Nodule Physiology and Proteomics of Stressed Legumes

Advances in Botanical Research

Volumn 56, Issue C, 2010, Pages 1-48

  Qureshi, M I ^a   Muneer, S ^a   Bashir, H ^a   Ahmad, J ^a   Iqbal, M ^b  

^a JAMIA MILLIA ISLAMIA CENTRAL UNIVERSITY   (India)

^b HAMDARD UNIVERSITY   (India)

Author keywords

Abiotic stress; Legumes; Mass spectrometry; Proteomics

Indexed keywords

EID: 78449253061     PISSN: 00652296     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-381518-7.00001-7     Document Type: Chapter

References (171)

1. Aebersold R., Mann M. Mass spectrometry-based proteomics. Nature 2003, 13:198-207.
2. Aghaei K., Ehsanpour A.A., Shah A.H., Komatsu S. Proteome analysis of soybean hypocotyl and root under salt stress. Amino Acids 2009, 36:91-98.
3. Ahsan N., Renaut J., Komatsu S. Recent developments in the application of proteomics to the analysis of plant response to heavy metals. Proteomics 2009, 9:2602-2621.
4. Ahsan N., Lee D.-G., Kim K.-H., Alam I., Lee S.-H., Lee K.-W., Lee H., Lee B.-H. Analysis of arsenic stress-induced differentially expressed proteins in rice leaves by two-dimensional gel electrophoresis coupled with mass spectrometry. Chemosphere 2010, 78:224-231.
5. Asamizu E., Nakamura Y., Sato S., Tabata S. Comparison of the transcript profiles from the root and the nodulating root of the model legume Lotus japonicus by serial analysis of gene expression. Molecular Plant-Microbe Interactions 2005, 18:487-498.
6. Ausili P., Borisov A., Lindblad P., Mãtensson A. Cadmium affects the interaction between peas and root nodule bacteria. Acta Agriculturae Scandinavica, Section B - Plant Soil Science 2002, 52:8-17.
7. Balestrasse K.B., Gallego S.M., Tomaro M.L. Cadmium-induced senescence in nodules of soybean (Glycine max L.) plants. Plant and Soil 2004, 262:373-381.
8. Barbour W.M., Hattermann D.R., Stacey G. Chemotaxis of Bradyrhizobium japonicum to soybean exudates. Applied and Environmental Microbiology 1991, 57:2635-2639.
9. Batut J., Daveran-Mlngot M.L., David M., Jacobs J., Garnerone A.M., Kahn D. fixK, a gene homologous with fnr and crp from Escherichia coli, regulates nitrogen fixation genes both positively and negatively in Rhizobium meliloti. The EMBO Journal 1989, 8:1279-1286.
10. Belanger L., Dimmick K.A., Fleming J.S., Charles T.C. Null mutations in Sinorhizobium meliloti exoS and chvI demonstrate the importance of this two-component regulatory system for symbiosis. Molecular Microbiology 2009, 74:1223-1237.
11. Bestel-Corre G., Dumas-Gaudot E., Poinsot V. Proteome analysis and identification of symbiosis-related proteins from Medicago trancatula by two-dimensional gel electrophoresis and mass spectrophotometry. Electrophoresis 2002, 23:122-137.
12. Bestel-Corre G., Dumas-Gaudot E., Gianinazzi S. Proteomics as a tool to monitor plant microbe endosymbiosomes in the rhizosphere. Mycorrhiza 2004, 14:1-10.
13. Bodzon-Kulakowska A., Bierczynska-Krzysik A., Dylag T., Drabik A., Suder P., Noga M., Jarzebinska J., Silberring J. Methods for samples preparation in proteomic research. Journal of Chromatography B Analytical Tools for Proteomics 2007, 849:1-31.
14. Bowler C., Montagu M.V., Inze D. Superoxide dismutase and stress tolerance. Annual Reviews of Plant Physiology and Plant Molecular Biology 1992, 43:83-116.
15. Brears T., Walker E.L., Coruui G.M. A promoter sequence involved in cell-specific expression of the pea glutamine synthetase GS34 gene in organs of transgenic tobacco and alfalfa. Plant Journal 1991, 1:235-244.
16. Brewin N.J. Development of the legume root nodule. Annual Review of Cell Biology 1991, 7:191-226.
17. Buer C.S., Imin N., Djordjevic M.A. Flavonoids: New roles for old molecules. Journal of Integrative Plant Biology 2010, 52:98-111.
18. Caetano-Anollés G., Gresshoff P.M. Plant genetic control of nodulation. Annual Review of Microbiology 1991, 45:345-382.
