A thaumatin-like protein, Rj4, controls nodule symbiotic specificity in soybean

Plant and Cell Physiology

Volumn 55, Issue 9, 2014, Pages 1679-1689

  Hayashi, Masaki ^a   Shiro, Sokichi ^b,c   Kanamori, Hiroyuki ^a   Mori Hosokawa, Satomi ^a   Sasaki Yamagata, Harumi ^a   Sayama, Takashi ^a   Nishioka, Miki ^a   Takahashi, Masakazu ^d   Ishimoto, Masao ^a   Katayose, Yuichi ^a   Kaga, Akito ^a   Harada, Kyuya ^a   Kouchi, Hiroshi ^a,e   Saeki, Yuichi ^b   Umehara, Yosuke ^a  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b UNIVERSITY OF MIYAZAKI   (Japan)

^c SHIMANE UNIVERSITY   (Japan)

^d NATIONAL AGRICULTURAL RESEARCH CENTER FOR KYUSHU OKINAWA REGION   (Japan)

^e INTERNATIONAL CHRISTIAN UNIVERSITY   (Japan)

Author keywords

Host restriction of nodulation; Nodule symbiotic specificity; Rj gene; Root nodule symbiosis; Soybean; Thaumatin like protein (TLP)

Indexed keywords

THAUMATIN PROTEIN, PLANT; VEGETABLE PROTEIN;

BRADYRHIZOBIUM; CHROMOSOME MAP; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENE LOCUS; GENETICS; GENOTYPE; METABOLISM; MOLECULAR GENETICS; NITROGEN FIXATION; NODULATION; NUCLEOTIDE SEQUENCE; PHENOTYPE; PHYLOGENY; PHYSIOLOGY; PLANT ROOT; SEQUENCE ALIGNMENT; SOYBEAN; SPECIES DIFFERENCE; SYMBIOSIS;

BASE SEQUENCE; BRADYRHIZOBIUM; CHROMOSOME MAPPING; GENE EXPRESSION REGULATION, PLANT; GENETIC LOCI; GENOTYPE; MOLECULAR SEQUENCE DATA; NITROGEN FIXATION; PHENOTYPE; PHYLOGENY; PLANT PROTEINS; PLANT ROOT NODULATION; PLANT ROOTS; ROOT NODULES, PLANT; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SOYBEANS; SPECIES SPECIFICITY; SYMBIOSIS;

EID: 84933049689     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcu099     Document Type: Article

References (47)

