A combined 15N tracing/proteomics study in Brassica napus reveals the chronology of proteomics events associated with N remobilisation during leaf senescence induced by nitrate limitation or starvation

Proteomics

Volumn 9, Issue 13, 2009, Pages 3580-3608

  Desclos, Marie ^a   Etienne, Philippe ^a   Coquet, Laurent ^b   Jouenne, Thierry ^b   Bonnefoy, Josette ^a   Segura, Raphaël ^a   Reze, Sandrine ^a   Ourry, Alain ^a   Avice, Jean Christophe ^a  

^a UNIVERSITÉ DE CAEN   (France)

^b UNIVERSITÉ DE ROUEN   (France)

Author keywords

2 D difference gel electrophoresis; Brassica napus; Proteolysis; Proteome analysis; Senescence

Indexed keywords

ASPARTIC PROTEINASE; CHLOROPHYLL; FTSH PROTEINASE; NITRATE; NITROGEN; NITROGEN 15; PROTEASOME BETA SUBUNIT A1; PROTEINASE; SENESCENSE ASSOCIATED GENE 12 PROTEINASE; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; TRACER;

ARTICLE; BIOMASS PRODUCTION; CAB GENE; CONTROLLED STUDY; GENE EXPRESSION; LEAF AGE; LEAF NITROGEN CONTENT; LEAF SENESCENCE; NONHUMAN; PLANT GENE; PLANT LEAF; PLANT METABOLISM; PLANT STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN SYNTHESIS; PROTEOMICS; RAPESEED; STARVATION; BIOMASS; CHEMISTRY; DRUG EFFECT; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

BRASSICA NAPUS;

BIOMASS; BRASSICA NAPUS; CHLOROPHYLL; NITRATES; PLANT LEAVES; PLANT PROTEINS; PROTEOMICS; RADIOACTIVE TRACERS;

EID: 67651208457     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.200800984     Document Type: Article

References (100)

