A comparative proteomic analysis of the early response to compatible symbiotic bacteria in the roots of a supernodulating soybean variety

Journal of Proteomics

Volumn 75, Issue 3, 2012, Pages 819-832

  Salavati, Afshin ^a,b   Bushehri, Ali Akbar Shahnejat ^b   Taleei, Alireza ^b   Hiraga, Susumu ^a   Komatsu, Setsuko ^a  

^a NATIONAL INSTITUTE OF CROP SCIENCE   (Japan)

^b UNIVERSITY OF TEHRAN   (Iran)

Author keywords

Proteomics; Root; Soybean; Supernodulating variety; Symbiosis

Indexed keywords

CYTOSOL AMINOPEPTIDASE; GAMMA GLUTAMYL HYDROLASE; GLUCAN ENDO 1,3 BETA GLUCOSIDASE; GLYCOPROTEIN; NODULIN; NODULIN 35; PEROXIDASE; PHOSPHOGLUCOMUTASE; PROTEASOME; PROTEASOME SUBUNIT ALPHA TYPE 6; UNCLASSIFIED DRUG;

ARTICLE; BRADYRHIZOBIUM JAPONICUM; COMPARATIVE PROTEOMICS; CONTROLLED STUDY; DOWN REGULATION; ENERGY YIELD; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; INOCULATION; NODULATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PLANT ROOT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEOMICS; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SOYBEAN; SYMBIOSIS; UPREGULATION;

BACTERIA; BACTERIAL PROTEINS; GENE EXPRESSION REGULATION, BACTERIAL; PLANT ROOTS; PROTEOMICS; SOYBEANS;

BACTERIA (MICROORGANISMS); GLYCINE MAX;

EID: 84355162923     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2011.09.022     Document Type: Article

References (56)

