Is vegetative area, photosynthesis, or grape C uploading involved in the climate change-related grape sugar/anthocyanin decoupling in Tempranillo?

Abstract

Foreseen climate change is expected to impact on grape composition, both sugar and pigment content. We tested the hypothesis that interactions between main factors associated with climate change (elevated CO2, elevated temperature, and water deficit) decouple sugars and anthocyanins, and explored the possible involvement of vegetative area, photosynthesis, and grape C uploading on the decoupling. Tempranillo grapevine fruit-bearing cuttings were exposed to CO2 (700 vs. 400 ppm), temperature (ambient vs. + 4 °C), and irrigation levels (partial vs. full) in temperature-gradient greenhouses. In a search for mechanistic insights into the underlying processes, experiments 1 and 2 were designed to maximize photosynthesis and enlarge leaf area range among treatments, whereas plant growth was manipulated in order to deliberately down-regulate photosynthesis and control vegetative area in experiments 3 and 4. Towards this aim, treatments were applied either from fruit set to maturity with free vegetation and fully irrigated or at 5–8% of pot capacity (experiments 1 and 2), or from veraison to maturity with controlled vegetation and fully irrigated or at 40% of pot capacity (experiments 3 and 4). Modification of air 13C isotopic composition under elevated CO2 enabled the further characterization of whole C fixation period and C partitioning to grapes. Increases of the grape sugars-to-anthocyanins ratio were highly and positively correlated with photosynthesis and grape 13C labeling, but not with vegetative area. Evidence is presented for photosynthesis, from fruit set to veraison, and grape C uploading, from veraison to maturity, as key processes involved in the establishment and development, respectively, of the grape sugars to anthocyanins decoupling.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Abbreviations

AN :

Net photosynthesis

PI:

Partially irrigated

PPFD:

Photosynthetic photon flux density

Tamb :

Ambient temperature

TGG:

Temperature-gradient greenhouse

TOM:

Total organic matter

TSS:

Total soluble solids

T+4 :

Elevated temperature

WI:

Well irrigated

WSC:

Water-soluble compounds

δ13C:

C isotopic composition

References

  1. Aranjuelo I, Pardo A, Biel C, Savé R, Azcón-Bieto J, Nogués S (2009) Leaf carbon management in slow-growing plants exposed to elevated CO2. Glob Change Biol 15:97–109

    Article  Google Scholar 

  2. Aranjuelo I, Cabrera-Bosquet L, Morcuende R, Avice JC, Nogués S, Araus JL, Martínez-Carrasco R, Pérez P (2011) Does ear C sink strength contribute to overcoming photosynthetic acclimation of wheat plants exposed to elevated CO2? J Exp Bot 62:3957–3969

    CAS  Article  Google Scholar 

  3. Arrizabalaga M, Morales F, Oyarzun M, Delrot S, Gomès E, Irigoyen JJ, Hilbert G, Pascual I (2018) Tempranillo clones differ in the response of berry sugar and anthocyanin accumulation to elevated temperature. Plant Sci 267:74–83

    CAS  Article  Google Scholar 

  4. Barnuud NN, Zerihun A, Gibberd M, Bates B (2014) Berry composition and climate: responses and empirical models. Int J Biometeorol 58:1207–1223

    Article  Google Scholar 

  5. Bock A, Sparks T, Estrella N, Menzel A (2013) Climate-induced changes in grapevine yield and must sugar content in Franconia (Germany) between 1805 and 2010. PLoS ONE 8:e69015

    CAS  Article  Google Scholar 

  6. Bonada M, Jeffery DW, Petrie PR, Moran MA, Sadras VO (2015) Impact of elevated temperature and water deficit on the chemical and sensory profiles of Barossa Shiraz grapes and wines. Aust J Grape Wine Res 21:240–253

    CAS  Article  Google Scholar 

  7. Caccavello G, Giaccone M, Scognamiglio P, Forlani M, Basile B (2017) Influence of intensity of post-veraison defoliation or shoot trimming on vine physiology, yield components, berry and wine composition in Aglianico grapevines. Aust J Grape Wine Res 23:226–239

    CAS  Article  Google Scholar 

  8. Carbonell-Bejerano P, Santa María E, Torres-Pérez R, Royo C, Lijavetzky D, Bravo G, Aguirreolea J, Sánchez-Díaz M, Antolín MC, Martínez-Zapater JM (2013) Thermotolerance responses in ripening berries of Vitis vinifera L. cv Muscat Hamburg. Plant Cell Physiol 54:1200–1216

