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Identification and functional characterization of grapevine transporters that mediate glucose-6-phosphate uptake into plastids

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Abstract

Main conclusion

Two grapevine glucose-6-Pi plastidial transporters differently expressed in plant organs and in response to environmental and hormonal signals are characterized. They are involved in starch accumulation in berries and canes.

In grapevine, starch accumulation in the trunk is important for winter storage of carbon and in the flower for reproductive development. Berries also accumulate starch in their plastids, which are also involved in the synthesis of aroma compounds important for fruit quality. The present work characterizes two glucose-phosphate translocators (VvGPT1, VvGPT2) that control the accumulation of starch in grape amyloplasts. Three different splicing variants identified for VvGPT2 (VvGPT2α, VvGPT2β and VvGPT2Ω) were more expressed in the leaves than in other organs. In contrast, VvGPT1 transcripts were more abundant in mature berries, canes and flowers than in the leaves. Expression of 35S-VvGPT1-GFP and 35S-VvGPT2Ω-GFP in tobacco leaf epidermal cells showed that the fusion proteins localized at the plastidial envelope. Complementation of the Arabidopsis pgi1-1 mutant impaired in leaf starch synthesis restored its ability to synthesize starch, demonstrating that VvGPT1 and VvGPT2Ω mediate the transport of glucose-6-Pi across the plastidial envelope. In grape cell suspensions, ABA, light and galactinol, together with sucrose and fructose, significantly increased the transcript abundance of VvGPT1, whereas VvGPT2Ω expression was affected only by sucrose. In addition, elicitation with methyl jasmonate strongly upregulated VvGPT1, VvGPT2Ω and VvPAL1, suggesting a role for GPTs in the production of secondary compounds in grapevine. Moreover, in grapevines cultivated in field conditions, VvGPT1 expression was higher in berries more exposed to the sun and subjected to higher temperatures. Although both VvGPT1 and VvGPT2 mediate the same function at the molecular level, they exhibit different expression levels and regulation in plant organs and in response to environmental and hormonal signals.

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Abbreviations

E (W):

East (West) exposed grape clusters

GFP:

Green fluorescent protein

GPT:

Glucose-6-phosphate/phosphate translocator

MeJA:

Methyl jasmonate

pPT:

Plastidial phosphate translocators

RDI:

Regulated deficit irrigation

SDI:

Sustained deficit irrigation

TPT:

Triose-phosphate/phosphate translocator

References

  • Athanasiou K, Dyson BC, Webster RE, Johnson GN (2010) Dynamic acclimation of photosynthesis increases plant fitness in changing environments. Plant Physiol 152:366–373

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Carbonell-Bejerano P, Diago MP, Matínez-Abaigar J, Martínez-Zapater JM, Tardáguila J, Núñez-Olivera E (2014) Solar ultraviolet radiation is necessary to enhance grapevine fruit ripening transcriptional and phenolic responses. BMC Plant Biol. doi:10.1186/1471-2229-14-183

    Google Scholar 

  • Castillo MC, León J (2008) Expression of the β-oxidation gene 3-ketoacyl-CoA thiolase 2 (KAT2) is required for the timely onset of natural and dark-induced leaf senescence in Arabidopsis. J Exp Bot 59:2171–2179

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Centeno DC, Osorio S, Nunes-Nesi A, Bertolo ALF, Carneiro RT, Araújo WL, Steinhauser MC, Michalska J, Rohrmann J, Geigenberger P, Oliver SN, Stitt M, Carrari C, Rose JKC, Fernie AR (2011) Malate plays a crucial role in starch metabolism, ripening, and soluble solid content of tomato fruit and affects postharvest softening. Plant Cell 23:162–184

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chaves MM, Zarrouk O, Francisco R, Costa JM, Santos T, Regalado AP, Rodrigues ML, Lopes CM (2010) Grapevine under deficit irrigation: hints from physiological and molecular data. Ann Bot 105:661–676

