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Protective proteins are differentially expressed in tomato genotypes differing for their tolerance to low-temperature storage

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Abstract

When stored at low temperature, tomato fruits exhibit chilling injury symptoms, such as rubbery texture and irregular ripening. To identify proteins related to chilling tolerance, we compared two tomato near isogenic lines differing for their texture phenotype at harvest in a fruit-storage trial including two temperatures (4 and 20°C) along several days of conservation. Fruit evolution was followed by assessing fruit color, ethylene emission and texture parameters. The most contrasted samples were submitted to proteomic analysis including two-dimensional electrophoresis and mass spectrometry of protein spots to identify the proteins, whose expression varied according to the genotype or the storage conditions. Unexpectedly, the most firm genotype at harvest was the most sensitive to cold storage. The other genotype exhibited a delay in fruit firmness loss leading to the texture differences observed after 20 days of 4°C storage. The proteome analysis of these contrasted fruits identified 85 proteins whose quantities varied with temperature or genotype. As expected, cold storage decreased the expression of proteins related to maturation process, such as acidic invertase, possibly controlled post-translational regulation of polygalacturonase and up-regulated proteins related to freezing tolerance. However, the study point out proteins involved in the differential resistance to chilling conditions of the two lines. This includes specific isoforms among the large family of small heat shocked proteins, and a set of proteins involved in the defense against of the reticulum endoplasmic stress.

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Abbreviations

CI:

Chilling injury

dF:

Loss of firmness

dW :

Loss of weight

E max :

Maximum elasticity

QTL:

Quantitative trait locus

ROS:

Reactive oxygen species

sHSP:

Small heat shock proteins

References

  • Ahn J-W, Verma R, Kim M, Lee J-Y, Kim Y-K, Bang J-W, Reiter W-D, Pai H-S (2006) Depletion of Udp-d-apiose/Udp-d-xylose synthases results in rhamnogalacturonan-ii deficiency, cell wall thickening, and cell death in higher plants. J Biol Chem 281:13708–13716

    Article  CAS  PubMed  Google Scholar 

  • Brummell DA, Harpster MH (2001) Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol Biol 47:311–339

    Article  CAS  PubMed  Google Scholar 

  • Brummell DA, Dal Cin V, Lurie S, Crisosto CH, Labavitch JM (2004) Cell wall metabolism during the development of chilling injury in cold-stored peach fruit: association of mealiness with arrested disassembly of cell wall pectins. J Exp Bot 55:2041–2052

    Article  CAS  PubMed  Google Scholar 

  • Casado-Vela J, Selles S, Martinez RB (2005) Proteomic approach to blossom-end rot in tomato fruits (Lycopersicon esculentum M.): antioxidant enzymes and the pentose phosphate pathway. Proteomics 5:2488–2496

    Article  CAS  PubMed  Google Scholar 

  • Causse M, Saliba-Colombani V, Lecomte L, Duffe P, Rousselle P, Buret M (2002) QTL analysis of fruit quality in fresh market tomato: a few chromosome regions control the variation of sensory and instrumental traits. J Exp Bot 53:2089–2098

    Article  CAS  PubMed  Google Scholar 

  • Chaib J, Devaux M-F, Grotte M-G, Robini K, Causse M, Lahaye M, Marty I (2007) Physiological relationships among physical, sensory, and morphological attributes of texture in tomato fruits. J Exp Bot 58:1915–1925

    Article  CAS  PubMed  Google Scholar 

  • Chaïb J, Lecomte L, Buret M, Causse M (2006) Stability over genetic backgrounds, generations and years of quantitative trait locus (QTLs) for organoleptic quality in tomato. Theor Appl Genet 112:934–944

    Article  PubMed  Google Scholar 

  • Chambroy Y, Souty M, Jacquemin G, Gomez RM, Audergon JM (1995) Research on the suitability of modified atmosphere packaging for shelf-life and quality improvement of apricot fruit. Acta Hort 384:633–638

    Google Scholar 

  • Denslow SA, Rueschhoff EE, Daub ME (2007) Regulation of the Arabidopsis thaliana vitamin B6 biosynthesis genes by abiotic stress. Plant Physol and Biochem 45:152–161

    Article  CAS  Google Scholar 

  • Deytieux C, Geny L, Lapaillerie D, Claverol S, Bonneu M, Doneche B (2007) Proteome analysis of grape skins during ripening. J Exp Bot 58:1851–1862

    Article  CAS  PubMed  Google Scholar 

  • Faurobert M, Mihr C, Bertin N, Pawlowski T, Negroni L, Sommerer N, Causse M (2007) Major proteome variations associated with cherry tomato pericarp development and ripening. Plant Physiol 143:1327–1346