    CAS  Article  Google Scholar 

  9. Cook BI, Wolkovich EM (2016) Climate change decouples drought from early winegrape harvests in France. Nature Clim Change 6:715–719

    Article  Google Scholar 

  10. Coombe BG, Iland PG (2005) Grape berry development and winegrape quality. In: Dry PR, Coombe BG (eds) Viticulture. Volume 1—resources. Winetitles, Adelaide, pp 210–248

    Google Scholar 

  11. Coombe BG, McCarthy MG (2000) Dynamics of grape berry growth and physiology of ripening. Aust J Grape Wine Res 6:131–135

    Article  Google Scholar 

  12. Curtis PS, Wang X (1998) A meta-analysis of elevated CO2 on woody plant mass, form and physiology. Oecologia 113:299–313

    Article  Google Scholar 

  13. Drake BG, González-Meler MA, Long SP (1997) More efficient plants: a consequence of rising atmospheric CO2. Annu Rev Plant Physiol Plant Mol Biol 48:609–639

    CAS  Article  Google Scholar 

  14. Drenjancevic M, Jukic V, Zmaic K, Kujundzic T, Rastija V (2017) Effects of early leaf removal on grape yield, chemical characteristics, and antioxidant activity of grape variety Cabernet Sauvignon and wine from eastern Croatia. Acta Agric Scand Sect B Soil Plant Sci 67:705–711

    CAS  Google Scholar 

  15. Duchêne E, Schneider C (2005) Grapevine and climatic changes: a glance at the situation in Alsace. Agron Sustain Dev 25:93–99

    Article  Google Scholar 

  16. Easterling DR, Horton B, Jones PD, Peterson TC, Karl TR, Parker DE, Salinger MJ, Razuvayev V, Plummer N, Jamason P, Folland CK (1997) Maximum and minimum temperatures for the globe. Science 277:364–366

    CAS  Article  Google Scholar 

  17. Etienne A, Génard M, Lobit P, Mbeguié-A-Mbéguié D, Bugaud C (2013) What controls fleshy fruit acidity? A review of malate and citrate accumulation in fruit cells. J Exp Bot 64:1451–1469

    CAS  Article  Google Scholar 

  18. Famiani F, Farinelli D, Palliotti A, Moscatello S, Battistelli A, Walker RP (2014) Is stored malate the quantitatively most important substrate utilised by respiration and ethanolic fermentation in grape berry pericarp during ripening? Plant Physiol Biochem 76:52–57

    CAS  Article  Google Scholar 

  19. Filippetti I, Movahed N, Allegro G, Valentini G, Pastore C, Colucci E, Intrieri C (2015) Effect of post-veraison source limitation on the accumulation of sugar, anthocyanins and seed tannins in Vitis vinifera cv. Sangiovese berries. Aust J Grape Wine Res 21:90–100

    CAS  Article  Google Scholar 

  20. Frioni T, Tombesi S, Silvestroni O, Lanari V, Bellincontro A, Sabbatini P, Gatti M, Poni S, Palliotti A (2016) Post-budburst spur-pruning reduces yield and delays fruit sugar accumulation in cv. Sangiovese in central Italy. Am J Enol Vitic 67:419–425

    CAS  Article  Google Scholar 

  21. García J, Zheng W, Balda P, Martínez de Toda F (2017) Varietal differences in the sugar content of red grapes at the onset of anthocyanin synthesis. Vitis 56:15–18

    Google Scholar 

  22. Giorgi F, Lionello P (2008) Climate change projections for the Mediterranean region. Glob Planet Change 63:90–104

    Article  Google Scholar 

  23. Godden PW, Gishen M (2005) Trends in the composition of Australian wine 1984–2004. Aust N Z Wine Ind J 20:21–46

    Google Scholar 

  24. Hannah L, Roehrdanz PR, Ikegami M, Shepard AV, Shaw MR, Tabor G, Zhi L, Marquet PA, Hijmans RJ (2013) Climate change, wine, and conservation. Proc Nat Acad Sci USA 110:6907–6912