19. Candiano G., Bruschi M., Musante L., Santucci L., Ghiggeri G.M., Carnemolla B., Orecchia P., Zardi L., Righetti P.G. Blue silver: A very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 2004, 25:1327-1333.
20. Cesco S., Neumann G., Tomasi N., Pinton R., Weisskopf L. Release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition. Plant and Soil 2010, 329:1-25.
21. Chen H.C., Higgins J., Kondorosi E. Identification of nolR-regulated proteins in Sinorhizobium meliloti strain 2011. Electrophoresis 2000, 21:3823-3832.
22. Chen Y.X., He Y.F., Yang Y., Yu Y.L., Zheng S.J., Tian G.M., Luo Y.M., Wong M.H. Effect of cadmium on nodulation and N2-fixation of soybean in contaminated soils. Chemosphere 2003, 50:781-787.
23. Chen H.C., Higgins J., Oresnik I.J. Proteome analysis demonstrates complex replicon and luteion interactions in Psyma-cured derivatives of Sinorhizobium meliloti strain 2011. Electrophoresis 2005, 16:438-443.
24. Chen H., Bodulovic G., Hall P.J., Moore A., Higgins T.J.V., Djordjevic M.A., Rolfe B.G. Unintended changes in protein expression revealed by proteomic analysis of seeds from transgenic pea expressing a bean α-amylase inhibitor gene. Proteomics 2009, 9:4406-4415.
25. Cheon C.I., Lee N.G., Siddique A.B.M., Bal A.K., Verma D.P.S. Roles of plant homologs of Rablp and Rab7p in the biogenesis of the peribacteroid membrane, a subcellular compartment formed de novo during root nodule symbioses. The EMBO Journal 1993, 12:4125-4135.
26. Clement M., Lambert A., Herouart D., Boncompagni E. Identification of new up-regulated genes under drought stress in soybean nodules. Trends in Plant Science 2008, 426:15-22.
27. Cobbett C.S., Goldsbrough P. Phytochelatins and metallothioneins: Roles in heavy metal detoxification and homeostasis. Annual Review of Plant Biology 2002, 53:159-182.
28. Cooper J.E. Early interactions between legumes and rhizobia: Disclosing complexity in a molecular dialogue. Journal of Applied Microbiology 2007, 103(5):1355-1365.
29. Creasy D.M., Cottrell J.S. Error tolerant searching of uninterpreted tandem mass spectrometry data. Proteomics 2002, 2:1426-1434.
30. D'Haeze W., Holesters M. Nod factor structures, responses, and perception during initiation of nodule development. Glycobiology 2002, 12:79-105.
31. D'Haeze W.D., Mergaert P., Prome J.C., Holesters M. Nod factor requirements for efficient stem and root nodulation of the tropical legume Sesbania rostrata. The Journal of Biochemistry 2000, 275:15675-15684.
32. Da Re S., Bertagnoli S., Fourment J., Reyrat J.M., Kahn D. lntramolecular signal transduction within the FixJ transcriptional activator: In vitro evidence for the inhibitory effect of the phosphorylatable regulatory domain. Nucleic Acids Research 1994, 22:1555-1561.
33. D'Amici G.M., Timperio A.M., Zolla L. Coupling of native liquid phase isoelectrofocusing and blue native polyacrylamide gel electrophoresis: A potent tool for native membrane multiprotein complex separation. Journal of Proteome Research 2008, 7:1326-1340.
34. David M., Daveran M.L., Batut J., Dedieu A., Domergue O., Ghai J., Hertig C., Boistard P., Kahn D. Cascade regulation of nif gene expression in Rhizobium meliloti. Cell 1988, 54:671-683.
35. De Maagd R.A., Yang W.C., Goosen-De Roo L., Mulders I.H.M., Roest H.P., Spaink H.P., Blsseling T., Lugtenberg B.J.J. Down-regulation of expression of the Rhizobium leguminosarum outer membrane protein gene ropA occurs abruptly in interzone 11-111 of pea nodules and can be uncoupled from nif gene activation. Molecular Plant-Microbe Interaction 1994, 7:276-281.
36. Deakin W.J., Broughton W.J. Symbiotic use of pathogen strategies: Rhizobial protein secretion. Nature Reviews Biology 2009, 7:312-320.
37. De-la-Peña C., Lei Z., Watson B.S., Sumner L.W., Vivanco J.M. Root-microbe communication through protein secretion. Journal of Biological Chemistry 2008, 283:25247-25255.
38. Den Herder G., Schroeyers K., Holsters M., Goormachtig S. Signaling and gene expression for water-tolerant legume nodulation. CRC Critical Review Plant Science 2006, 25:367-380.
