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The grapevine VvCAX3 is a cation/H+ exchanger involved in vacuolar Ca2+ homeostasis

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Abstract

Main conclusion

The grapevine VvCAX3 mediates calcium transport in the vacuole and is mostly expressed in green grape berries and upregulated by Ca 2+ , Na + and methyl jasmonate.

Calcium is an essential plant nutrient with important regulatory and structural roles in the berries of grapevine (Vitis vinifera L.). On the other hand, the proton-cation exchanger CAX proteins have been shown to impact Ca2+ homeostasis with important consequences for fruit integrity and resistance to biotic/abiotic stress. Here, the CAX gene found in transcriptomic databases as having one of the highest expressions in grapevine tissues, VvCAX3, was cloned and functionally characterized. Heterologous expression in yeast showed that a truncated version of VvCAX3 lacking its NNR autoinhibitory domain (sCAX3) restored the ability of the yeast strain to grow in 100–200 mM Ca2+, demonstrating a role in Ca2+ transport. The truncated VvCAX3 was further shown to be involved in the transport of Na+, Li+, Mn2+ and Cu2+ in yeast cells. Subcellular localization studies using fluorescently tagged proteins confirmed VvCAX3 as a tonoplast transporter. VvCAX3 is expressed in grapevine stems, leaves, roots, and berries, especially at pea size, decreasing gradually throughout development, in parallel with the pattern of calcium accumulation in the fruit. The transcript abundance of VvCAX3 was shown to be regulated by methyl jasmonate (MeJA), Ca2+, and Na+ in grape cell suspensions, and the VvCAX3 promotor contains several predicted cis-acting elements related to developmental and stress response processes. As a whole, the results obtained add new insights on the mechanisms involved in calcium homeostasis and intracellular compartmentation in grapevine, and indicate that VvCAX3 may be an interesting target towards the development of strategies for enhancement of grape berry properties.

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Abbreviations

CAX:

H+/cation exchanger

GFP (RFP, YFP):

Green (red, yellow) fluorescent protein

MeJA:

Methyl jasmonate

NRR:

Auto inhibitory domain

RDR:

Regulatory-dependent region

References

  • Arvidsson S, Kwasniewski M, Riano-Pachon DM, Mueller-Roeber B (2008) QuantPrime—a flexible tool for reliable high-throughput primer design for quantitative PCR. BMC Bioinform 9:465

    Article  Google Scholar 

  • Cabanne C, Donèche B (2003) Calcium accumulation and redistribution during the development of grape berry. Vitis 42:19–21

    CAS  Google Scholar 

  • Cagnac O, Aranda-Sicilia MN, Leterrier M, Rodriguez-Rosales MP, Venema K (2010) Vacuolar cation/H+ antiporters of Saccharomyces cerevisiae. J Biol Chem 285:33914–33922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cai X, Lytton J (2004) The cation/Ca2+ exchanger superfamily: phylogenetic analysis and structural implications. Mol Biol Evol 21:1692–1702

    Article  CAS  PubMed  Google Scholar 

  • Catala R, Santos E, Alonso JM, Ecker JR, Martinez-Zapater JM, Salinas J (2003) Mutations in the Ca2+/H+ transporter CAX1 increase CBF/DREB1 expression and the cold-acclimation response in Arabidopsis. Plant Cell 15:2940–2951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen H, Zhang X (2014) Subcellular localization of CAX proteins in plants. Mol Soil Biol 6:1–5

    Google Scholar 

  • Cheng N-H, Pittman JK, Shigaki T, Hirschi KD (2002) Characterization of CAX4, an Arabidopsis H+/cation antiporter. Plant Physiol 128:1245–1254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng N-H, Pittman JK, Barkla BJ, Shigaki T, Hirschi KD (2003) The Arabidopsis cax1 mutant exhibits impaired ion homeostasis, development, and hormonal responses and reveals interplay among vacuolar transporters. Plant Cell 15:347–364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng N-H, Pittman JK, Shigaki T, Lachmansingh J, LeClere S, Lahner B, Salt DE, Hirschi KD (2005) Functional association of Arabidopsis CAX1 and CAX3 is required for normal growth and ion homeostasis. Plant Physiol 138:2048–2060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cho D, Villiers F, Kroniewicz L, Lee S, Seo YJ, Hirschi KD, Leonhardt N, Kwak JM (2012) Vacuolar CAX1 and CAX3 influence auxin transport in guard cells via regulation of apoplastic pH. Plant Physiol 160:1293–1302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chung MY, Han J-S, Giovannoni J, Liu Y, Kim C-K, Lim KB, Chung JD (2010) Modest calcium increase in tomatoes expressing a variant of Arabidopsis cation/H+ antiporter. Plant Biotechnol Rep 4:15–21