1. Vitousek, P. M., Aber, J. D., Howarth, R. W., Likens, G. E. et al., Human alteration of the global nitrogen cycle. Ecological Appl. 1997, 7, 737-750.
2. Matson, P., Lohse, K. A., Hall, S. J., The globalization of nitrogen deposition: consequences for terrestrial ecosystems. Ambio 2002, 31, 113-119.
3. Hörtensteiner, S., Feller, U., Nitrogen metabolism and remobilization during senescence. J. Exp. Bot. 2002, 53, 927-937.
4. Zimmermann, P., Zentgraf, U., The correlation between oxidative stress and leaf senescence during plant development. Cell. Mol. Biol. Lett. 2005, 10, 515-535.
5. Gallais, A., Hirel, B., An approach of the genetics of nitrogen use efficiency in maize. J. Exp. Bot. 2004, 55, 295-306.
6. Good, A. G., Shrawat, A. K., Muench, D. G., Can less yield more? Is reducing nutrient input into the environment compatible with maintaining crop production? Trends Plant Sci. 2004, 9, 597-605.
7. Buchanan-Wollaston, V., The molecular biology of leaf senescence. J. Exp. Bot. 1997, 48, 181-199.
8. Yoshida, S., Molecular regulation of leaf senescence. Curr. Opin. Plant Biol. 2003, 6, 79-84.
9. Smart, C. M., Gene expression during leaf senescence. New Phytol. 1994, 126, 419-448.
10. Guo, Y., Cai, Z., Gan, S., Transcriptome of Arabidopsis leaf senescence. Plant Cell Environ. 2004, 27, 521-549.
11. Buchanan-Wollaston, V., Earl, S., Harrison, E., Mathas, E. et al., The molecular analysis of leaf senescence a genomic approach. Plant Biotech. J. 2003, 1, 3-22.
12. Diaz, C., Lemaître, T., Christ, A., Azzopardi, M. et al., Nitrogen recycling and remobilization are differentially controlled by leaf senescence and development stage in Arabidopsis under nitrogen nutrition. Plant Physiol. 2008, 147, 1437-1449.
13. Yamada, K., Matsushima, R., Nishimura, M. I., Hara-Nishimura, I., A slow maturation of a cysteine protease with a granulin domain in the vacuoles of senescing Arabidopsis leaves. Plant Physiol. 2001, 127, 1626-1634.
14. Noh, Y. S., Amasino, R. M., Regulation of developmental senescence is conserved between Arabidopsis and Brassica napus L. Plant Mol. Biol. 1999, 41, 195-206.
15. Gallardo, K., Firnhaber, C., Zuber, H., Héricher, D. et al., A combined proteome and transcriptome analysis of developing Medicago truncatula seeds. Mol. Cell. Proteomics 2007, 6, 2165-2179.
16. Wilson, K., Mc Manus, M., Gordon, M., Jordan, T. W., The proteomics of leaf senescence in leaves of white clover, Trifolium repens (L.). Proteomics 2002, 2, 1114-1122.
17. Schiltz, S., Gallardo, K., Huart,M., Negroni, L. et al., Proteome reference maps of vegetative tissues in Pisum sativum: an investigation of nitrogen mobilisation from leaves during seed filling. Plant Physiol. 2004, 135, 2241-2260.
18. Zhao, C., Wang, J., Cao, M., Zhao, K. et al., Proteomic changes in rice leaves during development of field-grown rice plants. Proteomics 2005, 5, 961-972.
19. Swidzinski, J. A., Leaver, C. J., Sweetlove, L. J., A proteomic analysis of plant programmed cell death. Phytochemistry 2004, 65, 1829-1838.
20. 15N-labeling and difference gel electrophoresis. Mol. Cell. Proteomics 2008, 7, 108-120.
21. Schjoerring, J. K., Bock, J. G. H., Gammelvind, L., Jensen, C. R., Mogensen, V. O., Nitrogen incorporation and remobilization in different shoot components of field-grown winter oilseed rape (Brassica napus L.) as affected by rate of nitrogen application and irrigation. Plant Soil 1995, 177, 255-264.
22. Malagoli, P., Lainé P., Rossato, L., Ourry, A., Dynamic of nitrogen uptake and mobilisation in field grown winter oilseed rape from stem extension to harvest I. Global N flows between vegetative and reproductive tissues in relation with leaf fall and their residual N. Ann. Bot. (Lond) 2005, 95, 853-861.