39. Den Herder J.D., Lievens S., Rombauts S., Holsters M., Goormachtig S. A symbiotic plant peroxidase involved in bacterial invasion of the tropical legume Sesbania rostrata. Plant Physiology 2007, 144:717-727.
40. Djordjevic M.A. Sinorhizobium meliloti metabolism in the root nodule: A proteomic perspective. Proteomics 2004, 4:1859-1872.
41. Dumas-Gaudot E., Amiour N., Weidmann S., Bestel-Corre G., Valot B., Lenogue S., Gianinazzi-Pearson V., Gianinazzi S. A technical trick for studying proteomics in parallel to transcriptomics in symbiotic root-fungus interactions. Proteomics 2004, 4:451-453.
42. Feller U., Anders I., Demirevska K. Degradation of rubisco and other chloroplast proteins under abiotic stress. General and Applied Plant Physiology 2008, 34:5-8.
43. Ferguson P.L., Smith R.D. Proteome analysis by mass spectrometry. Annual Review of Biophysics and Biomolecule Structure 2003, 32:399-424.
44. Fester T.M.K., Strack D. A mycorrhiza-responsive protein in wheat roots. Mycorrhiza 2003, 12:219-222.
45. Fischer H.M. Genetic regulation of nitrogen in rhizobia. Microbiology Review 1994, 58:352-368.
46. Forde B.G., Freeman J., Ollver J.E., Plneda M. Nuclear factors interact with conserved ATT-rich elements upstream of a nodule-enhanced glutamine synthetase gene from French bean. Plant Cell 1990, 2:925-939.
47. Fortin M.G., Zechelowska M., Verma D.P.S. Specific targeting of membrane nodulins to the bacteroid-enclosing compartment in soybean nodules. The EMBO Journal 1985, 4:3041-3046.
48. Foyer C.H., Lenandair M., Kunert K.K.J. Photooxidative stress in plants. Physiologia Plantarum 1994, 92:696-717.
49. Freiberg C., Fellay R., Bairoch A., Broughton W.J., Rosenthal A., Perret X. Molecular basis of symbiosis between Rhizobium and legumes. Nature 1997, 387:394-401.
50. Gamas P., De Billy Françoise, Truchet G. Symbiosis-specific expression of two Medicago truncatula nodulin genes, MtN1 and MtN13, encoding products homologous to plant defense proteins. Molecular Plant-Microbe Interactions 1998, 11:393-403.
51. Gehlenborg N., O'Donoghue S.I., Baliga N.S., Goesmann A., Hibbs M.A., Kitano H., Kohlbacher O., Neuweger H., Schneide R., Tenenbaum D., Gavin A.C. Visualization of omics data for systems biology. Nature Methods Supplement 2010, 7:S56-S68.
52. Geurts R., Bisseling T. Rhizobium nod factor perception and signalling. Plant Cell 2002, 14(Suppl):S239-249.
53. Gilles-Gonzalez M.A., Ditta G.S., Hellnski D.R. A haemoprotein with kinase activity encoded by the oxygen sensor of Rhizobium meliloti. Nature 1991, 350:170-172.
54. Glebov O.O., Bright N.A., Nichols B.J. Flotillin-1 defines a clathrin-independent endocytic pathway in mammalian cells. Nature Cell Biology 2006, 8:46-54.
55. Godovac-Zimmermann J., Kleiner O., Brown L.R., Drukier A.K. Perspectives in spicing up proteomics with splicing. Proteomics 2005, 5:699-709.
56. Görg A., Obermaier C., Boguth G., Harder A., Scheibe B., Wildgruber R., Weiss W. The current state of two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis 2000, 21:1037-1053.
57. Görg A., Weiss W., Dunn M.J. Current two dimensional electrophoresis technology for proteomics. Proteomics 2004, 5:826-827.
58. Govers G., Moerman M., Hooymans J., van Kammen A., Bisseling T. Microaerobiosis is not involved in the induction of pea nodulin-gene expression. Planta 1986, 169:513-517.
59. Graham P.H., Vance C.P. Nitrogen fixation in perspective: An overview of research and extension needs. Field Crop Research 2000, 65:93-106.
60. Grill E., Winnacker E.-L., Zenk M.H. Phytochelatins: The principle heavy-metal-complexing peptides of plants. Science 1985, 230:574-576.
61. Grimsrud P.A., Os D.D., Wenger C.D., Swaney D.L., Schwartz D., Sussman M.R., Ané J.M., Coon J.J. Large-scale phosphoprotein analysis in Medicago truncatula roots provides insight into in vivo kinase activity in legumes. Plant Physiology 2010, 152:19-28.
62. Gunes A., Pilbeam D.J., Inal A. Effect of arsenic-phosphorus interaction on arsenic-induced oxidative stress in chickpea plants. Plant and Soil 2009, 314:211-220.