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Chong J, Piron MC, Meyer S, Merdinoglu D, Bertsch C, Mestre P (2014) The SWEET family of sugar transporters in grapevine: VvSWEET4 is involved in the interaction with Botrytis cinerea. J Exp Bot. doi:10.1093/jxb/eru375

    PubMed Central  Google Scholar 

  • Conde C, Agasse A, Glissant D, Tavares R, Gerós H, Delrot S (2006) Pathways of glucose regulation of monosaccharide transport in grape cells. Plant Physiol 141:1563–1577

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • D’Onofrio C, Cox A, Davies C, Boss PK (2009) Induction of secondary metabolism in grape cell cultures by jasmonates. Funct Plant Biol 36:323–338

    Article  Google Scholar 

  • Dyson BC, Webster RE, Johnson GN (2014) GPT2: a glucose 6-phosphate/phosphate translocator with a novel role in the regulation of sugar signalling during seedling development. Ann Bot 113:643–652

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Entwistle G, ap Rees T (1990) Lack of fructose-1,6-bisphosphatase in a range of higher plants that store starch. Biochem J 271:467–472

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Felsenstein J (1986) PHYLIP – Phylogeny Inference Package (Version 3.2). Cladistics 5:164–166

  • Fischer K (2011) The import and export business in plastids: transport processes across the inner envelope membrane. Plant Physiol 155:1511–1519

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Flügge UI (1999) Phosphate translocators in plastids. Annu Rev Plant Physiol Plant Mol Biol 50:27–45

    Article  PubMed  Google Scholar 

  • Fortes AM, Agudelo-Romero P, Silva MS, Ali K, Sousa L, Maltese F, Choi YH, Grimplet J, Martinez-Zapater JM, Verpoorte R, Pais MS (2011) Transcript and metabolite analysis in Trincadeira cultivar reveals novel information regarding the dynamics of grape ripening. BMC Plant Biol. doi:10.1186/1471-2229-11-149

    PubMed Central  PubMed  Google Scholar 

  • Gigolashvili T, Yatusevich R, Rollwitz I, Humphry M, Gershenzon J, Flügge UI (2009) The plastidic bile acid transporter 5 is required for the biosynthesis of methionine-derived glucosinolates in Arabidopsis thaliana. Plant Cell 21:1813–1829

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gigolashvili T, Geier M, Ashykhmina N, Frerigmann H, Wulfert S, Krueger S, Mugford SG, Kopriva S, Haferkamp I, Flügge UI (2012) The Arabidopsis thylakoid ADP/ATP carrier TAAC has an additional role in supplying plastidic phosphoadenosine 5′-phosphate to the cytosol. Plant Cell 24:4187–4204

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hampel D, Mosandl A, Wüst M (2005) Induction of de novo volatile terpene biosynthesis via cytosolic and plastidial pathways by methyl jasmonate in foliage of Vitis vinifera L. J Agr Food Chem 53:2652–2657

    Article  CAS  Google Scholar 

  • Hedrich R, Raschke K, Stitt M (1985) A role for fructose-2,6-bisphosphate in regulating carbohydrate metabolism in guard cells. Plant Physiol 79:977–982

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jaillon O, Aury JM, Noel B et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

    Article  CAS  PubMed  Google Scholar 

  • Kammerer B, Fischer K, Hilpert B, Schubert S, Gutensohn M, Weber APM, Flügge UI (1998) Molecular characterization of a carbon transporter in plastids from heterotrophic tissues: the glucose 6-phosphate/phosphate antiporter. Plant Cell 10:105–117

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Knappe S, Flügge UI, Fischer K (2003) Analysis of the plastidic phosphate translocator gene family in Arabidopsis and identification of new phosphate translocator-homologous transporters, classified by their putative substrate-binding site. Plant Physiol 131:1178–1190

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Krisa S, Larronde F, Budzinski H, Decendit A, Deffieux G, Mérillon JM (1999) Stilbene production by Vitis vinifera cell suspension cultures, methyl jasmonate induction and 13C biolabeling. J Nat Prod 62:1688–1690

