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Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Berry quality and antioxidant properties in Vitis vinifera cv. Tempranillo as affected by clonal variability, mycorrhizal inoculation and temperature

Nazareth Torres A , Nieves Goicoechea A , Fermín Morales B and M. Carmen Antolín A C
+ Author Affiliations
- Author Affiliations

A Universidad de Navarra, Facultades de Ciencias y Farmacia y Nutrición, Grupo de Fisiología del Estrés en Plantas (Departamento de Biología Ambiental), Unidad Asociada al CSIC (EEAD, Zaragoza, ICVV, Logroño), c/ Irunlarrea 1, 31008, Pamplona, Spain.

B Estación Experimental de Aula Dei (EEAD), CSIC, Departamento Nutrición Vegetal, Apdo. 13034, 50080 Zaragoza, Spain.

C Corresponding author. Email: cantolin@unav.es

Crop and Pasture Science 67(9) 961-977 https://doi.org/10.1071/CP16038
Submitted: 21 September 2015  Accepted: 25 March 2016   Published: 24 August 2016

Abstract

The projected increase in mean temperatures caused by climate change is expected to have detrimental impacts on berry quality. Microorganisms as arbuscular mycorrhizal fungi (AMF) produce numerous benefits to host plants and can help plants to cope with abiotic stresses such as high temperature. The aims of this research were to characterise the response of three clones of Vitis vinifera L. cv. Tempranillo to elevated temperatures and to determine whether AMF inoculation can improve berry antioxidant properties under these conditions. The study was carried out on three fruit-bearing cuttings clones of cv. Tempranillo (CL-260, CL-1048 and CL-1089) inoculated with AMF or uninoculated and subjected to two temperature regimes (day–night: 24°C−14°C and 28°C−18°C) during berry ripening. Results showed that clonal diversity of Tempranillo resulted in different abilities to respond to elevated temperature and AMF inoculation. In CL-1048, AMF inoculation improved parameters related to phenolic maturity such as anthocyanin content and increased antioxidant activity under elevated temperature, demonstrating a protective role of AMF inoculation against warming effects on berry quality. The results therefore suggest that selection of new clones and/or the implementation of measures to promote the association of grapevines with AMF could be strategies to improve berry antioxidant properties under future warming conditions.

Additional keywords: DPPH assay, global warming, mycorrhizal efficiency index (MEI), polyphenols, technological maturity.


References

Anderson M, Smith R, Williams M, Wolpert J (2008) Evaluation of French and California Pinot Noir clones grown for the production of sparkling wine. American Journal of Enology and Viticulture 59, 188–193.

Antolín MC, Santesteban H, Ayari M, Aguirreolea J, Sánchez-Díaz M (2010) Grapevine fruiting cuttings: an experimental system to study grapevine physiology under water deficit conditions. In ‘Methodologies and results in grapevine research’. (Eds S Delrot, H Medrano Gil, E Or, L Bavaresco, S Grando) pp. 151–163. (Springer Science+Business Media: Dordrecht, The Netherlands)

Azuma A, Yakushiji H, Koshita Y, Kobayashi S (2012) Flavonoid biosynthesis-related genes in grape skin are differentially regulated by temperature and light conditions. Planta 236, 1067–1080.
Flavonoid biosynthesis-related genes in grape skin are differentially regulated by temperature and light conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVWnsLrP&md5=7b1bfb25ed44a7e7d3a74890a2541955CAS | 22569920PubMed |

Bagyaraj DJ (1994) Vesicular-arbuscular mycorrhiza: application in agriculture. In ‘Techniques for the study of mycorrhiza’. (Eds JR Norris, DJ Read, AK Varma) pp. 819–833. (Academic Press: London)

Balestrini R, Magurno F, Walker C, Lumini E, Bianciotto V (2010) Cohorts of arbuscular mycorrhizal fungi (AMF) in Vitis vinifera, a typical Mediterranean fruit crop. Environmental Microbiology Reports 2, 594–604.
Cohorts of arbuscular mycorrhizal fungi (AMF) in Vitis vinifera, a typical Mediterranean fruit crop.Crossref | GoogleScholarGoogle Scholar | 23766230PubMed |