63. Gusslin G.N., Ronson C.W., Ausubel F.M. Regulation of nitrogen fixation genes. Annual Review of Genetics 1986, 20:567-591.
64. Hajheidari M., Abdollahian-Noghabi M., Askari H. Proteome analysis of sugar beet leaves under drought stress. Proteomics 2005, 5:950-960.
65. Haney C.H., Long S.R. Plant flotillins are required for infection by nitrogen-fixing bacteria. Proceedings of National Academy of Sciences of the United States of America 2010, 107:478-483.
66. Herbert B., David G., Satinder A. Some practices and pitfalls of sample preparation for isoelectric focusing in proteomics. Separation Science and Technology 2005, 147-164. Academic Press.
67. Hirsch A.M. Developmental biology of legume nodulation. New Phytologist 1992, 122:211-237.
68. Ho S.C., Schindler M., Wang J.L. Carbohydrate binding activities of Bradyrhizobium japonicum. II. Isolation and characterization of a galactose-specific lectin. Journal of Cell Biology 1990, 111:1639-1643.
69. Hoogland C., Walther D., Palagi P.M., Bouchet G., Mostaguir K., Robin X., Appel R.D., Lisacek F. A suite of tools to analyse and publish 2-DE data. Bioinformatics 2008, 8:4907-4909.
70. Innes R.W. Genetic dissection of R gene signal transduction pathways. Current Opinion in Plant Biology 1998, 1:299-304.
71. Izmailov S.F. Calcium-based interactions of symbiotic partners in legumes: role of peribacteroid membrane. Russian Journal of Plant Physiology 2003, 50:553-566.
72. Jacobsen-Lyon K., Jensen E.O., Joergensen J.E., Marcker K.A., Peacock W.J., Dennls E.S. Symbiotic and nonsymbiotic hemoglobin genes of Casuarina glauca. Plant Cell 1995, 7:213-223.
73. Jamet A., Sigaud S., Van de Sype G., Puppo A., Hérouart D. Expression of the bacterial catalase genes during Sinorhizobium meliloti-Medicago sativa symbiosis and their crucial role during the infection process. Molecular Plant-Microbe Interactions 2003, 16:217-225.
74. Jones K.M., Kobayashi H., Davies B.W., Taga M.E., Walker G.C. How rhizobial symbionts invade plants: The Sinorhizobium-Medicago model. Nature Reviews Biology 2007, 5:619-633.
75. Kalo P., Gleason C., Edwards A., Marsh J., Mitra R.M., et al. Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science 2005, 308:1786-1789.
76. Kannenberg E.L., Brewin N.J. Expression of a cell surface antigen from Rhizobium leguminosarum 3841 is regulated by oxygen and pH. Journal of Bacteriology 1989, 171:4543-4548.
77. Kardailsky I., Yang W.C., Zalensky A., van Kammen A., Bisseting T. The pea late nodulin gene PsNOD6 is homologous to the early nodulin genes PsENODW4 and is expressed after leghaemoglobin genes. Plant Molecular Biology 1993, 23:1029-1037.
78. Kav N.N.V., Srivastava S., Goonewardene L., Blade S.F. Proteome level changes in the roots of Pisum sativum in response to salinity. Annals of Applied Biology 2007, 145:217-230.
79. Kijne J.W., Smit G., Diaz C.L., Lugtenberg B.J. Lectin-enhanced accumulation of manganese-limited Rhizobium leguminosarum cells on pea root hair tips. Journal of Bacteriology 1988, 170:2994-3000.
80. Kijne J.W. The Rhizobium infection process. Biological Nitrogen Fixation 1992, 348-397. Chapman & Hall, New York. G. Stacey, R.H. Burris, H.J. Evans (Eds.).
81. Komatsu S., Ahsan N. Soybean proteomics and its application to functional analysis. Journal of Proteomics 2009, 72:325-336.
82. Krey R., Pühler A., Klipp W. A defined amino acid exchange close to the putative nucleotide binding site is responsible for an oxygen-tolerant variant of the Rhizobium meliloti NifA protein. Molecular General Genetics 1992, 234:433-441.
83. Larrainzar E., Wienkoop S., Weckwerth W., Ladrera R., Arrese-Igor C., González E.M. Medicago truncatula root nodule proteome analysis reveals differential plant and bacteroid responses to drought stress. Plant Physiology 2007, 144:1495-1507.
84. Lefebvre B., Timmers T., Mbengue M., Moreau S., Hervé C., Tóth K., Bittencourt-Silvestre J., Klausa D., Deslandes L., Godiard L., et al. A remorin protein interacts with symbiotic receptors and regulates bacterial infection. Proceedings of National Academy of Sciences of the United States of America 2010, 107:2343-2348.