    Article  CAS  Google Scholar 

  • Larronde F, Krisa S, Decendit A, Chèze C, Deffieux G, Mérrillon JM (1998) Regulation of polyphenol production in Vitis vinifera cell suspension cultures by sugars. Plant Cell Rep 17:946–950

    Article  CAS  Google Scholar 

  • Lebon G, Duchêne E, Brun O, Clément C (2005) Phenology of flowering and starch accumulation in grape (Vitis vinifera L.) cuttings and vines. Ann Bot 95:943–948

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lecourieux F, Kappel C, Lecourieux D, Serrano A, Torres E, Arce-Johnson P, Delrot S (2014) An update on sugar transport and signaling in grapevine. J Exp Bot 65:821–832

    Article  CAS  PubMed  Google Scholar 

  • Liechti R, Farmer EE (2002) The jasmonate pathway. Science 296:1649–1650

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

  • N’tchobo H, Dali N, Nguyen-Quoc B, Foyer CH, Yelle S (1999) Starch synthesis in tomato remains constant throughout fruit development and is dependent on sucrose supply and sucrose synthase activity. J Exp Bot 50:1457–1463

    Article  Google Scholar 

  • Nguyen-Quoc B, Foyer CH (2001) A role for “futile cycles” involving invertase and sucrose synthase in sucrose metabolism in tomato fruit. J Exp Bot 52:881–889

    Article  CAS  PubMed  Google Scholar 

  • Nicholas KB, Nicholas HB, Deerfield DW (1997) Genedoc: analysis and visualization of genetic variation. EMBnet News 4:14

  • Niewiadomski P, Knappe S, Geimer S, Fisher K, Schulz B, Unte US, Rosso MG, Ache P, Flügge U, Schneider A (2005) The Arabidopsis plastidic glucose 6-phosphate/phosphate translocator GPT1 is essential for pollen maturation and embryo sac development. Plant Cell 17:760–775

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Noronha H, Agasse A, Martins AP, Berny MC, Gomes D, Zarrouk O, Thiebaud P, Delrot S, Chaumont F, Gerós H (2014) The grape aquaporin VvSIP1 transports water across the ER membrane. J Exp Bot 65:981–993

    Article  CAS  PubMed  Google Scholar 

  • Overlach S, Diekmann W, Raschke K (1993) Phosphate translocator of isolated guard-cell chloroplasts from Pisum sativum L. transports glucose-6-phosphate. Plant Physiol 101:1201–1207

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pauwels L, Goossens A (2011) The JAZ proteins: a crucial interface in the jasmonate signaling cascade. Plant Cell 23:3089–3100

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pourtau N, Jennings R, Pelzer E, Pallas J, Wingler A (2006) Effect of sugar-induced senescence on gene expression and implications for the regulation of senescence in Arabidopsis. Planta 224:556–568

  • Qu J, Zhang W, Yu X (2011) A combination of elicitation and precursor feeding leads to increased anthocyanin synthesis in cell suspension cultures of Vitis vinifera. Plant Cell Tiss Org 107:261–269

    Article  CAS  Google Scholar 

  • Reddy ASN, Marquez Y, Kalyna M, Barta A (2013) Complexity of the alternative splicing landscape in plants. Plant Cell 25:3657–3683

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Righetti L, Franceschetti M, Ferri M, Tassoni A, Bagni N (2007) Resveratrol production in Vitis vinifera cell suspensions treated with several elicitors. Caryologia 60:169–171

    Article  Google Scholar 

  • Santamaria AR, Mulinacci N, Valletta A, Innocenti M, Pasqua G (2011) Effects of elicitors on the production of resveratrol and viniferins in cell cultures of Vitis vinifera L. cv. Italia. J Agric Food Chem 59:9094–9101

    Article  CAS  PubMed  Google Scholar 

  • Santamaria AR, Innocenti M, Mulinacci N, Melani F, Valletta A, Sciandra I, Pasqua G (2012) Enhancement of viniferin production in Vitis vinifera L. cv. Alphonse Lavallée cell suspensions by low-energy ultrasound alone and in combination with methyl jasmonate. J Agr Food Chem 60:11135–11142