    Article  Google Scholar 

  • Conde C, Silva S, Fontes N, Dias ACP, Tavares RM, Sousa MJ, Agasse A, Delrot S, Gerós H (2007) Biochemical changes throughout grape berry development and fruit and wine quality. Food 1:1–22

    Google Scholar 

  • Conn SJ, Gilliham M, Athman A, Schreiber AW, Baumann U, Moller I, Cheng N-H, Stancombe MA, Hirschi KD, Webb AAR, Burton R, Kaiser BN, Tyerman SD, Leigh RA (2011) Cell-specific vacuolar calcium storage mediated by CAX1 regulates apoplastic calcium concentration, gas exchange, and plant productivity in Arabidopsis. Plant Cell 23:240–257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coombe BG (1995) Adoption of a system for identifying grapevine growth stages. Aust J Grape Wine Res 1:100–110

    Article  Google Scholar 

  • Cunningham KW, Fink GR (1996) Calcineurin inhibits VCX1-dependent H+/Ca2+ exchange and induces Ca2+ ATPases in Saccharomyces cerevisiae. Mol Cell Biol 16:2226–2237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Descendit A, Ramawat KG, Waffo P, Deffieux G, Badoc A, Merillon JM (1996) Anthocyanins, catechins, condensed tannins and piceid production in Vitis vinifera cell bioreactor cultures. Biotechnol Lett 18:659–662

    Article  Google Scholar 

  • Emery L, Whelan S, Hirschi KD, Pittman JK (2012) Protein phylogenetic analysis of Ca2+/cation antiporters and insights into their evolution in plants. Front Plant Sci 3:1–19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fontes N, Silva R, Vignault C, Lecourieux F, Gerós H, Delrot S (2010) Purification and functional characterization of protoplasts and intact vacuoles from grape cells. BMC Res Notes 3:19

    Article  PubMed  PubMed Central  Google Scholar 

  • Freitas ST, Amaranteb CVT, Labavitcha JM, Mitchama EJ (2010) Cellular approach to understand bitter pit development in apple fruit. Postharvest Biol Technol 57:6–13

    Article  Google Scholar 

  • Gainza-Cortés F, Pérez-Dïaz R, Pérez-Castro R, Tapia J, Casaretto JA, González S, Peña-Cortés H, Ruiz-Lara S, González E (2012) Characterization of a putative grapevine Zn transporter, VvZIP3, suggests its involvement in early reproductive development in Vitis vinifera L. BMC Plant Biol 12:111

    Article  PubMed  PubMed Central  Google Scholar 

  • Garcia-Molina A, Andrés-Colás N, Perea-García A, del Valle-Tascón S, Peñarrubia L, Puig S (2011) The intracellular Arabidopsis COPT5 transport protein is required for photosynthetic electron transport under severe copper deficiency. Plant J 65:848–860

    Article  CAS  PubMed  Google Scholar 

  • Hepler PK (2005) Calcium: a central regulator of plant growth and development. Plant Cell 17:2142–2155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirschi KD (1999) Expression of Arabidopsis CAX1 in tobacco: altered calcium homeostasis and increased stress sensitivity. Plant Cell 11:2113–2122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hirschi KD, Zhen RG, Cunningham KW, Rea PA, Fink GR (1996) CAX1, an H+/Ca2+ antiporter from Arabidopsis. P Natl Acad Sci USA 93:8782–8786

    Article  CAS  Google Scholar 

  • Hirschi KD, Korenkov VD, Wilganowski NL, Wagner GJ (2000) Expression of Arabidopsis CAX2 in tobacco. Altered metal accumulation and increased manganese tolerance. Plant Physiol 124:125–133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu X, Li W, Chen Q, Yang Y (2009) Early signal transduction linking the synthesis of jasmonic acid in plant. Plant Signal Behav 4:696–697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang X-M, Huang H-B, Wang H-C (2005) Cell walls of loosening skin in post-veraison grape berries lose structural polysaccharides and calcium while accumulate structural proteins. Sci Hortic 104:249–263