85. Lei Z., Elmer A.M., Watson B.S., Dixon R.A., Mendes P.J., Sumner L.W. A two-dimensional electrophoresis proteomic reference map and systematic identification of 1367 proteins from a cell suspension culture of the model legume Medicago truncatula. Molecular & Cellular Proteomics 2005, 4:1812-1825.
86. Lei Z., Nagaraj S., Watson B.S., Sumner L.W. Proteomics of Medicago truncatula. Plant Proteomics 2007, 121-136. Springer Heidelberg, Germany. J. Šamaj, J. Thelen (Eds.).
87. Lewis R.D., Handy R.B., Cordi B., Billinghurst Z., Depledge M.H. Stress proteins (HSP's): Methods of detection and their use as an environmental biomarker. Exotoxicology 1999, 8:351-368.
88. Lin D., Tabb D.L., Yates I.J.R. Large-scale protein identification using mass spectrometry. Biochemica et Biophysica Acta 2003, 1646:1-10.
89. Loh J., Stacey G. Nodulation gene regulation in Bradyrhizobium japonicum: A unique integration of global regulatory circuits. Applied Environmental Microbiology 2003, 69:10-17.
90. Ma J.F., Rayan P.R., Delhaize E. Almunium tolerance in plants and the complexing role of organic acids. Trends in Plant Science 2001, 6:273-278.
91. Maj D., Wielbo J., Marek-Kozaczuk M., Skorupska A. Response to flavonoids as a factor influencing competitiveness and symbiotic activity of Rhizobium leguminosarum. Microbiological Research 2010, 165:50-60.
92. Majoul T., Bancel E., Triboi E., Ben Hamida J., Branlard G. Proteomic analysis of the effect of heat stress on hexaploid wheat grain: Characterization of heat responsive proteins from non prolamins fraction. Proteomics 2004, 4:505-513.
93. Mandal S.M., Mandal M., Pati B.R., Das A.K., Gosh A.K. Proteomic view of rhizobium isolate response to arsenite [As (III)] stress. Acta Microbiology Immunology Hungarica 2009, 56:157-167.
94. Mastronunzio J.E., Huang Y., Benson D.R. Diminished exoproteome of Frankia spp. in culture and symbiosis. Applied and Environmental Microbiology 2009, 75:6721-6728.
95. 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 Physiology 2003, 133:499-509.
96. Mathesius U. Comparative proteomic studies of root-microbe interactions. Journal of Proteomics 2009, 72:353-366.
97. Matvlienko M., van de Sande K., Yang W.C., van Kammen A., Bissellng T., Franssen H. Comparison of soybean and pea fNOD40 cDNA clones representing genes expressed during both early and late stages of nodule development. Plant Molecular Biology 1994, 26:487-493.
98. Mellor R. Bacteroids in the Rhizobium-legume symbiosis inhabit a plant internal lytic compartment: Implications for other microbial endosymbioses. Journal of Experimental Botany 1989, 40:831-839.
99. Merrick M.J. Regulation of nitrogen fixation genes in free-living and symbiotic bacteria. Biological Nitrogen Fixation 1992, 835-876. Chapman and Hall, New York. G. Stacey, R.H. Burris, H.J. Evans (Eds.).
100. Merril C.R., Dunau M.L., Goldman D. A rapid sensitive silver stain for polypeptides in polyacrylamide gels. Anal Biochem 1981, 110:201-207.
101. Miao G.-H., Hong Z., Verma D.P.S. Topology and phosphorylation of soybean nodulin-26, an intrinsic protein of the peribacteroid membrane. Journal of Cell Biology 1992, 118:481-490.
102. 54 with the Klebsiella pneumoniae and Rhizobium meliloti nifH promoters: The role of NifA in the formation of an open promoter complex. Journal of Molecular Biology 1989, 210:65-77.
103. Muenchbach M., Dainese P., Staudenmann W., Narberhaus F., James P. Proteome analysis of heat shock expression in Bradyrhizobium japonicum. European Journal of Biochemistry 1999, 263:39-48.
104. Mylona P., Pawlowski K., Bisseling T. Symbiotic nitrogen fixation. The Plant Cell 1995, 7:869-885.
105. Nakano M., Nobuta K., Vemaraju K., Tej S.S., Skogen J.W., Meyers B.C. Plant MPSS databases: Signature-based transcriptional resources for analyses of mRNA and small RNA. Nucleic Acids Research 2006, 34:731-735.
106. Nap J.-P., Bisseling T. Developmental biology of a plant prokaryote symbiosis: The legume root nodule. Science 1990, 250:948-954.