1. Caldwell, B. E. (1966) Inheritance of a strain-specific ineffective nodulation in soybeans. Crop Sci. 6:427-428.
2. Caldwell, B. E., Hinson, K. and Johnson, H. W. (1966) A strain-specific ineffective nodulation reaction in the soybean Glycine max L. Merrill. Crop Sci. 6:495-496.
3. Cullimore, J. V., Ranjeva, R. and Bono, J. J. (2001) Perception of lipo-chitooligosaccharidic Nod factors in legumes. Trends Plant Sci. 6:24-30.
4. Deakin, W. J. and Broughton, W. J. (2009) Symbiotic use of pathogenic strategies: rhizobial protein secretion systems. Nat. Rev. Microbiol. 7:312-320.
5. Devine, T. E., Kuykendall, L. D. and O'Neill, J. J. (1988) DNA homology group and the identity of bradyrhizobial strains producing rhizobitoxineinduced foliar chrorosis on soybean. Crop Sci. 28:939-941.
6. D'Haeze, W. and Holsters, M. (2004) Surface polysaccharides enable bacteria to evade plant immunity. Trends Microbiol. 12:555-561.
7. Fierens, E., Gebruers, K., Voet, A. R., De Maeyer, M., Courtin, C. M. and Delcour, J. A. (2009) Biochemical and structural characterization of TLXI, the Triticum aestivum L. thaumatin-like xylanase inhibitor. J. Enzyme Inhib. Med. Chem. 24:646-654.
8. Grenier, J., Potvin, C., Trudel, J. and Asselin, A. (1999) Some thaumatin-like proteins hydrolyse polymeric beta-1, 3-glucans. Plant J. 19:473-480.
9. Hayashi, M., Kitamura, K. and Harada, K. (2009) Genetic mapping of Cgdef gene controlling accumulation of 7S globulin (b-conglycinin) subunits in soybean seeds. J. Hered. 100:802-806.
10. Hayashi, M., Saeki, Y., Haga, M., Harada, K., Kouchi, H. and Umehara, Y. (2012) Rj (rj) genes involved in nitrogen-fixing root nodule formation in soybean. Breed. Sci. 61:544-553.
11. Indrasumunar, A., Kereszt, A., Searle, I., Miyagi, M., Li, D., Nguyen, C. D. T. 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.
12. Indrasumunar, A., Searle, I., Lin, M. H., Kereszt, A., Men, A., Carroll, B. J. et al. (2011) Nodulation factor receptor kinase 1a controls nodule organ number in soybean (Glycine max L. Mrr). Plant J. 65:39-50.
13. Ishizuka, J., Suematsu, Y. and Mizogami, K. (1991a) Preference of Rj-soybean cultivars for Bradyrhizobium japonicum for nodulation. Soil Sci. Plant Nutr. 37:15-21.
14. Ishizuka, J., Yokoyama, A. and Suemasu, Y. (1991b) Relationship between serotypes of Bradyrhizobium japonicum and their compatibility with Rj-cultivars for nodulation. Soil Sci. Plant Nutr. 37:23-30.
15. Jami, S. K., Swathi, A. T., Guruprasad, L. and Kirti, P. B. (2007) Molecular, biochemical and structural characterization of osmotin-like protein from black nightshade (Solanum nigrum). J. Plant Physiol. 164:238-252.
16. Kouchi, H. and Hata, S. (1993) Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. Mol. Gen. Genet. 238:106-119.
17. 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.
18. Kuykendall, L. D. (1987) Isolation and identification of genetically marked strains of nitrogen fixation technology. In Symbiotic Nitrogen Fixation Technology. Edited by Elkan, G. H. pp. 205-220. Marcel Dekker Inc, New York.
19. Liu, J. J., Sturrock, R. and Ekramoddoullah, A. K. (2010) The superfamily of thaumatin-like proteins: its origin, evolution, and expression towards biological function. Plant Cell Rep. 29:419-436.
20. Maekawa, T., Kusakabe, M., Shimoda, Y., Sato, S., Tabata, S., Murooka, Y. et al. (2008) Polyubiquitin promoter-based binary vectors for overexpression and gene silencing in Lotus japonicus. Mol. Plant Microbe Interact. 21:375-382.
21. Maekawa, T., Maekawa-Yoshikawa, M., Takeda, N., Imaizumi-Anraku, H., Murooka., Y. and Hayashi, M. (2009) Gibberellin controls the nodulation signaling pathway in Lotus japonicus. Plant J. 58:183-194.
22. Michelmore, R. W., Paran, I. and Kesseli, R. V. (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc. Natl Acad. Sci. USA 88:9828-9832.
23. Minami, E., Kouchi, H., Cohn, J. R., Ogawa, T. and Stacey, G. (1996) Expression of the early nodulin, ENOD40, in soybean roots in response to various lipo-chitin signal molecules. Plant J. 10:23-32.
24. Murray, J. D. (2011) Invasion by invitation: rhizobial infection in legumes. Mol. Plant Microbe Interact. 24:631-639.
