Skip to main content
Log in

Acidic alpha galactosidase during the maturation and cold storage of cherry tomatoes

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

Acidic alpha galactosidase appears to have multiple roles in cherry tomato Solanum lycopersicum L. var. cerasiforme fruit development and post-harvest storage. The localization of the enzyme and its activity suggest that enzyme accumulation in seeds during development probably serves as a provision for germination. However, it is well known that alpha galactosidase also participates in cell wall degradation, raffinose class oligosaccharide metabolism and in cold acclimation in fruits kept at cold storage. Both the enzyme activity and gene transcript accumulation were elevated at the mature green stage (478.73 nm nitrophenol/min g FW and 0.245, respectively), the cold storage at 5 °C only the alpha galactosidase transcription levels were considerably elevated (210.80 nm nitrophenol/min g FW and 0.492 relative transcript accumulation) while at 10 °C for 120 h considerably affected both the enzyme activity and transcription levels (402.06 nm nitrophenol/min g FW and 0.596, respectively). Significant correlation was found between the loss of firmness of the fruits and the levels of soluble solids and the accumulation of transcripts of the alpha galactosidase gene. Finally, it is suggested that only one isoenzyme form of acidic alpha galactosidase is active during the maturation process in the cherry tomatoes of the cv. Concita. In conclusion, our findings suggest that alpha galactosidase contributes, along with other hydrolases, in several metabolic processes closely connected to the quality of tomato fruits during maturation and post-harvest storage.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

aGal:

Alpha galactosidase

MG:

Mature green

Br:

Breaker

RR:

Red ripe

5d5 °C:

Fruits stored at 5 °C for 120 h

5d10 °C:

Fruits stored at 10 °C for 120 h UBQ, Ubiquitin

r18s:

Ribosomal 18s subunit

References

  • Bassel GW, Mullen RT, Bewley JD (2001) α-Galactosidase is synthesized in tomato seeds during development and is localized in the protein storage vacuoles. Can J Bot 79:1417–1424

    CAS  Google Scholar 

  • Beckles DM (2012) Factors affecting the postharvest soluble solids and sugar content of tomato (Solanum lycopersicum L.) fruit. Postharv Biol Technol 63:129–140

    Article  CAS  Google Scholar 

  • Bewley JD, Burton RA, Morohashi Y, Fincher GB (1997) Molecular cloning of a cDNA encoding a (1 → 4)-β-mannan endohydrolase from the seeds of germinated tomato (Lycopersicon esculentum). Planta 203:454–459

    Article  CAS  PubMed  Google Scholar 

  • Blöchl A, Peterbauer T, Hofmann J, Richter A (2008) A enzymatic breakdown of raffinose oligosaccharides in pea seeds. Planta 228:99–110

    Article  PubMed  Google Scholar 

  • Carmi N, Zhang G, Petreikov M, Gao Z, Eyal Y, Granot D et al (2003) Cloning and functional expression of alkaline α-galactosidase from melon fruit: similarity to plant SIP proteins uncovers a novel family of plant glycosyl hydrolases. Plant J 33:97–106

    Article  CAS  PubMed  Google Scholar 

  • Carpentier SC, Witters E, Laukens K, Deckers P, Swennen R, Panis B (2005) Preparation of protein extracts from recalcitrant plant tissues: an evaluation of different methods for two-dimensional gel electrophoresis analysis. Proteomics 5:2497–2507

    Article  CAS  PubMed  Google Scholar 

  • Chrost B, Schmitz K (1997) Changes in soluble sugar and activity of α-galactosidases and acid invertase during muskmelon (Cucumis melo L.) fruit development. J Plant Physiol 151:41–45

    Article  CAS  Google Scholar 

  • Devitt LC, Sawbridge T, Holton TA, Mitchelson K, Dietzgen RG (2006) Discovery of genes associated with fruit ripening in Carica papaya using expressed sequence tags. Plant Sci 170:356–363

    Article  CAS  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Feurtado JA, Banik M, Bewley JD (2001) The cloning and characterization of α-galactosidase present during and following germination of tomato (Lycopersicon esculentum Mill.) seed. J Exp Bot 52:1239–1249

