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A ß-d-xylosidase and a PR-4B precursor identified as genes accounting for differences in peach cold storage tolerance

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Abstract

A transcriptome analysis was applied on two peach (Prunus persica L.) cultivars with different sensitivity to low temperature regimes to identify genes that might be involved in tolerance to extended low temperature storage. Peach fruit from ‘Morettini No2’ to ‘Royal Glory’, cultivars sensitive and tolerant to chilling injury (CI), respectively, were harvested at commercial maturity stage and allowed to ripen at room temperature (shelf-life, 25°C) or subjected to 4 and 6 weeks of cold storage (0°C, 95% R.H.) followed by ripening at room temperature. The use of μPEACH 1.0 microarray platform identified a number of genes that were differentially expressed in ‘Morettini No2’ and ‘Royal Glory’ fruit after the extended storage period. Based on their possible involvement in physiological processes related to cold storage and on their differential expression pattern, two heat shock proteins, a β-D-xylosidase, an expansin, a dehydrin and a pathogenesis-related (PR) protein were further selected for detailed analysis via RNA blot analysis. It is suggested that β-d-xylosidase and PR-4B precursor genes could be related to the different tolerance to CI observed in the two peach cultivars since generally higher expression levels were observed in cv. ‘Royal Glory’, the tolerant one. These two genes could play a role in peach tolerance to chilling injury.

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References

  • Alba R, Payton P, Fei ZJ, McQuinn R, Debbie P, Martin GB, Tanksley SD, Giovannoni JJ (2005) Transcriptome and selected metabolite analyses reveal multiple points of ethylene control during tomato fruit development. Plant Cell 17:2954–2965

    Article  PubMed  CAS  Google Scholar 

  • Bianco L, Lopez L, Scalone AG, Di Carli M, Desiderio A, Benvenuto E, Perrotta G (2009) Strawberry proteome characterization and its regulation during fruit ripening and in different genotypes. J Proteomics 72:586–607

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991–1995

    Article  PubMed  CAS  Google Scholar 

  • Close TJ (1997) Dehydrins: a commonality in the response of plants to dehydration and low temperature. Physiol Plant 100:291–296

    Article  CAS  Google Scholar 

  • Cosgrove DJ (2000) New genes and new biological roles for expansins. Curr Opin Plant Biol 3:73–78

    Article  PubMed  CAS  Google Scholar 

  • Dagar A, Friedman H, Lurie S (2010) Thaumatin-like proteins and their possible role in protection against chilling injury in peach fruit. Postharvest Biol Technol 57:77–85

    Article  CAS  Google Scholar 

  • Ding CK, Wang CY, Gross KC, Smith DL (2002) Jasmonate and salicylate induce the expression of pathogenesis-related-protein genes and increase resistance to chilling injury in tomato fruit. Planta 214:895–901

    Article  PubMed  CAS  Google Scholar 

  • Edgar R, Domrachev M, Lash AE (2002) Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30:207–210

    Article  PubMed  CAS  Google Scholar 

  • El-Sharkawy I, Jones B, Li ZG, Lelièvre JM, Pech JC, Latché A (2003) Isolation and characterization of four ethylene perception elements and their expression during ripening in pears (Pyrus communis L.) with/without cold requirement. J Exp Bot 54:1615–1625

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Fonseca S, Monteiro L, Barreiro MG, Pais MS (2005) Expression of genes encoding cell wall modifying enzymes is induced by cold storage and reflects changes in pear fruit texture. J Exp Bot 56:2029–2036

    Article  PubMed  CAS  Google Scholar 

  • Galli F, Archbold DD, Pomper KW (2008) Loss of ripening capacity of pawpaw fruit with extended cold storage. J Agric Food Chem 56:10683–10688

    Article  PubMed  CAS  Google Scholar 

  • Gonzalez-Aguero M, Pavez L, Ibanez F, Pacheco I, Campos-Vargas R, Meisel LA, Orellana A, Retamales J, Silva H, Gonzalez M, Cambiazo V (2008) Identification of woolliness response genes in peach fruit after post-harvest treatments. J Exp Bot 59:1973–1986

    Article  PubMed  Google Scholar 

  • Gonzalez-Aguilar GA, Tiznado-Hernandez ME, Zavaleta-Gatica R, Martinez-Tellez MA (2004) Methyl jasmonate treatments reduce chilling injury and activate the defense response of guava fruits. Biochem Biophys Res Commun 313:694–701