23. Gombert, J., Etienne, P., Ourry, A., Le Dilly, F., The enlargement of expression of the SAG12 gene displays a gradation of leaf senescence along the axis of Brassica napus L. whole plant. J. Exp. Bot. 2006, 57, 1949-1956.
24. Etienne, P., Desclos, M., Le Gou, L., Gombert, J. et al., Nprotein mobilisation associated with the leaf senescence process in oilseed rape is concomitant with the disappearance of trypsin inhibitor activity. Funct. Plant Biol. 2007, 34, 895-906.
25. Dejoux, J. F., Recous, S., Meynard, J. M., Trinsoutrot, I., Leterme, P., The fate of nitrogen from winter-frozen rapeseed leaves: mineralization, fluxes to the environment and uptake by rapeseed crop in spring. Plant Soil 2000, 218, 257-272.
26. Tilsner, J., Kassner, N., Struck, C., Lohaus, G., Amino acid contents and transport in oilseed rape (Brassica napus L.) under different nitrogen conditions. Planta 2005, 221, 328-338.
27. 13C pulse-chase labelling during regrowth of Alfalfa. Plant Physiol. 1996, 112, 281-290.
28. Desclos, M., Dubousset, L., Etienne, P., Bonnefoy, J. et al., A proteomic profiling approach to reveal a novel role of BnD22 (Brassica napus drought 22 kD)/water soluble chlorophyll binding protein in young leaves during nitrogen remobilization induced by stressful conditions. Plant Physiol. 2008, 147, 1830-1844.
29. Bradford, M. M., A rapid method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Anal. Biochem. 1976, 72, 248-254.
30. Blum, H., Beier, H., Gross, H. J., Improved silver staining of plant proteins, RNA and DNA in polyacrylamid gel. Electrophoresis 1987, 8, 93-99.
31. 15N to nitrogenous compounds at the vegetative growth stage of potato plants. Soil Sci. Plant Nutr. 1995, 41, 699-708.
32. Masclaux, C., Valadier, M. H., Brugière, N., Morot-Gaudry, J. F., Hirel, B., Characterization of the sink/source transition in tobacco (Nicotiana tabacum L.) shoots in relation to nitrogen management and leaf senescence. Planta 2000, 211, 510-518.
33. Bevan, M., Bancroft, I., Bent, E., Love, K. et al., Analysis of 19Mb of contiguous sequence from chromosome 4 of Arabidopsis thaliana. Nature 1998, 391, 485-488.
34. Noctor, G., Foyer, C. H., Ascorbate and glutathione: keeping active oxygen under control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1998, 49, 249-279.
35. Chen, Z., Gallie, D. R., Dehydroascorbate reductase affects leaf growth, development, and function. Plant Physiol. 2006, 142, 775-787.
36. Wilmouth, R. C., Turnbull, J. J.,Welford, R.W. D., Clifton, I. J. et al., Structure and mechanism of anthocyanidin synthase from Arabidopsis thaliana. Structure 2002, 10, 93-103.
37. Philpott, M., Gould, K. S., Lim, C., Ferguson, L. R., In situ and in vitro antioxidant activity of sweet potato anthocyanins. J. Agr. Food Chem. 2004, 52, 1511-1513.
38. Baier, M., Dietz, K. J., The plant 2-Cys peroxiredoxin BAS1 is a nuclear-encoded chloroplast protein: its expressional regulation, phylogenetic origin, and implications for its specific physiological function in plants. Plant J. 1997, 12, 179-190.
39. 2 mixed-function oxidation system. J. Biol. Chem. 1988, 263, 4704-4711.
40. Lim, Y. S., Cha, M. K., Uhm, T. B., Park, J. W., Kim, K. et al., Removals of hydrogen peroxide and hydroxyl radical by thiol-specific antioxidant protein as a possible role in vivo. Biochem. Biophys. Res. Commun. 1993, 192, 273-280.
41. Baier, M., Noctor, G. S., Foyer, C. H., Dietz, K. J., Antisense suppression of 2-cysteine peroxiredoxin in Arabidopsis specifically enhances the activities and expression of enzyme associated with ascorbate metabolism but not glutathione metabolism. Plant Physiol. 2000, 120, 823-832.
42. Chen, H. C., Klein, A., Xiang, M., Backhaus, R., Kuntz, M., Drought- and wound-induced expression in leaves of a gene encoding a chromoplast carotenoid-associated protein. Plant J. 1998, 14, 317-326.