107. Natera S.H.A., Guerreiro N., Djordjevic N.A. Proteome analysis of differentially displayed proteins as a tool for the investigation of symbiosis. Molecular Plant-Microbe Interactions 2000, 13:995-1009.
108. Newcomb W. Nodule morphogenesis and differentiation. International Review of Cytology Supplementary 1981, 13:246-298.
109. Noriega G.O., Balestrasse K.B., Batlle A., Tomaro M.L. Cadmium induced oxidative stress in soybean plants also by the accumulation of δ-aminolevulinic acid. Biometals 2007, 20:841-851.
110. Ouyang L.J., Whelan J., Weaver C.D., Roberts D.M., Day D.A. Protein phosphorylation stimulates the rate of malate uptake across the peribacteroid membrane of soybean nodules. The FEBS Letters 1991, 293:188-190.
111. Panda S.K., Upadhyay R.K., Nath S. Arsenic stress in plants. Journal of Agronomy and Crop Science 2010, 196:161-174.
112. Panter S., Thomson R., de Bruxelles G., Laver D., Trevaskis B., Udvardi M. Identification with proteomics of novel proteins associated with the peribacteroid membrane of soybean root nodules. American Phytopathological Society 2000, 13:325-333.
113. Peters N.K., Verma D.P.S. Phenolic compounds as regulators of gene expression in plant-microbe interactions. Molecular Plant-Microbe Interactions 1990, 3:4-8.
114. Qadir S., Qureshi M.I., Javed S., Abdin M.Z. Genotypic variation in phytoremediation potential of Brassica juncea cultivars exposed to Cd stress. Plant Science 2004, 167:1171-1181.
115. Qureshi M.I., Qadir S., Zolla L. Proteomics-based dissection of stress-responsive pathways in plants. Journal of Plant Physiology 2007, 164:1239-1260.
116. Qureshi M.I., D'Amici G.M., Fagioni M., Rinalducci S., Zolla L. Iron stabilizes thylakoid protein-pigment complexes in Indian mustard during Cd-phytoremediation as revealed by BN-SDS-PAGE and ESI-MS/MS. Journal Plant Physiology 2010, 167:761-770.
117. Rabilloud T., Strub J.M., Luche S., van Dorsselaer A., Lunardi J. A comparison between Sypro Ruby and ruthenium II tris (bathophenanthroline disulfonate) as fluorescent stains for protein detection in gels. Proteomics 2001, 1:699-704.
118. Ramlov K.B., Laursen N.G., Stougaard J., Marcker K.A. Site-directed mutagenesis of the organ-specific element in the soybean leghemoglobin lbc3 gene promoter. The Plant Journal 1993, 4:577-580.
119. Rampitsch C., Srinivasan M. The application of proteomics to plant biology: A review. Canadian Journal of Botany 2006, 84:883-892.
120. Ramu S.K., Peng H.-M., Cook D.R. Nod factor induction of reactive oxygen species production is correlated with expression of the early nodulin gene rip1 in Medicago truncatula. Molecular Plant-Microbe Interactions 2002, 15:522-528.
121. Requejo R., Tena M. Proteomic analysis of maize roots reveals that oxidative stress is a main contributing factor to plant arsenic toxicity. Phytochemistry 2005, 66:1533-1547.
122. Requejo R., Tena M. Maize response to acute arsenic toxicity as revealed by proteome analysis of plant shoots. Proteomics 2006, 6:S156-S162.
123. Rolfe B.G., Mathesius U., Djordjevic M., Weinman J., Hocart C., Weiller G., Dietz W.B. Proteomic analysis of legume-microbe interactions. Comparative and Functional Genomics 2003, 4:225-228.
124. Samac D.A., Graham M.A. Recent advances in legume-microbe interactions: Recognition, defense response, and symbiosis from a genomic perspective. Plant Physiology 2007, 144:582-587.
125. Santos R., Bocquet S., Puppo A., Touati D. Characterization of an atypical superoxide dismutase from Sinorhizobium meliloti. Journal of Bacteriology 1999, 181:4509-4516.
126. Santos R., Hérouart D., Puppo A., Touati D. Critical protective role of bacterial superoxide dismutase in Rhizobium-legume symbiosis. Molecular Microbiology 2000, 38:750-759.
127. Santos R., Hérouart D., Sigaud S., Touati D., Puppo A. Oxidative burst in alfalfa-Sinorhizobium meliloti symbiotic interaction. Molecular Plant-Microbe Interactions 2001, 14:86-89.
