Cell wall-related genes studies on peach cultivars with differential susceptibility to woolliness: looking for candidates as indicators of chilling tolerance


Key message

The results obtained indicate that a β-xylosidase gene may act as good indicator of chilling tolerance and provide new insights into the complex issue of peach fruit woolliness.


The storage of peaches at low temperatures for prolonged periods can induce a form of chilling injury (CI) called woolliness, characterized by a lack of juiciness and a mealy texture. As this disorder has been associated with abnormal cell wall dismantling, the levels of 12 transcripts encoding proteins involved in cell wall metabolism were analysed in cultivars with contrasting susceptibility to this disorder selected from five melting flesh peach cultivars. The resistant (‘Springlady’) and susceptible (‘Flordaking’) cultivars displayed differences in the level of expression of some of the selected genes during fruit softening and in woolly versus non-woolly fruits. From these genes, the level of expression of PpXyl, which encodes for a putative β-xylosidase, was the one that presented the highest correlation (negative) with the susceptibility to woolliness. PpXyl expression was also analysed in a cultivar (‘Rojo 2’) with intermediate susceptibility to woolliness, reinforcing the conclusion about the correlation of PpXyl expression to the presence of woolliness symptom. Moreover, the level of expression of PpXyl correlated to protein level detected by Western blot. Analyses of the promoter region of the PpXyl gene (1637 bp) isolated from the three cultivars showed no differences suggesting that cis-elements from other regions of the genome and/or trans elements could be responsible of the differential PpXyl expression patterns. Overall, the results obtained indicate that PpXyl may act as a good indicator of woolliness tolerance and that the regulation of expression of this gene in different cultivars does not depend on sequences upstream the coding sequence.

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Fig. 1
Fig. 2
Fig. 3



ACC (aminocyclopropane-1-carboxylic acid) oxidase 1


Chilling injury


Cold storage










Pectate lyase


Pectin methylesterase


Quantitative real-time reverse transcription-PCR




Soluble solid content




  1. Artes F, Cano A, Fernandez-Trujillo JP (1996) Pectolytic enzyme activity during intermittent warming storage of peaches. J Food Sci 61:311–313

    CAS  Article  Google Scholar 

  2. Artlip TS, Wisniewski ME, Bassett CL, Norelli JL (2013) CBF gene expression in peach leaf and bark tissues is gated by a circadian clock. Tree Physiol 33:866–877

    CAS  Article  PubMed  Google Scholar 

  3. Borsani J, Budde CO, Porrini L, Lauxmann MA, Lombardo VA, Murray R, Andreo CS, Drincovich MF, Lara MV (2009) Carbon metabolism of peach fruit after harvest: identification of key enzymes involved in organic acid and sugar level modifications. J Exp Bot 60:1823–1837

    CAS  Article  PubMed  Google Scholar 

  4. Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254

    CAS  Article  PubMed  Google Scholar 

  5. Brummell DA, Dal Cin V, Crisosto CH, Labavitch JM (2004a) Cell wall metabolism during maturation, ripening and senescence of peach fruit. J Exp Bot 55:2029–2039

    CAS  Article  PubMed  Google Scholar 

  6. Brummell DA, Dal Cin V, Lurie S, Crisosto CH, Labavitch JM (2004b) 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

    CAS  Article  PubMed  Google Scholar 

  7. Bustamante CA, Rosli HG, Añón MC, Civello PM, Martínez GA (2006) β-Xylosidase in strawberry fruit: isolation of a full-length gene and analysis of its expression and enzymatic activity in cultivars with contrasting firmness. Plant Sci 171:497–504

    CAS  Article  PubMed  Google Scholar 

  8. Bustamante CA, Budde CO, Borsani J, Lombardo VA, Lauxmann MA, Andreo CS, Lara MV, Drincovich MF (2012) Heat treatment of peach fruit: modifications in the extracellular compartment and identification of novel extracellular proteins. Plant Physiol Biochem 60:35–45

    CAS  Article  PubMed  Google Scholar 

  9. Childs KL, Hamilton JP, Zhu W, Ly E, Cheung F, Wu H, Rabinowicz PD, Town CD, Buell CR, Chan AP (2007) The TIGR plant transcript assemblies database. Nucleic Acids Res 35:D846–D851

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. Crisosto CH, Mitchell FG, Ju Z (1999) Susceptibility to chilling injury of peach, nectarine, and plum cultivars grown in California. HortScience 34:1116–1118

    Google Scholar 

  11. Dagar A, Friedman H, Lurie S (2012) Utilization of chillpeach microarray platform for comparing chilling injury-susceptible ‘hermoza’ and chilling injury-resistant ‘oded’ peaches. Acta Hortic 945:337–344

    Article  Google Scholar 

  12. Dellaporta SL, Wood J, Ticks JB (1983) A plant molecular DNA minipreparation version 2. Plant Mol Biol Rep 1:19–21

    CAS  Article  Google Scholar 

  13. Falara V, Manganaris GA, Ziliotto F, Manganaris A, Bonghi C, Ramina A, Kanellis AK (2011) A β-D-xylosidase and a PR-4B precursor identified as genes accounting for differences in peach cold storage tolerance. Funct Integr Genomic 11:357–368

    CAS  Article  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  15. Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178–D1186

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. Goujon T, Minic Z, El Amrani A, Lerouxel O, Aletti E, Lapierre C, Joselau J, Jouanin L (2003) AtBXL1, a novel higher plant (Arabidopsis thaliana) putative β-xylosidase gene, is involved in secondary cell wall metabolism and plant development. Plant J 33:677–690

