Strawberry is worldwide appreciated for its unique flavour and as a source of macronutrients and high levels of antioxidants which are closely related to fruit ripening. We report the investigation of the complex physiological processes of strawberry fruit ripening at proteomic level. Multiple approaches were used to investigate strawberry fruit proteome. In particular, a proteome reference map of strawberry fruit from Queen Elisa élite genotype was achieved by 2-D analyses of proteins extracted from berries at immature, turning and red stages to isolate a set of proteins commonly present in fruit during ripening. In addition, several hundreds of proteins were identified by a combination of multidimensional liquid chromatography/tandem mass spectrometry and one dimensional SDS-PAGE coupled with nano-liquid chromatography/tandem mass spectrometry. DIGE technology was also used to identify differentially accumulated proteins during ripening and to correlate fruit protein expression with quality traits of the reference variety Queen Elisa and its parental genotypes. A number of constitutive or differentially accumulated proteins were found. Generally, the pattern of protein expression as well as the putative function of identified proteins argues for a role in major fruit physiological developmental and ripening processes. The role of some of the identified proteins is discussed in relation to strawberry fruit ripening and to quality traits. Consequently, this study provides the first characterization of the strawberry fruit proteome and the time course of variation during maturation by using multiple approaches. © 2008 Elsevier B.V. All rights reserved.

Cited By :53Export Date: 16 July 2015Correspondence Address: Perrotta, G.; ENEA, Centro Ricerche Trisaia, Rotondella, Matera, Italy; email: gaetano.perrotta@trisaia.enea.itChemicals/CAS: Plant Proteins; ProteomeReferences: Giovannoni, J., Molecular biology of fruit maturation and ripening (2001) Annu Rev Plant Physiol Plant Mol Biol, 52, pp. 725-749;Folta, K.M., Davis, T.M., Strawberry genes and genomics (2006) CRC Crit Rev Plant Sci, 25, pp. 399-415; Katz, E., Fon, M., Lee, Y.J., Phinney, B.S., Sadka, A., Blumwald, E., The citrus fruit proteome: insights into citrus fruit metabolism (2007) Planta, 226, pp. 989-1005; Deytieux, C., Geny, L., Lapaillerie, D., Claverol, S., Bonneu, M., Donèche, B., Proteome analysis of grape skins during ripening (2007) J Exp Bot, 58, pp. 1851-1862; Alm, R., Ekefjärd, A., Krogh, M., Häkkinen, J., Emanuelsson, C., Proteomic variation is as large within as between strawberry varieties (2007) J Proteome Res, 6, pp. 3011-3020; Hjernø, K., Alm, R., Canbäck, B., Matthiesen, R., Trajkovski, K., Bjork, L., Down-regulation of the strawberry Bet v-homologous allergen in concert with the flavonoid biosynthesis pathway in colorless strawberry mutant (2006) Proteomics, 6, pp. 1574-1587; Clements, R.L., Protein patterns in fruit (1970) The biochemistry of fruit and their products, pp. 159-177. , Hulme A.C. (Ed), Academic press, London New York; Zivy, M., De Vienne, D., Proteomics: a link between genomics, genetics and physiology (2000) Plant Mol Biol, 44, pp. 575-580; Carpentier, S.C., Panis, B., Vertommen, A., Swennen, R., Sergeant, K., Renaut, J., Proteome analysis of non-model plants: a challenging but powerful approach (2008) Mass Spectrom Rev, 27, pp. 354-377; Okie, W.R., Register of new fruit and nut varieties (2004) HortScience, 39, pp. 1509-1523; Carbone, F., Mourgues, F., Biasioli, F., Gasperi, F., Märk, T.D., Rosati, C., Development of molecular and biochemical tools to investigate fruit quality