    Article  CAS  PubMed  Google Scholar 

  • Gilbert HF (1997) Protein disulfide isomerase and assisted protein folding. J Biol Chem 272:29399–29402

    Article  CAS  PubMed  Google Scholar 

  • Hodges DM (2003) Overview: postharvest oxidative stress in horticultural crops. In: Hodges DM (ed) Postharvest oxidative stress in horticultural crops. Food Product Press, New York, pp 1–12

    Google Scholar 

  • Hodges DM, Lester GE, Munro KD, Toivonen PMA (2004) Oxidative stress: importance for postharvest quality. Hortscience 39:924–929

    CAS  Google Scholar 

  • Hou F-Y, Huang J, Yu S-L, Zhang H-S (2007) The 6-phosphogluconate dehydrogenase genes are responsive to abiotic stresses in rice. J Int Plant Biol 49:655–663

    Article  CAS  Google Scholar 

  • Itai A, Ishihara K, Bewley JD (2003) Characterization of expression, and cloning, of {beta}-d-xylosidase and {alpha}-l-arabinofuranosidase in developing and ripening tomato (Lycopersicon esculentum Mill.) fruit. J Exp Bot 54:2615–2622

    Article  CAS  PubMed  Google Scholar 

  • Kevany BM, Tieman DM, Taylor MG, Cin VD, Klee HJ (2007) Ethylene receptor degradation controls the timing of ripening in tomato fruit. Plant J 51:458–467

    Article  CAS  PubMed  Google Scholar 

  • Lecomte L, Duffe P, Buret M, Servin B, Hospital F, Causse M (2004) Marker-assisted introgression of five QTLs controlling fruit quality traits into three tomato lines revealed interactions between QTLs and genetic backgrounds. Theor Appl Genet 109:658–668

    Article  CAS  PubMed  Google Scholar 

  • Lee H, Guo Y, Ohta M, Xiong LM, Stevenson B, Zhu JK (2002) LOS2, a genetic locus required for cold-responsive gene transcription encodes a bi-functional enolase. EMBO J 21:2692–2702

    Article  CAS  PubMed  Google Scholar 

  • Löw D, Brändle K, Nover L, Forreiter C (2000) Cytosolic heat-stress proteins Hsp17.7 class I and Hsp17.3 class II of tomato act as molecular chaperones in vivo. Planta 211:575–582

    Article  PubMed  Google Scholar 

  • Lurie S, Sabehat A (1997) Prestorage temperature manipulations to reduce chilling injury in tomatoes. Postharvest Biol Technol 11:57–62

    Article  Google Scholar 

  • Lyons JM (1973) Chilling injury in plants. Ann Rev Plant Physiol 24:445–466

    Article  CAS  Google Scholar 

  • Malacrida C, Valle EM, Boggio SB (2006) Postharvest chilling induces oxidative stress response in the dwarf tomato cultivar Micro-Tom. Physiol Plant 127:10–18

    Article  CAS  Google Scholar 

  • Manganaris GA, Vasilakakis M, Diamantidis G, Mignani I (2005) Cell wall cation composition and distribution in chilling-injured nectarine fruit. Postharvest Biol Technol 37:72–80

    Article  CAS  Google Scholar 

  • Martinez IM, Chrispeels MJ (2003) Genomic analysis of the unfolded protein response in arabidopsis shows its connection to important cellular processes. Plant Cell 15:561–576

    Article  CAS  PubMed  Google Scholar 

  • Maul F, Sargent SA, Sims CA, Baldwin EA, Balaban MO, Huber DJ (2000) Tomato flavor and aroma quality as affected by storage temperature. J Food Sci 65:1228–1237

    Article  CAS  Google Scholar 

  • Neta-Sharir I, Isaacson T, Lurie S, Weiss D (2005) Dual role for tomato heat shock protein 21: protecting photosystem ii from oxidative stress and promoting color changes during fruit maturation. Plant Cell 17:1829–1838

    Article  CAS  PubMed  Google Scholar 

  • Nishida I, Murata N (1996) Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids. Ann Rev Plant Physiol Plant Mol Biol 47:541–568

    Article  CAS  Google Scholar 

  • Paull RE (1999) Effect of temperature and relative humidity on fresh commodity quality. Postharvest Biol and Tech 15:263–277

    Article  Google Scholar 

  • Pedreschi R, Vanstreels E, Carpentier S, Hertog M, Lammertyn J, Robben J, Noben JP, Swennen R, Vanderleyden J, Nicolaï BM (2007) Proteomic analysis of core breakdown disorder in Conference pears (Pyrus communis). Proteomics 7:2083–2099

