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Plant function and evolutionary biology
RESEARCH ARTICLE

Mechanisms underlying photosynthetic acclimation to high temperature are different between Vitis vinifera cv. Syrah and Grenache

Agustina E. Gallo A B , Jorge E. Perez Peña A and Jorge A. Prieto https://orcid.org/0000-0002-1896-9456 A C
+ Author Affiliations
- Author Affiliations

A Instituto Nacional de Tecnología Agropecuaria (INTA), Estación Experimental Agropecuaria (EEA) Mendoza, San Martin 3853, Luján de Cuyo (5507), Mendoza, Argentina.

B Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Av. Rivadavia 1917, ciudad Autónoma de Buenos Aires, C1033AAJ, Argentina.

C Corresponding author. Email: prieto.jorge@inta.gob.ar

Functional Plant Biology - https://doi.org/10.1071/FP20212
Submitted: 18 July 2020  Accepted: 14 October 2020   Published online: 7 December 2020

Abstract

Photosynthesis acclimation to high temperature differs among and within species. Grapevine intra-specific variation in photosynthetic acclimation to elevated temperature has been scarcely assessed. Our objectives were to (i) evaluate the mechanisms underlying long-term acclimation of photosynthesis to elevated temperature in grapevine, and (ii) determine whether these responses are similar among two varieties. A warming experiment with well irrigated Grenache and Syrah field-grown plants was performed during two growing seasons comparing plants exposed at ambient temperature (control) with plants in open-top chambers (heating) that increased mean air temperature between 1.5 and 3.6°C. Photosynthetic acclimation was assessed through the response of net assimilation (An), Rubisco carboxylation rate (Vcmax) and electron transport rate (Jmax), at leaf temperatures from 20 to 40°C. Our results evidenced different mechanisms for photosynthetic acclimation to elevated temperature. Compared with control, Grenache heated increased An, maintaining higher Vcmax and Jmax at temperatures above 35°C. By contrast, Syrah heated and control presented similar values of An, Vcmax and Jmax, evidencing an adjustment of photosynthesis without increasing C assimilation. Both varieties increased the optimum temperature for An, but to a lesser extent when growth temperature was higher. Our study provides evidence that grapevine varieties present different acclimation mechanisms to expected warming.

Keywords: climate change, electron transport rate, Farquhar model, global warming, grapevine, Jmax, photosynthetic acclimation, photosynthesis, Rubisco carboxylation rate, temperature, Vcmax, viticulture.


References

Allakhverdiev SI, Kreslavski VD, Klimov VV, Los DA, Carpentier R, Mohanty P (2008) Heat stress: an overview of molecular responses in photosynthesis. Photosynthesis Research 98, 541–550.
Heat stress: an overview of molecular responses in photosynthesis.Crossref | GoogleScholarGoogle Scholar | 18649006PubMed |

Bauerle WL, Bowden JD, Wang GG (2007) The influence of temperature on within-canopy acclimation and variation in leaf photosynthesis: spatial acclimation to microclimate gradients among climatically divergent Acer rubrum L. genotypes. Journal of Experimental Botany 58, 3285–3298.
The influence of temperature on within-canopy acclimation and variation in leaf photosynthesis: spatial acclimation to microclimate gradients among climatically divergent Acer rubrum L. genotypes.Crossref | GoogleScholarGoogle Scholar | 17804430PubMed |

Bernacchi CJ, Singsaas EL, Pimentel C, Portis RJ, Long SP (2001) Improved temperature response functions for models of Rubisco-limited photosynthesis. Plant, Cell & Environment 24, 253–259.
Improved temperature response functions for models of Rubisco-limited photosynthesis.Crossref | GoogleScholarGoogle Scholar |

Bernacchi CJ, Portis AR, Nakano H, von Caemmerer S, Long SP (2002) Temperature response of mesophyll conductance. Implications for the determination of Rubisco enzyme kinetics and for limitations to photosynthesis in vivo. Plant Physiology 130, 1992–1998.
Temperature response of mesophyll conductance. Implications for the determination of Rubisco enzyme kinetics and for limitations to photosynthesis in vivo.Crossref | GoogleScholarGoogle Scholar | 12481082PubMed |

