Abstract
Cold-induced sweetening is one of the major factors limiting the quality of fried potato products. To understand the mechanisms of protein regulation for cold-induced sweetening in potato tubers, a comparative proteomic approach was used to analyse the differentially expressed proteins both during control (25 °C, 30 days) and cold treatment (4 °C, 30 days) using two-dimensional gel electrophoresis. Quantitative image analyses indicated that there were 25 protein spots with their intensities significantly altered more than twofold. Of these proteins, 9 were up-regulated, 13 were down-regulated, 2 were absent, and 1 was induced in the cold-stored tubers. The MALDI-TOF/TOF MS analyses led to the identification of differentially expressed proteins that are involved in several processes and might work cooperatively to maintain metabolic homeostasis in tubers during low-temperature storage. The preponderance of metabolic proteins reflects the inhibition of starch re-synthesis and the accumulation of sugars in carbon fluxes, linking starch–sugar conversion. The respiration-related proteins suggest the transfer of respiratory activity from aerobic respiration to anaerobic respiration in the cold-stored tubers. The proteins associated with defence appear to protect the tuber cells from low-temperature stress. Some heat shock proteins that act as chaperones also displayed a differential expression pattern, suggesting a potentially important role in cold-stored tubers, although their exact contribution remains to be investigated. The proposed hypothetical model might explain the interaction of these differentially expressed proteins that are associated with cold-induced sweetening in tubers.
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References
Aghaei K, Ehsanpour AA, Komatsu S (2008) Proteome analysis of potato under salt stress. J Proteome Res 7:4858–4868
Agrawal L, Chakraborty S, Jaiswal DK, Gupta S, Datta A, Chakraborty N (2008) Comparative proteomics of tuber induction, development and maturation reveal the complexity of tuberization process in potato (Solanum tuberosum L.). J Proteome Res 7:3803–3817
Ambard-Bretteville F, Sorin C, Rébeillé F, Hourton-Cabassa C, Colas des Francs-Small C (2003) Repression of formate dehydrogenase in Solanum tuberosum increases steady-state levels of formate and accelerates the accumulation of proline in response to osmotic stress. Plant Mol Biol 52:1153–1168
Araújo WL, Nunes-Nesi A, Trenkamp S, Bunik VI, Fernie AR (2008) Inhibition of 2-oxoglutarate dehydrogenase in potato tuber suggests the enzyme is limiting for respiration and confirms its importance in nitrogen assimilation. Plant Physiol 148:1782–1796
Barel G, Ginzberg I (2008) Potato skin proteome is enriched with plant defence components. J Exp Bot 59:3347–3357
Baysal T, Demirdoven A (2007) Lipoxygenase in fruits and vegetables: a review. Enzyme Microb Technol 40:491–496
Bethke PC, Busse JC (2008) Validation of a simple, colorimetric, microplate assay using amplex red for the determination of glucose and sucrose in potato tubers and other vegetables. Am J Potato Res 85:414–421
Bhaskar PB, Wu L, Busse JS, Whitty BR, Hamernik AJ, Jansky SH, Buell CR, Bethke PC, Jiang J (2010) Suppression of the vacuolar invertase gene prevents cold-induced sweetening in potato. Plant Physiol 154:939–948
Blenkinsop RW, Copp LJ, Yada RY, Marangoni AG (2002) Effect of chlorpropham (CIPC) on carbohydrate metabolism of potato tubers during storage. Food Res Int 35:651–655
Blenkinsop RW, Yada RY, Marangoni AG (2004) Metabolic control of low-temperature sweetening in potato tubers during postharvest storage. Hortic Rev 30:317–354
Borgmann K, Sinka P, Frommer WB (1994) Changes in the two-dimensional protein pattern and in gene expression during the sink-to-source transition of potato tubers. Plant Sci 99:97–108
Brummell DA, Chen RK, Harris JC, Zhang H, Hamiaux C, Kralicek AV, McKenzie MJ (2011) Induction of vacuolar invertase inhibitor mRNA in potato tubers contributes to cold-induced sweetening resistance and includes spliced hybrid mRNA variants. J Exp Bot 62:3519–3534
