Evaluation of protein pattern changes in roots and leaves of Zea mays plants in response to nitrate availability by two-dimensional gel electrophoresis analysis

BMC Plant Biology

Volumn 9, Issue , 2009, Pages

  Prinsi, Bhakti ^a   Negri, Alfredo S ^a   Pesaresi, Paolo ^a   Cocucci, Maurizio ^a   Espen, Luca ^a  

^a UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ZEA MAYS;

NITRATE; NITRATE REDUCTASE; PROTEOME; VEGETABLE PROTEIN;

ARTICLE; GENE EXPRESSION REGULATION; MAIZE; METABOLISM; PLANT LEAF; PLANT ROOT; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION REGULATION, PLANT; NITRATE REDUCTASE; NITRATES; PLANT LEAVES; PLANT PROTEINS; PLANT ROOTS; PROTEOME; ZEA MAYS;

EID: 70349227094     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-9-113     Document Type: Article

References (99)

1. H Marschner, Mineral Nutrition of Higher Plants London: Academic Press Limited 1995
2. Nitrogen. AV Barker GM Bryson, Handbook of Plant nutrition Boca Raton: CRC Press, Barker AV, Pilbeam DJ, 2007 21 50
3. Nitrate regulation of metabolism and growth. M Stitt, Curr Opin Plant Biol 1999 2 178 186 10.1016/S1369-5266(99)80033-8 10375569
4. Protein hydrolysis and nitrogen remobilisation in plant life and senescence. R Brouquisse C Masclaux U Feller P Raymond, Plant Nitrogen Hidelberg: Springer-Verlag Berlin Hidelberg, Lea PJ, Morot-Gaudry JF, 2001 275 293
5. Steps towards an integrated view of nitrogen metabolism. M Stitt C Müller P Matt Y Gibon P Carillo R Morcuende WR Sheible A Krapp, J Exp Bot 2002 53 959 970 10.1093/jexbot/53.370.959 11912238
6. Root nitrogen acquisition and assimilation. AJ Miller MD Cramer, Plant Soil 2004 274 1 36 10.1007/s11104-004-0965-1
7. Genome-wide programming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. WR Scheible R Morcuende T Czechowski C Fritz D Osuna N Palacios-Rojas D Schindelasch O Thimm MK Udvardi M Stitt, Plant Physiol 2004 136 2483 2499 10.1104/pp.104.047019 15375205
8. Roots, nitrogen transformation and ecosystem services. LE Jackson M Burger TR Cavagnaro, Annu Rev Plant Biol 2008 59 341 63 10.1146/annurev.arplant. 59.032607.092932 18444903
9. Nitrogen, plant growth and crop yield. DW Lawlor G Lemaire F Gastal, Plant Nitrogen Hidelberg: Springer-Verlag Berlin Hidelberg, Lea PJ, Morot-Gaudry JF, 2001 343 367
10. Towards a better understanding of the genetic and physiological basis for nitrogen use efficiency in maize. B Hirel P Bertin I Quillere W Bourdoncle C Attagnant C Dellay A Gouy S Cadiou C Retailliau M Falque A Gallais, Plant Physiol 2001 125 1258 1270 10.1104/pp.125.3.1258 11244107
11. Contrasting dynamics of dissolved inorganic and organic nitrogen in soil and surface waters of forested catchments with Gleysols. F Hagedorn JB Bucher P Schleppi, Geoderma 2001 100 173 192 10.1016/S0016-7061(00)00085-9 (Pubitemid 32152012)
12. Competition for amino acids between wheat roots and rhizosphere microorganisms and the role of amino acids in plant N acquisition. AG Owen DL Jones, Soil Biol Biochem 2001 33 651 657 10.1016/S0038-0717(00)00209-1 (Pubitemid 32241397)
13. Nitrate transport in Plants: which gene and which control? M Orsel S Filleur V Fraisier F Daniel-Vedele, J Exp Bot 2002 53 825 833 10.1093/jexbot/53.370.825 11912225
14. 3uptake and fusicoccin in root hairs of Limnobium stoloniferum. CI Ullrich AJ Novacky, Plant Physiol 1990 94 1561 1567 10.1104/pp.94.4.1561 16667890