Bernacchi CJ, Rosenthal DM, Pimentel C, Long SP, Farquhar GD (2009) Modeling the temperature dependence of C3 photosynthesis. In ‘Photosynthesis in silico: understanding complexity from molecules to ecosystems’. pp. 231–246. (Springer : Dordrecht, Netherlands)

Berry JA, Björkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology 31, 491–543.
Photosynthetic response and adaptation to temperature in higher plants.Crossref | GoogleScholarGoogle Scholar |

Brooks A, Farquhar GD (1985) Effect of temperature on the CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light – estimates from gas-exchange measurements on spinach. Planta 165, 397–406.
Effect of temperature on the CO2/O2 specificity of ribulose-1,5-bisphosphate carboxylase/oxygenase and the rate of respiration in the light – estimates from gas-exchange measurements on spinach.Crossref | GoogleScholarGoogle Scholar | 24241146PubMed |

Bunce JA (2000) Acclimation of photosynthesis to temperature in eight cool and warm climate herbaceous C3 species: temperature dependence of parameters of a biochemical photosynthesis model. Photosynthesis Research 63, 59–67.
Acclimation of photosynthesis to temperature in eight cool and warm climate herbaceous C3 species: temperature dependence of parameters of a biochemical photosynthesis model.Crossref | GoogleScholarGoogle Scholar | 16252165PubMed |

Bunce J (2018) Thermal acclimation of the temperature dependence of the Vcmax of Rubisco in quinoa. Photosynthetica 56, 1171–1176.
Thermal acclimation of the temperature dependence of the Vcmax of Rubisco in quinoa.Crossref | GoogleScholarGoogle Scholar |

Bunce JA (2019) Variation in responses of photosynthesis and apparent Rubisco kinetics to temperature in three soybean cultivars. Plants 8, 443
Variation in responses of photosynthesis and apparent Rubisco kinetics to temperature in three soybean cultivars.Crossref | GoogleScholarGoogle Scholar |

Cabré MF, Quénol H, Nuñez M (2016) Regional climate change scenarios applied to viticultural zoning in Mendoza, Argentina. International Journal of Biometeorology 60, 1325–1340.
Regional climate change scenarios applied to viticultural zoning in Mendoza, Argentina.Crossref | GoogleScholarGoogle Scholar | 26823161PubMed |

Carvalho LC, Coito JL, Colanço S, Sangiogo M, Amáncio S (2015) Heat stress in grapevine: the pros and cons of acclimation. Plant, Cell & Environment 38, 777–789.
Heat stress in grapevine: the pros and cons of acclimation.Crossref | GoogleScholarGoogle Scholar |

Cerasoli S, Wertin T, McGuire MA, Rodrigues A, Aubrey DP, Pereira JS, Teskey RO (2014) Poplar saplings exposed to recurring temperature shifts of different amplitude exhibit differences in leaf gas exchange and growth despite equal mean temperature. AoB Plants 6, plu018
Poplar saplings exposed to recurring temperature shifts of different amplitude exhibit differences in leaf gas exchange and growth despite equal mean temperature.Crossref | GoogleScholarGoogle Scholar | 24876300PubMed |

Charrier G, Delzon S, Domec JC, Zhang L, Delmas CEL, Merlin I, Corso D, King A, Ojeda H, Ollat N, Prieto JA, Scholach T, Skinner P, Van Leeuwen C, Gambetta GA (2018) Drought will not leave your glass empty: low risk of hydraulic failure revealed by long-term drought observations in world’s top wine regions. Science Advances 4, eaao6969
Drought will not leave your glass empty: low risk of hydraulic failure revealed by long-term drought observations in world’s top wine regions.Crossref | GoogleScholarGoogle Scholar | 29404405PubMed |

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. Annals of Botany 105, 661–676.
Grapevine under deficit irrigation: hints from physiological and molecular data.Crossref | GoogleScholarGoogle Scholar | 20299345PubMed |

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

Crous KY, Quentin AG, Lin YS, Medlyn BE, Williams DG, Barton CVM, Ellsworth DS (2013) Photosynthesis of temperate Eucalyptus globulus trees outside their native range has limited adjustment to elevated CO2 and climate warming. Global Change Biology 19, 3790–3807.
Photosynthesis of temperate Eucalyptus globulus trees outside their native range has limited adjustment to elevated CO2 and climate warming.Crossref | GoogleScholarGoogle Scholar | 23824839PubMed |

