Drought-induced changes in development and function of grapevine (Vitis spp.) organs and in their hydraulic and non-hydraulic interactions at the whole-plant level: a physiological and molecular update

This review deals with grapevine responses to water stress by examining perturbations to physiological and molecular processes at the root, shoot, leaf and berry levels. Long-distance signalling among organs is also considered. Isohydric or anisohydric Vitis genotypes are described in relation to their response to drought, which is linked to stomatal behaviour. Stomatal regulation of grapevine under abscisic acid and hydraulic control (the latter being linked to embolism formation and recovery in water pathways upstream the stomata) is reviewed and linked to impairments of photosynthetic assimilation. We define three stages of photosynthesis regulation in grapevines that are subjected to progressive water stress on the basis of the main causes of assimilation decline. Early and late contributions of aquaporins, which play a fundamental role in water stress control, are discussed. Metabolic mechanisms of dehydration tolerance are rewieved, and variation linked to differences in transcript abundance of genes involved in osmoregulation, photosynthesis, photorespiration, detoxification of free radicals and coping with photoinhibition. Results of these defence strategies accumulated in berries are reviewed, together with perturbations of their molecular pathways. Features observed in different organs show that grapevine fits well as a complex model plant for molecular and physiological studies on plant drought avoidance/tolerance.

[1]  W. Hartung,et al.  An abscisic acid-related reduced transpiration promotes gradual embolism repair when grapevines are rehydrated after drought. , 2008, The New phytologist.

[2]  W. Downton Osmotic adjustment during water stress protects the photosynthetic apparatus against photoinhibition , 1983 .

[3]  S. Tyerman,et al.  Hydraulic connection of grape berries to the vine: varietal differences in water conductance into and out of berries, and potential for backflow. , 2009, Functional plant biology : FPB.

[4]  E. Mapfumo,et al.  Xylem development in relation to water uptake by roots of grapevine (Vitis vinifera L.). , 1993, The New phytologist.

[5]  S. Delrot,et al.  Cloning and expression of two plasma membrane aquaporins expressed during the ripening of grape berry. , 2003, Functional plant biology : FPB.

[6]  J. Gamon,et al.  Photoinhibition in Vitis californica: interactive effects of sunlight, temperature and water status , 1990 .

[7]  S. Rambal,et al.  Stomatal conductance of some grapevines growing in the field under a Mediterranean environment. , 1990 .

[8]  C. Lovisolo,et al.  Mercury hinders recovery of shoot hydraulic conductivity during grapevine rehydration: evidence from a whole-plant approach. , 2006, The New phytologist.

[9]  Rainer Matyssek,et al.  Distinct roles of electric and hydraulic signals on the reaction of leaf gas exchange upon re-irrigation in Zea mays L. , 2007, Plant, cell & environment.

[10]  Jaume Flexas,et al.  Water stress induces different levels of photosynthesis and electron transport rate regulation in grapevines , 1999 .

[11]  S. Lund,et al.  Cellular expansion and gene expression in the developing grape (Vitis vinifera L.) , 2008, Protoplasma.

[12]  M. Sánchez-Díaz,et al.  Effects of partial rootzone drying on yield, ripening and berry ABA in potted Tempranillo grapevines with split roots , 2006 .

[13]  B. B. Deminicis,et al.  Photoinhibition of the photosynthesis. , 2009 .

[14]  Eric Lebon,et al.  Branch development controls leaf area dynamics in grapevine (Vitis vinifera) growing in drying soil. , 2006, Annals of botany.

[15]  M. Pindo,et al.  Cloning and characterization of small non-coding RNAs from grape. , 2009, The Plant journal : for cell and molecular biology.

[16]  A. Nardini,et al.  New evidence for a role of vessel‐associated cells and phloem in the rapid xylem refilling of cavitated stems of Laurus nobilis L. , 2004 .

[17]  R. Morillon,et al.  Plasma Membrane Aquaporins Are Involved in Winter Embolism Recovery in Walnut Tree1 , 2003, Plant Physiology.

[18]  Maria Manuela Chaves,et al.  ABA xylem concentrations determine maximum daily leaf conductance of field‐grown Vitis vinifera L. plants , 1995 .

[19]  J. Flexas,et al.  Photosynthesis limitations during water stress acclimation and recovery in the drought-adapted Vitis hybrid Richter-110 (V. berlandierixV. rupestris). , 2009, Journal of experimental botany.