15. Evidence for cotransport of nitrate and protons in maize roots. I. Effects of nitrate on the membrane potential. PR McClure LV Kochian RM Spanwick JE Shaff, Plant Physiol 1990 93 281 289 10.1104/pp.93.1.281 16667448
16. - transport across the plasma membrane of Arabidopsis thaliana root hairs: kinetic control by pH and membrane voltage. AA Meharg MR Blatt, J Membrane Biol 1995 145 49 66 10.1007/BF00233306
17. Molecular and physiological aspects of nitrate uptake in plants. NM Crawford ADM Glass, Trends Plant Sci 1998 3 389 395 10.1016/S1360-1385(98)01311- 9 (Pubitemid 28472065)
18. Cloning and functional characterization of an Arabidopsis nitrate transporter gene that encodes a constitutive component of low-affinity uptake. NC Huang KH Liu HJ Lo YF Tsay, Plant Cell 1999 11 1381 1392 10.1105/tpc.11.8. 1381 10449574
19. - transport and reduction on intracellular pH: an in vivo NMR study in maize roots. L Espen FF Nocito M Cocucci, J Exp Bot 2004 55 2053 2061 10.1093/jxb/erh231 15310818
20. +-ATPases: powerhouses for nutrient uptake. MG Palmgren, Annu Rev Plant Physiol Plant Mol Biol 2001 52 817 845 10.1146/annurev.arplant.52.1.817 11337417
21. +-ATPase isoforms. S Santi G Locci R Monte R Pinton Z Varanini, J Exp Bot 2003 54 1851 1864 10.1093/jxb/erg208 12869520
22. Energization of transport processes in plants. roles of the plasma membrane H1-ATPase. TE Sondergaard A Schulz MG Palmgren, Plant Physiol 2004 136 2475 2482 10.1104/pp.104.048231 15375204
23. Nitrogen metabolism in roots. A Oaks B Hirel, Annu Rev Plant Physiol 1985 36 345 365 10.1146/annurev.pp.36.060185.002021
24. Nitrate reduction and signalling. C Meyer M Stitt, Plant Nitrogen Hidelberg: Springer-Verlag Berlin Hidelberg, Lea PJ, Morot-Gaudry JF, 2001 37 59
25. Ammonia assimilation. B Hirel PJ Lea, Plant Nitrogen Hidelberg: Springer-Verlag Berlin Hidelberg, Lea PJ, Morot-Gaudry JF, 2001 79 99
26. Nitrate: nutrient and signal for plant growth. NM Crawford, Plant Cell 1995 7 859 868 10.1105/tpc.7.7.859 7640524
27. Sink regulation of photosynthesis. MJ Paul CH Foyer, J Exp Bot 2001 52 1383 1400 10.1093/jexbot/52.360.1383 11457898
28. Local and long-range signalling pathways regulating plant responses to nitrate. BG Forde, Annu Rev Plant Biol 2002 53 203 224 10.1146/annurev.arplant. 53.100301.135256 12221973
29. Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate. R Wang K Guegler ST LaBrie NM Crawford, Plant Cell 2000 12 1491 1509 10.1105/tpc.12.8.1491 10948265
30. Analysis of the plant proteome. M Rossignol, Curr Opin Biotech 2001 12 131 134 10.1016/S0958-1669(00)00186-5 11287225
31. Proteomics and future generation of plant molecular biologists. JKM Roberts, Plant Mol Biol 2002 48 143 154 10.1023/A:1013736322130 11862971
32. Advances in proteomic technologies. ML Yarmush A Jayaraman, Annu Rev Biomed Eng 2002 4 349 373 10.1146/annurev.bioeng.4.020702.153443 12117762
33. Proteomics: the first decade and beyond. SD Patterson RH Aebersold, Nat Genet Suppl 2003 33 Suppl 311 323 10.1038/ng1106 (Pubitemid 36278841)
34. Plant Proteomics update (2007-2008): Second-generation proteomic techniques, an appropriate experimental design, and data analysis to fulfil MIAPE standards, increase plant proteome coverage and expand biological knowledge. JV Jorrín-Novo AM Maldonato S EchevarríaZomeo L Valledor MA Castllejo M Curto J Valero B Sghaier G Donoso I Redonado, J Proteomics 2009 72 285 314 10.1016/j.jprot.2009.01.026 19367730
