation of groundnut by Bradyrhizobium: a simple infection process by crack entry. FEMS Microbiol. Rev. 21: 5-27.
5. Bonaldi, K., Gherbi, H., Franche, C., Bastien, G., Fardoux, J., Barker, D. et al. (2011) The Nod factor-independent symbiotic signaling pathway: development of Agrobacterium rhizogenes-mediated transformation for the legume Aeschynomene indica. Mol. Plant Microbe Interact. 23: 1537-1544.
6. Bonaldi, K., Gourion, B., Fardoux, J., Hannibal, L., Cartieaux, F., Boursot, M. 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.
7. Borjigin, N., Furukawa, K., Shimoda, Y., Tabata, S., Sato, S., Eda, S. et al. (2011) Identification of Mesorhizobium loti genes relevant to symbiosis by using signature-tagged mutants. Microbes Environ. 26: 165-171.
8. Chaintreuil, C., Giraud, E., Prin, Y., Lorquin, J., Ba, A., Gillis, M. et al. (2000) Photosynthetic bradyrhizobia are natural endophytes of the African wild rice Oryza breviligulata. Appl. Environ. Microbiol. 66: 5437-5447.
9. D'Haeseleer, K., De Keyser, A., Goormachtig, S. and Holsters, M. (2010) Transcription factor MtATB2: about nodulation, sucrose and senescence. Plant Cell Physiol. 51: 1416-1424.
10. Djedidi, S., Yokoyama, T., Ohkama-Ohtsu, N., Risal, C.P., Abdelly, C. and Sekimoto, H. (2011) Stress tolerance and symbiotic and phylogenic features of root nodule bacteria associated with Medicago species in different bioclimatic regions of Tunisia. Microbes Environ. 26: 36-45.
11. Doyle, J.J. and Luckow, M.A. (2003) The rest of the iceberg. Legume diversity and evolution in a phylogenetic context. Plant Physiol. 131: 900-910.
12. Giraud, E., Hannibal, L., Fardoux, J., Vermeglio, A. and Dreyfus, B. (2000) Effect of Bradyrhizobium photosynthesis on stem nodulation of Aeschynomene sensitiva. Proc. Natl Acad. Sci. USA 97: 14795-14800.
13. Giraud, E., Moulin, L., Vallenet, D., Barbe, V., Cytryn, E., Avarre, J.C. et al. (2007) Legumes symbioses: absence of Nod genes in photosynthetic bradyrhizobia. Science 316: 1307-1312.
14. Gourion, B., Delmotte, N., Bonaldi, K., Nouwen, N., Vorholt, J.A. and Giraud, E. (2011) Bacterial RuBisCO is required for efficient Bradyrhizobium/Aeschynomene symbiosis. PLoS One 6: e21900. González-Sama, A., Lucas, M.M., de Felipe, M.R. and Pueyo, J.J. (2004) An unusual mechanism of infection and nodule morphogenesis in lupin (Lupinus albus) lead to a unique nodule type. New Phytol. 163: 371-380.
15. Gorlach, K., Shingaki, R., Morisaki, H. and Hattori, T. (1994) Construction of eco-collection of paddy field soil bacteria for population analysis. J. Gen. Appl. Microbiol. 40: 509-517.
16. Ikeda, S., Okubo, T., Anda, M., Nakashita, H., Yasuda, M., Sato, S. et al. (2010) Community-and genome-based views of plant-associated bacteria: plant-bacterial interactions in soybean and rice. Plant Cell Physiol. 51: 1398-1410.
17. Ikeda, S., Okubo, T., Takeda, N., Banba, M., Sasaki, K., Imaizumi-Anraku, H. et al. (2011) The genotype of the calcium/calmodulin-dependent protein kinase gene (CCaMK) determines bacterial community diversity in rice roots under paddy and upland field conditions. Appl. Environ. Microbiol. 77: 4399-4405.