traits in strawberry elite genotypes (2006) Mol Breeding, 18, pp. 127-142; Unlu, M., Morgan, M.E., Minden, J.S., Difference gel electrophoresis: a single gel method for detecting changes in protein extracts (1997) Electrophoresis, 18, pp. 2071-2077; Laemmli, U., Cleavage of structural proteins during the assembly of the head of bacteriophage T4 (1970) Nature, 227, pp. 680-685; Neuhoff, V., Arold, N., Taube, D., Ehrhardt, W., 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 (1988) Electrophoresis, 9, pp. 255-262; Sappl, P.G., Heazlewood, J.L., Millar, A.H., Untangling multi-gene families in plants by integrating proteomics into functional genomics (2004) Phytochemistry, 65, pp. 1517-1530; Larsen, M.R., Roepstorff, P., Mass spectrometric identification of proteins and characterization of their post translational modifications in proteome analysis (2000) Fresenius J Anal Chem, 366, pp. 677-690; Son, D.Y., Scheurer, S., Hoffmann, A., Haustein, D., Vieths, S., Pollen-related food allergy: cloning and immunological analysis of isoforms and mutants of Mal d 1, the major apple allergen, and Bet v 1, the major birch pollen allergen (1999) Eur J Nutr, 38, pp. 201-215; Holm, J., Baerentzen, G., Gajhede, M., Ipsen, H., Larsen, J.N., Lowenstein, H., Molecular basis of allergic cross-reactivity between group 1 major allergens from birch and apple (2001) J Chromatogr B Biomed Sci Appl, 756, pp. 307-313; Laugesen, S., Roepstorff, P., Combination of two matrices results in improved performance of MALDI MS for peptide mass mapping and protein analysis (2003) J Am Soc Mass Spectrom, 4, pp. 992-1002; Halbwirth, H., Puhl, I., Haas, U., Jezik, K., Treutter, D., Stich, K., Two-phase flavonoid formation in developing strawberry (Fragaria x ananassa) fruit (2006) J Agric Food Chem, 54, pp. 1479-1485; Almeida, J.R.M., D’Amico, E., Preuss, A., Carbone, F., de Vos, C.H.R., Deiml, B., Characterization of major enzymes and genes involved in flavonoid and proanthocyanidin biosynthesis during fruit development in strawberry (Fragaria × ananassa) (2007) Arch Biochem Biophys, 465, pp. 61-71; Jimenez, A., Creissen, G., Kular, B., Firmin, J., Robinson, S., Verhoeyen, M., Changes in oxidative processes and components of the antioxidant system during tomato fruit ripening (2002) Planta, 214, pp. 751-758; Asada, K., (1996) Photosynthesis and the environment, , Baker N.R. (Ed), Kluwer, Dordrecht; Wang, W., Vinocur, B., Shoseyov, O., Altman, A., Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response (2004) Trends Plant Sci, 9, pp. 244-252; Arrigo, A.P., Small stress proteins: chaperones that act as regulators of intracellular redox state and programmed cell death (1998) Biol Chem, 379, pp. 19-26; Sun, W., Van Montagu, M., Verbruggen, N., Small heat shock proteins and stress tolerance in plants (2002) Biochim Biophys. Acta Gene Struct Expr, 1577, pp. 1-9; Kafkas, E., Kosar, M., Paydas, S., Kafkas, S., Baser, K.H.C., Quality characteristics of strawberry genotypes at different maturation stages (2007) Food Chem, 100, pp. 1229-1236; Hancock, J.F., Strawberries (1999) Crop production science in horticulture, , Cambridge University Press; Popova, T.N., Pinheiro de Carvalho, M.A.A., Citrate and isocitrate in plant metabolism (1998) Biochim Biophys Acta, Bioenerg, 1364, pp. 307-325; Boggio, S.B., Palatnik, J.F., Heldt, H.W., Valle, E.M., Changes in amino acid composition and nitrogen metabolizing enzymes in ripening fruits of Lycopersicon esculentum Mill (2000) Plant Sci, 159, pp. 125-133; Gallardo, F., Galvez, S., Gadal, P., Canovas, F.M., Changes in NADP+-linked isocitrate dehydrogenase during tomato