Proteomic and selected metabolite analysis of grape berry tissues under well-watered and water-deficit stress conditions

Proteomics

Volumn 9, Issue 9, 2009, Pages 2503-2528

  Grimplet, Jérôme ^a   Wheatley, Matthew D ^a   Jouira, Hatem Ben ^b   Deluc, Laurent G ^a   Cramer, Grant R ^a   Cushman, John C ^a  

^a UNIVERSITY OF NEVADA   (United States)

^b CENTRE DE BIOTECHNOLOGIE DE BORJ CÉDRIA   (Tunisia)

Author keywords

Metabolites; Tissue specific proteins; Two dimensional gel electrophoresis; Vitis vinifera L.; Water deficit stress

Indexed keywords

CATECHOL OXIDASE; FLAVONOID; GLUTAMATE DECARBOXYLASE; HEAT SHOCK PROTEIN; MESSENGER RNA; METHIONINE SYNTHASE; PROTEOME;

ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; CORRELATION ANALYSIS; DROUGHT STRESS; ENERGY METABOLISM; GRAPE; GRAPE BERRY; METABOLITE; NONHUMAN; PERICARP; PLANT SEED; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; TISSUE SPECIFICITY; WATER TREATMENT; WINE;

DEHYDRATION; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FRUIT; GENE EXPRESSION REGULATION, PLANT; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLANT PROTEINS; PROTEOMICS; STRESS, PHYSIOLOGICAL; VITIS;

VITACEAE; VITIS VINIFERA;

EID: 66249140254     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.200800158     Document Type: Article

References (102)

