Abstract
Vitis vinifera L. represents an economically important fruit species. Grape and wine flavour is made from a complex set of compounds. The acidity of berries is a major parameter in determining grape berry quality for wine making and fruit consumption. Despite the importance of malic and tartaric acid (TA) storage and transport for grape berry acidity, no vacuolar transporter for malate or tartrate has been identified so far. Some members of the aluminium-activated malate transporter (ALMT) anion channel family from Arabidopsis thaliana have been shown to be involved in mediating malate fluxes across the tonoplast. Therefore, we hypothesised that a homologue of these channels could have a similar role in V. vinifera grape berries. We identified homologues of the Arabidopsis vacuolar anion channel AtALMT9 through a TBLASTX search on the V. vinifera genome database. We cloned the closest homologue of AtALMT9 from grape berry cDNA and designated it VvALMT9. The expression profile revealed that VvALMT9 is constitutively expressed in berry mesocarp tissue and that its transcription level increases during fruit maturation. Moreover, we found that VvALMT9 is targeted to the vacuolar membrane. Using patch-clamp analysis, we could show that, besides malate, VvALMT9 mediates tartrate currents which are higher than in its Arabidopsis homologue. In summary, in the present study we provide evidence that VvALMT9 is a vacuolar malate channel expressed in grape berries. Interestingly, in V. vinifera, a tartrate-producing plant, the permeability of the channel is apparently adjusted to TA.
Similar content being viewed by others
Abbreviations
- ALMT:
-
Aluminium-activated malate transporter
- MA:
-
Malic acid
- TA:
-
Tartaric acid
- SUC:
-
Succinic acid
- AA:
-
l-Ascorbic acid
- PEPC:
-
Phosphoenolpyruvate carboxylase
- MDH:
-
Malate dehydrogenase
- ME:
-
Malic enzyme
- AttDT:
-
Arabidopsis thaliana tonoplast dicarboxylate transporter
- DAF:
-
Days after flowering
References
Briggs GG, Rigitano RLO, Bromilow RH (1987) Physico-chemical factors affecting uptake by roots and translocation to shoots of weak acids in barley. Pestic Sci 19:101–112
Conde C, Silva P, Fontes N, Dias ACP, Tavares RM, Sousa MJ, Agasse A, Delrot S, Geros H (2007) Biochemical changes throughout grape berry development and fruit and wine quality. Food 1:1–22
Coombe BG (1976) The development of fleshy fruits. Annu Rev Plant Physiol 27:207–228
Coombe BG (1992) Research on development and ripening on the grape berry. Am J Enol Vitic 43:101–110
Emmerlich V, Linka N, Reinhold T, Hurth MA, Traub M, Martinoia E, Neuhaus HE (2003) The plant homolog to the human sodium/dicarboxylic cotransporter is the vacuolar malate carrier. Proc Natl Acad Sci USA 100:11122–11126
Fernie AR, Martinoia E (2009) Malate: Jack of all trades or master of a few? Phytochemistry 70:828–832
Hoekenga OAL, Maron G, Piñeros MA, Cançado GM, Shaff J, Kobayashi Y, Ryan PR, Dong B, Delhaize E, Sasaki T, Matsumoto H, Yamamoto Y, Koyama H, Kochian LV (2006) AtALMT1, which encodes a malate transporter, is identified as one of several genes critical for aluminum tolerance in Arabidopsis. Proc Natl Acad Sci USA 103:9738–9743
Holsters M, Silva B, Van Vliet F, Genetello C, De Block M, Dhaese P, Depicker A, Inzé D, Engler G, Villarroel R (1980) The functional organization of the nopaline A. tumefaciens plasmid pTiC58. Plasmid 3:212–230
Kanellis AK, Roubelakis-Angelakis KA (1993) Grapes. In: Seymour GI, Taylor J, Tucker GA (eds) Biochemistry of fruit ripening. Chapman & Hall, London, pp 189–234