[20]  J. Pereira,et al.  Hydraulic and chemical signalling in the regulation of stomatal conductance and plant water use in field grapevines growing under deficit irrigation. , 2008, Functional plant biology : FPB.

[21]  B. Loveys,et al.  Gradients in stomatal conductance, xylem sap ABA and bulk leaf ABA along canes of Vitis vinifera cv. Shiraz: molecular and physiological studies investigating their source. , 2004, Functional plant biology : FPB.

[22]  Andrew L. Waterhouse,et al.  Effect of Maturity and Vine Water Status on Grape Skin and Wine Flavonoids , 2002, American Journal of Enology and Viticulture.

[23]  Andrew L. Waterhouse,et al.  The present and future of the international wine industry , 2002, Nature.

[24]  Stefano Mancuso,et al.  Hydraulic and electrical transmission of wound-induced signals in Vitis vinifera , 1999 .

[25]  M. Matthews,et al.  Functional xylem in the post-veraison grape berry. , 2005, Journal of experimental botany.

[26]  Jerome Grimplet,et al.  Tissue-specific mRNA expression profiling in grape berry tissues , 2007, BMC Genomics.

[27]  Jaume Flexas,et al.  Effect of water stress on partitioning of 14C-labelled photosynthates in Vitis vinifera. , 2004, Functional plant biology : FPB.

[28]  N. Zhang,et al.  Abscisic acid activates acid invertases in developing grape berry , 2005 .

[29]  Jaume Flexas,et al.  Mesophyll conductance to CO2: current knowledge and future prospects. , 2008, Plant, cell & environment.

[30]  J. Flexas,et al.  Photoinactivation of photosystem II in high light-acclimated grapevines , 2001 .

[31]  J. Cushman,et al.  Water and salinity stress in grapevines: early and late changes in transcript and metabolite profiles , 2007, Functional & Integrative Genomics.

[32]  S. Rambal,et al.  Influence of Water Stress on Grapevines Growing in the Field: From Leaf to Whole-Plant Response , 1993 .

[33]  N. Dokoozlian,et al.  Abscisic Acid Application Timing and Concentration Affect Firmness, Pigmentation, and Color of `Flame Seedless' Grapes , 2006 .

[34]  C. Lovisolo,et al.  Are xylem radial development and hydraulic conductivity in downwardly-growing grapevine shoots influenced by perturbed auxin metabolism? , 2002, The New phytologist.

[35]  E. Steudle,et al.  Direct measurement of hydraulic properties in developing berries of Vitis vinifera L. cv Shiraz and Chardonnay , 2008 .

[36]  B. Loveys Abscisic acid transport and metabolism in grapevine (Vitis vinifera L.) , 1984 .

[37]  Peter R. Dry,et al.  Factors influencing grapevine vigour and the potential for control with partial rootzone drying , 1998 .

[38]  Shaozhong Kang,et al.  Controlled alternate partial root-zone irrigation: its physiological consequences and impact on water use efficiency. , 2004, Journal of experimental botany.

[39]  M. Gullo,et al.  Hydraulic Parameters Measured in 1-Year-Old Twigs of some Mediterranean Species with Diffuse-Porous Wood: Changes in Hydraulic Conductivity and Their Possible Functional Significance , 1985 .

[40]  Andrea Nardini,et al.  Xylem cavitation and hydraulic control of stomatal conductance in Laurel (Laurus nobilis L.) , 2000 .

[41]  Matthew W. Fidelibus,et al.  Effects of Forchlorfenuron and Abscisic Acid on the Quality of ‘Flame Seedless’ Grapes , 2008 .

[42]  J. Marôco,et al.  Limitations to leaf photosynthesis in field-grown grapevine under drought - metabolic and modelling approaches. , 2002, Functional plant biology : FPB.

[43]  S. D.,et al.  Vine and soil-based measures of water status in a Tempranillo vineyard , 2006 .

[44]  Mark Stitt,et al.  The effect of water stress on photosynthetic carbon metabolism in four species grown under field conditions , 1992 .

[45]  Alain Deloire,et al.  Influence of Pre- and Postveraison Water Deficit on Synthesis and Concentration of Skin Phenolic Compounds during Berry Growth of Vitis vinifera cv. Shiraz , 2002 .