    Article  PubMed  CAS  Google Scholar 

  • Grimplet J, Romieu C, Audergon JM, Marty I, Albagnac G, Lambert P, Bouchet JP, Terrier N (2005) Transcriptomic study of apricot fruit (Prunus armeniaca) ripening among 13 006 expressed sequence tags. Physiol Plant 125:281–292

    Article  Google Scholar 

  • Hayama H, Shimada T, Fujii H, Ito A, Kashimura Y (2006) Ethylene-regulation of fruit softening and softening-related genes in peach. J Exp Bot 57:4071–4077

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Hon W-C, Griffith M, Mlynarz A, Kwok YC, Yang DSC (1995) Antifreeze proteins in winter rye are similar to pathogenesis-related proteins. Plant Physiol 109:879–889

    Article  PubMed  CAS  Google Scholar 

  • Hovav R, Chehanovsky N, Moy M, Jetter R, Schaffer AA (2007) The identification of a gene (Cwp1), silenced during Solanum evolution, which causes cuticle microfissuring and dehydration when expressed in tomato fruit. Plant J 52:627–639

    Article  PubMed  CAS  Google Scholar 

  • Imahori Y, Takemura M, BaiImahori J (2008) Chilling-induced oxidative stress and antioxidant responses in mume (Prunus mume) fruit during low temperature storage. Postharvest Biol Technol 49:54–60

    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  PubMed  CAS  Google Scholar 

  • Koag MC, Fenton RD, Wilkens S, Close TJ (2003) The binding of maize DHN1 to lipid vesicles. Gain of structure and lipid specificity. Plant Physiol 131:309–316

    Article  PubMed  CAS  Google Scholar 

  • Koyama K, Sadamatsu K, Goto-Yamamoto N (2010) Abscisic acid stimulated ripening and gene expression in berry skins of the Cabernet Sauvignon grape. Funct Integr Genomics. doi:10.1007/s10142-009-0145-8

    PubMed  Google Scholar 

  • Lurie S, Crisosto CH (2005) Chilling injury in peach and nectarine. Postharvest Biol Technol 37:195–208

    Article  Google Scholar 

  • Manganaris GA, Vasilakakis M, Diamantidis G, Mignani I (2006) Cell wall physicochemical aspects of peach fruit related to internal breakdown symptoms. Postharvest Biol Technol 39:69–74

    Article  CAS  Google Scholar 

  • Manganaris GA, Vasilakakis M, Mignani I, Manganaris A (2008) Cell wall physicochemical properties as indicators of peach quality during fruit ripening after cold storage. Food Sci Technol Int 14:385–39

    Article  CAS  Google Scholar 

  • Moore S, Payton P, Wright M, Tanksley S, Giovannoni J (2005) Utilization of tomato microarrays for comparative gene expression analysis in the Solanaceae. J Exp Bot 56:2885–2895

    Article  PubMed  CAS  Google Scholar 

  • Nilo R, Saffie C, Lilley K, Baeza-Yates R, Cambiazo V, Campos-Vargas R, González M, Meisel LA, Retamales J, Silva H, Orellana A (2010) Proteomic analysis of peach fruit mesocarp softening and chilling injury using difference gel electrophoresis (DIGE). BMC Genomics 11:43

    Article  PubMed  Google Scholar 

  • Ogundiwin EA, Marti C, Forment J, Pons C, Granell A, Gradziel TM, Peace CP, Crisosto CH (2008) Development of ChillPeach genomic tools and identification of cold-responsive genes in peach fruit. Plant Mol Biol 68:379–397

    Article  PubMed  CAS  Google Scholar 

  • Page D, Gouble B, Valot B, Bouchet JP, Callot C, Kretzschmar A, Causse M, Renard CMCG, Faurobert M (2010) Protective proteins are differentially expressed in tomato genotypes differing for their tolerance to low-temperature storage. Planta 232:483–500

    Article  PubMed  CAS  Google Scholar 

  • Porat R, Pasentsis K, Rozentzvieg D, Gerasopoulos D, Falara V, Samach A, Lurie S, Kanellis AK (2004) Isolation of a dehydrin cDNA from orange and grapefruit citrus fruit that is specifically induced by the combination of heat followed by chilling temperatures. Physiol Plant 120:256–264