Barnuud N, Zerihun A, Mpelasoka F, Gibberd M, Bates B (2014) Responses of grape berry anthocyanin and titratable acidity to the projected climate change across the Western Australian wine regions. International Journal of Biometeorology 58, 1279–1293.
Responses of grape berry anthocyanin and titratable acidity to the projected climate change across the Western Australian wine regions.Crossref | GoogleScholarGoogle Scholar | 24026877PubMed |

Baslam M, Esteban R, García-Plazaola JI, Goicoechea N (2013) Effectiveness of arbuscular mycorrhizal fungi (AMF) for inducing the accumulation of major carotenoids, chlorophylls and tocopherol in green and red leaf lettuces. Applied Microbiology and Biotechnology 97, 3119–3128.
Effectiveness of arbuscular mycorrhizal fungi (AMF) for inducing the accumulation of major carotenoids, chlorophylls and tocopherol in green and red leaf lettuces.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXkt1Kjtb4%3D&md5=779ec14f036eba28843af1ea95b57133CAS | 23108529PubMed |

Bettoni MM, Mogor A, Pauletti V, Goicoechea N (2014) Growth and metabolism of onion seedlings as affected by the application of humic substances, mycorrhizal inoculation and elevated CO2. Scientia Horticulturae 180, 227–235.
Growth and metabolism of onion seedlings as affected by the application of humic substances, mycorrhizal inoculation and elevated CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvVGit77E&md5=d6cf54599cc47e70aae266c60ebc739eCAS |

Bonada M, Sadras VO (2015) Review: critical appraisal of methods to investigate the effect of temperature on grapevine berry composition. Australian Journal of Grape and Wine Research 21, 1–17.
Review: critical appraisal of methods to investigate the effect of temperature on grapevine berry composition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvV2hs7Y%3D&md5=3c84ef8a3273e6c80bfa99efdd925e61CAS |

Boulton R, Singleton V, Bisson L, Kunkee R (1996) ‘Principles and practices in wine making.’ (Chapman and Hall Enology Library: New York)

Brand-Williams W, Cuvelier ME, Berset C (1995) Use of free radical method to evaluate antioxidant activity. LWT-Food Science and Technology 28, 25–30.
Use of free radical method to evaluate antioxidant activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjvV2itLw%3D&md5=2d48edcba2a5ac5477246172c1360eafCAS |

Cagnasso E, Rolle L, Caudana A, Gervi V (2008) Relationship between grape phenolic maturity and red wine phenolic composition. Italian Journal of Food Science 20, 365–380.

Carbonell-Bejerano P, Santa María E, Torres Pérez R, Royo R, 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 Physiology 54, 1200–1216.
Thermotolerance responses in ripening berries of Vitis vinifera L. cv. Muscat Hamburg.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVKqu7rE&md5=a71bb9cef028303fbcc29cb04594ea0dCAS |

Castellarin SD, Bavaresco L, Falginella L, Gonçalves MIVZ, Di Gaspero G (2012) Phenolics in grape berry and key antioxidants. In ‘The biochemistry of the grape berry’. (Eds H Gerós, MM Chaves, S Delrot) pp. 89–110. (Bentham Science Publishers: Dubai, UAE)

Cervera MT, Cabezas JA, Rodríguez-Torres I, Chávez J, Cabello F, Martínez-Zapater JM (2002) Varietal diversity within grapevine accessions of cv. Tempranillo. Vitis 41, 33–36.

Cohen SD, Tarara JM, Gambetta GA, Matthews MA, Kennedy JA (2012) Impact of diurnal temperature variation on grape berry development, proanthocyanidin accumulation, and the expression of flavonoid pathway genes. Journal of Experimental Botany 63, 2655–2665.
Impact of diurnal temperature variation on grape berry development, proanthocyanidin accumulation, and the expression of flavonoid pathway genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmvF2rsLw%3D&md5=8889f3ce5c6e078d5ad31ea28fbbd430CAS | 22268158PubMed |

Conde C, Silva P, 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.