128. Sarma A.D., Oehrle N.W., Emerich D.W. Metabolic intricacies of the symbiotic association between soybean and Bradyrhizobium japonicum: A proteomic outlook. Plant Proteomics 2007, 310-325. Springer Berlin Heidelberg, Germany. J. Šamaj, J.J. Thelen (Eds.).
129. Scharf K.D., Hohfeld I., Nover L. Heat stress response and heat stress transcription factors. Journal of Biosciences 1998, 23:313-329.
130. Scheres B., van de Wiel C., Zalensky A., Horvath B., Spaink H.P., van Eck H., Zwartkruis F., Wolters A.M., Gloudemans T., van Kammen A., Bisseling T. The ENODl2 gene product is involved in the infection process during pea-Rhizobium interaction. Cell 1990, 60:281-294.
131. Scheres B., van Engelen F., van der Knaap E., van de Wiel C., van Kammen A., Bisseling T. Sequential induction of nodulin gene expression in the developing pea nodule. Plant Cell 1990, 2:687-700.
132. Schmitt H.D., Wagner P., Pfaff E., Gallwitz D. The ras-related YPT7 gene product in yeast: A GTP-binding protein that might be involved in microtubule organization. Cell 1986, 47:401-412.
133. Schulte T., Paschke K.A., Laessing U., Lottspeich F., Stuermer C.A. Reggie-1 and reggie-2, two cell surface proteins expressed by retinal ganglion cells during axon regeneration. Development 1997, 124:577-587.
134. Schumpp O., Deakin W.J. How inefficient rhizobia prolong their existence within nodules. Trends in Plant Science 2010, (in press).
135. Shamseldin A., Werner D. High salt and high pH tolerance of new isolated R. etli strains from Egyptian soils. Current Microbiology 2006, 50:11-16.
136. Shinozaki K., Yamaguchi-Shinozaki K. Gene expression and signal transduction in water stress response. Plant Physiology 1997, 115:327-334.
137. Shvaleva A., de la Peña T.C., Rincón A., Morcillo C.N., García de la Torre V.S., Lucas M.M., Pueyo J.J. Flavodoxin overexpression reduces cadmium-induced damage in alfalfa root nodules. Plant and Soil 2010, 326:109-121.
138. Singer M. Beyond global warming: Interacting ecocrises and the critical anthropology of health. Anthropological Quarterly 2009, 82:795-819.
139. Singh N., Ma L.Q., Srivastava M., Rathinasabapathi B. Metabolic adaptations to arsenic-induced oxidative stress in Pteris vittata L. and Pteris ensiformis L. Plant Science 2006, 170:274-282.
140. Siria H.A., Natera Guerreiro N., Djordjevic M.A. Proteome analysis of differentially displayed proteins as a tool for the investigation of symbiosis. Plant Microbe Interactions 2000, 13:995-1009.
141. Smil V. Nitrogen in crop production. Global Biogeological Cycle 1999, 13:647-662.
142. 2+ -dependent cell surface protein in attachment of Rhizobium leguminosarum biovar viciae to pea root hair tips. Journal of Bacteriology 1989, 171:569-572.
143. Smit P., Raedts J., Portyanko V., Debellé F., Gough C., Bisseling T., Geurts R. NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. Science 2005, 308:1789-1791.
144. Smith E., Juhasz A.L., Weber J. Arsenic uptake and speciation in vegetables grown under greenhouse conditions. Environmental Geochemical Health 2009, 31:125-132.
145. Socolow R.H. Nitrogen management and the future of food: Lessons from the management of energy and carbon. Proceedings of National Academy of Sciences of the United States of America 1999, 96:6001-6008.
146. 2 -fixation gene expression within the alfalfa root nodule. Proceedings of National Academy of Sciences of the United States of America 1995, 92:3759-3763.
147. Souza A.L., Invitti A.L., Rego F.G., Monteiro R.A., Klassen G., Souza E.M., Chubatsu L.S., Pedrosa F.O., Rigo L.U. The involvement of the nif-associated ferredoxin-like genes fdxA and fdxN of Herbaspirillum seropedicae in nitrogen fixation. Journal of Microbiology 2010, 48:77-83.
148. Spaink H.P., Sheeley D.M., van Brussel A.A.N., Glushka J., York W.S., Tak T., Geiger O., Kennedy E.P., Reinhold V.N., Lugtenberg B.J.J. A novel highly unsaturated fatty acid moiety of lipo-oligosaccharide signals determines host specificity of Rhizobium. Nature 1991, 354:125-130.
149. Szabados L., Ratet P., Grunenberg B., de Bruijn F.J. Functional analysis of the Sesbania rostrata leghemoglobin glb3 gene 5'-upstream region in transgenic Lotus corniculatus and Nicotiana tabacum plants. Plant Cell 1990, 2:973-986.