35. MaizeGDB, the community database for maize genetics and genomics. CJ Lawrence Q Dong L Mary ML Polacco TE Seigfried V Brendel, Nucleic Acids Res 2004 32 393 D397 10.1093/nar/gkh011 14681441
36. The proteome of maize leaves: Use of gene sequences and expressed sequence tag data for identification of proteins with peptide mass Fingerprints. L Porubleva KV Velden S Kothari J David DJ Oliver R Parag PR Chitnis, Electrophoresis 2001 22 1724 1738 10.1002/1522-2683(200105)22:9<1724::AID- ELPS1724>3.0.CO;2-2 11425228
37. Functional differentiation of bundle sheath and mesophyll maize chloroplasts determined by comparative proteomics. W Majeran Y Cai Q Sun KJ van Wijk, Plant Cell 2005 17 3111 3140 10.1105/tpc.105.035519 16243905
38. Transcriptomic and proteomic analyses of pericycle cells of the maize primary root. D Dembinsky K Woll M Saleem Y Liu Y Fu LA Borsuk T Lamkemeyer C Fladerer J Madlung B Barbazuk A Nordheim D Nettleton PS Schnable F Hochholdinger, Plant Physiol 2007 145 575 588 10.1104/pp.107.106203 17766395
39. Differential protein expression assessed by two-dimensional gel electrophoresis for two wheat varieties grown at four nitrogen levels. N Bahrman J Le Gouls L Negroni L Amilhat P Leroy AL Lané O Jaminon, Proteomics 2004 4 709 719 10.1002/pmic.200300571 14997493
40. Differential change in root protein pattern of two wheat varieties under high and low nitrogen nutrition levels. N Bahrman A Gouy F Devienne-Barret B Hirel F Vedele J Le Gouis, Plant Sci 2005 168 81 87 10.1016/j.plantsci.2004.07. 035 (Pubitemid 39464767)
41. Interactions between carbon and nitrogen metabolism. CH Foyer S Ferrario-Méry G Noctor, Plant Nitrogen Hidelberg: Springer-Verlag Berlin Hidelberg, Lea PJ, Morot-Gaudry JF, 2001 237 254
42. Regulation of the accumulation and reduction of nitrate by nitrogen and carbon metabolites in maize seedlings. S Sivasankar S Rothstein A Oaks, Plant Physiol 1997 114 583 589 12223730
43. Regulation of nitrate reductase expression in leaves by nitrate and nitrogen metabolism is completely overridden when sugars fall below a critical level. D Klein R Morcuende M Stitt A Krapp, Plant Cell Environ 2000 23 863 871 10.1046/j.1365-3040.2000.00593.x (Pubitemid 30608851)
44. Appearance of novel glucose-6-phosphate dehydrogenase isoforms in Chlamydomonas reinhardtii during growth on nitrate. HC Huppe DH Turpin, Plant Physiol 1996 110 1431 1433 12226271
45. Nitrate-induce genes in tomato roots. Array analysis reveals novel genes that may play a role in nitrogen nutrition. YH Wang DF Garvin LV Kochian, Plant Physiol 2001 127 345 359 10.1104/pp.127.1.345 11553762
46. Differential expression of six glutamine synthetase genes in Zea mays. M Li R Villemur PJ Hussey CD Silflow JS Gantt DP Snustad, Plant Mol Biol 1993 23 401 407 10.1007/BF00029015 8106013
47. Differential effects of nitrate and light on the expression of glutamine synthetases and ferredoxin-dependent glutamate synthase in maize. H Sakakibara S Kawabata T Hase T Sugiyama, Plant Cell Physiol 1992 33 1193 1198
48. Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. P Rockel F Strube A Rockel J Wildt WM Kaiser, J Exp Bot 2002 53 103 110 10.1093/jexbot/53.366.103 11741046