Coombe BG (1987) Influence of temperature on composition and quality of grapes. Acta Horticulturae 206, 23–36.
Influence of temperature on composition and quality of grapes.Crossref | GoogleScholarGoogle Scholar |

Coombe BG (1995) Adoption of a system for identifying grapevine growth stages. Australian Journal of Grape and Wine Research 1, 104–110.
Adoption of a system for identifying grapevine growth stages.Crossref | GoogleScholarGoogle Scholar |

Dai ZW, Léon C, Feil R, Lunn JE, Delrot S, Gomès E (2013) Metabolic profiling reveals coordinated switches in primary carbohydrate metabolism in grape berry (Vitis vinifera L.), a non-climacteric fleshy fruit. Journal of Experimental Botany 64, 1345–1355.
Metabolic profiling reveals coordinated switches in primary carbohydrate metabolism in grape berry (Vitis vinifera L.), a non-climacteric fleshy fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXktFKqsLk%3D&md5=528ec9f931260b3abd303eaeda28f177CAS | 23364938PubMed |

De Nisco M, Manfra M, Bolognese A, Sofo A, Scopa A, Tenore GC, Pagano F, Milite C, Russo MT (2013) Nutraceutical properties and polyphenolic profile of berry skin and wine of Vitis vinifera L. (cv. Aglianico). Food Chemistry 140, 623–629.
Nutraceutical properties and polyphenolic profile of berry skin and wine of Vitis vinifera L. (cv. Aglianico).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVamurbN&md5=e40d878ccc02e5eabff44c6acddf3f8eCAS | 23692745PubMed |

Duchêne E, Schneider C (2005) Grapevine and climatic changes: a glance at the situation in Alsace. Agronomy for Sustainable Development 25, 93–99.
Grapevine and climatic changes: a glance at the situation in Alsace.Crossref | GoogleScholarGoogle Scholar |

Duchêne E, Huard F, Dumas V, Schneider C, Merdinoglu D (2010) The challenge of adapting grapevine varieties to climate change. Climate Research 41, 193–204.
The challenge of adapting grapevine varieties to climate change.Crossref | GoogleScholarGoogle Scholar |

Duque F (1971) Determinación conjunta de fósforo, potasio, calcio, hierro, manganeso, cobre y zinc en plantas. Anales de Edafología y Agrobiología 30, 207–229.

EEC (1990) European Union Commission Regulation No. 2676/90. Official Journal of the European Communities L 272, 1–92.

Eftekhari M, Alizadeh M, Ebrahimi P (2012) Evaluation of the total phenolics and quercetin content of foliage in mycorrhizal grape (Vitis vinifera L.) varieties and effect of postharvest drying on quercetin yield. Industrial Crops and Products 38, 160–165.
Evaluation of the total phenolics and quercetin content of foliage in mycorrhizal grape (Vitis vinifera L.) varieties and effect of postharvest drying on quercetin yield.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjt1Wgurc%3D&md5=c21771ef6a871ddd1240679a99918649CAS |

Fraga H, Malheiro AC, Moutinho-Pereira J, Santos JA (2013) Future scenarios for viticultural zoning in Europe: ensemble projections and uncertainties. International Journal of Biometeorology 57, 909–925.
Future scenarios for viticultural zoning in Europe: ensemble projections and uncertainties.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3s3osFaksw%3D%3D&md5=b13f520ad4a35d5c1163f0615fe7eb8bCAS | 23306774PubMed |

Georgiev V, Ananga A, Tsolova V (2014) Recent advances and uses of grape flavonoids as nutraceuticals. Nutrients 6, 391–415.
Recent advances and uses of grape flavonoids as nutraceuticals.Crossref | GoogleScholarGoogle Scholar | 24451310PubMed |

Greer DH, Weston C (2010) Heat stress affects flowering, berry growth, sugar accumulation and photosynthesis of Vitis vinifera cv. Semillon grapevines grown in a controlled environment. Functional Plant Biology 37, 206–214.
Heat stress affects flowering, berry growth, sugar accumulation and photosynthesis of Vitis vinifera cv. Semillon grapevines grown in a controlled environment.Crossref | GoogleScholarGoogle Scholar |

Grover M, Sk ZA, Sandhya V, Rasul A, Venkateswarlu B (2011) Role of microorganisms in adaptation of agriculture crops to abiotic stresses. World Journal of Microbiology & Biotechnology 27, 1231–1240.
Role of microorganisms in adaptation of agriculture crops to abiotic stresses.Crossref | GoogleScholarGoogle Scholar |

Hayman DS, Barea JM, Azcón R (1976) Vesicular-arbuscular mycorrhiza in southern Spain: its distribution in crops growing in soil of different fertility. Phytopathologia Mediterranea 15, 1–6.