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Gao Z, Schaffer AA (1999) A novel alkaline a-galactosidase from melon fruit with a substrate preference for raffinose. Plant Physiol 119:979–987

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gibbs D (1974) Chemotaxonomy of flowering plants, vol III. McGill-Queens University Press, Montreal, p 1762

    Google Scholar 

  • Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. Plant Cell 16:S170–S180

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jagadeesh BH, Prabha TN, Srinivasan K (2004) Activities of glycosidases during fruit development and ripening of tomato (Lycopersicum esculentum L.): implication in fruit ripening. Plant Sci 166:1451–1459

    Article  CAS  Google Scholar 

  • Javanmardi J, Kubota C (2006) Variation of lycopene, antioxidant activity, total soluble solids and weight loss of tomato during postharvest storage. Postharv Biol Technol 41:151–155

    Article  CAS  Google Scholar 

  • Kim WD, Kobayashi O, Kaneko S, Sakakibara Y, Park GG, Kusakabe I, Tanaka H, Kobayashi H (2002) a-Galactosidase from cultured rice (Oryza sativa L. var. Nipponbare) cells. Phytochemistry 61:621–630

    Article  CAS  PubMed  Google Scholar 

  • Klee HJ, Giovannoni JJ (2011) Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet 45:41–59

    Article  CAS  PubMed  Google Scholar 

  • Lombardo VA, Osorio S, Borsani J, Lauxmann MA, Bustamante CA, Budde CO, Andreo CS, Lara MV, Fernie AR, Drincovich MF (2011) Metabolic profiling during peach fruit development and ripening reveals the metabolic networks that underpin each developmental stage. Plant Physiol 157:1696–1710

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Marraccini P, Rogers WJ, Caillet V, Deshayes A, Granato D, Lausanne F, Lechat S, Pridmore D, Pétiard V (2005) Biochemical and molecular characterization of α-d-galactosidase from coffee beans. Plant Physiol Biochem 43:909–920

    Article  CAS  PubMed  Google Scholar 

  • Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 147:1251–1263

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Oms-Oliu G, Hertog MLATM, Van de Poel B, Ampofo-Asiama J, Geeraerd AH, Nicolaï BM (2011) Metabolic characterization of tomato fruit during preharvest development, ripening, and postharvest shelf-life. Postharv Biol Technol 62:7–16

    Article  CAS  Google Scholar 

  • Pennycooke JC, Jones ML, Stushnoff C (2003) Down-regulating α-galactosidase enhances freezing tolerance in transgenic Petunia. Plant Physiol 133:901–909

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pennycooke JC, Vepachedu R, Stushnoff C, Jones ML (2004) Expression of an α-galactosidase gene in petunia is up-regulated during low temperature deacclimation. J Am Soc Hortic Sci 129:491–496

    CAS  Google Scholar 

  • Peters S, Egert A, Stieger B, Keller F (2010) Functional identification of Arabidopsis ATSIP2 (At3g57520) as an alkaline alpha-galactosidase with substrate specificity for raffinose and an apparent sink-specific expression pattern. Plant Cell Physiol 51:1815–1819

    Article  CAS  PubMed  Google Scholar 

  • Rounis V, Skarmoutsos K, Tsaniklidis G, Nikoloudakis N, Delis C, Karapanos I, Aivalakis G (2015) Seeded and parthenocarpic cherry tomato fruits exhibit similar sucrose, glucose and fructose levels, despite dissimilarities in UGPase and SPS gene expression and enzyme activity. J Plant Growth Regul 34:47–56

    Article  CAS  Google Scholar 

  • Saladié M, Matas AJ, Isaacson T, Jenks MA, Goodwin SM, Niklas KJ, Xiaolin R, Labavitch JM, Shackel KA, Fernie AR et al (2007) A reevaluation of the key factors that influence tomato fruit softening and integrity. Plant Physiol 144:1012–1028

    Article  PubMed Central  PubMed  Google Scholar 

  • Sanghera GS, Wani SH, Hussain W, Singh NB (2011) Engineering cold stress tolerance in crop plants. Curr Genom 12:30–43

