Skip to main content
Log in

l-Ascorbic acid metabolism in parthenocarpic and seeded cherry tomatoes

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The auxin treatment in tomato plants during anthesis has been extensively used for setting fruits in adverse climatic conditions (e.g., low temperatures and inadequate light), which is well known that reduces pollen availability and fertility. Since auxin application may affect fruit composition and quality, we examined l-ascorbic acid metabolism in seeded fruit (set by natural pollination) and parthenocarpic fruit (set by auxin) in cherry tomato cv. Conchita. Specifically, we studied the oxidized and total ascorbic acid contents, the expression of all characterized genes of l-ascorbic acid metabolism, the activity of ascorbate peroxidase and dehydroascorbate reductase and the immunolocalization of ascorbate peroxidase. Differences were detected between seeded and parthenocarpic fruits, in the expression of some of the genes of ascorbic acid metabolism. However, strong presence of l-ascorbic acid peroxidase protein was detected on the developing seeds. Our data indicate that induced parthenocarpy in auxin treated plants has a significant influence in ascorbic acid metabolism comparing to seeded tomato fruits.

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
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

AsA:

l-Ascorbic acid

DHA:

Dehydroascorbic acid

tAsA:

Total ascorbate (reduced AsA + DHA)

ImG:

Immature green

Mg:

Mature green

Br:

Breaker

RR:

Red ripe

APX:

Ascorbate peroxidase

MDHAR:

Monodehydroascorbate reductase

DHAR:

Dehydroascorbate reductase

GR:

Glutathione reductase

ROS:

Reactive oxygen species

References

  • Alhagdow M, Mounet F, Gilbert L, Nunes-Nesi A, Garcia V, Just D, Petit J, Beauvoit B, Fernie AR, Rothan C, Baldet P (2007) Silencing of the mitochondrial ascorbate synthesizing enzyme l-galactono-1,4-lactone dehydrogenase affects plant and fruit development in tomato. Plant Physiol 145:1408–1422

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Aoki K, Yano K, Suzuki A, Kawamura S, Sakurai N, Suda K, Kurabayashi A, Suzuki T, Tsugane T, Watanabe M, Ooga K, Torii M, Narita T, Shin IT, Kohara Y, Yamamoto N, Takahashi H, Watanabe Y, Egusa M, Kodama M, Ichinose Y, Kikuchi M, Fukushima S, Okabe A, Arie T, Sato Y, Yazawa K, Satoh S, Omura T, Ezura H, Shibata D (2010) Large-scale analysis of full-length cDNAs from the tomato (Solanum lycopersicum) cultivar Micro-Tom, a reference system for the Solanaceae genomics. BMC Genomics 11:210–215

    Article  PubMed Central  PubMed  Google Scholar 

  • Arrigoni O, De Gara L, Tommasi F, Liso R (1992) Changes in the ascorbate system during seed development of Vicia faba L. Plant Physiol 99:235–238

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Badejo AA, Wada K, Gao Y, Maruta T, Sawa Y, Shigeoka S, Ishikawa T (2012) Translocation and the alternative d-galacturonate pathway contribute to increasing the ascorbate level in ripening tomato fruits together with the d-mannose/l-galactose pathway. J Exp Bot 63:229–239

    Article  CAS  PubMed  Google Scholar 

  • Bartoli CG, Yu J, Gomez F, Fernandez L, McIntosh L, Foyer CH (2006) Inter-relationships between light and respiration in the control of ascorbic acid synthesis and accumulation in Arabidopsis thaliana leaves. J Exp Bot 57:1621–1631

    Article  CAS  PubMed  Google Scholar 

  • Bulley SM, Rassam M, Hoser D, Otto W, Schunemann N, Wright M, MacRae E, Gleave A, Laing W (2009) Gene expression studies in kiwifruit and gene over-expression in Arabidopsis indicates that GDP-l-galactose guanyltransferase is a major control point of vitamin C biosynthesis. J Exp Bot 60:765–778

    Article  CAS  PubMed  Google Scholar 

  • Chen Z, Gallie DR (2006) Dehydroascorbate reductase affects leaf growth, development, and function. Plant Physiol 142:775–787

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen Z, Young TE, Ling J, Chang SC, Gallie DR (2003) Increasing vitamin C content of plants through enhanced ascorbate recycling. PNAS 100:3525–3530

    Article  CAS  PubMed  Google Scholar 

  • Davey M (2003) Rocket-powered high-performance liquid chromatographic analysis of plant ascorbate and glutathione. Anal Biochem 316:74–81