1. Cullimore J.V., Ranjeva R., Bono J.J. Perception of lipo-chitooligosaccharidic Nod factors in legumes. Trends Plant Sci 2001, 6:24-30.
2. Jones K.M., Kobayashi K., Davies B.W., Taga M.E., Walker G.C. How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nat Rev Microbiol 2007, 5:619-633.
3. Brewin N.J. Plant cell wall remodelling in the rhizobium-legume symbiosis. Crit Rev Plant Sci 2004, 23:293-316.
4. Foucher F., Kondorosi E. Cell cycle regulation in the course of nodule organogenesis in Medicago. Plant Mol Biol 2000, 43:773-786.
5. Verma D.P.S., Hong Z. Biogenesis of the peribacteroid membrane in root nodules. Trends Microbiol 1996, 4:364-368.
6. Brewin N.J. Development of the legume root nodule. Annu Rev Cell Biol 1991, 7:126-191.
7. Horchani F., Prevot M., Boscari A., Evangelisti E., Meilhoc E., Bruand C., et al. Both plant and bacterial nitrate reductases contribute to nitric oxide production in Medicago truncatula nitrogen-fixing nodules. Plant Physiol 2011, 155:1023-1036.
8. Stougaard J. Regulators and regulation of legume root nodule development. Plant Physiol 2000, 124:531-540.
9. Kinkema M., Scott P.T., Gresshoff P.M. Legume nodulation: successful symbiosis through short- and long-distance signalling. Funct Plant Biol 2006, 33:1-15.
10. Oka-Kira E., Kawaguchi M. Long-distance signaling to control root nodule number. Curr Opin Plant Biol 2006, 9:496-502.
11. Boller T. Peptide signalling in plant development and self/non-self perception. Curr Opin Plant Biol 2005, 17:116-122.
12. Ferguson B.J., Indrasumunar A., Hayashi S., Lin M.-H., Lin Y.-H., Reid D.E., et al. Molecular analysis of legume nodule development and autoregulation. J Integr Plant Biol 2010, 52:61-76.
13. Carroll B.J., Mcneil D.L., Gresshoff P.M. A supernodulation and nitrate tolerant symbiotic (nts) soybean mutant. Plant Physiol 1985, 78:34-40.
14. Schnabel E., Journet E.P., de Carvalho-Niebel F., Frugoli G.D.J. The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length. Plant Mol Biol 2005, 58:809-822.
15. Shibuya N., Minami E. Oligosaccharide signalling for defence responses in plant. Physiol Mol Plant Pathol 2001, 59:223-233.
16. Takemoto D., Hardham A.R. The cytoskeleton as a regulator and target of biotic interactions in plants. Plant Physiol 2004, 136:3864-3876.
17. 2+ and calmodulin-dependent protein kinase required for bacterial and fungal symbioses. Science 2004, 303:1361-1364.
18. Stacey G., Libault M., Brechenmacher L., Wan J., May G.D. Genetics and functional genomics of legume nodulation. Curr Opin Plant Biol 2006, 9:110-121.
19. Delmotte N., Ahrens C.H., Knief C., Qeli E., Koch M., Fischer H.M., et al. An integrated proteomics and transcriptomics reference data set provides new insights into the Bradyrhizobium japonicum bacteroid metabolism in soybean root nodules. Proteomics 2010, 10:1391-1400.
20. Oehrle N.W., Sarma A.D., Waters J.K., Emerich D.W. Proteomic analysis of soybean nodule cytosol. Phytochemistry 2008, 69:2426-2438.
21. Matamoros M.A., Dalton D.A., Ramos J., Clemente M.R., Rubio M.C., Becana M. Biochemistry and molecular biology of antioxidants in the rhizobia-legume symbiosis. Plant Physiol 2003, 133:499-509.
22. Larrainzar E., Wienkoop S., Weckwerth W., Ladrera R., Arrese-Igor C., Gonzalez E.M. Medicago truncatula root nodule proteome analysis reveals differential plant and bacteroid responses to drought stress. Plant Physiol 2007, 144:1495-1507.
23. Oldroyd G.E.D., Harrison M.J., Paszkowski U. Reprogramming plant cells for endosymbiosis. Science 2009, 324:753-754.
24. Poppa C., Ott T. Regulation of signal transduction and bacterial infection during root nodule symbiosis. Curr Opin Plant Biol 2011, 14:1-10.
25. Nakamura T., Nakayama N., Yamamoto R., Shimamura S., Kim Y., Hiraga S., et al. Nitrogen utilization in the supernodulating soybean variety "Sakukei 4" and its parental varieties, "Enrei" and "Tamahomare". Plant Prod Sci 2010, 13:123-131.
26. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
27. Schmutz J., Cannon S.B., Schlueter J., Ma J., Mitros T., Nelson W., et al. Genome sequence of the palaeopolyploid soybean. Nature 2010, 463:178-183.
28. Ihaka R., Gentleman R. R: a language for data analysis and graphics. J Comput Graph Stat 1996, 5:299-314.
29. Bevan M., Bancroft I., Bent E., Love K., Goodman H., Dean C., et al. Analysis of 1.9 Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana. Nature 1998, 391:485-488.
30. Peng Y., Luo Y., Yu T., Xu X., Fan K., Zhao Y., et al. Blue Native-PAGE analysis of membrane protein complexes in Clostridium thermocellum. BMC Microbiol 2011, 11:22.
31. Jones K.M., Sharopova N., Lohar D.P., Zhang J.Q., VandenBosch K.A., Walker G.C. Differential response of the plant Medicago truncatula to its symbiont Sinorhizobium meliloti or an exopolysaccharide-deficient mutant. Proc Natl Acad Sci U S A 2008, 105:704-709.