IPCC (2014) Summary for policymakers. Climate change 2014. In ‘Mitigation of climate change. Contribution of Working Group III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change’. (Eds O Edenhofer et al.) (Cambridge University Press: Cambridge, UK/New York)

Jones GV, White MA, Cooper OR, Storchmann KH (2005) Climate change and global wine quality. Climatic Change 73, 319–343.
Climate change and global wine quality.Crossref | GoogleScholarGoogle Scholar |

Kallithraka S, Aliaj L, Makris DP, Kefalas P (2009) Anthocyanin profiles of major red grape (Vitis vinifera L.) varieties cultivated in Greece and their relationship with in vitro antioxidant characteristics. International Journal of Food Science & Technology 44, 2385–2393.
Anthocyanin profiles of major red grape (Vitis vinifera L.) varieties cultivated in Greece and their relationship with in vitro antioxidant characteristics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFCgtLvJ&md5=b99ca60350206bbd50b15f898f97e9bbCAS |

Karagiannidis N, Nikolaou N, Ipsilantis I, Zioziou E (2007) Effects of different N fertilizers on the activity of Glomus mosseae and on grapevine nutrition and berry composition. Mycorrhiza 18, 43–50.
Effects of different N fertilizers on the activity of Glomus mosseae and on grapevine nutrition and berry composition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlClt7vI&md5=6e3b29d5f9ad42bacc0b5b56e39ee808CAS | 17987325PubMed |

Keller M (2010) Managing grapevines to optimise fruit development in a challenging environment: a climate change primer for viticulturists. Australian Journal of Grape and Wine Research 16, 56–69.
Managing grapevines to optimise fruit development in a challenging environment: a climate change primer for viticulturists.Crossref | GoogleScholarGoogle Scholar |

Krüger M, Krüger C, Walker C, Stockinger H, Schüßler A (2012) Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level. New Phytologist 193, 970–984.
Phylogenetic reference data for systematics and phylotaxonomy of arbuscular mycorrhizal fungi from phylum to species level.Crossref | GoogleScholarGoogle Scholar | 22150759PubMed |

Kuhn N, Guan L, Dai WZ, Wu B-H, Lauvergeat V, Gomès E, Li SH, Godoy F, Arce-Johnson P, Delrot S (2014) Berry ripening: recently heard through the grapevine. Journal of Experimental Botany 65, 4543–4559.
Berry ripening: recently heard through the grapevine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xht1Wqu7rE&md5=1273f255cf1aade542aefeeca707f8a1CAS | 24285825PubMed |

Lebon G, Wojnarowiez G, Holzapfel B, Fontaine F, Vaillant-Gaveau N, Clement C (2008) Sugars and flowering in the grapevine (Vitis vinifera L.). Journal of Experimental Botany 59, 2565–2578.
Sugars and flowering in the grapevine (Vitis vinifera L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXot1Wisb4%3D&md5=e9c19b96f7f9db58614d27fbfa386915CAS | 18508810PubMed |

Linderman RG, Davis EA (2001) Comparative response of selected grapevine rootstocks and cultivars to inoculation with different mycorrhizal fungi. American Journal of Enology and Viticulture 52, 8–11.