18. Indrasumunar, A., Kereszt, A., Searle, I., Miyagi, M., Li, D., Nguyen, C.D. et al. (2010) Inactivation of duplicated nod factor receptor 5 (NFR5) genes in recessive loss-of-function non-nodulation mutants of allotetraploid soybean (Glycine max L. Merr.). Plant Cell Physiol. 51: 201-214.
19. Isawa, T., Yasuda, M., Awazaki, H., Minamisawa, K., Shinozaki, S. and Nakashita, H. (2010) Azospirillum sp. strain B510 enhances rice growth and yield. Microbes Environ. 25: 58-61.
20. Itakura, M., Saeki, K., Omori, H., Yokoyama, T., Kaneko, T. et al. (2009) Genomic comparison of Bradyrhizobium japonicum strains with different symbiotic nitrogen-fixing capabilities and other Bradyrhizobiaceae members. ISME J. 3: 326-339.
21. Kaga, H., Mano, H., Tanaka, F., Watanabe, A., Kaneko, S. and Morisaki, H. (2009) Rice seeds as sources of endophytic bacteria. Microbes Environ. 24: 154-162.
22. Kawaguchi, M. and Minamisawa, K. (2010) Plant-microbe communications for symbiosis. Plant Cell Physiol. 51: 1377-1380.
23. Kobae, Y. and Hata, S. (2010) Dynamics of periarbuscular membranes visualized with a fluorescent phosphate transporter in arbuscular mycorrhizal roots of rice. Plant Cell Physiol. 51: 341-353.
24. Kobae, Y., Tamura, Y., Takai, S., Banba, M. and Hata, S. (2010) Localized expression of arbuscular mycorrhiza-inducible ammonium transporters in soybean. Plant Cell Physiol. 51: 1411-1415.
25. Kouchi, H., Imaizumi-Anraku, H., Hayashi, M., Hakoyama, T., Nakagawa, T., Umehara, Y. et al. (2010) How many peas in a pod? Legume genes responsible for mutualistic symbioses underground. Plant Cell Physiol. 51: 1381-1397.
26. Kucho, K., Hay, A.E. and Normand, P. (2010) The determinants of the actinorhizal symbiosis. Microbes Environ. 25: 241-252.
27. Lavin, M., Pennington, R.T., Klitgaard, B.B., Sprent, J.I., de Lima, H.C. and Gasson, P.E. (2001) The dalbergioid legumes (Fabaceae): delimitation of a pantropical monophyletic clade. Amer. J. Bot. 88: 503-533.
28. Lim, B.L. (2010) TonB-dependent receptors in nitrogen-fixing bacteria. Microbes Environ. 25: 67-74.
29. Lim, C.W., Lee, Y.W. and Hwang, C.H. (2011) Soybean noduleenhanced CLE peptides in roots act as signals in GmNARKmediated nodulation suppression. Plant Cell Physiol. 52: 1613-1627.
30. Madsen, L.H., Tirichine, L., Jurkiewicz, A., Sullivan, J.T., Heckmann, A.B., Bek, A.S. et al. (2010) The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat. Commun. 1: 10.
31. Mano, H. and Morisaki, H. (2008) Endophytic bacteria in the rice plant. Microbes Environ. 23: 109-117.
32. Maruya, J. and Saeki, K. (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 Physiol. 51: 1443-1452.
33. Masuda, S., Eda, S., Sugawara, C., Mitsui, H. and Minamisawa, K. (2010) The cbbL gene is required for thiosulfate-dependent autotrophic growth of Bradyrhizobium japonicum. Microbes Environ. 25: 220-223.
34. Miche, L., Moulin, L., Chaintreuil, C., Contreras-Jimenez, J.L., Munive-Hernandez, J.A., 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.
35. Mochida, K. and Shinozaki, K. (2010) Genomics and bioinformatics resources for crop improvement. Plant Cell Physiol. 51: 497-523.