    Article  CAS  PubMed  Google Scholar 

  • Pimpl P, Taylor JP, Snowden C, Hillmer S, Robinson DG, Denecke J (2006) Golgi-mediated vacuolar sorting of the endoplasmic reticulum chaperone bip may play an active role in quality control within the secretory pathway. Plant Cell 18:198–211

    Article  CAS  PubMed  Google Scholar 

  • Ramakrishna W, Deng Z, Ding C-K, Handa AK, Ozminkowski RH Jr (2003) A novel small heat shock protein gene, vis1, contributes to pectin depolymerization and juice viscosity in tomato fruit. Plant Physiol 131:725–735

    Article  CAS  PubMed  Google Scholar 

  • Rocco M, D’Ambrosio C, Arena S, Faurobert M, Scaloni A, Marra M (2006) Proteomic analysis of tomato fruits from two ecotypes during ripening. Proteomics 6:3781–3791

    Article  CAS  PubMed  Google Scholar 

  • Roitsch T, Gonzalez M-C (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 9:606–613

    Article  CAS  PubMed  Google Scholar 

  • Sabehat A, Weiss D, Lurie S (1996) The correlation between heat-shock protein accumulation and persistence and chilling tolerance in tomato fruit. Plant Physiol 110:531–537

    Article  CAS  PubMed  Google Scholar 

  • Sabehat A, Lurie S, Weiss D (1998) Expression of small heat-shock proteins at low temperatures—a possible role in protecting against chilling injuries. Plant Physiol 117:651–658

    Article  CAS  PubMed  Google Scholar 

  • Saliba-Colombani V, Causse M, Langlois D, Philouze J, Buret M (2001) Genetic analysis of organoleptic quality in fresh market tomato. 1. Mapping QTLs for physical and chemical traits. Theor Appl Genet 102:259–272

    Article  CAS  Google Scholar 

  • Sarry J-E, Sommerer N, Sauvage F-X, Bergoin A, Rossignol M, Albagnac G, Romieu C (2004) Grape berry biochemistry revisited upon proteomic analysis of the mesocarp. Proteomics 4:201–215

    Article  CAS  PubMed  Google Scholar 

  • Seemann M, Rohmer M (2007) Isoprenoid biosynthesis via the methylerythritol phosphate pathway: GcpE and LytB, two novel iron-sulphur proteins. Comptes Rendus Chimie 10:748–755

    Article  CAS  Google Scholar 

  • Speirs J, Lee E, Holt K, Kim Y, Scott NS, Loveys B, Schuch W (1998) Genetic manipulation of alcohol dehydrogenase levels in ripening tomato fruit affects the balance of some flavor aldehydes and alcohols. Plant Physiol 117:1047–1058

    Article  CAS  PubMed  Google Scholar 

  • Sun W, Van Montagu M, Verbruggen N (2002) Small heat shock proteins and stress tolerance in plants. Biochim Biophys Acta 1577:1–9

    CAS  PubMed  Google Scholar 

  • Swindell WR, Huebner M, Weber AP (2007) Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. Bmc Genomics 8:125

    Google Scholar 

  • Tomassen MMM, Barrett DM, van der Valk HCPM, Woltering EJ (2007) Isolation and characterization of a tomato non-specific lipid transfer protein involved in polygalacturonase-mediated pectin degradation. J Exp Bot 58:1151–1160

    Article  CAS  PubMed  Google Scholar 

  • Van Dijk C, Boeriu C, Peter F, Stolle-Smits T, Tijskens LMM (2006a) The firmness of stored tomatoes (cv. Tradiro). 1. Kinetic and near infrared models to describe firmness and moisture loss. J Food Eng 77:575–584

    Article  Google Scholar 

  • Van Dijk C, Boeriu C, Stolle-Smits T, Tijskens LMM (2006b) The firmness of stored tomatoes (cv. Tradiro). 2. Kinetic and near infrared models to describe pectin degrading enzymes and firmness loss. J Food Eng 77:585–593

    Article  Google Scholar 

Download references

Acknowledgments

The authors acknowledge support from EU-SOL (FOOD-CT-2006-016214) and ANR QUALITOM-FIL (ANR-06-PNRA009). Many thanks to the technical team of GAFL and Yolande Carretero for taking care of the plants, to Patrice Reiling from SQPOV team for ethylene measurement and management of fruit storage.

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Page, D., Gouble, B., Valot, B. et al. Protective proteins are differentially expressed in tomato genotypes differing for their tolerance to low-temperature storage. Planta 232, 483–500 (2010). https://doi.org/10.1007/s00425-010-1184-z

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