32. Skorupska A., Janczarek M., Marczak M., Mazur A., Król J. Rhizobial exopolysaccharides: genetic control and symbiotic functions. Microb Cell Fact 2006, 5:7.
33. Wei M., Yokoyama T., Minamisawa K., Mitsui H., Itakura M., Kaneko T., et al. Soybean seed extracts preferentially express genomic loci of Bradyrhizobium japonicum in the initial interaction with soybean, Glycine max (L.) Merr. DNA Res 2008, 15:201-214.
34. Mithöfer A. Suppression of plant defence in rhizobia-legume symbiosis. Trends Plant Sci 2002, 7:440-444.
35. Scholl D., Nixon B.T. Cooperative binding of DctD to the dctA upstream activation sequence of Rhizobium meliloti is enhanced in a constitutively active truncated mutant. J Biol Chem 1996, 271:26435-26442.
36. Karunakaran P., Ramachandran V.K., Seaman J.C., East A.K., Mouhsine B., Mauchline T.H., et al. Transcriptomic analysis of Rhizobium leguminosarum Biovar viciae in symbiosis with host plants Pisum sativum and Vicia cracca. J Bacteriol 2009, 191:4002-4014.
37. Kunze G., Zipfel C., Robatzek S., Niehaus K., Boller T., Felix G. The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis Plants. Plant Cell 2004, 16:3496-3507.
38. Lim C.W., Park J.Y., Lee S.H., Hwang C.H. Comparative proteomic analysis of soybean nodulation using a supernodulation mutant, SS2-2. Biosci Biotechnol Biochem 2010, 74:2396-2404.
39. Janion C., Inducible S.O.S. Inducible SOS response system of DNA repair and mutagenesis in Escherichia coli. Int J Biol Sci 2008, 4:338-344.
40. Shimoni Y., Altuvia S., Margalit H., Biham O. Stochastic analysis of the SOS response in Escherichia coli. PLoS One 2009, 4:5363.
41. Lepek V.C., D'Antuono A.L., Tomatis P.E., Ugalde J.E., Giambiagi S., Ugalde R.A. Analysis of Mesorhizobium loti glycogen operon: effect of phosphoglucomutase (pgm) and glycogen synthase (glgA) null mutants on nodulation of Lotus tenuis. Mol Plant Microbe Interact 2002, 15:368-375.
42. El Yahyaoui F., Kuster H., Amor B.B., Hohnjec N., Puhler A., Becker A., et al. Expression profiling in Medicago truncatula identifies more than 750 genes differentially expressed during nodulation, including many potential regulators of the symbiotic program. Plant Physiol 2004, 136:3159-3176.
43. Vance C.P., Gantt J.S. Control of nitrogen and carbon metabolism in root nodules. Physiol Plant 1992, 85:266-274.
44. Colebatch C., Kloska S., Trevaskis B., Freund S., Altmann T., Udvardi M.K. Novel aspects of symbiotic nitrogen fixation uncovered by transcript profiling with cDNA arrays. Mol Plant Microbe Interact 2002, 15:411-420.
45. Penheiter A.R., Duff S.M.G., Sarath G. Soybean root nodule acid phosphatase. Plant Physiol 1997, 114:597-604.
46. Meuriot F., Noquet C., Avice J.C., Volenec J.J., Cunningham S.M., Sors T.G., et al. Methyl jasmonate alters N partitioning, N reserves accumulation and induces gene expression of a 32-kDa vegetative storage protein that possesses chitinase activity in Medicago sativa taproots. Physiol Plant 2004, 120:113-123.
47. García-Garrido J.M., Ocampo J.A. Regulation of the plant defence response in arbuscular mycorrhizal symbiosis. J Exp Bot 2002, 53:1377-1386.
48. Shaw S.L., Long S.R. Nod factor inhibition of reactive oxygen efflux in a host legume. Plant Physiol 2003, 132:2196-2204.
49. Hiraga S., Sasaki K., Ito H., Ohashi Y., Matsui H. A large family of class III plant peroxidases. Plant Cell Physiol 2001, 42:46246-46248.
50. Lohar D.P., Sharopova N., Endre G., Penuela S., Samac D., Town C., et al. Vanden Bosch KA. Transcript analysis of early nodulation events in Medicago truncatula. Plant Physiol 2006, 140:221-234.
51. Lodwig E.M., Leonard M., Marroqui S.R., Wheeler T., Findlay K., Downie J.A., et al. Role of polyhydroxybutyrate and glycogen as carbon storage compounds in pea and bean bacteroids. Mol Plant Microbe Interact 2005, 18:67-74.
52. Mulder L., Hogg H., Bersoult A., Cullimore J.V. Integration of signalling pathways in the establishment of the legume-rhizobia symbiosis. Physiol Plant 2005, 123:207-218.
53. Ferguson B.J., Mathesius U. Signaling interactions during nodule development. J Plant Growth Regul 2003, 22:47-72.
54. Oldroyd G.E.D., Downie J.A. Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu Rev Plant Biol 2008, 59:519-546.
55. Wu G., Cao M.J., Chen Y., Liu B.X., Su W.J. Leucine aminopeptidase from red sea bream (Pagrus major) skeletal muscle: purification, characterization, cellular location, and tissue distribution. J Agric Food Chem 2008, 56:9653-9660.
56. Gygi S.P., Rochon Y., Franza B.R., Aebersold R. Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 1999, 19:1720-1730.