    CAS  Article  Google Scholar 

  25. Hayes MA, Davies C, Dry IB (2007) Isolation, functional characterization, and expression analysis of grapevine (Vitis vinifera L.) hexose transporters: differential roles in sink and source tissues. J Exp Bot 58:1985–1997

    CAS  Article  Google Scholar 

  26. Herrera JC, Bucchetti B, Sabbatini P, Comuzzo P, Zulini L, Vecchione A, Peterlunger E, Castellarin SD (2015) Effect of water deficit and severe shoot trimming on the composition of Vitis vinifera L. Merlot grapes and wines. Aust J Grape Wine Res 21:254–265

    CAS  Article  Google Scholar 

  27. Iland P, Gago P (2002) Australia wines. Styles and tastes. Patrick Iland Wine Promotions, Campbelltown

    Google Scholar 

  28. IPCC (2014) Intergovernmental panel on climate change. Summary for policymakers. In: Edenhofer O, Pichs-Madruga R, Sokona Y, Farahani E, Kadner S, Seyboth K, Adler A, Baum I, Brunner S, Eickemeier P, Kriemann B, Savolainen J, Schlömer S, von Stechow C, Zwickel T, Minx JC (eds) Climate change, mitigation of climate change. contribution of working group III to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge

    Google Scholar 

  29. Irigoyen JJ, Goicoechea N, Antolín MC, Pascual I, Sánchez-Díaz M, Aguirreolea J, Morales F (2014) Growth, photosynthetic acclimation and yield quality in legumes under climate change simulations: an updated survey. Plant Sci 226:22–29

    CAS  Article  Google Scholar 

  30. Jackson DI, Lombard PB (1993) Environmental and management practices affecting grape composition and wine quality—a review. Am J Enol Vitic 44:409–430

    CAS  Google Scholar 

  31. Jones GV, Davis RE (2000) Climate influences on grapevine phenology, grape composition, and wine production and quality for Bordeaux, France. Am J Enol Vitic 51:249–261

    Google Scholar 

  32. Jones GV, Duchêne E, Tomasi D, Yuste J, Braslavska O, Schultz HR, Martínez C, Boso S, Langellier F, Perruchot C, Guimberteau G (2005) Changes in European winegrape phenology and relationships with climate. In: Proceedings of the XIV GESCO Symposium, Vol. 1, Geisenheim, Germany, pp 55–61

  33. Keller M, Mills LJ, Wample RL, Spayd SE (2005) Cluster thinning effects on three deficit-irrigated Vitis vinifera cultivars. Am J Enol Vitic 56:91–103

    Google Scholar 

  34. Kizildeniz T, Mekni I, Santesteban H, Pascual I, Morales F, Irigoyen JJ (2015) Effects of climate change including elevated CO2 concentration, temperature and water deficit on growth, water status, and yield quality of grapevine (Vitis vinifera L.) cultivars. Agric Water Manag 159:155–164

    Article  Google Scholar 

  35. Kizildeniz T, Irigoyen JJ, Pascual I, Morales F (2018a) Simulating the impact of climate change (elevated CO2 and temperature, and water deficit) on the growth of red and white Tempranillo grapevine in three consecutive growing seasons (2013–2015). Agric Water Manag 202:220–230

    Article  Google Scholar 

  36. Kizildeniz T, Pascual I, Irigoyen JJ, Morales F (2018b) Using fruit-bearing cuttings of grapevine and temperature gradient greenhouses to evaluate effects of climate change (elevated CO2 and temperature, and water deficit) on the cv. red and white Tempranillo. Yield and must quality in three consecutive growing seasons (2013–2015). Agric Water Manag 202:299–310

    Article  Google Scholar 

  37. Kliewer WM, Dokoozlian NK (2005) Leaf areal crop weight ratios of grapevines: Influence on fruit composition and wine quality. Am J Enol Vitic 56:170–181

    Google Scholar 

  38. Koufos G, Mavromatis T, Koundouras S, Fyllas NM, Jones GV (2014) Viticulture-climate relationships in Greece: the impacts of recent climate trends on harvest date variation. Int J Climatol 34:1445–1459

    Article  Google Scholar 

  39. Lakso AN, Kliewer WM (1975) The influence of temperature on malic acid metabolism in grape berries. Plant Physiol 56:370–372

    CAS  Article  Google Scholar 

  40. Long SP (1991) Modification of the response of photosynthetic productivity to rising temperature by atmospheric CO2 concentrations: Has its importance been underestimated? Plant Cell Environ 14:729–739