    Article  CAS  PubMed  Google Scholar 

  • Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17:268–281

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • de Jong M, Wolters-Arts M, Feron R, Mariani C, Vriezen WH (2009) The Solanum lycopersicum auxin response factor 7 (SlARF7) regulates auxin signaling during tomato fruit set and development. Plant J 57:160–170

    Article  PubMed  Google Scholar 

  • de Pinto MC, de Gara L (2004) Changes in the ascorbate metabolism of apoplastic and symplastic spaces are associated with cell differentiation. J Exp Bot 55:2559–2569

    Article  PubMed  Google Scholar 

  • Delis C, Krokida A, Georgiou S, Pena-Rodriguez LM, Kavroulakis N, Ioannou E, Roussis V, Osbourn AE, Papadopoulou KK (2011) Role of lupeol synthase in Lotus japonicus nodule formation. New Phytol 189:335–346

    Article  CAS  PubMed  Google Scholar 

  • di Matteo A, Sacco A, Anacleria M, Pezzotti M, Delledonne M, Ferrarini A, Frusciante L, Barone A (2010) The ascorbic acid content of tomato fruits is associated with the expression of genes involved in pectin degradation. BMC Plant Biol 10:163–173

    Article  PubMed Central  PubMed  Google Scholar 

  • Eltelib HA, Fujikawa Y, Esaka M (2012) Overexpression of the acerola (Malpighia glabra) monodehydroascorbate reductase gene in transgenic tobacco plants results in increased ascorbate levels and enhanced tolerance to salt stress. S Afr J Bot 78:295–301

    Article  CAS  Google Scholar 

  • Forti G, Elli G (1995) The function of ascorbic acid in photosynthetic phosphorylation. Plant Physiol 109:1207–1211

    CAS  PubMed Central  PubMed  Google Scholar 

  • Foyer CH, Noctor G (2011) Ascorbate and glutathione: the heart of the redox hub. Plant Physiol 155:2–18

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gest N, Gautier H, Steevens R (2013) Ascorbate as seen through plant evolution: the rise of a successful molecule? J Exp Bot 64:33–53

    Article  CAS  PubMed  Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930

    Article  CAS  PubMed  Google Scholar 

  • Grantz AA, Brummell DA, Bennett AB (1995) Ascorbate free radical reductase mRNA levels are induced by wounding. Plant Physiol 108:411–418

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Haroldsen VM, Chi-Ham CL, Kulkarni S, Lorence A, Bennett AB (2011) Constitutively expressed DHAR and MDHAR influence fruit, but not foliar ascorbate levels in tomato. Plant Physiol Biochem 49:1244–1249

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Hazra P, Dutta AK (2010) Inheritance of parthenocarpy in tomato (Solanum lycopersicum) and its association with two marker characters. Int J Plant Sci 1:144–149

    Google Scholar 

  • Henmi K, Demura T, Tsuboi S, Fukuda H, Iwabuchi M, Ogawa K (2005) Change in the redox state of glutathione regulates differentiation of tracheary elements in Zinnia cells and Arabidopsis roots. Plant Cell Physiol 46:1757–1765

    Article  CAS  PubMed  Google Scholar 

  • Ioannidi E, Kalamaki MS, Engineer C, Pateraki I, Alexandrou D, Mellidou I, Giovannonni J, Kanellis AK (2009) Expression profiling of ascorbic acid-related genes during tomato fruit development and ripening and in response to stress conditions. J Exp Bot 60:663–678

    Article  CAS  PubMed  Google Scholar 

  • Ishikawa T, Shigeoka S (2008) Recent advances in ascorbate biosynthesis and the physiological significance of ascorbate peroxidase in photosynthesizing organisms. Biosci Biotech Biochem 72:1143–1154

    Article  CAS  Google Scholar 

  • Ishikawa T, Dowdle J, Smirnoff N (2006) Progress in manipulating ascorbic acid biosynthesis and accumulation in plants. Physiol Plant 126:343–355

    Article  CAS  Google Scholar 

  • Jimenez A, Creissen G, Kular B, Firmin J, Robinson S, Verhoeyen M, Mullineaux P (2002) Changes in oxidative processes and components of the antioxidant system during tomato fruit ripening. Planta 214:751–758

    Article  CAS  PubMed  Google Scholar 

  • Kataya AR, Reumann S (2010) Arabidopsis glutathione reductase 1 is dually targeted to peroxisomes and the cytosol. Plant Signal Behav 5:171–175

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kim IJ, Chung WI (1998) Molecular characterization of a cytosolic ascorbate peroxidase in strawberry fruit. Plant Sci 133:69–77