Liu HF, Wu BH, Fan SH, Li LS (2006) Sugar and acid concentrations in 98 grape cultivars analyzed by principal component analysis. Journal of the Science of Food and Agriculture 86, 1526–1536.
Sugar and acid concentrations in 98 grape cultivars analyzed by principal component analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnsVOqu7Y%3D&md5=7eaa362cb2c1fd37a6068732e235402dCAS |

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 Science 236, 168–176.
Climate change conditions (elevated CO2 and temperature) and UV-B radiation affect grapevine (Vitis vinifera cv. Tempranillo) leaf carbon assimilation, altering fruit ripening rates.Crossref | GoogleScholarGoogle Scholar | 26025530PubMed |

Maya MA, Matsubara Y (2013) Influence of arbuscular mycorrhiza on the growth and antioxidative activity in cyclamen under heat stress. Mycorrhiza 23, 381–390.
Influence of arbuscular mycorrhiza on the growth and antioxidative activity in cyclamen under heat stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpsVyrtbw%3D&md5=9f1915ef2f542ea99eaaa67d23c7d56dCAS | 23334657PubMed |

Mira de Orduña R (2010) Climate change associated effects on grape and wine quality and production. Food Research International 43, 1844–1855.
Climate change associated effects on grape and wine quality and production.Crossref | GoogleScholarGoogle Scholar |

Morales F, Pascual I, Sánchez-Díaz M, Aguirreolea J, Irigoyen JJ, Goicoechea N, Antolín MC, Oyárzun M, Urdiáin A (2014) Methodological advances: Using greenhouses to simulate climate change scenarios. Plant Science 226, 30–40.
Methodological advances: Using greenhouses to simulate climate change scenarios.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmtlCltL8%3D&md5=252d5c10b546981b6c0a7f335b6cdb9bCAS | 25113448PubMed |

Mori K, Goto-Yamamoto N, Kitayama M, Hashizume K (2007) Loss of anthocyanins in red-wine grape under high temperature. Journal of Experimental Botany 58, 1935–1945.
Loss of anthocyanins in red-wine grape under high temperature.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXosFeksLs%3D&md5=b621f38032e8a562a8bbf23e415044e9CAS | 17452755PubMed |

Mullins MG (1966) Test-plants for investigations of the physiology of fruiting in Vitis vinifera L. Nature 209, 419–420.
Test-plants for investigations of the physiology of fruiting in Vitis vinifera L.Crossref | GoogleScholarGoogle Scholar |

Nadal M (2010) Phenolic maturity in red grapes. In ‘Methodologies and results in grapevine research’. (Eds S Delrot, H Medrano Gil, E Or, L Bavaresco, S Grando) pp. 389–409. (Springer Science+Business Media: Dordrecht, The Netherlands)

Niculcea M, López J, Sánchez-Díaz M, Antolín MC (2014) Involvement of berry hormonal content in the response to pre- and post-veraison water deficit in different grapevine (Vitis vinifera L.) cultivars. Australian Journal of Grape and Wine Research 20, 281–291.
Involvement of berry hormonal content in the response to pre- and post-veraison water deficit in different grapevine (Vitis vinifera L.) cultivars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXoslCisbg%3D&md5=466960d46061d505da699522c0c345b2CAS |

Nikolaou N, Angelopoulos K, Karagiannidis N (2003) Effects of drought stress on mycorrhizal and non-mycorrhizal Cabernet Sauvignon grapevine, grafted onto various rootstocks. Experimental Agriculture 39, 241–252.
Effects of drought stress on mycorrhizal and non-mycorrhizal Cabernet Sauvignon grapevine, grafted onto various rootstocks.Crossref | GoogleScholarGoogle Scholar |

Nogales A, Aguirreolea J, María ES, Camprubí A, Calvet C (2009) Response of mycorrhizal grapevine to Armillaria mellea inoculation: disease development and polyamines. Plant and Soil 317, 177–187.
Response of mycorrhizal grapevine to Armillaria mellea inoculation: disease development and polyamines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjslWqsLc%3D&md5=9f1f7c4318d4c22de49b29f8411993d8CAS |

Nogales A, Camprubí A, Estaún V, Marfà V, Calvet C (2010) In vitro interaction studies between Glomus intraradices and Armillaria mellea in vines. Spanish Journal of Agricultural Research 8, 62–68.
In vitro interaction studies between Glomus intraradices and Armillaria mellea in vines.Crossref | GoogleScholarGoogle Scholar |

OIV (2014) ‘Compendium of international methods of analysis of wines and musts.’ (International Organisation of Vine and Wine: Paris)

Ollat N, Gény L, Soyer JP (1998) Les boutures fructifères de vigne: validation d’un modèle d’étude de la physiologie de la vigne. I. Principales caractéristiques de l’appareil végétatif. Journal International des Sciences de la Vigne et du Vin 32, 1–9.