1. This, P., Lacombe, T., Thomas, M., Historical origins and genetic diversity of wine grapes. Trends Genet. 2006, 22, 511-519.
2. Arroyo-Garcia, R., Ruiz-Garcia, L., Boiling, L., Ocete, R. etal., Multiple origins of cultivated grapevine (Vitis vinifera L. ssp. sativa) based on chloroplast DNA polymorphisms. Mol. Ecol. 2006, 15, 3707-3714.
3. Iriti, M., Faoro, F., Grape phytochemicals: A bouquet of old and new nutraceuticals for human health. Med. Hypotheses 2006, 67, 833-838.
4. Monagas, M., Hernandez-Ledesma, B., Gomez-Cordoves, C., Bartolome, B., Commercial dietary ingredients from Vitis vinifera L. leaves and grape skins: Antioxidant and chemical characterization. J. Agric. Food Chem. 2006, 54, 319-327.
5. This, P., Lacombe, T., Cadle-Davidson, M., Owens, C., Wine grape (Vitis vinifera L.) color associates with allelic variation in the domestication gene VvmybA1. Theor. Appl. Genet. 2007, 114, 723-730.
6. Bogs, J., Jaffe, F., Takos, A., Walker, A., Robinson, S., The grapevine transcription factor VvMYBPA1 regulates proan- thocyanidin synthesis during fruit development. Plant Phy- siol. 2007, 143, 1347-1361.
7. Fernandez, K., Kennedy, J., Agosin, E., Characterization of Vitis vinifera L. Cv. Carmenere grape and wine proantho- cyanidins. J. Agric. Food Chem. 2007, 55, 3675-3680.
8. Lund, S., Bohlmann, J., The molecular basis for wine grape quality - A volatile subject. Science 2006, 311, 804-805.
9. Moreno-Arribas, M., Cabello, F., Polo, M., Martin-Alvarez, P., Pueyo, E., Assessment of the native electrophoretic analysis of total grape must proteins for the characterization of Vitis vinifera L. cultivars. J. Agric. Food Chem. 1999, 47, 114-120.
10. Hayasaka, Y., Adams, K., Pocock, K., Baldock, G. etal.,Use of electrospray mass spectrometry for mass determination of grape (Vitis vinifera) juice pathogenesis-related proteins: A potential tool for varietal differentiation. J. Agric. Food Chem. 2001, 49, 1830-1839.
11. Monteiro, S., Picarra-Pereira, M., Teixeira, A., Loureiro, V., Ferreira, R., Environmental conditions during vegetative growth determine the major proteins that accumulate in mature grapes. J. Agric. Food Chem. 2003, 51, 4046-4053.
12. Vincent, D., Wheatley, M., Cramer, G., Optimization of protein extraction and solubilization for mature grape berry clusters. Electrophoresis 2006, 27, 1853-1865.
13. Sarry, J.-E., Sommerer, N., Sauvage, F.-X., Bergoin, A. et al., Grape berry biochemistry revisited upon proteomic analysis of the mesocarp. Proteomics 2004, 4, 201-215.
14. Carvalho, L., Esquivel, M., Martins, I., Ricardo, C., Amancio, S., Monitoring the stability of Rubisco in micropropagated grapevine (Vitis vinifera L.) by two-dimensional electrophoresis. J. Plant Physiol. 2005, 162, 365-374.
15. Castro, A., Carapito, C., Zorn, N., Magne, C. etal., Proteomic analysis of grapevine (Vitis vinifera L.) tissues subjected to herbicide stress. J. Exp. Bot. 2005, 56, 2783-2795.
16. Vincent, D., Ergul, A., Bohlman, M., Tattersall, E. etal., Proteomic analysis reveals differences between Vitis vinifera L. cv. Chardonnay and cv. Cabernet Sauvignon and their responses to water deficit and salinity. J. Exp. Bot. 2007, 58, 1873-1892.
17. Sauvage, F.-X., Pradal, M., Chatelet, P., Tesniere, C., Proteome changes in leaves from grapevine (Vitis vinifera L.) transformed for alcohol dehydrogenase activity. J. Agric. Food Chem. 2007, 55, 2597-2603.
18. Deytieux, C., Geny, L., Lapaillerie, D., Claverol, S. etal., Pro- teome analysis of grape skins during ripening. J. Exp. Bot. 2007, 58,851-1862.
19. Giribaldi, M., Perugini, I., Sauvage, F., Schubert, A., Analysis of protein changes during grape berry ripening by 2-DE and MALDI-TOF. Proteomics 2007, 7, 3154-3170.
20. Negri, A., Prinsi, B., Rossoni, M., Failla, O. et al., Proteome changes in the skin of the grape cultivar Barbara among different stages of ripening. BMC Genomics 2008, 9, 378.
21. Moser, C., Segala, C., Fontana, P., Salakhudtinov, I. etal., Comparative analysis of expressed sequence tags from different organs of Vitis vinifera L. Funct. Integr. Genomics 2005, 5, 208-217.