49. Nitric oxide scavenging by barley hemoglobin is facilitated by a monodehydroascorbate reductase-mediated ascorbate reduction of methemoglobin. AU Igamberdiev NV Bycova RD Hill, Planta 2006 223 1033 1040 10.1007/s00425-005- 0146-3 16341544
50. Nitric oxide: the versatility of an extensive signal molecule. L Lamattina C Garca-Mata G Pagnussat, Annu Rev Plant Biol 2003 54 109 136 10.1146/annurev.arplant.54.031902.134752 14502987
51. Formation and possible roles of nitric oxide in plant roots. C Stöhr S Stremlau, J Exp Bot 2006 57 463 470 10.1093/jxb/erj058 16356940
52. Nitric oxide is involved in nitrate-induced inhibition of root elongation in Zea mays. DY Zhao QY Tian LH Li WH Zhang, Ann Bot 2007 100 497 503 10.1093/aob/mcm142 17709366
53. Characterization and expression of transcripts induced by oxygen deprivation in maize (Zea mays L.). VM Peschke MM Sachs, Plant Physiol 1994 104 387 394 10.1104/pp.104.2.387 7909162
54. Nitrate NO and haemoglobin in plant adaptation to hypoxia: an alternative to classic fermentation pathways. AU Igamberdiev RD Hill, J Exp Bot 2004 408 2473 2482 10.1093/jxb/erh272
55. Regulation of secondary metabolism by the carbon-nitrogen status in tobacco: nitrate inhibits large sectors of phenylpropanoid metabolism. C Fritz N Palacios-Rojas R Fell M Stitt, Plant J 2006 46 533 548 10.1111/j.1365-313X. 2006.02715.x 16640592
56. Stress-induced changes in protease composition are determined by nitrogen supply in non-nodulating white clover. AH Kingston-Smith AL Bollard FR Minchin, J Exp Bot 2005 56 745 753 10.1093/jxb/eri049 15647316
57. Structure and function of plant aspartic proteinases. I Simes C Faro, Eur J Biochem 2004 271 2067 2075 10.1111/j.1432-1033.2004.04136.x 15153096
58. Rice aspartic proteinases, oryzasin, expressed during seed ripening and germination, has a gene organization distinct from those of animal and microbial aspartic proteinases. T Askura H Watanabe K Abe S Arai, Eur J Biochem 1995 232 77 83 10.1111/j.1432-1033.1995.tb20783.x 7556174
59. + in growing plants? JA Raven, New Phytol 1986 104 175 206 10.1111/j.1469-8137.1986.tb00644.x
60. Revision of biochemical pH-stat: involvement of alternative pathway metabolisms. K Sakano, Plant Cell Physiol 1998 39 467 473
61. Nitrogen acquisition, PEP carboxylase, and cellular pH homeostasis: new views on old paradigms. DT Britto HJ Kronzucker, Plant Cell Environ 2005 28 1396 1409 10.1111/j.1365-3040.2005.01372.x (Pubitemid 43920129)
62. Regulatory monoubiquitination of phosphoenolpyruvate carboxylase in germinating castor oil seeds. RG Uhrig YM She CA Leach WC Plaxton, JBC 2008 283 29650 29657 10.1074/jbc.M806102200
63. Two genes encoding GF14 (14-3-3) proteins in Zea mays. Structure, expression, and potential regulation by G-box-binding complex. NC de Vetten RJ Ferl, Plant Physiol 1994 106 1593 1604 10.1104/pp.106.4.1593 7846163
64. Localization of 14-3-3 proteins in the nuclei of Arabidopsis and maize. EA Bihn AL Paul SW Wang GW Erdos RJ Ferl, Plant J 1997 12 1439 1445 10.1046/j.1365-313x.1997.12061439.x 9450348
65. Regulatory 14-3-3 protein-protein interactions in plant cells. MR Roberts, Curr Opin Plant Biol 2000 3 400 405 10.1016/S1369-5266(00)00103-5 11019808