36. Mochida, K. and Shinozaki, K. (2011) Advances in omics and bioinformatics tools for systems analyses of plant functions. Plant Cell Physiol. 52: 2017-2038.
37. Mornico, D., Miché, L., Béna, G., Nouwen, N., Verméglio, A., Vallenet, D. et al. (2012) Comparative genomics of Aeschynomene symbionts: insights into the ecological lifestyle of Nod-independent photosynthetic bradyrhizobia. Genes 3: 35-61.
38. Murakami, E., Nagata, M., Shimoda, Y., Kucho, K., Higashi, S., Abe, M. et al. (2011) Nitric oxide production induced in roots of Lotus japonicus by lipopolysaccharide from Mesorhizobium loti. Plant Cell Physiol. 52: 610-617.
39. Ohkama-Ohtsu, N. and Wasaki, J. (2010) Recent progress in plant nutrition research: cross-talk between nutrients, plant physiology and soil microorganisms. Plant Cell Physiol. 51: 1255-1264.
40. Ohta, H. and Hattori, T. (1983) Agromonas oligotrophica gen. nov., sp. nov., a nitrogen-fixing oligotrophic bacterium. Antonie Van Leeuwenhoek 49: 429-446.
41. Okubo, T., Tsukui, T., Maita, H., Okamoto, S., Oshima, K., Fujisawa, T. et al. (2012) Complete genome sequence of Bradyrhizobium sp. S23321: insights into symbiosis evolution in soil oligotrophs. Microbes Environ. 27: 306-315.
42. Oono, R., Denison, R.F. and Kiers, E.T. (2009) Controlling the reproductive fate of rhizobia: how universal are legume sanctions?. New Phytol. 183: 967-979.
43. Oono, R., Schmitt, I., Sprent, J.I. and Denison, R.F. (2010) Multiple evolutionary origins of legume traits leading to extreme rhizobial differentiation. New Phytol. 187: 508-520.
44. Pueppke, S.G. and Broughton, W.J. (1999) Rhizobium sp. strain NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges. Mol. Plant Microbe Interact. 12: 293-318.
45. Qin, H., Gu, Q., Zhang, J., Sun, L., Kuppu, S., Zhang, Y. et al. (2011) Regulated expression of an isopentenyltransferase gene (IPT) in peanut significantly improves drought tolerance and increases yield under field conditions. Plant Cell Physiol. 52: 1904-1914.
46. Rasolomampianina, R., Bailly, X., Fetiarison, R., Rabevohitra, R., Béna, G., Ramaroson, L. et al. (2005) Nitrogen-fixing nodules from rose wood legume trees (Dalbergia spp.) endemic to Madagascar host seven different genera belonging to alpha-and beta-Proteobacteria. Mol. Ecol. 14: 4135-4146.
47. Sarr, P.S., Yamakawa, T., Fujimoto, S., Saeki, Y., Thao, H.T. and Myint, A.K. (2009) Phylogenetic diversity and symbiotic effectiveness of root-nodulating bacteria associated with cowpea in the South-West area of Japan. Microbes Environ 24: 105-112.
48. Sprent, J.I. (1989) Which steps are essential for the formation of functional legume nodules?. New Phytol. 111: 129-153.
49. Sprent, J.I. and James, E.K. (2007) Legume evolution: where do nodules and mycorrhizas fit in?. Plant Physiol. 144: 575-581.
50. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731-2739.
51. Yokota, K., Soyano, T., Kouchi, H. and Hayashi, M. (2010) Function of GRAS proteins in root nodule symbiosis is retained in homologs of a non-legume, rice. Plant Cell Physiol. 51: 1436-1442.
52. Yoshida, C., Funayama-Noguchi, S. and Kawaguchi, M. (2010) Plenty, a novel hypernodulation mutant in Lotus japonicus. Plant Cell Physiol. 51: 1425-1435.