    Article  CAS  Google Scholar 

  • Smith AM, Zeeman SC (2006) Quantification of starch in plant tissues. Nat Protoc 1:1342–1345

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Uversky VN (2014) Wrecked regulation of intrinsically disordered proteins in diseases: pathogenicity of deregulated regulators. Front Mol Biosci 1:6

  • Van Leeuwen C, Schultz HR, Garcia de Cortazar-Atauri I, Duchêne E, Ollat N, Pieri P, Bois B, Goutouly JP, Quénol H, Touzard JM, Malheiro AC, Bavaresco L, Delrot S (2013) Why climate change will not dramatically decrease viticultural suitability in main wine-producing areas by 2050. Proc Natl Acad Sci USA 110:3051–3052

    Article  Google Scholar 

  • Vitulo N, Forcato C, Carpinelli EC, Telatin A, Campagna D, D’Angelo M, Zimbello R, Corso M, Vannozzi A, Bonghi C, Lucchin M, Valle G (2014) A deep survey of alternative splicing in grape reveals changes in the splicing machinery related to tissue, stress condition and genotype. BMC Plant Biol. doi:10.1186/1471-2229-14-99

    PubMed Central  PubMed  Google Scholar 

  • Wasternack C, Hause B (2002) Jasmonates and octadecanoids, signals in plant stress responses and development. Prog Nucleic Acid Res Mol Biol 72:165–221

    Article  CAS  PubMed  Google Scholar 

  • Weber APM, Linka N (2011) Connecting the plastid: transporters of the plastid envelope and their role in linking plastidial with cytosolic metabolism. Annu Rev Plant Biol 62:53–77

    Article  CAS  PubMed  Google Scholar 

  • Yu T, Lue W, Wang S, Chen J (2000) Mutation of Arabidopsis plastid phosphoglucose isomerase affects leaf starch synthesis and floral initiation. Plant Physiol 123:319–325

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zapata C, Deléens E, Chaillou S, Magné C (2004) Partitioning and mobilization of starch and N reserves in grapevine (Vitis vinifera L.). J Plant Physiol 161:1031–1040

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We would like to thank Dr. Anja Schneider from the Ludwig-Maximilians, University of Munich for kindly providing Arabidopsis pgi1-1 seed. This work is supported by European Union Funds (FEDER/COMPETE Operational Competitiveness Programme) and Portuguese national Funds (FCT-Portuguese Foundation for Science and Technology): KBBE-2012-6-3117 “Inovinne”, FCOMP-01-0124-FEDER-022692 and PTDC/AGR-ALI/100636/2008. HN was supported by a PhD grant from FCT (SFRH/BD/74257/2010). This work also benefited from the networking activities within the European funded COST ACTION FA1106 “QualityFruit”.

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No conflicts of interest declared.

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Authors and Affiliations

  1. Centro de Investigação e de Tecnologias Agro-ambientais e Biológicas CITAB, Vila Real, Portugal

    Henrique Noronha & Hernâni Gerós

  2. Grupo de Investigação em Biologia Vegetal Aplicada e Inovação Agroalimentar AgroBioPlant, Departamento de Biologia, Escola de Ciências, Universidade do Minho, Braga, Portugal

    Henrique Noronha & Hernâni Gerós

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

    Carlos Conde

  4. I3S, Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, Portugal

    Carlos Conde

  5. INRA, ISVV, Ecophysiologie et Génomique Fonctionnelle de la Vigne, UMR 1287, Université de Bordeaux, Villenave D’Ornon, France

    Serge Delrot

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  1. Henrique Noronha
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  2. Carlos Conde
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Correspondence to Hernâni Gerós.

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Noronha, H., Conde, C., Delrot, S. et al. Identification and functional characterization of grapevine transporters that mediate glucose-6-phosphate uptake into plastids. Planta 242, 909–920 (2015). https://doi.org/10.1007/s00425-015-2329-x

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  • DOI: https://doi.org/10.1007/s00425-015-2329-x

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