    Article  PubMed  CAS  Google Scholar 

  • Rizzolo A, Vanoli M, Visai C (1995) Effect of cold storage on volatile constituents of peaches and nectarines. Acta Hortic 379:467–474

    CAS  Google Scholar 

  • Ruperti B, Bonghi C, Rasori A, Ramina A, Tonutti P (2001) Characterization and expression of two members of the peach 1-aminocyclopropane-1-carboxylate oxidase gene family. Physiol Plant 111:336–344

    Article  PubMed  CAS  Google Scholar 

  • Ruperti B, Cattivelli L, Pagni S, Ramina A (2002) Ethylene-responsive genes are differentially regulated during abscission, organ senescence and wounding in peach (Prunus persica). J Exp Bot 53:429–437

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Tittarelli A, Santiago M, Morales A, Meisel LA, Silva H (2009) Isolation and functional characterization of cold-regulated promoters, by digitally identifying peach fruit cold-induced genes from a large EST dataset. BMC Plant Biology 9:121

    Google Scholar 

  • Trainotti L, Zanin D, Casadoro G (2003) A cell wall-oriented genomic approach reveals a new and unexpected complexity of the softening in peaches. J Exp Bot 54:1821–1832

    Article  PubMed  CAS  Google Scholar 

  • Trainotti L, Bonghi C, Ziliotto F, Zanin D, Rasori A, Casadoro G, Ramina A, Tonutti P (2006) The use of microarray μPEACH1.0 to investigate transcriptome changes during transition from pre-climacteric to climacteric phase in peach fruit. Plant Sci 170:606–613

    Article  CAS  Google Scholar 

  • Trainotti L, Tadiello A, Casadoro G (2007) The involvement of auxin in the ripening of climacteric fruits comes of age: the hormone plays a role of its own and has an intense interplay with ethylene in ripening peaches. J Exp Bot 58:3299–3308

    Article  PubMed  CAS  Google Scholar 

  • Usadel B, Nagel A, Steinhauser D, Gibon Y, Bläsing OE, Redestig H, Sreenivasulu N, Krall L, Hannah MA, Poree F, Fernie AR, Stitt M (2006) PageMan: an interactive ontology tool to generate, display, and annotate overview graphs for profiling experiments. BMC Bioinform 7:535

    Article  Google Scholar 

  • Vizoso P, Meisel LA, Tittarelli A, Latorre M, Saba J, Caroca R, Maldonado J, Cambiazo V, Campos-Vargas R, Gonzalez M, Orellana A, Silva H (2009) Comparative EST transcript profiling of peach fruits under different post-harvest conditions reveals candidate genes associated with peach fruit quality. BMC Genomics 10:423

    Article  PubMed  Google Scholar 

  • Waters DLE, Holton TA, Ablett EM, Lee LS, Henry RJ (2005) cDNA microarray analysis of developing grape (Vitis vinifera cv. Shiraz) berry skin. Funct Integr Genomics 5:40–58

    Article  PubMed  CAS  Google Scholar 

  • Worrall D, Elias L, Ashford D, Smallwood M, Sidebottom C, Lillford P, Telford J, Holt C, Bowles D (1988) A carrot leucine-rich-repeat protein that inhibits ice recrystallization. Science 282:115–117

    Article  Google Scholar 

  • Yin X, Allan AC, Zhang B, Wu R, Burdon J, Wang P, Ferguson IB (2009) Ethylene-related genes show a differential response to low temperature during ‘Hayward’ kiwifruit ripening. Postharvest Biol Technol 52:9–15

    Article  CAS  Google Scholar 

  • Zhang CF, Tian SP (2009) Crucial contribution of membrane lipids’ unsaturation to acquisition of chilling-tolerance in peach fruit stored at 0°C. Food Chem 115:405–411

    Article  CAS  Google Scholar 

  • Zhou HW, Ben-Arie R, Lurie S (2000) Pectin esterase, polygalacturonase and gel formation in peach pectin fractions. Phytochem 55:191–195

    Article  CAS  Google Scholar 

  • Zhou HW, Dong L, Ben-Arie R, Lurie S (2001) The role of ethylene in the prevention of chilling injury in nectarines. J Plant Physiol 158:55–61

    Article  CAS  Google Scholar 

  • Ziliotto F, Begheldo M, Rasori A, Bonghi C, Tonutti P (2008) Transcript profiling of ripening nectarine fruit treated with the inhibitor of ethylene action 1-methylcyclopropene. J Exp Bot 59:2781–2791

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This research was financially supported by grants co-funded by the European Social Fund & National Resources-EPEAEK II-ARCHIMIDIS II. GAM was supported by an E.U. Marie Curie Individual Fellowship (Grant MEIF-CT-2006-038997) and VF by a mobility grant from COST-924 action.