    CAS  Article  Google Scholar 

  41. Lopez-Bustins J-A, Pla E, Nadal M, de Herralde F, Savé R (2014) Global change and viticulture in the Mediterranean region: a case of study in north-eastern Spain. Span J Agric Res 12:78–88

    Article  Google Scholar 

  42. Martínez de Toda F, Sancha JC, Balda P (2013) Reducing the sugar and pH of the grape (Vitis vinifera L. cvs. Grenache and Tempranillo) through a single shoot trimming. S Afr J Enol Vitic 34:246–251

    Google Scholar 

  43. Martínez-Lüscher J, Sánchez-Díaz M, Delrot S, Aguirreolea J, Pascual I, Gomès E (2014) Ultraviolet-B radiation and water deficit interact to alter flavonol and anthocyanin profiles in grapevine berries through transcriptomic regulation. Plant Cell Physiol 55:1925–1936

    Article  Google Scholar 

  44. Martínez-Lüscher J, Morales F, Sánchez-Díaz M, Delrot S, Aguirreolea J, Gomès E, Pascual I (2015) Climate change conditions (elevated CO2 and temperature) and UV-B radiation affect grapevine (Vitis vinifera cv. Tempranillo) leaf carbon assimilation, altering fruit ripening rates. Plant Sci 236:168–176

    Article  Google Scholar 

  45. Martínez-Lüscher J, Kizildeniz T, Vučetić V, Dai Z, Luedeling E, van Leeuwen C, Gomès E, Pascual I, Irigoyen JJ, Morales F, Delrot S (2016a) Sensitivity of grapevine phenology to water availability, temperature and CO2 concentration. Front Environ Sci 4:48

    Article  Google Scholar 

  46. Martínez-Lüscher J, Sánchez-Díaz M, Delrot S, Aguirreolea J, Pascual I, Gomès E (2016b) Ultraviolet-B alleviates the uncoupling effect of elevated CO2 and increased temperature on grape berry (Vitis vinifera cv. Tempranillo) anthocyanin and sugar accumulation. Aust J Grape Wine Res 22:87–95

    Article  Google Scholar 

  47. Maurer C, Hammerl C, Koch E, Hammerl T, Pokorny E (2011) Extreme grape harvest data of Austria, Switzerland and France from A.D. 1523 to 2007 compared to corresponding instrumental/reconstructed temperature data and various documentary sources. Theor Appl Climatol 106:55–68

    Article  Google Scholar 

  48. Medrano H, Escalona JM, Cifre J, Bota J, Flexas J (2003) A ten-year study on the physiology of two Spanish grapevine cultivars under field conditions: effects of water availability from leaf photosynthesis to grape yield and quality. Funct Plant Biol 30:607–619

    CAS  Article  Google Scholar 

  49. Molero G, Aranjuelo I, Teixidor P, Araus JL, Nogués S (2011) Measurement of 13C and 15N isotope labeling by gas chromatography/combustion/isotope ratio mass spectrometry to study amino acid fluxes in a plant-microbe symbiotic association. Rapid Commun Mass Sp 25:599–607

    CAS  Article  Google Scholar 

  50. Morales F, Pascual I, Sánchez-Díaz M, Aguirreolea J, Irigoyen JJ, Goicoechea N, Antolín MC, Oyarzun M, Urdiain A (2014) Methodological advances: using greenhouses to simulate climate change scenarios. Plant Sci 226:30–40

    CAS  Article  Google Scholar 

  51. Morales F, Antolín MC, Aranjuelo I, Goicoechea N, Pascual I (2016) From vineyards to controlled environments in grapevine research: investigating responses to climate change scenarios using fruit-bearing cuttings. Theor Exp Plant Physiol 28:171–191

    Article  Google Scholar 

  52. Moran MA, Sadras VO, Petrie PR (2017) Late pruning and carry-over effects on phenology, yield components and berry traits in Shiraz. Aust J Grape Wine Res 23:390–398

    CAS  Article  Google Scholar 

  53. Mori K, Goto-Yamamoto N, Kitayama M, Hashizume K (2007) Loss of anthocyanins in red-wine grape under high temperature. J Exp Bot 58:1935–1945