[46]  Eric Lebon,et al.  Towards a simple indicator of water stress in grapevine (Vitis vinifera L.) based on the differential sensitivities of vegetative growth components , 2005 .

[47]  C. Antolín,et al.  Influence of Training System on the Reproductive Development and Hormonal Levels of Vitis vinifera L. cv. Tempranillo , 2001 .

[48]  A. Chouzouri,et al.  Optimization of irrigation water use in grapevines using the relationship between transpiration and plant water status , 2005 .

[49]  A. Mas,et al.  Eight cDNA encoding putative aquaporins in Vitis hybrid Richter-110 and their differential expression. , 2001, Journal of experimental botany.

[50]  M. Esaka,et al.  Effects of plant hormones and shading on the accumulation of anthocyanins and the expression of anthocyanin biosynthetic genes in grape berry skins , 2004 .

[51]  J. Flexas,et al.  Regulation of photosynthesis of C3 plants in response to progressive drought: stomatal conductance as a reference parameter. , 2002, Annals of botany.

[52]  D. J. Naylor,et al.  Proline accumulation in developing grapevine fruit occurs independently of changes in the levels of delta1-pyrroline-5-carboxylate synthetase mRNA or protein. , 1999, Plant physiology.

[53]  S. Delrot,et al.  VvHT1 encodes a monosaccharide transporter expressed in the conducting complex of the grape berry phloem. , 2005, Journal of experimental botany.

[54]  Christian Hermans,et al.  Proline accumulation in plants: a review , 2008, Amino Acids.

[55]  J. Joets,et al.  Proteomic analysis reveals differences between Vitis vinifera L. cv. Chardonnay and cv. Cabernet Sauvignon and their responses to water deficit and salinity. , 2007, Journal of experimental botany.

[56]  C. R. Souza,et al.  Grape berry metabolism in field-grown grapevines exposed to different irrigation strategies , 2005 .

[57]  J. Pereira,et al.  Afternoon Depression In Photosynthesis in Grapevine Leaves—Evidence for a High Light Stress Effect , 1990 .

[58]  Stephen R. Martin,et al.  Shoot growth on de-fruited grapevines: a physiological indicator for irrigation scheduling , 2000 .

[59]  J. Fromm,et al.  Electrical signaling and gas exchange in maize plants of drying soil , 1998 .

[60]  M. M. Alsina,et al.  Aquaporin expression in response to different water stress intensities and recovery in Richter-110 (Vitis sp.): relationship with ecophysiological status , 2007, Planta.

[61]  Jason P. Smith,et al.  Ripening grape berries remain hydraulically connected to the shoot. , 2006, Journal of experimental botany.

[62]  L. Williams,et al.  The Influence of Vitis riparia Rootstock on Water Relations and Gas Exchange of Vitis vinifera cv. Carignane Scion Under Non-Irrigated Conditions , 2000, American Journal of Enology and Viticulture.

[63]  E. Mapfumo,et al.  Anatomical changes of grapevine (Vitis vinifera L. cv. Shiraz) roots related to radial resistance to water movement , 1994 .

[64]  J. Poulain,et al.  The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla , 2007, Nature.

[65]  Rob R. Walker,et al.  Regulation of canopy conductance and transpiration and their modelling in irrigated grapevines. , 2003, Functional plant biology : FPB.

[66]  S. Delrot,et al.  Transcriptomic analysis of grape berry softening during ripening , 2008 .

[67]  V. Lauvergeat,et al.  Characterization of a Grapevine R2R3-MYB Transcription Factor That Regulates the Phenylpropanoid Pathway1[W] , 2005, Plant Physiology.

[68]  P. Høj,et al.  Identification and Characterization of a Fruit-Specific, Thaumatin-Like Protein That Accumulates at Very High Levels in Conjunction with the Onset of Sugar Accumulation and Berry Softening in Grapes , 1997, Plant physiology.

[69]  J. Flexas,et al.  Analysis of the relative increase in photosynthetic O(2) uptake when photosynthesis in grapevine leaves is inhibited following low night temperatures and/or water stress , 1999, Plant physiology.

[70]  H. Schultz,et al.  Field evaluation of water transport in grape berries during water deficits , 1996 .

[71]  A. Fernie,et al.  Control of stomatal aperture , 2011, Plant signaling & behavior.

[72]  M. Matthews,et al.  Direct in situ measurement of cell turgor in grape (Vitis vinifera L.) berries during development and in response to plant water deficits. , 2006, Plant, cell & environment.