fruit ripening. Characterization of the predominant cytosolic enzyme from green and ripe pericarp (1995) Planta, 196, pp. 148-154; Fuke, S., Konosu, S., Taste-active components in some foods: a review of Japanese research (1991) Physiol Behav, 49, pp. 863-868; Omura, T., Watanabe, S., Iijima, Y., Aoki, K., Shibata, D., Ezura, H., Molecular and genetic characterization of transgenic tomato expressing 3-hydroxy-3-methylglutaryl coenzyme A reductase (2007) Plant Biotec, 24, pp. 107-115; D’Amico, E., Perrotta, G., Genomics of berry fruits antioxidant components (2005) BioFactors, 23, pp. 179-187; Nguyen-Quoc, B., Foyer, C.H., A role for ’futile cycles’ involving invertase and sucrose synthase in sucrose metabolism of tomato fruit (2001) J Exp Bot, 52, pp. 881-889; Smith, H.B., Sucrose synthase and the fruit of its labor (1999) Plant Cell, 11, pp. 2261-2262; Winter, H., Huber, S.C., Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes (2000) Crit Rev Biochem Mol Biol, 35, pp. 253-289; Koch, K., Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development (2004) Curr Opin Plant Biol, 7, pp. 235-246; Wein, M., Lewinsohn, E., Schwab, W., Metabolic fate of isotopes during the biological transformation of carbohydrates to 2,5-dimethyl-4-hydroxy-3(2H)-furanone in strawberry fruits (2001) J Agric Food Chem, 49, pp. 2427-2432; Schwab, W., Roscher, R., 4-Hydroxy-3(2H)-furanones: natural and maillard products (1997) Recent Res Dev Phytochem, 1, pp. 643-673; Sanz, C., Richardson, D.G., Pérez, A.G., 2,5-Dimethyl-4-hydroxy-3(2H)-furanone and derivatives in strawberries during ripening (1995) Fruit flavors: biogenesis, characterization, and authentication. ACS Symposium Series 596, pp. 268-275. , Rouseff R.L., and Leahy M.M. (Eds), American Chemical Society, Washington, DC; Roscher, R., Bringmann, G., Schreier, P., Schwab, W., Radiotracer studies on the formation of 2,5- dimethyl-4-hydroxy-3(2H)-furanone in detached ripening strawberry fruits (1998) J Agric Food Chem, 46, pp. 1488-1493; Schwab, W., Metabolome diversity: too few genes, too many metabolites? (1998) Phytochemistry, 62, pp. 837-849; Wein, M., Lewinson, E., Schwab, W., Metabolic fate of isotopes during the biological transformation of carbohydrates to 2,5-dimethyl-4-hydroxy-3(2H)-furanone in strawberry fruits (2001) J Agric Food Chem, 49, pp. 2427-2432; Raab, T., Lopez-Raez, J.A., Klein, D., Caballero, J.L., Moyano, E., Schwab, W., FaQR, required for the biosynthesis of the strawberry flavor compound 4-hydroxy-2,5-dimethyl-3(2H)-furanone, encodes an enone oxidoreductase (2006) Plant Cell, 18, pp. 1023-1037; Wilkinson, J.Q., Lanahan, M.B., Conner, T.W., Klee, H.J., Identification of mRNAs with enhanced expression in ripening strawberry fruit using polymerase chain reaction differential display (1995) Plant Mol Biol, 27, pp. 1097-1108; Proust, J., Houlné, G., Schantz, M.L., Schantz, R., Characterization and gene expression of an annexin during fruit development in Capsicum annuum (1996) FEBS Lett, 383, pp. 208-212; Bonghi, C., Ferrarese, L., Ruperti, B., Tonutti, P., Ramina, A., Endo-beta-1,4-glucanases are involved in peach fruit growth and ripening, and regulated by ethylene (1998) Physiol Plant, 102, pp. 346-352; Rao, G.U., Paran, I., Polygalacturonase: a candidate gene for soft flesh and deciduous fruit mutation in Capsicum (2003) Plant Mol Biol, 51, pp. 135-141; Pressey, R., Avants, J.K., Differences in polygalacturonase composition of clingstone and freestone peaches (1978) J Food Sci, 43, pp. 1415-1421; Lester, D.R., Speirs, G., Orr, G., Brady, C.J., Peach (Prunus persica) endo-PG cDNA isolation and mRNA analysis in