    CAS  Article  Google Scholar 

  54. NOAA-ESRL (2014) National Oceanic and Atmospheric Administration (NOAA)- Earth System Research Laboratory (ESRL), USA. Monthly CO2 concentration data set. http://co2now.org/Current-CO2/CO2-Now/noaa-mauna-loa-co2-data.html

  55. Nogués S, Tcherkez G, Cornic G, Ghashghaie J (2004) Respiratory carbon metabolism following illumination in intact french bean leaves using C-13/C-12 isotope labeling. Plant Physiol 136:3245–3254

    Article  Google Scholar 

  56. Ollat N, Gaudillêre J (2000) Carbon balance in developing grapevine berries. Acta Hortic 526:345–350

    Article  Google Scholar 

  57. Pastenes C, Villalobos L, Ríos N, Reyes F, Turgeon R, Franck N (2014) Carbon partitioning to berries in water stressed grapevines: the role of active transport in leaves and fruits. Environ Exp Bot 107:154–166

    CAS  Article  Google Scholar 

  58. Petrie PR, Sadras VO (2008) Advancement of grapevine maturity in Australia between 1993 and 2006: putative causes, magnitude of trends and viticultural consequences. Aust J Grape Wine Res 14:33–45

    Article  Google Scholar 

  59. Petrie PR, Brooke SJ, Moran MA, Sadras VO (2017) Pruning after budburst to delay and spread grape maturity. Aust J Grape Wine Res 23:378–389

    Article  Google Scholar 

  60. Ribéreau-Gayon J, Stonestreet E (1965) Le dosage des anthocyanes dans le vin rouge. Bulletin de la Societé de Chimie 9:2649–2652

    Google Scholar 

  61. Rienth M, Torregrosa L, Sarah G, Ardisson M, Brillouet J-M, Romieu C (2016) Temperature desynchronizes sugar and organic acid metabolism in ripening grapevine fruits and remodels their transcriptome. BMC Plant Biol 16:1–23

    Article  Google Scholar 

  62. Roby G, Harbertson JF, Adams DA, Matthews MA (2004) Berry size and vine water deficits as factors in winegrape composition: anthocyanins and tannins. Aust J Grape Wine Res 10:100–107

    CAS  Article  Google Scholar 

  63. Sadras VO, Moran MA (2012) Elevated temperature decouples anthocyanins and sugars in berries of Shiraz and Cabernet Franc. Aust J Grape Wine Res 18:115–122

    CAS  Article  Google Scholar 

  64. Sadras VO, Stevens R, Pech J, Taylor E, Nicholas P, McCarthy M (2007) Quantifying phenotypic plasticity of berry traits using an allometric-type approach: a case study on anthocyanins and sugars in berries of Cabernet Sauvignon. Aust J Grape Wine Res 13:72–80

    CAS  Article  Google Scholar 

  65. Sadras VO, Moran MA, Bonada M (2013) Effects of elevated temperature in grapevine. I Berry sensory traits. Aust J Grape Wine Res 19:95–106

    Article  Google Scholar 

  66. Salazar-Parra C, Aguirreolea J, Sánchez-Díaz M, Irigoyen JJ, Morales F (2010) Effects of climate change scenarios on Tempranillo grapevine (Vitis vinifera L.) ripening: response to a combination of elevated CO2 and temperature, and moderate drought. Plant Soil 337:179–191

    CAS  Article  Google Scholar 

  67. Salazar-Parra C, Aguirreolea J, Sánchez-Díaz M, Irigoyen JJ, Morales F (2012) Photosynthetic response of Tempranillo grapevine to climate change scenarios. Ann Appl Biol 161:277–292

    CAS  Article  Google Scholar 

  68. Salazar-Parra C, Aranjuelo I, Pascual I, Erice G, Sanz-Sáez A, Aguirreolea J, Sánchez-Díaz M, Irigoyen JJ, Araus JL, Morales F (2015) Carbon balance, partitioning and photosynthetic acclimation in fruit-bearing grapevine (Vitis vinifera L. cv. Tempranillo) grown under simulated climate change (elevated CO2, elevated temperature and moderate drought) scenarios in temperature gradient greenhouses. J Plant Physiol 174:97–109

    CAS  Article  Google Scholar 

  69. Shellie K (2015) Foliar reflective film and water deficit increase anthocyanin to soluble solids ratio during berry ripening in Merlot. Am J Enol Vitic 66:348–356