Dayer S, Scharwies JD, Ramesh SA, Sullivan W, Doerflinger FC, Pagay V, Tyerman SD (2020) Comparing hydraulics between two grapevine cultivars reveals differences in stomatal regulation under water stress and exogenous ABA applications. Frontiers in Plant Science 11, 705
Comparing hydraulics between two grapevine cultivars reveals differences in stomatal regulation under water stress and exogenous ABA applications.Crossref | GoogleScholarGoogle Scholar | 32636852PubMed |

de Rosas I, Ponce MT, Malovini E, Deis L, Cavagnaro B, Cavagnaro P (2017) Loss of anthocyanins and modification of the anthocyanin profiles in grape berries of Malbec and Bonarda grown under high temperature conditions. Plant Science 258, 137–145.
Loss of anthocyanins and modification of the anthocyanin profiles in grape berries of Malbec and Bonarda grown under high temperature conditions.Crossref | GoogleScholarGoogle Scholar | 28330557PubMed |

Deis L, de Rosas I, Malovini E, Cavagnaro M, Cavagnaro JB (2015) Impacto del cambio climático en Mendoza. Variación climática en los últimos 50 años. Mirada desde la fisiología de la vid. Revista de la Facultad de Ciencias Agrarias 47, 67–92.

Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2020) Centro de Transferencia InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. InfoStat version. Available at http://www.infostat.com.ar [Verified 20 October 2020]

Diaz-Espejo A (2013) New challenges in modelling photosynthesis: temperature dependencies of Rubisco kinetics. Plant, Cell & Environment 36, 2104–2107.
New challenges in modelling photosynthesis: temperature dependencies of Rubisco kinetics.Crossref | GoogleScholarGoogle Scholar |

Duursma RA (2015) Plantecophys – an R package for analysing and modelling leaf gas exchange data. PLoS One 10, e0143346
Plantecophys – an R package for analysing and modelling leaf gas exchange data.Crossref | GoogleScholarGoogle Scholar | 26581080PubMed |

Edwards EJ, Smithson L, Graham DC, Clingeleffer PR (2011) Grapevine canopy response to a high-temperature event during deficit irrigation. Australian Journal of Grape and Wine Research 17, 153–161.
Grapevine canopy response to a high-temperature event during deficit irrigation.Crossref | GoogleScholarGoogle Scholar |

Farquhar GD, von Caemmerer S, Berry JA (1980) A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species. Planta 149, 78–90.
A biochemical model of photosynthetic CO2 assimilation in leaves of C3 species.Crossref | GoogleScholarGoogle Scholar | 24306196PubMed |

Ferrini F, Mattii GB, Nicese FP (1995) Effect of temperature on key physiological responses of grapevine leaf. American Journal of Enology and Viticulture 46, 375–379.

Flexas J, Ribas-Carbó M, Díaz-Espejo A, Galmés J, Medrano H (2008) Mesophyll conductance to CO2: current knowledge and future prospects. Plant, Cell & Environment 31, 602–621.
Mesophyll conductance to CO2: current knowledge and future prospects.Crossref | GoogleScholarGoogle Scholar |

Flexas J, Galmés J, Gallé A, Gulías J, Pou A, Ribas-Carbó M, Tomàs M, Medrano H (2010) Improving water use efficiency in grapevines: potential physiological targets for biotechnological improvement. Australian Journal of Grape and Wine Research 16, 106–121.
Improving water use efficiency in grapevines: potential physiological targets for biotechnological improvement.Crossref | GoogleScholarGoogle Scholar |

Galat Giorgi E, Sadras VO, Keller M, Perez Peña JE (2019) Interactive effects of high temperature and water deficit on Malbec grapevines. Australian Journal of Grape and Wine Research 25, 345–356.
Interactive effects of high temperature and water deficit on Malbec grapevines.Crossref | GoogleScholarGoogle Scholar |

Galat Giorgi E, Keller M, Sadras V, Roig FA, Perez Peña J (2020) High temperature during budswell phase of grapevines increases shoot water transport capacity. Agricultural and Forest Meteorology 295, 108173
High temperature during budswell phase of grapevines increases shoot water transport capacity.Crossref | GoogleScholarGoogle Scholar |