[73]  D. Smart,et al.  Transverse hydraulic redistribution by a grapevine , 2005 .

[74]  Shaozhong Kang,et al.  Soil water distribution, water use, and yield response to partial root zone drying under a shallow groundwater table condition in a pear orchard , 2002 .

[75]  A. Condon,et al.  Transpiration efficiency and carbon-isotope discrimination of grapevines grown under well-watered conditions in either glasshouse or vineyard , 2001 .

[76]  B. Loveys,et al.  DIURNAL CHANGES IN THE PHOTOSYNTHESIS OF FIELD-GROWN GRAPE VINES. , 1987, The New phytologist.

[77]  N. Baker,et al.  Photoinhibition of photosynthesis , 1994 .

[78]  C. Gaillard,et al.  A Grape ASR Protein Involved in Sugar and Abscisic Acid Signaling Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.013854. , 2003, The Plant Cell Online.

[79]  M. M. Alsina,et al.  Adjustments of water use efficiency by stomatal regulation during drought and recovery in the drought-adapted Vitis hybrid Richter-110 (V. berlandieri x V. rupestris). , 2008, Physiologia plantarum.

[80]  S. K. Boey,et al.  Plasma Membrane , 2005 .

[81]  M. Chaumont,et al.  Seasonal and diurnal changes in photosynthesis and carbon partitioning in Vitis vinifera leaves in vines withand without fruit , 1994 .

[82]  Hans R. Schultz,et al.  Growth, osmotic, adjustment, and cell-wall mechanics of expanding grape leaves during water deficits , 1993 .

[83]  Josep Cifre,et al.  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. , 2003, Functional plant biology : FPB.

[84]  M. S. Grando,et al.  ASEV Honorary Research Lecture 2007: Beyond the Genome, Opportunities for a Modern Viticulture: A Research Overview , 2008 .

[85]  M. Rossignol,et al.  Grape berry biochemistry revisited upon proteomic analysis of the mesocarp , 2004, Proteomics.

[86]  H. Schultz Extension of a Farquhar model for limitations of leaf photosynthesis induced by light environment, phenology and leaf age in grapevines (Vitis vinifera L. cvv. White Riesling and Zinfandel). , 2003, Functional plant biology : FPB.

[87]  J. Flexas,et al.  Steady-state chlorophyll fluorescence (Fs) measurements as a tool to follow variations of net CO2 assimilation and stomatal conductance during water-stress in C3 plants. , 2002, Physiologia plantarum.

[88]  M. Skolnick,et al.  Sequencing and assembly of highly heterozygous genome of Vitis vinifera L. cv Pinot Noir: problems and solutions. , 2008, Journal of biotechnology.

[89]  Enrico Peterlunger,et al.  Effect of Soil Moisture Availability on Merlot: From Leaf Water Potential to Grape Composition , 2005, American Journal of Enology and Viticulture.

[90]  B. Loveys,et al.  Stomatal closure fully accounts for the inhibition of photosynthesis by abscisic acid. , 1988, The New phytologist.

[91]  Xiao-jing Wang,et al.  Abscisic Acid Stimulates a Calcium-Dependent Protein Kinase in Grape Berry1[W] , 2006, Plant Physiology.

[92]  J. Flexas,et al.  Genetic variability of photosynthesis and water use in Balearic grapevine cultivars , 2001 .

[93]  P. Dry,et al.  Hormonal changes induced by partial rootzone drying of irrigated grapevine. , 2000, Journal of experimental botany.

[94]  J. Sperry,et al.  Size and function in conifer tracheids and angiosperm vessels. , 2006, American journal of botany.

[95]  J. Flexas,et al.  Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress , 2006 .

[96]  R. Morillon,et al.  Plasma Membrane Aquaporins Play a Significant Role during Recovery from Water Deficit1 , 2002, Plant Physiology.

[97]  I. Moyaa,et al.  A new instrument for passive remote sensing : 2 . Measurement of leaf and canopy reflectance changes at 531 nm and their relationship with photosynthesis and chlorophyll fluorescence , 2004 .

[98]  Mark A. Matthews,et al.  Water deficits accelerate ripening and induce changes in gene expression regulating flavonoid biosynthesis in grape berries , 2007, Planta.