25. Nishimura, R., Hayashi, M., Wu, G. J., Kouchi, H., Imaizumi-Anraku, H., Murakami, Y. et al. (2002) HAR1 mediates systemic regulation of symbiotic organ development. Nature 420:426-429.
26. Okazaki, S., Okabe, S., Higashi, M., Shimoda, Y., Sato, S., Tabata, S. et al. (2010) Identification and functional analysis of type III effector proteins in Mesorhizobium loti. Mol. Plant Microbe Interact. 23:223-234.
27. Okazaki, S., Zehner, S., Hempel, J., Lang, K. and Göttfert, M. (2009) Genetic organization and functional analysis of the type III secretion system of Bradyrhizobium elkanii. FEMS Microbiol. Lett. 295:88-95.
28. Oldroyd, G. E. D. (2013) Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat. Rev. Microbiol. 11:252-263.
29. Osmond, R. I., Hrmova, M., Fontaine, F., Imberty, A. and Fincher, G. B. (2001) Binding interactions between barley thaumatin-like proteins and (1, 3) - beta-D-glucans. Kinetics, specificity, structural analysis and biological implications. Eur. J. Biochem. 268:4190-4199.
30. Radutoiu, S., Madsen, L. H., Madsen, E. B., Jurkiewicz, A., Fukai, E., Quistgaard, E. M. et al. (2007) LysM domains mediate lipochitin-oligosaccharide recognition and Nfr genes extend the symbiotic host range. EMBO J. 26:3923-3935.
31. Saeki, Y., Akagi, I., Takaki, H. and Nagatomo, Y. (2000) Diversity of indigenous Bradyrhizobium strains isolated from three different Rj-soybean cultivars in terms of randomly amplified polymorphic DNA and intrinsic antibiotic resistance. Soil Sci. Plant Nutr. 46:917-926.
32. Searle, I. R., Men, A. E., Laniya, T. S., Buzas, D. M., Iturbe-Ormaetxe, I., Carroll, B. J. et al. (2003) Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase. Science 299:109-112.
33. Shiro, S., Yamamoto, A., Umehara, Y., Hayashi, M., Yoshida, N., Nishiwaki, A. et al. (2012) Effect of Rj genotype and cultivation temperature on the community structure of soybean-nodulating bradyrhizobia. Appl. Environ. Microbiol. 78:1243-1250.
34. Song, Q. J., Marek, L. F., Shoemaker, R. C., Lark, V. C., Concibido, X., Delannay, J. E. et al. (2004) A new integrated genetic linkage map of the soybean. Theor. Appl. Genet. 109:122-128.
35. Spaink, H. P. (1995) The molecular basis of infection and nodulation by rhizobia: the ins and outs of sympathogenesis. Annu. Rev. Phytopathol. 33:345-368.
36. Tachi, H., Fukuda-Yamada, K., Kojima, T., Shiraiwa, M. and Takahara, H. (2009) Molecular characterization of a novel soybean gene encoding a neutral PR-5 protein induced by high-salt stress. Plant Physiol. Biochem. 47:73-79.
37. 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.
38. Tang, F., Yang, S., Liu, J., Gao, M. and Zhu, H. (2014) Fine mapping of the Rj4 locus, a gene controlling nodulation specificity in soybean. Mol. Breed 33:691-700.
39. Trese, A. T. (1995) A single dominant gene in McCall soybean prevents effective nodulation with Rhizobium fredii USDA257. Euphytica 81:279-282.
40. Tsukui, T., Eda, S., Kaneko, T., Sato, S., Okazaki, S., Kakizaki-Chiba, K. et al. (2013) The type III secretion system of Bradyrhizobium japonicum USDA122 mediates symbiotic incompatibility with Rj2 soybean plants. Appl. Environ. Microbiol. 79:1048-1051.
41. Van Der Wel, H. and Loewe, K. (1972) Isolation and characterization of thaumatin I and II, the sweet-tasting proteins from Thaumatococcus daniellii Benth. Eur. J. Biochem. 31:221-225.
42. Van Loon, L. C., Rep, M. and Pieterse, C. M. (2006) Significance of inducible defense-related proteins in infected plants. Annu. Rev. Phytopathol. 44:135-162.
43. Velazhahan, R., Datta, S. K. and Muthukrishnan, S. (1999) The PR-5 family: thaumatin-like proteins in plants. In Pathogenesis-Related Proteins in Plants. Edited by Datta, S. K. and Muthukrishnan, S. pp. 107-129. CRC Press, Boca Raton, FL.
44. Vest, G. (1970) Rj3-a gene conditioning ineffective nodulation in soybean. Crop Sci. 10:34-35.
45. Vest, G. and Caldwell, B. E. (1972) Rj4-a gene conditioning ineffective nodulation in soybean. Crop Sci. 12:692-693.
46. Weiser, G. V., Skipper, H. D. and Wollum, A. G. (1990) Exclusion of inefficient Bradyrhizobium japonicum serogroups by soybean genotypes. Plant Soil 121:99-105.
47. Yang, S., Tang, F., Gao, M., Krishnan, H. B. and Zhu, H. (2010) R gene controlled host specificity in the legume-rhizobia symbiosis. Proc. Natl Acad. Sci. USA 107:18735-18740.