    Article  CAS  Google Scholar 

  • Jaillon O, Aury J-M, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

    Article  CAS  PubMed  Google Scholar 

  • Kader MA, Lindberg S (2010) Cytosolic calcium and pH signaling in plants under salinity stress. Plant Signal Behav 5:233–238

    Article  PubMed  PubMed Central  Google Scholar 

  • Kamiya T, Maeshima M (2004) Residues in internal repeats of the rice cation/H+ exchanger are involved in the transport and selection of cations. J Biol Chem 279:812–819

    Article  CAS  PubMed  Google Scholar 

  • Kamiya T, Akahori T, Ashikari M, Maeshima M (2006) Expression of the vacuolar Ca2+/H+ exchanger, OsCAX1a, in rice: cell and age specificity of expression, and enhancement by Ca2+. Plant Cell Physiol 47:96–106

    Article  CAS  PubMed  Google Scholar 

  • Karimi M, Inze D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7:193–195

    Article  CAS  PubMed  Google Scholar 

  • Klaumann S, Nickolaus SD, Fürst SH, Starck S, Schneider S, Neuhaus HE, Trentmann O (2011) The tonoplast copper transporter COPT5 acts as an exporter and is required for interorgan allocation of copper in Arabidopsis thaliana. New Phytol 192:393–404

    Article  CAS  PubMed  Google Scholar 

  • Kotrba P, Najmanova J, Macek T, Ruml T, Mackova M (2009) Genetically modified plants in phytoremediation of heavy metal and metalloid soil and sediment pollution. Biotechnol Adv 27:799–810

    Article  CAS  PubMed  Google Scholar 

  • Kumar A, Singh UM, Manohar M, Gaur VS (2015) Calcium transport from source to sink: understanding the mechanism(s) of acquisition, translocation, and accumulation for crop biofortification. Acta Physiol Plant 37:1722

    Article  Google Scholar 

  • Luo GZ, Wang HW, Huang J, Tian A-G, Wang Y-J, Zhang J-S, Chen S-Y (2005) A putative plasma membrane cation/proton antiporter from soybean confers salt tolerance in Arabidopsis. Plant Mol Biol 59:809–820

    Article  CAS  PubMed  Google Scholar 

  • Manohar M, Shigaki T, Hirschi KD (2011) Plant cation/H+ exchangers (CAXs): biological functions and genetic manipulations. Plant Biol 13:561–569

    Article  CAS  PubMed  Google Scholar 

  • Martins V, Cunha A, Gerós H, Hanana M, Blumwald E (2012a) Mineral compounds in grape berry. In: Gerós H, Chaves M-M, Delrot S (eds) The biochemistry of the grape berry. Bentham eBooks, Bentham Science Publishers, pp 23–43

  • Martins V, Hanana M, Blumwald E, Gerós H (2012b) Copper transport and compartmentation in grape cells. Plant Cell Physiol 53:1866–1880

    Article  CAS  PubMed  Google Scholar 

  • Martins V, Bassil E, Hanana M, Blumwald E, Gerós H (2014a) Copper homeostasis in grapevine: functional characterization of the Vitis vinifera copper transporter 1. Planta 240:91–101

    Article  CAS  PubMed  Google Scholar 

  • Martins V, Teixeira A, Bassil E, Hanana M, Blumwald E, Gerós H (2014b) Copper-based fungicide Bordeaux mixture regulates the expression of Vitis vinifera copper transporters (VvCTrs). Aust J Grape Wine Res 20:451–458

    Article  CAS  Google Scholar 

  • Mei H, Zhao J, Pittman JK, Lachmansingh J, Park S, Hirschi KD (2007) In planta regulation of the Arabidopsis Ca2+/H+ antiporter CAX1. J Exp Bot 58:3419–3427

    Article  CAS  PubMed  Google Scholar 

  • Melchionda M, Pittman JK, Mayor R, Pate S (2016) Ca2+/H+exchange by acidic organelles regulates cell migration in vivo. J Cell Biol 212:803–813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morris J, Hawthorne KM, Hotze T, Abrams SA, Hirschi KD (2008) Nutritional impact of elevated calcium transport activity in carrots. Proc Natl Acad Sci USA 105:1431–1435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Park S, Kim C-K, Pike LM, Smith RH, Hirschi KD (2004) Increased calcium in carrots by expression of an Arabidopsis H+/Ca2+ transporter. Mol Breed 14:275–282