    Article  CAS  Google Scholar 

  • Smith DL, Starrett DA, Gross KC (1998) A gene coding for tomato fruit β-galactosidase II is expressed during fruit ripening. Plant Physiol 117:417–423

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Soh CP, Ali ZM, Lazan H (2006) Characterisation of an alpha-galactosidase with potential relevance to ripening related texture changes. Phytochemistry 67:242–254

    Article  CAS  PubMed  Google Scholar 

  • Sozzi GO, Camperi SA, Cascone O, Fraschina AA (1998) Galactosidases in tomato fruit ontogeny: decreased galactosidase activities in antisense ACC synthase fruit during ripening and reversal with exogenous ethylene. Aust J Plant Physiol 25:237–244

    Article  CAS  Google Scholar 

  • Tacken E, Ireland H, Gunaseelan K et al (2010) the role of ethylene and cold temperature in the regulation of the apple POLYGALACTURONASE1 gene and fruit softening. Plant Physiol 153:294–305

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi- Shinozaki K, Shinozaki K (2002) Important roles of drought- and cold- inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29:417–426

    Article  CAS  PubMed  Google Scholar 

  • Tong Z, Gao Z, Wang F, Zhou J, Zhang Z (2009) Selection of reliable reference genes for gene expression studies in peach using real-time PCR. BMC Mol Biol 10:71

    Article  PubMed Central  PubMed  Google Scholar 

  • Tsaniklidis G, Delis C, Liakopoulos G, Karapanos I, Katinakis P, Passam HC, Aivalakis G (2012) Induced parthenocarpic cherry tomato fruits did not shown significant differences in l-ascorbate content but showed different pattern in GalLDH and GME expression. Plant Growth Regul 68:493–502

    Article  CAS  Google Scholar 

  • Tsaniklidis G, Diamantis C, Aivalakis G (2014) Study of alternative oxidase in seeded and parthenocarpic cherry tomato fruits during their development and postharvest storage. Acta Physiol Plant 36:2925–2933

    Article  CAS  Google Scholar 

  • van den Ende W (2013) Multifunctional fructans and raffinose family oligosaccharides. Front Plant Sci 4(247):1–11

    Google Scholar 

  • Waldek S, Feriozzi S (2014) Fabry nephropathy: a review—how can we optimize the management of Fabry nephropathy? BMC Nephrol 15:72–85

    Article  PubMed Central  PubMed  Google Scholar 

  • Wang F, Sanz A, Benner ML, Smith A (1993) Sucrose synthase, starch accumulation, and tomato fruit sink strength. Plant Physiol 101:321–327

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yamamoto R, Inouhe M, Masuda Y (1988) Galactose inhibition of auxin-induced growth of mono- and dicotyledonous plants. Plant Physiol 86:1223–1227

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yao BN, Tano K, Konan HK, Bédié BK, Oulé MK, Koffi-Nevry R, Arul J (2012) The role of hydrolases in the loss of firmness and of the changes in sugar content during the post-harvest maturation of Carica papaya L. var solo 8. J Food Sci Technol. doi:10.1007/s13197-012-0858-x

    Google Scholar 

  • Yativ M, Harary I, Wolf S (2010) Sucrose accumulation in watermelon fruits: genetic variation and biochemical analysis. J Plant Physiol 167:589–596

    Article  CAS  PubMed  Google Scholar 

  • Zha HG, Flowers VL, Yang M, Chen LY, Sun H (2012) Acidic α-galactosidase, the most abundant nectarin in floral nectar of common tobacco (Nicotiana tabacum L.). Ann Bot 109:735–745

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Georgios Tsaniklidis.

Additional information

Communicated by J. Gao.

G. Tsaniklidis and A. Benovias contributed equally to this study.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 85 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tsaniklidis, G., Benovias, A., Delis, C. et al. Acidic alpha galactosidase during the maturation and cold storage of cherry tomatoes. Acta Physiol Plant 38, 57 (2016). https://doi.org/10.1007/s11738-016-2075-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-016-2075-0

Keywords

Navigation