    CAS  Article  PubMed  Google Scholar 

  17. 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

    CAS  Article  PubMed  Google Scholar 

  18. Itai A, Ishihara K, Bewley D (2003) Characterization of expression, and cloning, of β-d-xylosidase and α-l-arabinofuranosidase in developing and ripening tomato (Lycopersicon esculentum Mill.) fruit. J Exp Bot 54:2615–2622

    CAS  Article  PubMed  Google Scholar 

  19. Jung S, Staton M, Lee T, Blenda A, Svancara R, Abbott A, Main D (2008) GDR (Genome Database for Rosaceae): integrated web-database for Rosaceae genomics and genetics data. Nucleic Acids Res 36:D1034–D1040

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  20. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    CAS  Article  PubMed  Google Scholar 

  21. Lazzari B, Caprera A, Vecchietti A, Merelli I, Barale F, Milanesi L, Stella A, Pozzi C (2008) Version VI of the ESTree db: an improved tool for peach transcriptome analysis. BMC Bioinformatics 9:S9

    Article  PubMed  PubMed Central  Google Scholar 

  22. Lee RC, Hrmova M, Burton RA, Lahnstein J, Fincher GB (2003) Bifunctional family 3 glycoside hydrolases from barley with α-l-arabinofuranosidase and β-d-xylosidase activity. J Biol Chem 278:5377–5387

    CAS  Article  PubMed  Google Scholar 

  23. Lee EJ, Matsumura Y, Soga K, Hoson T, Koizumi N (2007) Glycosyl hydrolases of cell wall are induced by sugar starvation in Arabidopsis. Plant Cell Physiol 48:405–413

    CAS  Article  PubMed  Google Scholar 

  24. Liang L, Zhang B, Yin X-R, Xu C-J, Sun C-D, Chen K-S (2013) Differential expression of the CBF gene family during postharvest cold storage and subsequent shelf-life of Peach fruit. Plant Mol Biol Rep 31:1358–1367

    CAS  Article  Google Scholar 

  25. Lill RE, Van Der Mespel GJ (1988) A method for measuring the juice content of mealy nectarines. Sci Hortic 36:267–271

    Article  Google Scholar 

  26. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−∆∆CT. Methods 25:402–408

    CAS  Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  28. Manganaris GA, Vicente AR, Crisosto CH, Labavitch JM (2008) Cell wall modifications in chilling-injured plum fruit (Prunus salicina). Postharvest Biol Technol 48:77–83

    CAS  Article  Google Scholar 

  29. Martínez GA, Chaves AR, Civello PM (2004) β-xylosidase activity and expression of a β-Xylosidase gene during strawberry fruit ripening. Plant Physiol Biochem 42:89–96

    Article  PubMed  Google Scholar 

  30. Meisel L, Fonseca B, González S, Baezayates R, Cambiazo V, Campos R, Gonzalez M, Orellana A, Retamales J, Silva H (2005) A rapid and efficient method for purifying high quality total RNA from peaches (Prunus persica) for functional genomics analyses. Biol Res 38:83–88

    CAS  Article  PubMed  Google Scholar 

  31. Minic Z, Rihouey C, Trung Do C, Lerouge P, Jouanin L (2004) Purification and characterization of enzymes exhibiting β-d-xylosidase activities in stem tissues of Arabidopsis. Plant Physiol 135:1–12

    Article  Google Scholar 

  32. Müller GL, Budde CO, Lauxmann MA, Triassi A, Andreo CS, Drincovich MF, Lara MV (2013) Expression profile of transcripts encoding cell wall remodelling proteins in tomato fruit cv. Micro-Tom subjected to 15 °C storage. Funct Plant Biol 40:449–458

    Article  Google Scholar 

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

    Article  Google Scholar 

  34. Obenland DM, Crisosto CH, Rose JKC (2003) Expansin protein levels decline with the development of mealiness in peaches. Postharvest Biol Technol 29:11–18

    CAS  Article  Google Scholar 

  35. 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

    CAS  Article  PubMed  Google Scholar 

  36. Page D, Gouble B, Valot B, Bouchet JP, Callot C, Kretzchmar 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

    CAS  Article  PubMed  Google Scholar 

  37. Pons C, Martí C, Forment J, Crisosto CH, Dandekar AM, Granell A (2014) A bulk segregant gene expression analysis of a peach population reveals components of the underlying mechanism of the fruit cold response. PLoS One 9:e90706

    Article  PubMed  PubMed Central  Google Scholar 

  38. 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 Plantarum 111:336–344

    CAS  Article  Google Scholar 

  39. Tonutti P, Bonghi C, Ruperti B, Tornielli GB, Ramina A (1997) Ethylene evolution and 1-aminocyclopropane-1-carboxylate oxidase gene expression during early development and ripening of peach fruit. J Am Soc Hortic Sci 122:642–647

    CAS  Google Scholar 

  40. 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 Genom 10:423–440

    Article  Google Scholar 

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

    CAS  Article  Google Scholar 

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This work was supported by Agencia Nacional de Promoción de Actividades Científicas y Técnicas (Argentina, PICT 2010-0097). CSA, MVL, MFD and CAB are members of the Researcher Career of CONICET and MGi and LLM are fellows of the same Institution. JG and COB are members of INTA. The authors thank Drs. G. Martínez and P. Civello (IIB-INTECH) for kind gift of the anti-β-Xyl antibody.

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Correspondence to Claudia A. Bustamante.

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Communicated by A. Dhingra.

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Genero, M., Gismondi, M., Monti, L.L. et al. Cell wall-related genes studies on peach cultivars with differential susceptibility to woolliness: looking for candidates as indicators of chilling tolerance. Plant Cell Rep 35, 1235–1246 (2016). https://doi.org/10.1007/s00299-016-1956-4

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  • Cell wall metabolism
  • Chilling injury
  • Peach
  • Prunus persica
  • Woolliness
  • Xylosidase