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Correspondence to Claudio Bonghi or Angelos K. Kanellis.

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Vasiliki Falara and George A. Manganaris contributed equally to this work.

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Fig. S1

Differentially expressed transcripts in a peach fruit of cultivars ‘Morettini No2’ and ‘Royal Glory’ after 4 and 6 weeks of cold storage (0°C) plus 1 day shelf-life (25°C). Numbers associated to light grey bars represent up-regulated (above) and dark grey represent down-regulated (bottom) transcripts identified via microarray analysis in the four samples compared to a fruit 1 day after harvest. A total of 185 and 355 transcripts have been considered for ‘Morettini No2’ (left) and ‘Royal Glory’ (right) comparisons, respectively, according to SAM (Table S2, supplementary material). Numbers of the up- and down-regulated transcripts in the 4-week samples showing the same expression pattern with the 6-week samples are indicated within the dotted lines. Numbers associated with the white bars indicate constitutively expressed mRNA after 4 and 6 weeks of cold storage plus 1 day shelf-life. (GIF 21 kb)

Figure S1

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Table S1

(DOC 50 kb)

Table S2

List of probes showing significant expression values after Significant Analysis for Microarrays (SAM analysis) in each of the four comparisons performed in the trial. A total of 444 probes showed significant expression values after SAM analysis in at least two of the four (4 w + 1d vs. 0 w + 1 d 'Morettini No2'; 6w + 1 d vs. 0 w + 1d 'Morettini No2'; 4 w + 1d vs. 0 w + 1 d 'Royal Glory'4 w + 1d vs. 0 w + 1 d 'Royal Glory') hybridizations performed in the trial. “Ctg” refers to the peach contig number present in the database and used to synthesize the oligo probes for the μPEACH1.0 microarray. “Oligo ID” is the code assigned to each transcript (444 out of 4,806) by the manufacturer (Operon). “At gene” is the AGI Locus (ATH AGI code TAIR 7) of the Arabidopsis gene best hit for each peach contigs obtained using BLASTX against the TAIR protein 7 database. “Description” is the name assigned to Arabidopsis gene best hit for peach contigs. “Mapman BIN” is the BIN and subBIN (http://www.gabipd.org/projects/MapMan/) assigned to the Arabidopsis gene best hit for peach contigs. The following eight columns report the microarray results: 4 w (0°C) + 1 d (25°C)/1 d (25°C) 'Morettini No2' and stdev report [log2 (intensity 4weeks/intensity T0 and relative standard deviation value]; 6weeks (0°C) + 1 day (25°C) /1 day (25°C) 'Morettini No2' and stdev report reports [log2 (intensity 6 weeks (0°C) + 1 day (25°C)/intensity 1 day (25°C)) and relative standard deviation value]; 4weeks (0°C) + 1 day (25°C) /1 day (25°C) 'Royal Glory' and stdev report [log2 (intensity 4weeks (0°C) + 1 day (25°C)/intensity 1 day (25°C)) and relative standard deviation value]; 6weeks/1 day (25°C) 'Royal Glory' and stdev reports [log2 (intensity 6 weeks(0°C) + 1 day (25°C)/intensity 1 day (25°C)) and relative standard deviation value]. Green is used to highlight down-regulated genes (log2 ratio ≤ −1.0), red to highlight up-regulated genes (log2 ratio ≥ 1.0), and yellow for genes showing no differential expression (log2 ratio > −1 and <1). Ns and NA indicate probes that were not significant at SAM analysis and data not available, respectively. (XLS 176 kb)

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Falara, V., Manganaris, G.A., Ziliotto, F. et al. A ß-d-xylosidase and a PR-4B precursor identified as genes accounting for differences in peach cold storage tolerance. Funct Integr Genomics 11, 357–368 (2011). https://doi.org/10.1007/s10142-010-0204-1

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  • DOI: https://doi.org/10.1007/s10142-010-0204-1

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