43. Kim, H. U., Wu, S. S. H., Ratnayake, C., Huang, H. A. C., Brassica rapa has three genes that encode proteins associated with different neutral lipids in plastids of specific tissues. Plant Physiol. 2001, 126, 330-341.
44. Buchanan-Wollaston, V., Ainsworth, C., Leaf senescence in Brassica napus: cloning of senescence related genes by subtractive hybridization. Plant Mol. Biol. 1997, 33, 821-834.
45. Pic, E., de la serve, B. T., Tardieu, F., Turc, O., Leaf senescence induced by mild water deficit follows the same sequence of macroscopic, biochemical, and molecular events as monocarpic senescence in pea. Plant Physiol. 2002, 128, 236-273.
46. Andrews, S. C., Arosio, P., Bottke, W., Briat, J. F. et al., Structure, function, and evolution of ferritins. J. Inorg. Biochem. 1992, 47, 161-174.
47. Murgia, I., Vazzola, V., Tarantino, D., Cellier, F. et al., Knock-out of ferritin AtFer1 causes earlier onset of age-dependent leaf senescence in Arabidopsis. Plant Physiol. Bioch. 2007, 45, 898-907.
48. Humbeck, K., Quast, S., Krupinska, K., Functional and molecular changes in the photosynthetic apparatus during senescence of flag leaves from field-grown barley plants. Plant Cell Environ. 1996, 19, 337-344.
49. Batt, T., Woolhouse, H. W., Changing activities during senescence and sites of synthesis of photosynthetic enzymes in leaves of the labiate, Perilla frutescens (L.) Britt. J. Exp. Bot. 1975, 26, 569-579.
50. Jiang, C. Z., Rodermel, S. R., Shibles, R. M., Photosynthesis, rubisco activity and amount, and their regulation by transcription in senescing soybean leaves. Plant Physiol. 1993, 101, 105-112.
51. Bate, N. J., Rothstein, S. J., Thompson, J. E., Expression of nuclear and chloroplast photosynthesis-specific genes during leaf senescence. J. Exp. Bot. 1991, 42, 801-811.
52. Raines, C. A., Lloyd, J. C., Willingham, N. M., Potts, S., Dyer, T. A., cDNA and gene sequences of wheat chloroplast sedoheptulose-1,7-bisphosphatase reveal homology with fructose-1,6-bisphosphatases. Eur. J. Biochem. 1992, 205, 1053-1059.
53. Nicolas, L. T., Heazlewood, J. L., Day, D. A., Millar, A. H., Lipoic acid-dependent oxidative catabolism of a-keto acids in mitochondria provides evidence for branched chain amino acid catabolism in Arabidopsis. Plant Physiol. 2004, 134, 838-848.
54. Giegé P., Heazlewood, J. L., Roessner-Tunalli, U., Millar, A. H. et al., Enzymes of glycolysis are functionally associated with the mitochondrion in Arabidopsis cells. Plant Cell 2003, 15, 2140-2151.
55. Thomas, H., Stoddart, J. L., Leaf senescence. Annu. Rev.Plant Physiol. 1980, 31, 83-111.
56. Solomos, T., Respiration in senescing plant organs: its nature, regulation, and physiological significance, in: Noodén, L. D., Leopold, A. C., (Eds.), Senescence and Aging in Plants, Academic Press, San Diego 1988, pp. 111-145.
57. Liu, L., Zhou, Y., Zhou, G., Ye, R. et al., Identification of early senescence-associated genes in rice flag leaves. Plant Mol. Biol. 2008, 67, 37-55.
58. Noguchi, K., Yoshida, K., Interaction between photosynthesis and respiration in illuminated leaves. Mitochondrion 2007, 8, 87-99.
59. Wang, X., Yang, P., Gao, Q., Liu, X. et al., Proteomic analysis of the response to high-salinity stress in Physcomitrella patens. Planta 2008, 228, 167-177.
60. Ahsan, N., Lee, D. G., Lee, S. H., Kang, K. Y. et al., A comparative proteomic analysis of tomato leaves in response to waterlogging stress. Physiol. Plant. 2007, 131, 555-570.
61. May, M. J., Vernoux, T., Leaver, C., van Montagu, M., Inze, D., Glutathione homeostasis in plants: implications for environmental sensing and plant development. J. Exp. Bot. 1998, 49, 649-667.