    Article  CAS  Google Scholar 

  • Li MJ, Ma FW, Zhang M, Pu F (2008) Distribution and metabolism of ascorbic acid in apple fruits (Malus domestica Borkh cv. Gala). Plant Sci 174:606–612

    Article  CAS  Google Scholar 

  • Li F, Wu QY, Sun YL, Wang LY, Yang XH, Meng QW (2010a) Overexpression of chloroplastic monodehydroascorbate reductase enhanced tolerance to temperature and methyl viologen-mediated oxidative stresses. Physiol Plant 139:421–434

    CAS  PubMed  Google Scholar 

  • Li M, Ma F, Liu J, Li J (2010b) Shading the whole vines during young fruit development decreases ascorbate accumulation in kiwi. Physiol Plant 140:225–237

    CAS  PubMed  Google Scholar 

  • Marin A, Ferreres F, Tomás-Barberán F, Gil MI (2004) Characterization and quantification of antioxidant constituents of sweet pepper. J Agric Food Chem 52:3861–3869

    Article  CAS  PubMed  Google Scholar 

  • Najami N, Janda T, Barriah W, Kayam G, Tal M, Guy M, Volokita M (2008) Ascorbate peroxidase gene family in tomato: its identification and characterization. Mol Genet Genomics 279:171–182

    Article  CAS  PubMed  Google Scholar 

  • Noctor G, Gomez L, Vanacker H, Foyer CH (2002) Interactions between biosynthesis, compartmentation and transport in the control of glutathione homeostasis and signaling. J Exp Bot 53:1283–1304

    Article  CAS  PubMed  Google Scholar 

  • Panchuk II, Volkov RA, Schoffl F (2002) Heat stress and heat shock transcription factor-dependent expression and activity of ascorbate peroxidase in Arabidopsis. Plant Physiol 129:838–853

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pandolfini T, Rotino GL, Camerini S, Defez R, Spena A (2002) Optimization of transgene action at the post-transcriptional level: high quality parthenocarpic fruits in industrial tomatoes. BMC Biotech 2:1–11

    Article  Google Scholar 

  • Raffo A, Leonardi C, Fogliano V, Ambrosino P, Salucci M, Gennaro L, Bugianesi R, Giuffrida F, Quaglia G (2002) Nutritional value of cherry tomatoes (Lycopersicon esculentum cv. Naomi F1) harvested at different ripening stages. J Agric Food Chem 50:6550–6556

    Article  CAS  PubMed  Google Scholar 

  • Schantz ML, Schreiber H, Guillemaut P, Schantz R (1995) Changes in ascorbate peroxidase activities during fruit ripening in Capsicum annuum. FEBS Lett 23:149–152

    Article  Google Scholar 

  • Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319

    Article  CAS  PubMed  Google Scholar 

  • Shu DF, Wang LW, Duan M, Deng YS, Meng QW (2011) Antisense-mediated depletion of tomato chloroplast glutathione reductase enhances susceptibility to chilling stress. Plant Physiol Biochem 49:1228–1237

    Article  CAS  PubMed  Google Scholar 

  • Smirnoff N (2011) Vitamin C: the metabolism and functions of ascorbic acid in plants. Adv Bot Res 9:109–177. doi:10.1016/B978-0-12-385853-5.00003-9

    Google Scholar 

  • Stevens R, Buret M, Duffé P, Garchery C, Baldet P, Rothan C, Causse M (2007) Candidate genes and quantitative trait loci affecting fruit ascorbic acid content in three tomato populations. Plant Physiol 1431:943–953

    Google Scholar 

  • Tommasi F, Paciolla C, Arrigoni O (1999) The ascorbate system in recalcitrant and orthodox seeds. Physiol Plant 105:193–198

    Article  CAS  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 

  • Zhang W, Lorence A, Gruszewski HA, Chevone BI, Nessler CL (2009) AMR1, an Arabidopsis gene that coordinately and negatively regulates the mannose/l-galactose ascorbic acid biosynthetic pathway. Plant Physiol 150:942–950

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zou L, Li H, Ouyang B, Zhang J, Ye Z (2006) Cloning and mapping of genes involved in tomato ascorbic acid biosynthesis and metabolism. Plant Sci 170:120–127

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Georgios Tsaniklidis.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 21 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tsaniklidis, G., Delis, C., Nikoloudakis, N. et al. l-Ascorbic acid metabolism in parthenocarpic and seeded cherry tomatoes. Plant Growth Regul 72, 141–153 (2014). https://doi.org/10.1007/s10725-013-9845-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-013-9845-0

Keywords

Navigation