melting and non-melting peach cultivars (1994) Plant Physiol, 105, pp. 225-231; Hadfield, K.A., Bennett, A.B., Polygalacturonases: many genes in search of a function (1998) Plant Physiol, 117, pp. 337-343; Li, Y., Jones, L., McQueen-Mason, S., Expansins and cell growth (2003) Current Op Plant Biol, 6, pp. 603-610; Faurobert, M., Mihr, C., Bertin, N., Pawlowski, T., Negroni, L., Major proteome variations associated with cherry tomato pericarp development and ripening[OA] (2007) Plant Physiol, 143, pp. 1327-1346; Romero, H.M., Berlett, B.S., Jensen, P.J., Pell, E., Tien, M., Investigations into the role of the plastidial peptide methionine sulfoxide reductase in response to oxidative stress in arabidopsis (2004) Plant Physiol, 136, pp. 3784-3794; Lincoln, J.E., Cordes, S., Read, E., Fischer, R.L., Regulation of gene expression by ethylene during Lycopersicon esculentum (tomato) fruit development (1987) Proc Natl Acad Sci USA, 84, pp. 2793-2797; Lopez, A.P., Portales, R.B., Lopez-Raez, J.A., Medina-Escobar, N., Blanco, J.M., Characterization of a strawberry late-expressed and fruit-specific peptide methionine sulphoxide reductase (2006) Physiol Plant, 126, pp. 129-139; Reichheld, J.P., Vernoux, T., Lardon, F., Van Montagu, M., Inzé, D., Specific checkpoints regulate plant cell cycle progression in response to oxidative stress (1999) Plant J, 17, pp. 647-656; Thompson, J.E., Hopkins, M.T., Taylor, C., Wang, T.W., Regulation of senescence by eukaryotic translation initiation factor 5A: implications for plant growth and development (2004) Trends Plant Sci, 9, pp. 174-179; Wang, T.W., Lu, L., Wang, D., Thompson, J.E., Isolation and characterization of senescence-induced cDNAs encoding deoxyhypusine synthase and eukaryotic translation initiation factor 5A from tomato (2001) J Biol Chem, 276, pp. 17541-17549; Lopez, A.P., Franco, A.R., Cloning and expression of cDNA encoding translationally controlled tumor protein from strawberry fruits (2006) Biol Plantarum, 50, pp. 447-449; Gachet, Y., Lee, M., Sawitzki, M., Tournier, S., Poulton, T., Intracellular colocalisation of the translationally controlled protein P23 with cytoskeletal structures (1997) Biochem Soc Trans, 25, p. 269; Duck, N., McCormick, S., Winter, J., Heat shock protein Hsp70 cognate gene expression in vegetative and reproductive organs of Lycopersicon esculentum (1989) Proc Natl Acad Sci USA, 86, pp. 3674-3678; Neta-Sharir, I., Isaacson, T., Lurie, S., Weiss, D., Dual role for tomato heat shock protein 21: protecting photosystem II from oxidative stress and promoting color changes during fruit maturation (2005) Plant Cell, 17, pp. 1829-1838; Honkanen, E., Hirvi, T., The flavour of berries (1990) Food flavours, pp. 125-193. , Morton I.D., and MacLeod A.J. (Eds), Elsevier Scientific Publications, Amsterdam; Latrasse, A., Fruits III (1991) Volatile compounds in foods and beverages, pp. 329-387. , Maarse H. (Ed), Dekker, New York; Douillard, C., Guichard, E., Comparison by multidimensional analysis of concentrations of volatile compounds in fourteen frozen strawberry varieties (1989) Sci Aliments, 9, pp. 53-76; Douillard, C., Guichard, E., The aroma of strawberry (Fragaria ananassa): characterisation of some cultivars and influence of freezing (1990) J Sci Food Agric, 50, pp. 517-531; Larsen, M., Poll, L., Odor thresholds of some important aroma compounds in strawberries (1992) Z Lebensm Unters Forsch, 195, pp. 120-123; Larsen, M., Poll, L., Olsen, C.E., Evaluation of the aroma composition of some strawberry (Fragaria ananassa Duch) cultivars by use of odour threshold values (1992) Z Lebensm Unters Forsch, 195, pp. 536-539