Galmés J, Kapralov M V., Copolovici LO, Hermida-Carrera C, Niinemets Ü (2015) Temperature responses of the Rubisco maximum carboxylase activity across domains of life: phylogenetic signals, trade-offs, and importance for carbon gain. Photosynthesis Research 123, 183–201.
Temperature responses of the Rubisco maximum carboxylase activity across domains of life: phylogenetic signals, trade-offs, and importance for carbon gain.Crossref | GoogleScholarGoogle Scholar | 25515770PubMed |

Greer DH (2018) The short-term temperature-dependency of CO2 photosynthetic responses of two Vitis vinifera cultivars grown in a hot climate. Environmental and Experimental Botany 147, 125–137.
The short-term temperature-dependency of CO2 photosynthetic responses of two Vitis vinifera cultivars grown in a hot climate.Crossref | GoogleScholarGoogle Scholar |

Greer DH (2019) Modelling the seasonal changes in the gas exchange response to CO2 in relation to short-term leaf temperature changes in Vitis vinifera cv. Shiraz grapevines grown in outdoor conditions. Plant Physiology and Biochemistry 142, 372–383.
Modelling the seasonal changes in the gas exchange response to CO2 in relation to short-term leaf temperature changes in Vitis vinifera cv. Shiraz grapevines grown in outdoor conditions.Crossref | GoogleScholarGoogle Scholar | 31400541PubMed |

Greer DH (2020) Changes in the temperature-dependency of the photosynthetic response to chloroplast CO2 concentrations of outdoor-grown Vitis vinifera cv. Shiraz vines with a mid-season crop removal. Environmental and Experimental Botany 169, 103914
Changes in the temperature-dependency of the photosynthetic response to chloroplast CO2 concentrations of outdoor-grown Vitis vinifera cv. Shiraz vines with a mid-season crop removal.Crossref | GoogleScholarGoogle Scholar |

Greer DH, Weedon MM (2012) Modelling photosynthetic responses to temperature of grapevine (Vitis vinifera cv. Semillon) leaves on vines grown in a hot climate. Plant, Cell & Environment 35, 1050–1064.
Modelling photosynthetic responses to temperature of grapevine (Vitis vinifera cv. Semillon) leaves on vines grown in a hot climate.Crossref | GoogleScholarGoogle Scholar |

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 |

Gunderson CA, O’hara KH, Campion CM, Walker AV, Edwards NT (2010) Thermal plasticity of photosynthesis: the role of acclimation in forest responses to a warming climate. Global Change Biology 16, 2272–2286.
Thermal plasticity of photosynthesis: the role of acclimation in forest responses to a warming climate.Crossref | GoogleScholarGoogle Scholar |

IPCC, Shukla PR, Skea J, Buendia EC, Masson-Delmotte V, Pörtner H-O, Roberts DC, Zhai P, Slade R, Connors S, Diemen R, van Ferrat M, Haughey E, Luz S, Neogi S, Pathak M, Petzold J, Pereira JP, Vyas P, Huntley E, Kissick K, Belkacemi M, Malley J (2019). Summary for policymakers. Climate change and land: an IPCC special report on climate change, desertification, land degradation, sustainable land management, food security, and greenhouse gas fluxes in terrestrial ecosystems. Available at www.ipcc.ch [Verified 20 October 2020]

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

Kattge J, Knorr W (2007) Temperature acclimation in a biochemical model of photosynthesis: a reanalysis of data from 36 species. Plant, Cell & Environment 30, 1176–1190.
Temperature acclimation in a biochemical model of photosynthesis: a reanalysis of data from 36 species.Crossref | GoogleScholarGoogle Scholar |

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. Agricultural Water Management 159, 155–164.
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.Crossref | GoogleScholarGoogle Scholar |

Kriedemann PE (1968) Photosynthesis in vine leaves as a function of light intensity, temperature, and leaf age. Vitis 7, 213–220.