62. Ochs, G., Shock, G., Trischler, M., Kosemund, K., Wild, A., Complexity and expression of the glutamine synthetase multigene family in the amphidiploid crop Brassica napus. Plant Mol. Biol. 1999, 39, 395-405.
63. Finneman, J., Schjoerring, J., Post-translocational regulation of cytosolic glutamine synthetase by reversible phosphorylation and 14-3-3 protein interaction. Plant J. 2000, 24, 171-184.
64. Paris, S., Wessel, P. M., Dumas, R., Overproduction, puri-fication, and characterization of recombinant aspartate semialdehyde dehydrogenase from Arabidopsis thaliana. Protein Expres. Purif. 2002, 24, 99-102.
65. Yang, S. F., Hoffman, N. E., Ethylene biosynthesis and its regulation in higher plants. Annu. Rev. Plant Physiol. 1984, 35, 155-159.
66. Oh, S. A., Park, J. H., Lee, G. I., Paek, K. H. et al., Identification of three genetic loci controlling leaf senescence in Arabidopsis thaliana. Plant J. 1997, 12, 527-535.
67. Wiedemuth, K., M. uller, J., Kahlau, A., Amme, S. et al., Successive maturation and senescence of individual leaves during barley whole plant ontogeny reveals temporal and spatial regulation of photosynthetic function in conjunction with C and N metabolism. J. Plant Physiol. 2005, 162, 1226-1236.
68. Kimura, M., Yamamoto, Y. Y., Seki, M., Sakurai, T. et al., Identification of Arabidopsis genes regulated by high lightstress using cDNA microarray. Photochem. Photobiol. 2003, 77, 226-233.
69. Jebanathirajah, J. A., Coleman, J. R., Association of carbonic anhydrase with a Calvin cycle enzyme complex in Nicotiana tabacum. Planta 1998, 204, 177-182.
70. Slaymaker, D. H., Navarre, D. A., Clark, D., del Pozo, O. et al., The tobacco salicylic acid-binding protein 3 (SABP3) is the chloroplastic carbonic anhydrase, which exhibits antioxidant activity and plays a role in hypersensitive defence response. Proc. Natl. Acad. Sci. USA 2002, 99, 11640-11645.
71. Sanan-Mishra, N., Pham, X. H., Sopory, S. K., Tuteja, N., Pea DNA helicase 45 overexpression in tobacco confers high salinity tolerance without affecting yield. Proc. Natl. Acad. Sci. USA 2005, 102, 509-514.
72. García-Hernandez, M., Davies, E., Baskin, T., Staswick, P. E., Association of plant p40 protein with ribosomes is enhanced when polyribosomes form during periods of active tissue growth. Plant Physiol. 1996, 111, 559-568.
73. 2+ binding protein in radish vacuoles. Plant Physiol. 2000, 124, 1063-1078.
74. Snedden, W. A., Fromm, H., Calmodulin as a versatile signal transducer in plants. New Phytol. 2001, 151, 36-66.
75. Lois, L. M., Campos, M., Putra, S. R., Danielsen, K. et al., Cloning and characterization of a gene from Escherichia coli encoding a transketolase-like enzyme that catalyzes the synthesis of D-1-deoxyxylulose 5-phosphate, a common precursor for isoprenoid, thiamin, and pyridoxol biosynthesis. Proc. Natl. Acad. Sci. USA 1998, 95, 2105-2110.
76. Close, T. J., Dehydrins: emergence of a biochemical role of a family of plant dehydration proteins. Physiol. Plant. 1996, 97, 795-803.
77. Koag, M. C., Fenton, R. D., Wilkens, S., Timothy, J. C., The binding of maize DHN1 to lipid vesicles. Gain of structure and lipid specificity. Plant Physiol. 2003, 131, 309-316.
78. Tommasini, L., Svensson, J. T., Rodriguez, E. M., Wahid, A. et al., Dehydrin gene expression provides an indicator of low temperature and drought stress: transcriptome-based analysis of Barley (Hordeum vulgare L.). Funct. Integr. Genomic. 2008, 8, 387-405.
79. Xu, J., Zhang, Y. X., Wei, W., Han, L. et al., BjDHNs confer heavy-metal tolerance in plants. Mol. Biotechnol. 2008, 38, 91-98.
80. Bartling, D., Seedorf, M., Schmidt, R. C., Weiler, E. W., Molecular characterization of two cloned nitrilases from Arabidopsis thaliana: key enzymes in biosynthesis of the plant hormone indole- 3-acetic acid. Proc. Natl. Acad. Sci. USA 1994, 91, 6021-6025.
