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.
Similar content being viewed by others
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
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
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
Church GM, Gilbert W (1984) Genomic sequencing. Proc Natl Acad Sci USA 81:1991–1995
Close TJ (1997) Dehydrins: a commonality in the response of plants to dehydration and low temperature. Physiol Plant 100:291–296
Cosgrove DJ (2000) New genes and new biological roles for expansins. Curr Opin Plant Biol 3:73–78
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
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
Edgar R, Domrachev M, Lash AE (2002) Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30:207–210
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
Lurie S, Crisosto CH (2005) Chilling injury in peach and nectarine. Postharvest Biol Technol 37:195–208
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
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
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
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
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
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
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
Rizzolo A, Vanoli M, Visai C (1995) Effect of cold storage on volatile constituents of peaches and nectarines. Acta Hortic 379:467–474
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
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
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
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
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
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
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
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
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
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
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
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
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
Zhou HW, Ben-Arie R, Lurie S (2000) Pectin esterase, polygalacturonase and gel formation in peach pectin fractions. Phytochem 55:191–195
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
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
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.
Author information
Authors and Affiliations
Corresponding authors
Additional information
Vasiliki Falara and George A. Manganaris contributed equally to this work.
Electronic supplementary material
Below is the link to the electronic supplementary material.
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
High resolution (TIFF 620 kb)
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)
Rights and permissions
About this article
Cite this article
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
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10142-010-0204-1