22. da Silva, F., Iandolino, A., Al-Kayal, F., Bohlmann, M. et al., Characterizing the grape transcriptome. Analysis of expressed sequence tags from multiple Vitis species and development of a compendium of gene expression during berry development. Plant Physiol. 2005, 139, 574-597.
23. Peng, F., Reid, K., Liao, N., Schlosser, J. et al., Generation of ESTs in Vitis vinifera wine grape (Cabernet Sauvignon) and table grape (Muscat Hamburg) and discovery of new candidate genes with potential roles in berry development. Gene 2007, 402, 40-50.
24. Waters, L., Holton, T., Ablett, E., Lee, L., Henry, R., cDNA microarrays analysis of developing grape (Vitis vinifera cv. Shiraz) berry skin. Funct. Integr. Genomics 2005, 5, 40-58.
25. Terrier, N., Glissant, D., Grimplet, J., Barrieu, F. etal., Isogene specific oligo arrays reveal multifaceted changes in gene expression during grape berry (Vitis vinifera L.) development. Planta 2005, 222, 832-847.
26. Pilati, S., Perazzolli, M., Malossini, A., Cestaro, A. et al., Genome-wide transcriptional analysis of grapevine berry ripening reveals a set of genes similarly modulated during three seasons and the occurrence of an oxidative burst at veraison. BMC Genomics 2007, 8, 428.
27. Deluc, L., Grimplet, J., Wheatley, M., Tillett, R. et al., Tran- scriptomic and metabolite analyses of Cabernet Sauvignon grape berry development. BMC Genomics 2007, 8, 429.
28. Fernandez, L., Torregrosa, L., Terrier, N., Sreekantan, L. etal., Identification of genes associated with flesh morphogenesis during grapevine fruit development. Plant Mol. Biol. 2007, 63, 307-323.
29. Waters, D., Holton, T., Ablett, E., Slade, L., Henry, R., The ripening wine grape berry skin transcriptome. Plant Sci. 2006, 171, 132-138.
30. Grimplet, J., Deluc, L., Tillett, R., Wheatley, M. etal., Tissue- specific mRNA expression profiling in grape berry tissues. BMC Genomics 2007, 8, 187.
31. Coombe, B., Adoption of a system for identifying grapevine growth stages. Aust. J. Grape Wine Res. 1995, 1, 104-110.
32. McCutchan, J., Shackel, K., Stem-water potential as a sensitive indicator of water stress in prune trees (Prunus domestica L. cv. French). J.Am. Soc. Hort. Sci. 1992, 117, 607-611.
33. Saravanan, R., Rose, J., A critical evaluation of sample extraction techniques for enhanced proteomic analysis of recalcitrant plant tissues. Proteomics 2004, 4, 2522-2532.
34. Hurkman, W., Tanaka, C., Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophore- sis. Plant Physiol. 1986, 81, 802-806.
35. O'Farrell, P., High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 1975, 250, 4007-4021.
36. Neuhoff, V., Arold, N., Taube, D., Ehrhardt, W., Improved staining of proteins in polyacrylamide gels including iso- electric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 1988, 9, 255-262.
37. Rosenfeld, J., Capdevielle, J., Guillemot, J., Ferrara, P., In-gel digestion of proteins for internal sequence analysis after one- or two-dimensional gel electrophoresis. Anal. Bio-chem. 1992, 203, 173-179.
38. Zhu, X., Papayannopoulos, I., Improvement in the detection of low concentration protein digests on a MALDI TOF/TOF workstation by reducing alpha-cyano-4-hydroxycinnamic acid adductions. J. Biomol. Tech. 2003, 14, 298-307.
39. Didier, G., Brezellec, P., Remy, E., Henaut, A., GeneANOVA-gene expression analysis of variance. Bioinformatics 2002, 18, 490-491.
40. Broeckling, C., Huhman, D., Farag, M., Smith, J. et al., Metabolic profiling of Medicago truncatula cell cultures reveals the effects of biotic and abiotic elicitors on metabolism. J. Exp. Bot. 2005, 56, 323-336.
41. Kopka, J., Schauer, N., Krueger, S., Birkemeyer, C. et al., GMD@CSB.DB: The Golm Metabolome Database. Bioinfor- matics 2005, 21, 1635-1638.
42. Chone, X., Van Leeuwen, C., Dubourdieu, D., Gaudillere, J., Stem water potential is a sensitive indicator of grapevine water status. Ann. Bot. (Lond.) 2001, 87, 477-483.