Lebon E, Pellegrino A, Louarn G, Lecoeur J (2006) Branch development controls leaf area dynamics in grapevine (Vitis vinifera) growing in drying soil. Annals of Botany 98, 175–185.
Branch development controls leaf area dynamics in grapevine (Vitis vinifera) growing in drying soil.Crossref | GoogleScholarGoogle Scholar | 16679414PubMed |

Leuning R (2002) Temperature dependence of two parameters in a photosynthesis model. Plant, Cell & Environment 25, 1205–1210.
Temperature dependence of two parameters in a photosynthesis model.Crossref | GoogleScholarGoogle Scholar |

Lin YS, Medlyn BE, Ellsworth DS (2012) Temperature responses of leaf net photosynthesis: the role of component processes. Tree Physiology 32, 219–231.
Temperature responses of leaf net photosynthesis: the role of component processes.Crossref | GoogleScholarGoogle Scholar | 22278379PubMed |

Lin YS, Medlyn BE, De Kauwe MG, Ellsworth DS (2013) Biochemical photosynthetic responses to temperature: how do interspecific differences compare with seasonal shifts? Tree Physiology 33, 793–806.
Biochemical photosynthetic responses to temperature: how do interspecific differences compare with seasonal shifts?Crossref | GoogleScholarGoogle Scholar | 23843350PubMed |

Medlyn BE, Dreyer E, Ellsworth D, Forstreuter M, Harley PC, Kirschbaum MUF, Le Roux X, Montpied P, Strassemeyer J, Walcroft A, Wang K, Loustau D (2002a) Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data. Plant, Cell & Environment 25, 1167–1179.
Temperature response of parameters of a biochemically based model of photosynthesis. II. A review of experimental data.Crossref | GoogleScholarGoogle Scholar |

Medlyn BE, Loustau D, Delzon S (2002b) Temperature response of parameters of a biochemically based model of photosynthesis. I. Seasonal changes in mature maritime pine (Pinus pinaster Ait.). Plant, Cell & Environment 25, 1155–1165.
Temperature response of parameters of a biochemically based model of photosynthesis. I. Seasonal changes in mature maritime pine (Pinus pinaster Ait.).Crossref | GoogleScholarGoogle Scholar |

Miserere A, Searles PS, Manchó G, Maseda PH, Rousseaux MC (2019) Sap flow responses to warming and fruit load in young olive trees. Frontiers in Plant Science 10, 1199
Sap flow responses to warming and fruit load in young olive trees.Crossref | GoogleScholarGoogle Scholar | 31632428PubMed |

Prieto JA, Lebon E, Ojeda H (2010) Stomatal behavior of different grapevine cultivars in response to soil water status and air water vapor pressure deficit. Journal International des Sciences de la Vigne et du Vin 44, 9–20.
Stomatal behavior of different grapevine cultivars in response to soil water status and air water vapor pressure deficit.Crossref | GoogleScholarGoogle Scholar |

R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. Available at https://www.r-project.org [Verified 20 October 2020]

Rogiers SY, Greer DH, Hutton RJ, Landsberg JJ (2009) Does night-time transpiration contribute to anisohydric behaviour in a Vitis vinifera cultivar? Journal of Experimental Botany 60, 3751–3763.
Does night-time transpiration contribute to anisohydric behaviour in a Vitis vinifera cultivar?Crossref | GoogleScholarGoogle Scholar | 19584116PubMed |

Sadras VO, Soar CJ (2009) Shiraz vines maintain yield in response to a 2–4°C increase in maximum temperature using an open-top heating system at key phenostages. European Journal of Agronomy 31, 250–258.
Shiraz vines maintain yield in response to a 2–4°C increase in maximum temperature using an open-top heating system at key phenostages.Crossref | GoogleScholarGoogle Scholar |

Sadras VO, Montoro A, Moran MA, Aphalo PJ (2012) Elevated temperature altered the reaction norms of stomatal conductance in field-grown grapevine. Agricultural and Forest Meteorology 165, 35–42.
Elevated temperature altered the reaction norms of stomatal conductance in field-grown grapevine.Crossref | GoogleScholarGoogle Scholar |

Sadras VO, Petrie PR, Moran MA (2013) 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 |

Sage RF, Kubien DS (2007) The temperature response of C3 and C4 photosynthesis. Plant, Cell & Environment 30, 1086–1106.
The temperature response of C3 and C4 photosynthesis.Crossref | GoogleScholarGoogle Scholar |