    Article  Google Scholar 

  • Park S, Cheng N-H, Pittman JK, Yoo KS, Park J, Smith RH, Hirschi KD (2005a) Increased calcium levels and prolonged shelf life in tomatoes expressing Arabidopsis H+/Ca2+ transporters. Plant Physiol 139:1194–1206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park S, Kang T-S, Kim C-K, Han J-S, Kim S, Smith RH, Pike LM, Hirschi KD (2005b) Genetic manipulation for enhancing calcium content in potato tuber. J Agric Food Chem 53:5598–5603

    Article  CAS  PubMed  Google Scholar 

  • Park S, Elless MP, Park J, Jenkins A, Lim W, Chambers E IV, Hirschi KD (2009) Sensory analysis of calcium-biofortified lettuce. Plant Biotechnol J 7:106–117

    Article  CAS  PubMed  Google Scholar 

  • Pittman JK (2011) Vacuolar Ca2+ uptake. Cell Calcium 50:139–146

    Article  CAS  PubMed  Google Scholar 

  • Pittman JK (2012) Multiple transport pathways for mediating intracellular pH homeostasis: the contribution of H+/ion exchangers. Front Plant Sci 3:1–8

    Article  PubMed  PubMed Central  Google Scholar 

  • Pittman JK, Hirschi KD (2016) CAX-ing a wide net: cation/H+ transporters in metal remediation and abiotic stress signalling. Plant Biol 18:741–749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pittman JK, Shigaki T, Cheng N-H, Hirschi KD (2002a) Mechanism of N-terminal autoinhibition in the Arabidopsis Ca2+/H+ antiporter CAX1. J Biol Chem 277:26452–26459

    Article  CAS  PubMed  Google Scholar 

  • Pittman JK, Sreevidya CS, Shigaki T, Ueoka-Nakanishi H, Hirschi KD (2002b) Distinct N-terminal regulatory domains of Ca2+/H+ antiporters. Plant Physiol 130:1054–1062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pittman JK, Shigaki T, Marshall JL, Morris JL, Cheng NH, Hirschi KD (2004) Functional and regulatory analysis of the Arabidopsis thaliana CAX2 cation transporter. Plant Mol Biol 56:959–971

    Article  CAS  PubMed  Google Scholar 

  • Pittman JK, Shigaki T, Hirschi KD (2005) Evidence of differential pH regulation of the Arabidopsis vacuolar Ca2+/H+ antiporters CAX1 and CAX2. FEBS Lett 579:2648–2656

    Article  CAS  PubMed  Google Scholar 

  • Qi BS, Li CG, Chen YM, Lu PL, Hao FS, Shen GM, Chen J, Wang XC (2005) Functional analysis of rice Ca2+/H+ antiporter OsCAX3 in yeast and its subcellular localization in plant. Prog Biochem Biophys 32:876–881

    CAS  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • Rengel Z (1992) The role of calcium in salt toxicity. Plant Cell Environ 15:625–632

    Article  CAS  Google Scholar 

  • Shigaki T, Cheng NH, Pittman JK, Hirschi KD (2001) Structural determinants of Ca2+ transport in the Arabidopsis H+/Ca2+ antiporter CAX1. J Biol Chem 276:43152–43159

    Article  CAS  PubMed  Google Scholar 

  • Shigaki T, Sreevidya C, Hirschi KD (2002) Analysis of the Ca2+ domain in the Arabidopsis H+/Ca2+ antiporters CAX1 and CAX3. Plant Mol Biol 50:475–483

    Article  CAS  PubMed  Google Scholar 

  • Shigaki T, Barkla BJ, Miranda-Vergara MC, Zhao J, Pantoja O, Hirschi KD (2005) Identification of a crucial histidine involved in metal transport activity in the Arabidopsis cation/H+ exchanger CAX1. J Biol Chem 280:30136–30142

    Article  CAS  PubMed  Google Scholar 

  • Shigaki T, Rees I, Nakhleh L, Hirschi KD (2006) Identification of three distinct phylogenetic groups of CAX cation/proton antiporters. J Mol Evol 63:815–825

    Article  CAS  PubMed  Google Scholar 

  • Sparkes IA, Runions J, Kearns A, Hawes C (2006) Rapid, transient expression of fluorescent fusion protein in tobacco plants and generation of stably transformed plants. Nat Protoc 1:2019–2025