Bunik VI, Fernie AR (2009) Metabolic control exerted by the 2-oxoglutarate dehydrogenase reaction: a cross-kingdom comparison of the crossroad between energy production and nitrogen assimilation. Biochem J 422:405–421
Bykova NV, Stensballe A, Egsgaard H, Jensen ON, Moller IM (2003) Phosphorylation of formate dehydrogenase in potato tuber mitochondria. J Biol Chem 278:26021–26030
Campbell M, Segear E, Beers L, Knauber D, Suttle J (2008) Dormancy in potato tuber meristems: chemically induced cessation in dormancy matches the natural process based on transcript profiles. Funct Integr Genomics 18:317–328
Chen S, Harmon AC (2006) Advances in plant proteomics. Proteomics 6:5504–5516
Chen S, Hajirezaei MR, Zanor MI, Hornyik C, Debast S, Lacomme C, Fernie AD, Sonnewald U, Bornke F (2008) RNA interference-mediated repression of sucrose-phosphatase in transgenic potato tubers (Solanum tuberosum) strongly affects the hexose-to-sucrose ratio upon cold storage with only minor effects on total soluble carbohydrate accumulation. Plant Cell Environ 31:165–176
Cottrell JE, Duffus CM, Paterson L, Mackay GR, Allison MJ, Bain H (1993) The effect of storage temperature on reducing sugar concentration and the activities of three amylolytic enzymes in tubers of the cultivated potato, Solanum tuberosum L. Potato Res 36:107–117
Cross JM, Clancy M, Shaw JR, Greene TW, Schmidt RR, Okita TW, Hannah LC (2004) Both subunits of ADP-glucose pyrophosphorylase are regulatory. Plant Physiol 135:137–144
Dale MFB, Bradshaw JE (2003) Progress in improving processing attributes in potato. Trends Plant Sci 8:310–312
De Wilde T, De Meulenaer B, Mestdagh F, Govaert Y, Vandeburie S, Ooghe W, Fraselle S, Demeulemeester K, Van Peteghem C, Calus A, Degroodt JM, Verhe RA (2005) Influence of storage practices on acrylamide formation during potato frying. J Agric Food Chem 53:6550–6557
Delaplace P, Fauconnier ML, Sergeant K, Dierick JF, Oufir M, van der Wal F, America AH, Renaut J, Hausman JF, du Jardin P (2009) Potato (Solanum tuberosum L.) tuber ageing induces changes in the proteome and antioxidants associated with the sprouting pattern. J Exp Bot 60:1273–1288
Espen L, Morgutti S, Cocucci SM (1999) Changes in the potato (Solanum tuberosum L.) tuber at the onset of dormancy and during storage at 23°C and 3°C. II. Evaluation of protein patterns. Potato Res 42:203–214
FAO (2011) World potato production and area. FAOSTAT http://faostat.fao.org
Feng JT, Liu YK, Song HY, Dai Z, Qin LX, Almofti R, Fang CY, Lu HJ, Yang PY, Tang ZY (2005) Heat-shock protein 27: a potential biomarker for hepatocellular carcinoma identified by serum proteome analysis. Proteomics 17:4581–4588
Geigenberger P, Fernie AR (2006) Starch biosynthesis in the potato tuber. Food biochemistry and food processing. Blackwell Publishing, Oxford, pp 253–270
Geigenberger P, Still M, Fernie AR (2004) Metabolic control analysis and regulation of the conversion of sucrose to starch in growing potato tubers. Plant Cell Environ 27:655–673
Hajirezaei M, Bornke F, Peisker M, Lerchi J, Sonnewald U (2003) Decreased sucrose content triggers starch breakdown and respiration in stored potato (Solanum tuberosum L.). J Exp Bot 382:477–488
Hamernik AJ, Hanneman RE, Jansky SH (2009) Introgression of wild species germplasm with extreme resistance to cold sweetening into the cultivated potato. Crop Sci 49:529–542
Hammond JBW, Burrel MM, Kruger NJ (1990) Effect of low temperature on the activity of phosphofructokinase from potato tubers. Planta 180:613–616
Handa M, Guidotti G (1996) Purification and cloning of a soluble ATP-diphosphohydrolase (apyrase) from potato tubers (Solanum tuberosum). Biochem Biophys Res Commun 218:916–923
Hanson AD, Roje S (2001) One-carbon metabolism in higher plants. Annu Rev Plant Physiol Plant Mol Biol 52:119–137
Heike G, Heibges A, Salamini E, Gebhardt C (2002) Members of the Kunitz-type protease inhibitor gene family of potato inhibits soluble tuber invertase in vitro. Potato Res 45:163–176