    CAS  Article  Google Scholar 

  70. Spayd S, Tarara J, Mee D, Ferguson J (2002) Separation of sunlight and temperature effects on the composition of Vitis vinifera cv. Merlot berries. Am J Enol Vitic 53:171–182

    CAS  Google Scholar 

  71. Sweetman C, Sadras VO, Hancock RD, Soole KL, Ford CM (2014) Metabolic effects of elevated temperature on organic acid degradation in ripening Vitis vinifera fruit. J Exp Bot 65:5975–5988

    CAS  Article  Google Scholar 

  72. Tardáguila J, Diago MP, Martínez de Toda F, Poni S, Vilanova M (2008) Effects of timing of leaf removal on yield, berry maturity, wine composition, and sensory properties of Grenache wines grown in dry farmed conditions. J Int Sci Vigne Vin 42:221–229

    Google Scholar 

  73. Tomasi D, Jones GV, Giust M, Lovat L, Gaiotti F (2011) Grapevine phenology and climate change: relationships and trends in the Veneto region of Italy for 1964–2009. Am J Enol Vitic 62:329–339

    Article  Google Scholar 

  74. Torregrosa L, Bigard A, Doligez A, Lecourieux D, Rienth M, Luchaire N, Pieri P, Chatbanyong R, Shahood R, Farnos M, Roux C, Adiveze A, Pillet J, Sire Y, Zumstein E, Veyret M, Le Cunff L, Lecourieux F, Saurin N, Muller B, Ojeda H, Houel C, Péros J-P, This P, Pellegrino A, Romieu C (2017) Developmental, molecular and genetic studies on grapevine response to temperature open breeding strategies for adaptation to warming. OENO One 51:155–165

    Article  Google Scholar 

  75. Torres N, Goicoechea N, Morales F, Antolín MC (2016) Berry quality and antioxidant properties in Vitis vinifera cv. Tempranillo as affected by clonal variability, mycorrhizal inoculation and temperature. Crop Pasture Sci 67:961–977

    CAS  Article  Google Scholar 

  76. Xu Z, Shimizu H, Yagasaki Y, Ito S, Zheng Y, Zhou G (2013) Interactive effects of elevated CO2, drought, and warming on plants. J Plant Growth Regul 32:692–707

    CAS  Article  Google Scholar 

  77. Yamane T, Jeong ST, Goto-Yamamoto N, Koshita Y, Kobayashi S (2006) Effects of temperature on anthocyanin biosynthesis in grape berry skins. Am J Enol Vitic 57:54–59

    CAS  Google Scholar 

  78. Zhang XY, Wang XL, Wang XF, Xia GH, Pan QH, Fan RC, Wu FQ, Yu XC, Zhang DP (2006) A shift of phloem unloading from symplasmic to apoplasmic pathway is involved in developmental onset of ripening in grape berry. Plant Physiol 142:220–232

    CAS  Article  Google Scholar 

  79. Zhang PZ, Wu XW, Needs S, Liu D, Fuentes S, Howell K (2017) The influence of apical and basal defoliation on the canopy structure and biochemical composition of Vitis vinifera cv. Shiraz grapes and wine. Front Chem 5:48

    Article  Google Scholar 

  80. Zheng W, del Galdo V, García J, Balda P, Martínez de Toda F (2017) Use of minimal pruning to delay fruit maturity and improve berry composition under climate change. Am J Enol Vitic 68:136–140

    Article  Google Scholar 

Download references

Acknowledgements

Science and Innovation (BFU2008-01405/BFI), Economy and Competitiveness (AGL2014-56075-C2-1-R) Spanish Ministries, Aragón Government (A03 group) and the Basque Government (IT-932-16) for financial support, Navarra University “Asociación de Amigos” for Carolina Salazar-Parra grant, A. Urdiain, M. Oyarzun for excellent technical assistance, and EVENA for dormant cuttings supply.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Fermín Morales.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Salazar-Parra, C., Aranjuelo, I., Pascual, I. et al. Is vegetative area, photosynthesis, or grape C uploading involved in the climate change-related grape sugar/anthocyanin decoupling in Tempranillo?. Photosynth Res 138, 115–128 (2018). https://doi.org/10.1007/s11120-018-0552-6

Download citation

Keywords

  • Climate change
  • Grapevine
  • Harvest date
  • Leaf area
  • Photosynthesis
  • Sugars/anthocyanins decoupling