81. Noodén, L. D., Guiamet, J. J., John, I., Senescence mechanisms. Physiol. Plant. 1997, 101, 746-753.
82. Quirino, B. F., Normanly, J., Amasino, R. M., Diverse range of gene activity during Arabidopsis thaliana leaf senescence includes pathogen-independent induction of defense-related genes. Plant Mol. Biol. 1999, 40, 267-278.
83. Gan, S., Amasino, R., Making sense of senescence, molecular genetic regulation and manipulation of leaf senescence. Plant Physiol. 1997, 113, 313-319.
84. Aloni, R., Schwalm, K., Langhans, M., Ullrich, C. I., Gradual shifts in sites of free-auxin production during leaf-primordium development and their role in vascular differentiation and leaf morphogenesis in Arabidopsis. Planta 2003, 216, 841-853.
85. He, Y. H., Fukushige, H., Hildebrande, D. F., Gan, S., Evidence supporting a role for jasmonic acid in Arabidopsis leaf senescence. Plant Physiol. 2002, 128, 876-884.
86. Rakwal, R., Komatsu, S., Role of jasmonate in the rice (Oryza sativa L.) self-dense mechanism using proteome analysis. Electrophoresis 2000, 21, 2492-2500.
87. Feller, U., Fischer, A., Nitrogen metabolism in senescing leaves. Crit. Rev. Plant Sci. 1994, 13, 241-273.
88. Wang, W., Vincour, B., Shosevov, O., Altman, A., Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci. 2004, 9, 244-252.
89. Koumoto, Y., Tsugeki, R., Shimada, T., Mori, H. et al., Isolation and characterization of a cDNA encoding mitochondrial chaperonin 10 from Arabidopsis thaliana by functional complementation of an Escherichia coli groES mutant. Plant J. 1996, 10, 1119-1125.
90. Salvucci, M. E., Association of Rubisco activase with chaperonin-60b: a possible mechanism for protecting photosynthesis during heat stress. J. Exp. Bot. 2008, 59, 1923-1933.
91. Wadahama, H., Kamauchi, S., Ishimoto, M., Kawada, T., Urade, R., Protein disulfide isomerase family proteins involved in soybean protein biogenesis. FEBS Lett. 2007, 274, 687-703.
92. Lindahl, A. J., Spetea, C., Hundal, T., Oppenheim, A. B. et al., The thylakoid FtsH protease plays a role in the light-induced turnover of the photosystem II D1 protein. Plant Cell 2000, 12, 419-431.
93. Zelisko, A., García-Lorenzo, M., Jackowski, G., Jansson, S., Funk, C., AtFtsH6 is involved in the degradation of the light harvesting complex II during high-light acclimation and senescence. Proc. Natl. Acad. Sci. USA 2005, 102, 13699-13704.
94. Dessi, P., Rudhe, C., Glaser, E., Studies on the topology of the protein import channel in relation to the plant mitochondrial processing peptidase integrated into the cytochrome bc1 complex. Plant J. 2000, 24, 637-644.
95. Braun, H. P., Schmitz, U. K., Are the core proteins of the mitochondrial bc(1) complex evolutionary relics of a processing protease? Trends Biochem. Sci. 1995, 20, 171-175.
96. Gakh, O., Cavadini, P., Isaya, G., Mitochondrial processing peptidases. Biochim. Biophys. Acta 2002, 1592, 63-77.
97. Baumeister, W., Walz, J., Z. uhl, F., Seem. uller, E., The proteasome: paradigm of a self-compartmentalizing protease. Cell 1998, 92, 367-380.
98. Etienne, P., Petitot, A. S., Houot, V., Blein, J. P., Suty, L., Induction of tcI7, a gene encoding a β-subunit of proteasome, in tobacco plants treated by elicitins, salicylic ac or hydrogen peroxide. FEBS Lett. 2000, 446, 213-218.
99. Otegui, M. S., Noh, Y. S., Martinez, D. E., Vila Petroff, M. G. et al., Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean. Plant J. 2005, 41, 831-844.
100. Sirover, M. A., New insights into an old protein: the functional diversity of mammalian glyceraldehydes-3-phosphate dehydrogenase. Biochim. Biophys. Acta 1999, 1432, 159-184.