Hourton-Cabassa C, Ambard-Bretteville F, Moreau F, Davy de Virville J, Rémy R, Colas des Francs-Small C (1998) Stress induction of mitochondrial formate dehydrogenase in potato leaves. Plant Physiol 116:627–635
Jiang Y, Yang B, Harris NS, Deyholos MK (2007) Comparative proteomics analysis of NaCl stress-responsive proteins in Arabidopsis roots. J Exp Bot 58:3591–3607
Kaplan F, Kopka J, Sung DY, Zhao W, Popp M, Porat R, Guy CL (2007) Transcript and metabolite profiling during cold acclimation of Arabidopsis reveals an intricate relationship of cold-regulated gene expression with modifications in metabolite content. Plant J 50:967–981
Koistinen KM, Hassinen VH, Gynther PAM, Lehesranta SJ, Keinänen SI, Kokko HI, Oksanen EJ, Tervahauta AI, Auriola S, Kärenlampi SO (2002) Birch PR-10c is induced by factors causing oxidative stress but appears not to confer tolerance to these agents. New Phytol 155:381–391
Kosová K, Vítámvás P, Prásil IT, Renaut J (2011) Plant proteome changes under abiotic stress—contribution of proteomics studies to understanding plant stress response. J Proteomics 74:1301–1322
Lehesranta SJ, Davies HV, Shepherd LVT, Nunan N, McNicol JM, Auriola S, Koistinen KM, Suomalainen KM, Kokko HI, Kärenlampi SO (2005) Comparison of tuber proteomes of potato varieties, landraces, and genetically modified lines. Plant Physiol 138:1690–1699
Lehesranta SJ, Davies HV, Shepherd LVT, Koistinen KM, Massat N, Nunan NM, McNicol JW, Kärenlampi SO (2006) Proteomic analysis of the potato tuber life cycle. Proteomics 6:6042–6052
Li L, Paulo MJ, Strahwald J, Lübeck J, Hofferbert HR, Tacke E, Junghans H, Wunder J, Draffehn A, van Eeuwijk F (2008) Natural DNA variation at candidate loci is associated with potato chip color, tuber starch content, yield and starch yield. Theor Appl Genet 116:1167–1181
Liu Y, Burch-Smith T, Schiff M, Feng S, Dinesh-Kumar SP (2004) 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 279:2101–2108
Lytovchenko A, Schauer N, Willmitzer L, Fernie AR (2005) Tuber-specific cytosolic expression of a bacterial phosphoglucomutase in potato (Solanum tuberosum L.) dramatically alters carbon partitioning. Plant Cell Physiol 46:588–597
Malone JG, Mittova V, Ratcliffe RG, Kruger NJ (2006) The response of carbohydrate metabolism in potato tubers to low temperature. Plant Cell Physiol 47:1309–1322
Manjunath S, Lee CH, Van Winkle P, Bailey-Serres J (1998) Molecular and biochemical characterization of cytosolic phosphoglucomutase in maize. Expression during development and in response to oxygen deprivation. Plant Physiol 117:997–1006
Matsuura-Endo C, Kobayashi A, Noda T, Takigawa S, Yamauchi H, Mori M (2004) Changes in sugar content and activity of vacuolar acid invertase during low-temperature storage of potato tubers from six Japanese cultivars. J Plant Res 117:131–137
McKenzie MJ, Sowokinos JR, Shea IM, Gupta SK, Lindlauf RR, Anderson JAD (2005) Investigations on the role of acid invertase and UDP-glucose pyrophosphorylase in potato clones with varying resistance to cold-induced sweetening. Am J Potato Res 82:231–239
Menendez CM, Ritter E, Schafer-Pregl R, Walkemeier B, Kalde A, Salamini F, Gebhardt C (2002) Cold sweetening in diploid potato: mapping quantitative trait loci and candidate genes. Genetics 162:1423–1434
Mizuno M, Kamei M, Tsuchida H (1998) Ascorbate peroxidase and catalase cooperate for protection against hydrogen peroxide generated in potato tubers during low-temperature storage. IUBMB Life 44:717–726
Mottram DS, Wedzicha BL, Dodson AT (2002) Acrylamide is formed in the Maillard reaction. Nature 419:448–449
Müller-Thurgau H (1882) Über Zuckeranhäufung in Pflanzentheilen in Folge niederer Temperatur. Landwirtsch Jahrb 11:751–828
Muttucumaru N, Elmore JS, Curtis T, Mottram DS, Parry MAJ, Halford NG (2008) Reducing acrylamide precursors in raw materials derived from wheat and potato. J Agric Food Chem 56:6167–6172
Nägele T, Henkel S, Hörmiller I, Sauter T, Sawodny O, Ederer M, Heyer AG (2010) Mathematical modeling of the central carbohydrate metabolism in Arabidopsis reveals a substantial regulatory influence of vacuolar invertase on whole plant carbon metabolism. Plant Physiol 153:260–272