Salazar-Parra C, Aguirreolea J, Sánchez-Díaz M, Irigoyen JJ, Morales F (2012) Photosynthetic response of Tempranillo grapevine to climate change scenarios. Annals of Applied Biology 161, 277–292.
Photosynthetic response of Tempranillo grapevine to climate change scenarios.Crossref | GoogleScholarGoogle Scholar |

Salazar-Parra C, Aranjuelo I, Pascual I, Erice G, Sanz-Sáez Á, 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. Journal of Plant Physiology 174, 97–109.
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.Crossref | GoogleScholarGoogle Scholar | 25462972PubMed |

Salvucci ME, Crafts-Brandner SJ (2004) Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis. Physiologia Plantarum 120, 179–186.
Inhibition of photosynthesis by heat stress: the activation state of Rubisco as a limiting factor in photosynthesis.Crossref | GoogleScholarGoogle Scholar | 15032851PubMed |

Santillán D, Iglesias A, La Jeunesse I, Garrote L, Sotes V (2019) Vineyards in transition: a global assessment of the adaptation needs of grape producing regions under climate change. The Science of the Total Environment 657, 839–852.
Vineyards in transition: a global assessment of the adaptation needs of grape producing regions under climate change.Crossref | GoogleScholarGoogle Scholar | 30677949PubMed |

Schultz HR (2003a) Extension of a Farquhar model for limitations of leaf photosynthesis induced by light environment, phenology and leaf age in grapevine (Vitis vinifera L. cvv. White Riesling and Zinfandel). Functional Plant Biology 30, 673–687.
Extension of a Farquhar model for limitations of leaf photosynthesis induced by light environment, phenology and leaf age in grapevine (Vitis vinifera L. cvv. White Riesling and Zinfandel).Crossref | GoogleScholarGoogle Scholar | 32689052PubMed |

Schultz HR (2003b) Differences in hydraulic architecture account for near- isohydric and anisohydric behaviour of two field-grown Vitis vinifera L. cultivars. Plant, Cell & Environment 26, 1393–1405.
Differences in hydraulic architecture account for near- isohydric and anisohydric behaviour of two field-grown Vitis vinifera L. cultivars.Crossref | GoogleScholarGoogle Scholar |

Sharkey TD, Bernacchi CJ, Farquhar GD, Singsaas EL (2007) Fitting photosynthetic carbon dioxide response curves for C3 leaves. Plant, Cell & Environment 30, 1035–1040.
Fitting photosynthetic carbon dioxide response curves for C3 leaves.Crossref | GoogleScholarGoogle Scholar |

Soar CJ, Speirs J, Maffei SM, Penrose AB, McCarthy MG, Loveys BR (2006) Grapevine varieties Shiraz and Grenache differ in their stomatal response to VPD: apparent links with ABA physiology and gene expression in leaf tissue. Australian Journal of Grape and Wine Research 12, 2–12.
Grapevine varieties Shiraz and Grenache differ in their stomatal response to VPD: apparent links with ABA physiology and gene expression in leaf tissue.Crossref | GoogleScholarGoogle Scholar |

Soar CJ, Collins MJ, Sadras VO (2009) Irrigated Shiraz vines (Vitis vinifera) upregulate gas exchange and maintain berry growth in response to short spells of high maximum temperature in the field. Functional Plant Biology 36, 801–814.
Irrigated Shiraz vines (Vitis vinifera) upregulate gas exchange and maintain berry growth in response to short spells of high maximum temperature in the field.Crossref | GoogleScholarGoogle Scholar | 32688690PubMed |

Stinziano JR, Way DA, Bauerle WL (2018) Improving models of photosynthetic thermal acclimation: Which parameters are most important and how many should be modified? Global Change Biology 24, 1580–1598.
Improving models of photosynthetic thermal acclimation: Which parameters are most important and how many should be modified?Crossref | GoogleScholarGoogle Scholar | 28991405PubMed |

Sukhov V (2016) Electrical signals as mechanisms of photosynthesis regulation in plants. Photosynthesis Research 130, 373–387.
Electrical signals as mechanisms of photosynthesis regulation in plants.Crossref | GoogleScholarGoogle Scholar | 27154573PubMed |