    Article  CAS  PubMed  Google Scholar 

  • Sun Q-P, Guo Y, Sun Y, Sun D-Y, Wang X-J (2006) Influx of extracellular Ca2+ involved in jasmonic-acid-induced elevation of [Ca2+]cyt and JR1 expression in Arabidopsis thaliana. J Plant Res 119:343–350

    Article  CAS  PubMed  Google Scholar 

  • Tuteja N, Mahajan S (2007) Calcium signaling network in plants. Plant Signal Behav 2:79–85

    Article  PubMed  PubMed Central  Google Scholar 

  • Ueoka-Nakanishi H, Tsuchiya T, Sasaki M, Nakanishi Y, Cunningham KW, Maeshima M (2000) Functional expression of mung bean Ca2+/H+ antiporter in yeast and its intracellular localization in the hypocotyl and tobacco cells. Eur J Biochem 267:3090–3098

    Article  CAS  PubMed  Google Scholar 

  • Van Mullem V, Wery M, De Bolle X, Vandenhaute J (2003) Construction of a set of Saccharomyces cerevisiae vectors designed for recombinational cloning. Yeast 20:739–746

    Article  PubMed  Google Scholar 

  • White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92:487–511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Barkla BJ, Marshall J, Pittman JK, Hirschi KD (2008) The Arabidopsis cax3 mutants display altered salt tolerance, pH sensitivity and reduced plasma membrane H+-ATPase activity. Planta 227:659–669

    Article  CAS  PubMed  Google Scholar 

  • Zhao J, Connorton JM, Guo Y, Li X, Shigaki T, Hirschi KD, Pittman JK (2009a) Functional studies of split Arabidopsis Ca2+/H+ exchangers. J Biol Chem 284:34075–34083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Shigaki T, Mei H, Guo Y, Cheng N-H, Hirschi KD (2009b) Interaction between Arabidopsis Ca2+/H+ exchangers CAX1 and CAX3. J Biol Chem 284:4605–4615

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank Professor Kyle W. Cunningham (Department of Biology, Johns Hopkins University, USA) for providing the yeast strain K667. The authors also acknowledge Professor Manuela Côrte-Real and Dr. Nuria Genicio Bouza (Department of Biology, University of Minho, Portugal) for technical support in flow cytometry and critical analysis of the results. This work is supported by European investment funds by FEDER/COMPETE/POCI-Operacional Competitiveness and Internationalization Programme, under the Projects INTERACT-NORTE-01-0145-FEDER-000017-Linha VitalityWine-ON 0013 and POCI-01-0145-FEDER-006958, and by National Funds by FCT–Portuguese Foundation for Science and Technology, under the project UID/AGR/04033/2013, and CherryCrackLess (PTDC/AGR-PRO/7028/2014). VM was supported by a FCT postdoctoral Grant (SFRH/BPD/107905/2015).

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    1. Centro de Investigação e de Tecnologias Agro-ambientais e Biológicas, CITAB-UMinho Pole, Departamento de Biologia, Escola de Ciências, Universidade do Minho, Braga, Portugal

      Viviana Martins, Filipa Carneiro & Hernâni Gerós

    2. i3S-Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, Portugal

      Carlos Conde

    3. IBMC, Instituto de Biologia Molecular e Celular, Universidade do Porto, Porto, Portugal

      Carlos Conde

    4. CIBIO-InBIO, Universidade do Porto, Campus de Vairão, Rua Padre Armando Quintas, Vairão, Portugal

      Mariana Sottomayor

    5. Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Porto, Portugal

      Mariana Sottomayor

    6. Centro de Biologia Molecular e Ambiental (CBMA), Departamento de Biologia, Escola de Ciências, Universidade do Minho, Braga, Portugal

      Hernâni Gerós

    7. Centro de Engenharia Biológica (CEB), Universidade do Minho, Braga, Portugal

      Hernâni Gerós

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    1. Viviana Martins
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    Correspondence to Viviana Martins.

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    Viviana Martins and Filipa Carneiro contributed equally to this work.

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    Martins, V., Carneiro, F., Conde, C. et al. The grapevine VvCAX3 is a cation/H+ exchanger involved in vacuolar Ca2+ homeostasis. Planta 246, 1083–1096 (2017). https://doi.org/10.1007/s00425-017-2754-0

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