Navrátil O, Fischer L, Čmejlová J, Linhart M, Vacek J (2007) Decreased amount of reducing sugars in transgenic potato tubers and its influence on yield characteristics. Biol Plant 51:56–60
Palcy S, Chevet E (2006) Integrating forward and reverse proteomics to unravel protein function. Proteomics 6:5467–5480
Plesner L (1995) Ecto-ATPases: identities and functions. Int Rev Cytol 158:141–214
Pradet-Balade B, Boulme F, Beug H, Muliner EW, Garcia-Sanz JA (2001) Translation control: bridging the gap between genomics and proteomics? Trends Biochem Sci 26:225–229
Queitsch C, Sangster TA, Lindquist S (2002) Hsp90 as a capacitor of phenotypic variation. Nature 417:618–624
Reimholz R, Geiger M, Haake V, Deiting U, Krause KP, Sonnewald U, Stitt M (1997) Potato plants contain multiple forms of sucrose phosphate synthase, which differ in their tissue distributions, their levels during development, and their responses to low temperature. Plant Cell Environ 20:291–305
Reverberi M, Picardo M, Ricelli A, Camera E, Fanelli C, Fabbri AA (2001) Oxidative stress, growth factor production and budding in potato tubers during cold storage. Free Radic Res 35:833–841
Riewe D, Grosman L, Fernie AR, Wucke C, Geigenberger P (2008) The potato-specific apyrase is apoplastically localized and has influence on gene expression, growth, and development. Plant Physiol 147:1092–1109
Shah S, Lee YJ, Hannapel DJ, Rao AG (2011) Protein profiling of the potato petiole under short day and long day photoperiods. J Proteomics 74:212–230
Shallenberger RS, Smith O, Treadway RH (1959) Role of sugars in the browning reaction in potato chips. J Agric Food Chem 7:274–277
Smith AM, Zeeman SC, Smith SM (2005) Starch degradation. Annu Rev Plant Biol 56:73–98
Sowokinos JR (2001) Biochemical and molecular control of cold-induced sweetening in potatoes. Am J Potato Res 78:221–236
Stadler RH, Blank I, Varga N, Robert F, Hau J, Guy PA, Robert M, Riediker S (2002) Acrylamide from Maillard reaction products. Nature 419:449–450
Tetlow IJ, Morell MK, Emes MJ (2004) Recent developments in understanding the regulation of starch metabolism in higher plants. J Exp Bot 55:2131–2145
Tiessen A, Hendriks JHM, Stitt M, Branscheid A, Gibon Y, Farré EM, Geigenberger P (2002) Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell 14:2191–2213
Tran HT, Qian WQ, Hurley BA, She YM, Wang D, Plaxton WC (2010) Biochemical and molecular characterization of AtPAP12 and AtPAP26: the predominant purple acid phosphatase isozymes secreted by phosphate-starved Arabidopsis thaliana. Plant Cell Environ 33:1789–1803
Trevanion SJ, Kruger NJ (1991) Effect of temperature on the kinetic properties of pyrophosphate: fructose-6-phosphate phosphotransferase from potato tuber. J Plant Physiol 137:753–759
Wang W, Vioncur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trans Plant Sci 9:244–252
Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803
Yang Y, Qiang X, Owsiany K, Zhang S, Thannhauser TW, Li L (2011) Evaluation of different multidimensional LC–MS/MS pipelines for isobaric tags for relative and absolute quantitation (iTRAQ)-based proteomic analysis of potato tubers in response to cold storage. J Proteome Res 10:4647–4660
Acknowledgments
This work was supported by program for National Natural Science Foundation (30960205, 31171477), New Century Excellent Talents in University (NCET-07-0214), Innovative Basic Research Groups of Gansu (1308RJIA005), International S&T Cooperation Program of China (2014DFG31570), Gansu Provincial Key Laboratory of Aridland Crop Science (GSCS-02), Gansu Educational Science Foundation (1002-07), Sheng Tongsheng Science Technology and Innovation Foundation of Gansu Agricultural University (GSAU-STS-1223).
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Cheng, L., Zhang, X., Zhao, Q. et al. Comparative proteomic analysis of cold-induced sweetening in potato (Solanum tuberosum L.) tuber. Acta Physiol Plant 36, 1197–1210 (2014). https://doi.org/10.1007/s11738-014-1496-x
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DOI: https://doi.org/10.1007/s11738-014-1496-x