Sukhov V, Gaspirovich V, Mysyagin S, Vodeneev V (2017) High-temperature tolerance of photosynthesis can be linked to local electrical responses in leaves of pea. Frontiers in Physiology 8, 763
High-temperature tolerance of photosynthesis can be linked to local electrical responses in leaves of pea.Crossref | GoogleScholarGoogle Scholar | 29033854PubMed |

Sun Y, Geng Q, Du Y, Yang X, Zhai H (2017) Induction of cyclic electron flow around photosystem I during heat stress in grape leaves. Plant Science 256, 65–71.
Induction of cyclic electron flow around photosystem I during heat stress in grape leaves.Crossref | GoogleScholarGoogle Scholar | 28167040PubMed |

Tarara JM, Hoheisel GA (2007) Low-cost shielding to minimize radiation errors of temperature sensors in the field. HortScience 42, 1372–1379.
Low-cost shielding to minimize radiation errors of temperature sensors in the field.Crossref | GoogleScholarGoogle Scholar |

Vico G, Way DA, Hurry V, Manzoni S (2019) Can leaf net photosynthesis acclimate to rising and more variable temperatures? Plant, Cell & Environment 42, 1913–1928.
Can leaf net photosynthesis acclimate to rising and more variable temperatures?Crossref | GoogleScholarGoogle Scholar |

von Caemmerer S, Farquhar GD, Berry J (2009) Biochemical Model of C3 Photosynthesis. In ‘Photosynthesis in silico: understanding complexity from molecules to ecosystems’. pp. 209–230. (Springer: Dordrecht, Netherlands)

Walcroft A, Le Roux X, Diaz-Espejo A, Dones N, Sinoquet H (2002) Effects of crown development on leaf irradiance, leaf morphology and photosynthetic capacity in a peach tree. Tree Physiology 22, 929–938.
Effects of crown development on leaf irradiance, leaf morphology and photosynthetic capacity in a peach tree.Crossref | GoogleScholarGoogle Scholar | 12204849PubMed |

Way DA, Yamori W (2014) Thermal acclimation of photosynthesis: on the importance of adjusting our definitions and accounting for thermal acclimation of respiration. Photosynthesis Research 119, 89–100.
Thermal acclimation of photosynthesis: on the importance of adjusting our definitions and accounting for thermal acclimation of respiration.Crossref | GoogleScholarGoogle Scholar | 23812760PubMed |

Weston DJ, Bauerle WL (2007) Inhibition and acclimation of C3 photosynthesis to moderate heat: perspective from thermally contrasting genotypes of Acer rubrum (red maple). Tree Physiology 27, 1083–1092.
Inhibition and acclimation of C3 photosynthesis to moderate heat: perspective from thermally contrasting genotypes of Acer rubrum (red maple).Crossref | GoogleScholarGoogle Scholar | 17472935PubMed |

Yamori W, Hikosaka K, Way DA (2014) Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation. Photosynthesis Research 119, 101–117.
Temperature response of photosynthesis in C3, C4, and CAM plants: temperature acclimation and temperature adaptation.Crossref | GoogleScholarGoogle Scholar | 23801171PubMed |

Zaka S, Frak E, Julier B, Gastal F, Louarn G (2016) Intraspecific variation in thermal acclimation of photosynthesis across a range of temperatures in a perennial crop. AoB Plants 8, plw035
Intraspecific variation in thermal acclimation of photosynthesis across a range of temperatures in a perennial crop.Crossref | GoogleScholarGoogle Scholar | 27178065PubMed |

Zhou H, Xu M, Hou R, Zheng Y, Chi Y, Ouyang Z (2018) Thermal acclimation of photosynthesis to experimental warming is season-dependent for winter wheat (Triticum aestivum L.). Environmental and Experimental Botany 150, 249–259.
Thermal acclimation of photosynthesis to experimental warming is season-dependent for winter wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar |

Zufferey V (2016) Leaf respiration in grapevine (Vitis vinifera ‘Chasselas’) in relation to environmental and plant factors. Vitis 55, 65–72.

Zufferey V, Murisier F (2002) Photosynthèse des feuilles de vigne (cv Chasselas). II. Adaptation aux conditions environnementales. Revue Suisse de Viticulture, d’Arboriculture et d’Horticulture 34, 197–204.