43. Parker, R., Flowers, T., Moore, A., Harpham, N., An accurate and reproducible method for proteome profiling of the effects of salt stress in the rice leaf lamina. J. Exp. Bot. 2006, 57, 1109-1118.
44. Hajduch, M., Casteel, J., Hurrelmeyer, K., Song, Z. et al., Proteomic analysis of seed filling in Brassica napus. Developmental characterization of metabolic isozymes using high-resolution two-dimensional gel electrophoresis. Plant Physiol. 2006, 141, 32-46.
45. Asirvatham, V., Watson, B., Sumner, L., Analytical and biological variances associated with proteomic studies of Medicago truncatula by two-dimensional polyacrylamide gel electrophoresis. Proteomics 2002, 2, 960-968.
46. Grimplet, J., Deluc, L., Cramer, G., Cushman, J., in: Matthew, A., Jenks, P. M. H., Jain, S. M. (Eds.), Advances in Molecular- Breeding Toward Droughtand SaltTolerantCrops, Springer, Dordrecht, The Netherlands 2007.
47. Escalona, J., Flexas, J., Bota, J., Medrano, H., Distribution of leaf photosynthesis and transpiration within grapevine canopies under different drought conditions. Vitis 2003, 42, 57-64.
48. Ageorges, A., Fernandez, L., Vialet, S., Merdinoglu, D. et al., Four specific isogenes of the anthocyanin metabolic pathway are systematically co-expressed with the red colour of grape berries. Plant Sci. 2006, 170, 372-383.
49. Shi, J., Yu, J., Pohorly, J., Kakuda, Y., Polyphenolics in grape seeds-biochemistry and functionality. J. Med. Food 2003, 6, 291-299.
50. Ibdah, M., Zhang, X., Schmidt, J., Vogt, T., A novel Mg(2+)- dependent O-methyltransferase in the phenylpropanoid metabolism of Mesembryanthemum crystallinum. J. Biol. Chem. 2003, 278, 43961-43972.
51. Castellarin, S., Di Gaspero, G., Marconi, R., Nonis, A. et al., Colour variation in red grapevines (Vitis vinifera L.): Geno- mic organisation, expression of flavonoid 3'-hydroxylase, flavonoid 3',5'-hydroxylase genes and related metabolite profiling of red cyanidin-/blue delphinidin-based anthocya- nins in berry skin. BMC Genomics 2006, 7, 12.
52. Kobayashi, S., Ishimaru, M., Hiraoka, K., Honda, C., Myb- related genes of the Kyoho grape (Vitis labruscana) regulate anthocyanin biosynthesis. Planta 2002, 215, 924-933.
53. Kobayashi, S., Goto-Yamamoto, N., Hirochika, H., Retro- transposon-induced mutations in grape skin color. Science2004, 304, 982.
54. Ford, C., Boss, P., Hoj, P., Cloning and characterization of Vitis vinifera UDP-glucose:flavonoid 3-O-glucosyltransfer- ase, a homologue of the enzyme encoded by the maize Bronze-1 locus that may primarily serve to glucosylate anthocyanidins in vivo. J. Biol. Chem. 1998, 273, 9224-9233.
55. Alfenito, M., Souer, E., Goodman, C., Buell, R. et al., Functional complementation of anthocyanin sequestration in the vacuole by widely divergent glutathione S-transferases. Plant Cell 1998, 10, 1135-1149.
56. Kobayashi, S., Ishimaru, M., Ding, C., Yakushiji, H., Goto, N., Comparison of UDP-glucose:flavonoid 3-O-glucosyl- transferase (UFGT) gene sequences between white grapes (Vitis vinifera) and their sports with red skin. Plant Sci. 2001, 160, 543-550.
57. Wang, X., He, X., Lin, J., Shao, H. etal., Crystal structure of isoflavone reductase from Alfalfa (Medicago sativa L.). J. Mol. Biol. 2006, 358, 1341-1352.
58. Famiani, F., Walker, R., Tecsi, L., Chen, Z. etal., An immuno- histochemical study of the compartmentation of metabolism during the development of grape (Vitis vinifera L.) berries. J. Exp. Bot. 2000, 51, 675-683.
59. Edwards, J., Walker, E., Coruzzi, G., Cell-specific expression in transgenic plants reveals nonoverlapping roles for chlor- oplast and cytosolic glutamine synthetase. Proc. Natl. Acad. Sci. USA 1990, 87, 3459-3463.
60. Pripis-Nicolau, L., de Revel, G., Bertrand, A., Lonvaud-Funel, A., Methionine catabolism and production of volatile sulphur compounds by Oenococcus oeni. J. Appl. Microbiol. 2004, 96, 1176-1184.
61. Hernandez-Orte, P., Cacho, J., Ferreira, V., Relationship between varietal amino acid profile of grapes and wine aromatic composition. Experiments with model solutions and chemometric study. J. Agric. Food Chem. 2002, 50, 2891-2899.