66. 14-3-3 proteins associate with the regulatory phosphorylation site of spinach leaf nitrate reductase in an isoform-specific manner and reduce dephosphorylation of Ser-543 by endogenous protein phosphatases. M Bachmann JL Huber GS Athwal K Wu RJ Ferl SC Huber, FEBS Lett 1996 398 26 30 10.1016/S0014-5793(96)01188-X 8946947
67. Specific binding of a 14-3-3 protein to autophosphorylated WPK4, an SNF1-related wheat protein kinase, and to WPK-4-phosphorylated nitrate reductase. Y Ikeda N Koizumi T Kusano H Sano, JBC 2000 275 31695 31700 10.1074/jbc.M004892200
68. Reconstitution of higher plant chloroplast chaperonin 60 tetradecamers active in protein folding. R Dickson C Weiss RJ Howard SP Alldrick RJ Ellis G Lorimer A Azem PV Viitenen, JBC 2000 275 11829 11835 10.1074/jbc.275.16.11829 (Pubitemid 30237750)
69. Co-operation between cytosolic and plastidic oxidative pentose phosphate pathways revealed by 6-phosphogluconate dehydrogenase-deficient genotypes of maize. RH Averill J Bailey-Serres NJ Kruger, Plant J 1998 14 449 457 10.1046/j.1365-313X.1998.00143.x (Pubitemid 28295397)
70. Photosynthesis. R Malkin K Niyogi, Biochemistry and Molecular Biology of Plants American Society of Plant Physiologists Rockville, Buchanan B, Gruissem W, Jones R, 2000 568 628
71. Modulation of thiamine metabolism in Zea mays seedlings under conditions of abiotic stress. M Rapala-Kozik E Kowalaska K Ostrowska, J Exp Bot 2008 59 4133 4143 10.1093/jxb/ern253 18940932
72. 4phothosynthesis versus the dual-cell (Kranz) paradigm. GE Edwards VR Franceschi EV Voznesenskaya, Annu Rev Plant Biol 2004 55 173 196 10.1146/annurev.arplant.55.031903.141725 15377218
73. Immunological analysis of the phosphorylation state of maize C4-form phosphoenolpyruvate carboxylase with specific antibodies raised against a synthetic phosphorylated peptide. Y Ueno E Imanari J Emura K Yoshizawa-Kumagaye K Nakajiama K Inami T Shiba H Sakakibara T Sugiyama K Izui, Plant J 2000 21 17 26 10.1046/j.1365-313x.2000.00649.x 10652147
74. Phosphoenolpyruvate carboxylase: a new era of structural biology. K Izui H Matsumura T Furumoto Y Kai, Annu Rev Plant Biol 2004 55 69 84 10.1146/annurev.arplant.55.031903.141619 15725057
75. Duplicate maize 13-lipoxygenase genes are differentially regulated by circadian rhythm, cold stress, wounding, pathogen infection, and hormonal treatments. A Nemchenko S Kunze I Feussner M Kolomietes, J Exp Bot 2006 57 3767 3779 10.1093/jxb/erl137 17005920
76. All three acyl moieties of trilinolein are efficiently oxygenated by recombinant His-tagged lipid body lipoxygenase in vitro. I Feussner A Bachmann M Höhne H Kindl, FEBS Lett 1998 431 433 436 10.1016/S0014-5793(98)00808-4 9714558
77. Nucleotide sequence of cDNA encoding the precursor of the 23 kDa protein of the photosynthetic oxygen-evolving complex from wheat. HE James C Robinson, Plant Mol Biol 1991 17 179 182 10.1007/BF00036827 1868221
78. Characterization of a cDNA clone encoding 23 kDa polypeptide of the oxygen-evolving complex of photosystem II in rice. Y Yoshiba K Yamaguchi-Shinozaki K Shinozaki Y Harada, Plant Cell Physiol 1995 36 1677 1682 8589938
79. Expression, assembly and auxiliary functions of photosystem II oxygen-evolving proteins in higher plants. M Sourosa EM Aro, Photosynth Res 2007 93 89 100 10.1007/s11120-007-9154-4 17380423
