Abstract
Citrus fruit are natural source of several phytochemicals useful in the maintenance of a satisfactory status of the human health. As citric acid is one of the main determinant of citrus fruit quality, researches focusing the elucidation of citrate metabolism have been constantly carried out, often leading to a deeper understanding of the biochemical and physiological changes occurring during fruit development and ripening. Lower interest has been directed to the knowledge of the metabolic fate of citrate during fruit storage, although the temperature controlled conservation is a spread and, in many cases, mandatory practise. In this work, we evaluated the expression of the main enzymes involved in the citrate metabolism, such citrate synthase, citrate lyase and both the cytosolic and mitochondrial isoforms of aconitase, in blood oranges subjected to cold storage (4 °C × 15 days). Total acidity (TA) and total soluble solid (TSS) were also determined to correlate such fruit quality parameters with gene expression. The results suggest that cold storage influences both the analytical parameters and gene expression, in particular, a strong induction of the transcription of all the selected gene was observed simultaneously with the sudden reduction in acidity. These findings suggest that aconitase gene products localized in the cytosolic compartment are strongly implicated in the consumption of the citrate released from vacuoles and meanwhile mitochondrial aconitase is involved in the catabolism of organelle-localized citrate. The expression of citrate lyase turned out to be also induced during cold storage of blood oranges. The alternative breakdown of citrate through the citrate lyase, which is ruled out during fruit development and ripening, might be a pathway exclusively activated in response to cold storage and therefore correlated with the sharp cold induction of the flavonoid biosynthesis which is supplied by the citrate lyase reaction products.
Similar content being viewed by others
Abbreviations
- CitSyn:
-
citrate synthase
- CitLya:
-
citrate lyase
- Aco:
-
aconitate hydratase
- TA:
-
total acidity
- TSS:
-
total solubile solid
References
Amarowicz R, Carle R, Dongowski G, Durazzo A, Galensa R, Kammerer D, Maiani G, Piskula MK (2009) Influence of postharvest processing and storage on the content of phenolic acids and flavonoids in foods. Mol Nutr Food Res 53:S151–S183
Cercòs M, Soler G, Iglesias DJ, Gadea J, Forment J, Talon M (2006) Global analysis of gene expression during development and ripening of citru fruit flesh. A proposed mechanism for citric acid utilization. Plant Mol Biol 62:513–527
Cotroneo PS, Russo MP, Ciuni M, Reforgiato Recupero G, Lo Piero AR (2006) Quantitative real-time RT-PCR profiling of anthocyanin biosynthetic genes during orange fruit ripening. J Amer Soc Hort Sci 131:537–543
Crifò T, Petrone G, Lo Cicero L, Lo Piero AR (2012) Short cold storage enhances the anthocyanin contents and level of transcripts related to their biosynthesis in blood oranges. J Agric Food Chem 60:476–481
Crifò T, Puglisi I, Petrone G, Reforgiato Recupero G, Lo Piero AR (2011) Expression analysis in response to low temperature stress in blood oranges: implication of the flavonoid biosynthetic pathway. Gene 476:1–9
De Pascual-Teresa S, Moreno DA, Garcia-Viguera C (2010) Flavanols and anthocyanins in cardiovascular health: a review of current evidence. Int J Mol Sci 11:679–1703
De Pascual-Teresa S, Sanchez-Ballesta MT (2008) Anthocyanins: from plant to health. Phytochem Rev 7:281–299
Hayashi M, De Bellis L, Alpi A, Nishimura M (1995) Citosolic aconitase participates in the glyoxylate cycle in etiolated pumpkin cotyledons. Plant Cell Physiol 36:669–680
Heid C, Stevens J, Livak K, Williams P (1996) Real time quantitative PCR. Genome Methods: Genome Research; Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY
Iglesias DJ, Cercòs M, Colmenero-Flores JM, Naranjo MA, Rìos G, Carrera E, Ruiz-Rivero O, Lliso I, Morillin R, Tadeo FR, Talon M (2007) Physiology of citrus fruiting. Braz J Plant Physiol 19:333–362
Lo Piero AR, Consoli A, Puglisi I, Orestano G, Reforgiato Recupero G, Petrone G (2005a) Anthocyaninless cultivars of sweet orange lack to express the UDP-glucose flavonoid 3-O-glucosyl transferase. J Plant Biochem Biotech 14:9–14
Lo Piero AR, Mercurio V, Puglisi I, Petrone G (2009) Gene isolation and expression analysis of two distinct sweet orange [Citrus sinensis L. (Osbeck)] tau-type glutathione transferases. Gene 443:143–150
Lo Piero AR, Puglisi I, Petrone G (2011) Characterization of the purified actinidin as a plant coagulant of bovine milk. Eur Food Res Technol 233:517–524
Lo Piero AR, Puglisi I, Rapisarda P, Petrone G (2005b) Anthocyanin accumulation and related gene expression in blood orange fruit induced by low temperature storage. J Agric Food Chem 53:9083–9088
Plaza L, Crespo I, de Pascual-Teresa S, de Ancos B, Sànchez-Moreno C, Munõz M, Pilar Cano M (2011) Impact of minimal processing on orange bioactive compounds during refrigerated storage. Food Chem 124:646–651
Rapisarda P, Bellomo SE, Intelisano S (2001) Storage temperature effects on blood orange fruit quality. J Agric Food Chem 49:3230–3235
Rangasamy D, Ratledge C (2000) Compartmentation of ATP: citrate lyase in plants. Plant Physiol 122:1225–1230
Sadka A, Dahan E, Cohen L, Marsh KB (2000) Aconitase activity and expression during the development of lemon fruit. Physiol Plant 108:255–262
Schirra M, Mulas M, Fadda A, Cauli E (2004) Cold quarantine responses of blood oranges to postharvest hot water and hot air treatments. Postharvest Biol Technol 31:191–200
Shimada T, Nakano R, Shulaev V, Sadka A, Blumwald E (2006) Vacuolar citrate/H+ symporter of citrus juice cells. Planta 224:472–480
Tadeo FR, Cercós M, Colmenero–Flores JM, Iglesias DJ, Naranjo MA, Ríos G, Carrera GE, Ruiz-Rivero O, Lliso I, Morillon R, Ollitrault P, Talon M (2008) Molecular physiology of development and quality of Citrus. Adv Bot Res 47:147–223
Terol J, Soler G, Talon M, Cercos M (2010) The aconitate hydratase family from Citrus. BMC Plant Biology 10:222–233
Acknowledgments
Financial support was provided by the University of Catania, Fondi del Bilancio Universitario, Progetti di Ricerca di Ateneo (PRA), 2009, assigned to Dr. Angela Roberta Lo Piero. Thanks are due to Prof. Carmela Maria Lanza which kindly provided the refractometer used in TSS determination and to Dr. Giuseppe Reforgiato Recupero who supplied the materials.
Author information
Authors and Affiliations
Corresponding author
Additional information
Angela Roberta Lo Piero suggested the research direction, designed the experiments, carried out data analysis and wrote the manuscript; Luca Lo Cicero and Ivana Puglisi performed both experimental work and data analysis.
Rights and permissions
About this article
Cite this article
Lo Piero, A.R., Lo Cicero, L. & Puglisi, I. The metabolic fate of citric acid as affected by cold storage in blood oranges. J. Plant Biochem. Biotechnol. 23, 161–166 (2014). https://doi.org/10.1007/s13562-013-0197-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13562-013-0197-7