150. Szczyglowski K., Szabados L., Fujimoto S.Y., Silver D., de Bruijn F.J. Site-specific mutagenesis of the nodule-infected cell expression (NICE) element and the AT-rich element ATRE-BS2' of the Sesbania rostrata leghemoglobin glb3 promoter. Plant Cell 1994, 6:317-332.
151. Timperio A.M., Edidi M.G., Zolla L. Proteomics applied on plant abiotic stresses: Role of heat shock proteins (HSP). Journal of Proteomics 2008, 71:391-411.
152. Trevaskis B., Colebatch G., Desbrosses G., Wanrey M., Wienkoop S., Saalbach G., Udvardi M. Differentiation of plants cells during symbiotic nitrogen fixation. Comparative Functional Genomics 2002, 3:151-157.
153. Truchet G., Roche P., Lerouge P., Vasse J., Camut S., de Billy F., Promé J.-C., Dénarié J. Sulphated lipo-oligosaccharide signals of R. meliloti elicit root nodule organogenesis in alfalfa. Nature 1991, 351:670-673.
154. Van de Velde W., Zehirov G., Szatmari A., Debreczeny M., Ishihara H., Kevei Z., Farkas A., Mikulass K., Nagy A., Tiricz H., et al. Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 2010, 327:1122-1126.
155. Van Rhijn P., Vanderleyden J. The Rhizobium-plant symbiosis. Microbiological Reviews 1995, 59:124-142.
156. Van Wijk K. Challenges and prospects of plant proteomics. Plant Physiology 2001, 126:501-508.
157. Vasse J., de Billy F., Camut S., Truchet G. Correlation between ultrastructural differentiation of bacteroids and nitrogen fixation in alfalfa nodules. Journal of Bacteriology 1990, 172:4295-4306.
158. Verma D.P.S. Signals in root nodule organogenesis and endocytosis of Rhizobium. Plant Cell 1992, 4:373-382.
159. Vesper S.J., Malik S.A., Bauer W.D. Transposon mutants of Bradyrhizobium japonicum altered in attachment to host roots. Applied Environmental Microbiology 1987, 53:1959-1961.
160. Wan J., Torres M., Ganapathy A., Thelen J., DaGue B.B., Mooney B., Xu D., Stacey G. Proteomic analysis of soybean root hairs after infection by Bradyrhizobium japonicum. Moecularl Plant Microbe Interactions 2005, 18:458-467.
161. Wang W., Vinocur B., Shoseyov O., Altman A. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Science 2004, 9:244-252.
162. Wang D., Griffitts J., Starker C., Fedorova E., Limpens E., Ivanov S., Bisseling T., Long S. A nodule-specific protein secretory pathway required for nitrogen-fixing symbiosis. Science 2010, 327:126-1129.
163. Weaver C.D., Shower N.H., Louis C.F., Roberts D.M. Nodulin-26, a nodule specific symbiosome membrane protein from soybean, is an ion channel. Journal of Biological Chemistry 1994, 269:17858-17862.
164. Werner D. Physiology of nitrogen-fixing legume nodules: Compartments and functions. Biological Nitrogen Fixation 1992, 399-431. Chapman and Hall, New York. G. Stacey, R.H. Burris, H.J. Evans (Eds.).
165. Wienkoop S., Saalbach G. Proteome analysis: Novel proteins identified at the peribacteroid membrane from Lotus japonicus root nodules. Plant Physiology 2003, 131:1080-1090.
166. Willey J.M., Sherwood L.M., Woolverton C.J. Microbiology. Prescot, Harley, and Klein's Microbiology 2008, McGraw Hill, New York. 7th ed.
167. Wood S.M., Newcomb W. Nodule morphogenesis: The early infection of alfalfa (Medicago sativa) root hairs by Rhizobium meliloti. Canadian Journal of Botany 1989, 67:3108-3122.
168. Yang W.C., Horvath B., Hontelez J., van Kammen A., Bisseling T. In situ localization of Rhizobium mRNAs in pea root nodules: nifA and nifH localization. Molecular Plant-Microbe Interactions 1991, 4:464-468.
169. Yang Q., Wang Y., Zhang J., Shi W., et al. Identification of aluminium responsive proteins in rice roots by a proteomic approach: Cysteine synthetase as a key player in Al response. Proteomics 2007, 7:737-749.
170. Zhen Y., Qi J.L., Wang S.S., Su J., et al. Comparative proteome analysis of differentially expressed proteins induced by Al toxicity in soybean. Plant Physiology 2007, 131:542-554.
171. Zhou S., Sauvé R., Thannhauser T.W. Proteome changes induced by aluminium stress in tomato roots. Journal of Experimental Botany 2009, 60:1849-1857.