62. Hashizume, K., Tozawa, K., Endo, M., Aramaki, I., S-Adeno- syl-L-methionine-dependent O-methylation of 2-hydroxy-3- alkylpyrazine in wine grapes: A putative final step of meth- oxypyrazine biosynthesis. Biosci. Biotechnol. Biochem. 2001, 65,795-801.
63. Stines, A., Naylor, D., Hoj, P., van Heeswijck, R., Proline accumulation in developing grapevine fruit occurs independently of changes in the levels of delta1-pyrroline-5-carboxylate synthetase mRNA or protein. Plant Physiol. 1999, 120, 923-931.
64. Ibarz, M., Ferreira, V., Hernandez-Orte, P., Loscos, N., Cacho, J., Optimization and evaluation of a procedure for the gas chromatographic-mass spectrometric analysis of the aromas generated by fast acid hydrolysis of flavor precursors extracted from grapes. J. Chromatogr. A 2006, 1116, 217-229.
65. Rojas-Beltran, J., Dubois, F., Mortiaux, F., Portetelle, D. etal., Identification of cytosolic Mg2+-dependent soluble inorganic pyrophosphatases in potato and phylogenetic analysis. Plant Mol. Biol. 1999, 39, 449-461.
66. Davies, C., Robinson, S., Differential screening indicates a dramatic change in mRNA profiles during grape berry ripening. Cloning and characterization of cDNAs encoding putative cell wall and stress response proteins. Plant Phy- siol. 2000, 122, 803-812.
67. Tamburrini, M., Cerasuolo, I., Carratore, V., Stanziola, A. et al., Kiwellin, a novel protein from kiwi fruit. Purification, biochemical characterization and identification as an allergen. Protein J. 2005, 24, 423-429.
68. Fahlbusch, B., Rudeschko, O., Schumann, C., Steurich, F. et al., Further characterization of IgE-binding antigens in kiwi, with particular emphasis on glycoprotein allergens. J. Investig. Allergol. Clin. Immunol. 1998, 8, 325-332.
69. Huby, R., Dearman, R., Kimber, I., Why are some proteins allergens? Toxicol. Sci. 2000, 55, 235-246.
70. Reuter, A., Fortunato, D., Garoffo, L., Napolitano, L. et al., Novel isoforms of Pru av 1 with diverging immunoglobulin E binding properties identified by a synergistic combination of molecular biology and proteomics. Proteomics 2005, 5, 282-289.
71. Caporale, C., Facchiano, A., Bertini, L., Leonardi, L. et al., Comparing the modeled structures of PR-4 proteins from wheat. J. Mol. Model. 2003, 9, 9-15.
72. Aziz, A., Heyraud, A., Lambert, B., Oligogalacturonide signal transduction, induction of defense-related responses and protection of grapevine against Botrytis cinerea. Planta 2004, 218, 767-774.
73. Wimmer, B., Lottspeich, F., van der Klei, I., Veenhuis, M., Gietl, C., The glyoxysomal and plastid molecular chaper- ones (70 kDa heat shock protein) ofwatermelon cotyledons are encoded by a single gene. Proc. Natl. Acad. Sci. USA 1997, 94, 13624-13629.
74. Liu, Y., Burch-Smith, T., Schiff, M., Feng, S., Dinesh-Kumar, S., Molecular chaperone Hsp90 associates with resistance protein N and its signaling proteins SGT1 and Rar1 to modulate an innate immune response in plants. J. Biol. Chem. 2004, 279, 2101-2108.
75. Boulton, R., Singleton, V., Bisson, L., Kunkee, R., Principles and Practices of Winemaking, Aspen Publishers, New York 1998.
76. Dry, I., Robinson, S., Molecular cloning and characterisation of grape berry polyphenol oxidase. Plant Mol. Biol. 1994, 26, 495-502.
77. Rathjen, H., Robinson, S., Characterisation of a variegated grapevine mutant ahowing reduced polyphenol oxidase activity. Funct. Plant Biol. 1992, 19, 43-54.
78. Battaglia, M., Olvera-Carrillo, Y., Garciarrubio, A., Campos, F., Covarrubias, A., The enigmatic LEA proteins and other hydrophilins. Plant Physiol. 2008, 148, 6-24.
79. Soulages, J., Kim, K., Arrese, E., Walters, C., Cushman, J., Conformation of a group 2 late embryogenesis abundant protein from soybean. Evidence of poly (L-proline)-type II structure. Plant Physiol. 2003, 131, 963-975.
80. DeBolt, S., Cook, D., Ford, C., L-tartaric acid synthesis from vitamin C in higher plants. Proc. Natl. Acad. Sci. USA 2006, 103, 5608-5613.