Passioura JB (2006) The perils of pot experiments. Functional Plant Biology 33, 1075–1079.
The perils of pot experiments.Crossref | GoogleScholarGoogle Scholar |

Petit E, Glubler WD (2006) Influence of Glomus intraradices on black foot disease caused by Cylindrocarpon macrodidymum on Vitis rupestris under controlled conditions. Plant Disease 90, 1481–1484.
Influence of Glomus intraradices on black foot disease caused by Cylindrocarpon macrodidymum on Vitis rupestris under controlled conditions.Crossref | GoogleScholarGoogle Scholar |

Petrie PR, Sadras VO (2008) Advancement of grapevine maturity in Australia between 1993 and 2006: putative causes, magnitude of trends and viticultural consequences. Australian Journal of Grape and Wine Research 14, 33–45.
Advancement of grapevine maturity in Australia between 1993 and 2006: putative causes, magnitude of trends and viticultural consequences.Crossref | GoogleScholarGoogle Scholar |

Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55, 158–161.
Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection.Crossref | GoogleScholarGoogle Scholar |

Poorter H, Bühler J, van Dusschoten D, Climent J, Postma JA (2012) Pot size matters: a meta-analysis of the effects of rooting volume on plant growth. Functional Plant Biology 39, 839–850.
Pot size matters: a meta-analysis of the effects of rooting volume on plant growth.Crossref | GoogleScholarGoogle Scholar |

Preiner D, Tupajić P, Kontić JK, Andabaka Ž, Marković Z, Maletić E (2013) Organic acids profiles of the most important Dalmatian native grapevine (V. vinifera L.) cultivars. Journal of Food Composition and Analysis 32, 162–168.
Organic acids profiles of the most important Dalmatian native grapevine (V. vinifera L.) cultivars.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvFWju7vE&md5=3c9f927a9e8c67833aac2a85c1807cddCAS |

Rebelein H (1973) Rapid quantitative determination of tartaric acid. Chemie, Mikrobiologie Technologie der Lebensmittel 2, 33–38.

Ribéreau-Gayon J, Stonestreet E (1965) Le dosage des anthocyanes dans le vin rouge. Bulletin de la Société Chimique de France 9, 2649–2652.

Sadras VO, Morán MA (2012) Elevated temperature decouples anthocyanins and sugars in berries of Shiraz and Cabernet Franc. Australian Journal of Grape and Wine Research 18, 115–122.
Elevated temperature decouples anthocyanins and sugars in berries of Shiraz and Cabernet Franc.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVyntbnN&md5=b1496e50d3a88b75da5edc9a2d94b2feCAS |

Sadras VO, Morán MA (2013) Nonlinear effects of elevated temperature on grapevine phenology. Agricultural and Forest Meteorology 173, 107–115.
Nonlinear effects of elevated temperature on grapevine phenology.Crossref | GoogleScholarGoogle Scholar |

Sadras VO, Petrie PR (2011) Climate shifts in south-eastern Australia: early maturity of Chardonnay, Shiraz, and Cabernet Sauvignon is associated with early onset rather than faster ripening. Australian Journal of Grape and Wine Research 17, 199–205.
Climate shifts in south-eastern Australia: early maturity of Chardonnay, Shiraz, and Cabernet Sauvignon is associated with early onset rather than faster ripening.Crossref | GoogleScholarGoogle Scholar |

Sadras VO, Moran MA, Bonada M (2013a) Effects of elevated temperature in grapevine. I. Berry sensory traits. Australian Journal of Grape and Wine Research 19, 95–106.
Effects of elevated temperature in grapevine. I. Berry sensory traits.Crossref | GoogleScholarGoogle Scholar |

Sadras VO, Petrie PR, Moran MA (2013b) Effects of elevated temperature in grapevine. II. Juice pH, titratable acidity and wine sensory attributes. Australian Journal of Grape and Wine Research 19, 107–115.
Effects of elevated temperature in grapevine. II. Juice pH, titratable acidity and wine sensory attributes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjvVaqt78%3D&md5=37e611de68e465c86aca776be4827bf6CAS |

Saint-Cricq N, Vivas N, Glories Y (1998) Maturité phénolique: définition et contrôle. Revue Française d’Oenologie 173, 22–25.