80. PsbP protein, but not PsbQ protein, is essential for the regulation and stabilization of photosystem II in higher plants. K Ifuku Y Yamamoto T Ono S Ishihara F Sato, Plant Physiol 2005 139 1175 1184 10.1104/pp.105.068643 16244145
81. Nitrogen deficiency in Arabidopsis affects galactolipid composition and gene expression and results in accumulation of fatty acid phytyl esters. N Gaude C Bréhélin G Tischendorf F Kessler P Dörmann, Plant J 2007 49 729 739 10.1111/j.1365-313X.2006.02992.x 17270009
82. Digalactosyldiacylglycerol is required for stabilization of the oxygen-evolving complex in photosystem II. I Sakurai N Mizusawa H Wada N Sato, Plant Physiol 2007 145 1361 1370 10.1104/pp.107.106781 17921339
83. Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. DA Cataldo M Haroon LE Schrader VL Youngs, Commun Soil Sci Plant Anal 1975 6 71 80 10.1080/00103627509366547
84. Overexpression of nitrate reductase in tobacco delays drought-induced decreases in nitrate reductase activity and mRNA. S Ferrario-Méry MH Valadier CH Foyer, Plant Physiol 1998 117 293 302 10.1104/pp.117.1.293 9576799
85. A photometric adaptation of the Somogy method for the determination of glucose. NA Nelson, JBC 1944 153 375 384
86. A modified ninhydrin reagent for the photometric determination of amino acids and related compounds. S Moore WH Stein, JBC 1954 211 907 913
87. A simple, rapid and quantitative method for preparing Arabidopsis protein extracts for immunoblot analysis. JF Martínez-Garcia E Monte PH Quall, Plant J 1999 20 251 257 10.1046/j.1365-313x.1999.00579.x 10571885
88. Chlorophylls and carotenoids: Pigments of photosynthetic biomembranes. HK Lichtenthaler, Met Enzymol 1987 148 350 382 10.1016/0076-6879(87)48036-1
89. Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. RL Heat K Packer, Arch Biochem Biophys 1968 125 189 198 10.1016/0003-9861(68)90654-1 5655425
90. Chlorophyll fluorescence and photosynthesis: the basics. GH Krause E Weis, Annu Rev Plant Physiol Plant Mol Biol 1991 42 313 349 10.1146/annurev.pp. 42.060191.001525
91. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. B Genty JM Briantais NR Baker, BBA 1989 990 87 92
92. Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. WJ Hurkman CK Tanaka, Plant Physiol 1986 81 802 806 10.1104/pp.81.3.802 16664906
93. Cleavage of structural proteins during the assembly of the head of bacteriophage. T4. UK Laemmli, Nature 1970 227 680 685 10.1038/227680a0 5432063
94. Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. V Neuhoff N Arold D Taube W Ehrhardt, Electrophoresis 1988 9 255 262 10.1002/elps.1150090603 2466658
95. Combined electrophoretic approaches for the study of white lupin mature seed storage proteome. C Magni A Scarafoni A Herndl F Sessa B Prinsi L Espen M Duranti, Phytochemistry 2007 68 997 1007 10.1016/j.phytochem.2007.01.003 17320919
96. National Center for Biotechnology Information. http://www.ncbi.nlm.nih. gov/
97. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. JK Eng AL McCormack JR Yates III, J Am Soc Mass Spectrom 1994 5 976 989 10.1016/1044-0305(94)80016-2
98. Getting more from less: algorithms for rapid protein identification with multiple short peptide sequences. AJ Mackey TAJ Haystead WR Pearson, Mol Cell Proteomics 2002 1 139 147 10.1074/mcp.M100004-MCP200 12096132
99. ExPASy Proteomics Server. http://www.expasy.org/