81. Possner, D., Kliewer, W., The localization of acids, sugars, potassium and calcium in developing grape berries. Vitis 1985, 24, 229-240.
82. Debolt, S., Melino, V., Ford, C., Ascorbate as a biosynthetic precursor in plants. Ann. Bot. (Lond.)2007, 99, 3-8.
83. Mato, I., Suarez-Luque, S., Huidobro, J., Simple determination of main organic acids in grape juice and wine by using capillary zone electrophoresis with direct UV detection. Food Chem. 2007, 102, 104-112.
84. Conde, C., Agasse, A., Glissant, D., Tavares, R. et al., Pathways of glucose regulation of monosaccharide transport in grape cells. Plant Physiol. 2006, 141, 1563-1577.
85. Hawker, J. S., Ruffner, H., Walker, R., The sucrose content of some australian grapes. Am. J. Enol. Viticult. 1976, 27, 125129.
86. Garlick, A., Moore, C., Kruger, N., Monitoring flux through the oxidative pentose phosphate pathway using [1-14C]glu- conate. Planta 2002, 216, 265-272.
87. Peinado, R., Moreno, J., Medina, M., Mauricio, J., Potential application of a glucose-transport-deficient mutant of Schi- zosaccharomyces pombe for removing gluconic acid from grape must. J. Agric. Food Chem. 2005, 53, 1017-1021.
88. Gomez, L., Baud, S., Graham, I., The role of trehalose-6- phosphate synthase in Arabidopsis embryo development. Biochem. Soc. Trans. 2005, 33, 280-282.
89. D'Arcy-Lameta, A., Ferrari-Iliou, R., Contour-Ansel, D., Pham-Thi, A., Zuily-Fodil, Y., Isolation and characterization of four ascorbate peroxidase cDNAs responsive to water deficit in cowpea leaves. Ann. Bot. (Lond.) 2006 97, 133-140.
90. Castellarin, S., Pfeiffer, A., Sivilotti, P., Degan, M. et al., Transcriptional regulation of anthocyanin biosynthesis in ripening fruits of grapevine under seasonal water deficit. Plant Cell. Environ. 2007, 30, 1381-1399.
91. Castellarin, S., Matthews, M., Di Gaspero, G., Gambetta, G., Water deficits accelerate ripening and induce changes in gene expression regulating flavonoid biosynthesis in grape berries. Planta 2007, 227, 101-112.
92. Fait, A., Fromm, H., Walter, D., Galili, G., Fernie, A., Highway or byway: The metabolic role of the GABA shunt in plants. Trends Plant Sci. 2007 13, 14-19.
93. Bytof, G., Knopp, S.-E., Schieberle, P., Teutsch, I., Selmar, D., Influence of processing on the generation of gamma-ami- nobutyric acid in green coffee beans. Eur. Food Res. Tech-nol. 2005, 220, 245-250.
94. Rhodes, D., Handa, S., Bressan, R., Metabolic changes associated with adaptation of plant cells to water stress. Plant Physiol. 1986, 82, 890-903.
95. Taji, T., Ohsumi, C., Iuchi, S., Seki, M. etal., Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J. 2002, 29, 417-426.
96. Robinson, S., Jacobs, A., Dry, I., A class IV chitinase is highly expressed in grape berries during ripening. Plant Physiol. 1997, 114, 771-778.
97. Tesniere, C., Torregrosa, L., Pradal, M., Souquet, J. et al., Effects of genetic manipulation of alcohol dehydrogenase levels on the response to stress and the synthesis of secondary metabolites in grapevine leaves. J. Exp. Bot. 2006, 57, 91-99.
98. Coleman, H., Ellis, D., Gilbert, M., Mansfield, S., Up-reg-ulation of sucrose synthase and UDP-glucose pyrophos- phorylase impacts plant growth and metabolism. Plant Biotechnol. J. 2006, 4, 87-101.
99. Watson, B., Asirvatham, V., Wang, L., Sumner, W., Mapping the proteome of barrel medic (Medicago truncatula). Plant Physiol. 2003, 131, 1104-1123.
100. Liu, Y., Lamkemeyer, T., Jakob, A., Mi, G. et al., Comparative proteome analyses of maize (Zea mays L.) primary roots prior to lateral root initiation reveal differential protein expression in the lateral root initiation mutant rum1. Proteomics 2006, 6, 4300-4308.
101. Faurobert, M., Mihr, C., Bertin, N., Pawlowski, T. et al., Major proteome variations associated with cherry tomato pericarp development and ripening. Plant Physiol. 2007, 143, 1327-1346.
102. Gion, J.-M., Lalanne, C., Le Provost, G., Ferry-Dumazet, H. etal., The proteome of maritime pine wood forming tissue. Proteomics 2005, 5, 3731-3751.