Kovermann P, Meyer S, Hörtensteiner S, Picco C, Scholz-Starke J, Ravera S, Lee Y, Martinoia E (2007) The Arabidopsis vacuolar malate channel is a member of the ALMT family. Plant J 52:1169–1180
Melino VJ, Soole KL, Ford CM (2009) Ascorbate metabolism and the developmental demand for tartaric and oxalic acids in ripening grape berries. BMC Plant Biol 9:145
Meyer S, Mumm P, Imes D, Endler A, Weder B, Al-Rasheid KA, Geiger D, Marten I, Martinoia E, Hedrich R (2010) AtALMT12 represents an R-type anion channel required for stomatal movement in Arabidopsis guard cells. Plant J 63:1054–1062
Meyer S, Scholz-Starke J, De Angeli A, Kovermann P, Burla B, Gambale F, Martinoia E (2011) Malate transport by the vacuolar AtALMT6 channel in guard cells is subject to multiple regulation. Plant J 67:247–257
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9):e45
Reid KE, Olsson N, Schlosser J, Peng F, Lund ST (2006) An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development. BMC Plant Biol 6:27
Saito K, Kasai Z (1968) Accumulation of tartaric acid in the ripening process of grapes. Plant Cell Physiol 9:529–537
Saito K, Kasai Z (1969) Tartaric acid synthesis from l-ascorbic acid-1-14C in grape berries. Phytochemistry 8:2177–2182
Sweetman C, Deluc G, Cramer GR, Ford CM, Soole KL (2009) Regulation of malate metabolism in grape berry and other developing fruits. Phytochemistry 70:1329–1344
Taureilles-Saurel C, Romieu CG, Robin JP, Flanzy C (1995a) Grape (Vitis vinifera L.) malate dehydrogenase. I. Intracellular compartmentationof the isoforms. Am J Enol Vitic 46:22–28
Taureilles-Saurel C, Romieu CG, Robin JP, Flanzy C (1995b) Grape (Vitis vinifera L.) malate dehydrogenase. II. Characterization of the major mitochondrial and cytosolic isoforms and their role in ripening. Am J Enol Vitic 46:29–36
Terrier N, Sauvage FX, Ageorges A, Romieu C (2001) Changes in acidity and in proton transport at the tonoplast of grape berries during development. Planta 213:20–28
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Weast RC, Astle MJ (1982–1983) CRC Handbook of chemistry and physics. CRC Press. Boca Raton
Acknowledgments
We would like to thank Prof. Enrico Martinoia (University of Zurich, Switzerland) for his scientific support and helpful discussions, Dr. Stefan Meyer (University of Zurich, Switzerland) for discussions, Dr. Nelson Saibo (Genomics of Plant Stress Laboratory–ITQB, Universidade Nova de Lisboa, Portugal) for kindly providing the cloning vectors and Duarte Figueiredo (Genomics of Plant Stress Laboratory–ITQB, Universidade Nova de Lisboa), Tânia Serra (Genomics of Plant Stress Laboratory–ITQB, Universidade Nova de Lisboa) and André Cordeiro (Genomics of Plant Stress Laboratory–ITQB, Universidade Nova de Lisboa) for technical support with the preliminary Nicotiana agroinfiltration experiments. AR and RF acknowledge FCT for the financial support through fellow FRH/BPD/34986/2007 and SFRH/BPD/74210/2010, respectively. AD was supported by a long-term EMBO fellowship (ALTF 87-2009), JZ by the Chinese Scholarship Council and UB by the Swiss National Foundation (31003A_141090/1).
Author information
Authors and Affiliations
Corresponding author
Additional information
A. De Angeli and U. Baetz contributed equally to the work.
Rights and permissions
About this article
Cite this article
De Angeli, A., Baetz, U., Francisco, R. et al. The vacuolar channel VvALMT9 mediates malate and tartrate accumulation in berries of Vitis vinifera . Planta 238, 283–291 (2013). https://doi.org/10.1007/s00425-013-1888-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-013-1888-y