Schreiner RP (2007) Effects of native and non-native arbuscular mycorrhizal fungi on growth and nutrient uptake of ‘Pinot noir’ (Vitis vinifera L.) in two soils with contrasting levels of phosphorus. Applied Soil Ecology 36, 205–215.
Effects of native and non-native arbuscular mycorrhizal fungi on growth and nutrient uptake of ‘Pinot noir’ (Vitis vinifera L.) in two soils with contrasting levels of phosphorus.Crossref | GoogleScholarGoogle Scholar |

Skinner PW, Matthews MA (1989) Reproductive development in grape (Vitis vinifera L.) under phosphorus-limited conditions. Scientia Horticulturae 38, 49–60.
Reproductive development in grape (Vitis vinifera L.) under phosphorus-limited conditions.Crossref | GoogleScholarGoogle Scholar |

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. Journal of Experimental Botany 65, 5975–5988.
Metabolic effects of elevated temperature on organic acid degradation in ripening Vitis vinifera fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXis12qsrk%3D&md5=b153760d55759c6b2726387ea582f9a7CAS | 25180109PubMed |

Tarara JM, Lee J, Spayd SE, Scagel CF (2008) Berry temperature and solar radiation alter acylation, proportion, and concentration of anthocyanin in Merlot grapes. American Journal of Enology and Viticulture 59, 235–247.

Teixeira A, Eiras-Dias J, Castellarin SD, Gerós H (2013) Berry phenolics of grapevine under challenging environments. International Journal of Molecular Sciences 14, 18711–18739.
Berry phenolics of grapevine under challenging environments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsFKmur0%3D&md5=e95289d172a3479f02f376d3fb658c80CAS | 24030720PubMed |

Torres N, Goicoechea N, Antolín MC (2015) Antioxidant properties of leaves from different accessions of grapevine (Vitis vinifera L.) cv. Tempranillo after applying biotic and/or environmental modulator factors. Industrial Crops and Products 76, 77–85.
Antioxidant properties of leaves from different accessions of grapevine (Vitis vinifera L.) cv. Tempranillo after applying biotic and/or environmental modulator factors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtVekt7fI&md5=452de2e2e6348a424f26aad74263b4b3CAS |

van Leeuwen C, Roby JP, Alonso-Villaverde V, Gindro K (2013) Impact of clonal variability in Vitis vinifera Cabernet franc on grape composition, wine quality, leaf blade stilbene content, and downy mildew resistance. Journal of Agricultural and Food Chemistry 61, 19–24.
Impact of clonal variability in Vitis vinifera Cabernet franc on grape composition, wine quality, leaf blade stilbene content, and downy mildew resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslKhs7rF&md5=99e60f6c3ab708439286f5d00fa83280CAS | 23205623PubMed |

Vimard B, St-Arnaud M, Furlan V, Fortin JA (1999) Colonization potential of in vitro-produced arbuscular mycorrhizal fungus spores compared with a root-segment inoculum from open pot culture. Mycorrhiza 8, 335–338.
Colonization potential of in vitro-produced arbuscular mycorrhizal fungus spores compared with a root-segment inoculum from open pot culture.Crossref | GoogleScholarGoogle Scholar |

Webb LB, Watterson I, Bhend J, Whetton PH, Barlow EWR (2013) Global climate analogues for wine growing regions in future periods: projections of temperature and precipitation. Australian Journal of Grape and Wine Research 19, 331–341.
Global climate analogues for wine growing regions in future periods: projections of temperature and precipitation.Crossref | GoogleScholarGoogle Scholar |

Xia E-Q, Deng G-F, Guo Y-J, Li H-B (2010) Biological activities of polyphenols from grapes. International Journal of Molecular Sciences 11, 622–646.
Biological activities of polyphenols from grapes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXitVelsrg%3D&md5=408691495c58b41b4937aa486a9d4c88CAS | 20386657PubMed |