[99]  E. Dreyer,et al.  Vulnerability to embolism differs in roots and shoots and among three Mediterranean conifers: consequences for stomatal regulation of water loss? , 2005, Trees.

[100]  Hunseung Kang,et al.  An Expression Analysis of a Gene Family Encoding Plasma Membrane Aquaporins in Response to Abiotic Stresses in Arabidopsis Thaliana , 2004, Plant Molecular Biology.

[101]  W. Hartung,et al.  Whole-plant hydraulic conductance and root-to-shoot flow of abscisic acid are independently affected by water stress in grapevines. , 2002, Functional plant biology : FPB.

[102]  M. Walker,et al.  Application of abscisic acid rapidly upregulated UFGT gene expression and improved color of grape berries , 2015 .

[103]  M. Stitt,et al.  Osmotic Adjustment in Water Stressed Grapevine Leaves in Relation to Carbon Assimilation , 1993 .

[104]  J. Flexas,et al.  Is photosynthesis limited by decreased Rubisco activity and RuBP content under progressive water stress? , 2004, The New phytologist.

[105]  K. Shinozaki,et al.  Identification of a cis-regulatory region of a gene in Arabidopsis thaliana whose induction by dehydration is mediated by abscisic acid and requires protein synthesis , 1995, Molecular and General Genetics MGG.

[106]  J. Flexas,et al.  Down-regulation of photosynthesis by drought under field conditions in grapevine leaves , 1998 .

[107]  C. Crisosto,et al.  Application of abscisic acid (ABA) at veraison advanced red color development and maintained postharvest quality of ‘Crimson Seedless’ grapes , 2007 .

[108]  Jérôme Grimplet,et al.  Water deficit alters differentially metabolic pathways affecting important flavor and quality traits in grape berries of Cabernet Sauvignon and Chardonnay , 2009, BMC Genomics.

[109]  J. Flexas,et al.  Mesophyll conductance to CO 2 : current knowledge and future prospects , 2008 .

[110]  João Maroco,et al.  Partial rootzone drying: regulation of stomatal aperture and carbon assimilation in field-grown grapevines (Vitis vinifera cv. Moscatel). , 2003, Functional plant biology : FPB.

[111]  João Maroco,et al.  Deficit irrigation in grapevine improves water‐use efficiency while controlling vigour and production quality , 2007 .

[112]  Cornelis van Leeuwen,et al.  Stem Water Potential is a Sensitive Indicator of Grapevine Water Status , 2001 .

[113]  M. Ribas-Carbó,et al.  Aquaporins and plant water balance. , 2008, Plant, cell & environment.

[114]  Christophe Maurel,et al.  Plant aquaporins: membrane channels with multiple integrated functions. , 2008, Annual review of plant biology.

[115]  B. Loveys,et al.  Grape vine varieties Shiraz and Grenache differ in their stomatal response to VPD: apparent links with ABA physiology and gene expression in leaf tissue , 2006 .

[116]  E. Ábrahám,et al.  Differential expression of two P5CS genes controlling proline accumulation during salt-stress requires ABA and is regulated by ABA1, ABI1 and AXR2 in Arabidopsis. , 1997, The Plant journal : for cell and molecular biology.

[117]  A. Moing,et al.  Grape berry development: a review , 2002 .

[118]  C. R. Souza,et al.  Effects of deficit irrigation strategies on cluster microclimate for improving fruit composition of Moscatel field-grown grapevines , 2007 .

[119]  B. Loveys,et al.  DIURNAL CHANGES IN WATER RELATIONS AND ABSCISIC ACID IN FIELD-GROWN , 1984 .

[120]  A. Patakas,et al.  Cell Wall Elasticity as a Mechanism to Maintain Favorable Water Relations During Leaf Ontogeny in Grapevines , 1997, American Journal of Enology and Viticulture.

[121]  E. Peterlunger,et al.  Transcriptional regulation of anthocyanin biosynthesis in ripening fruits of grapevine under seasonal water deficit. , 2007, Plant, cell & environment.

[122]  E. Ábrahám,et al.  Duplicated P5CS genes of Arabidopsis play distinct roles in stress regulation and developmental control of proline biosynthesis. , 2008, The Plant journal : for cell and molecular biology.

[123]  Melané A Vivier,et al.  Genetically tailored grapevines for the wine industry. , 2002, Trends in biotechnology.

[124]  B. Loveys,et al.  Internal Control of Stomatal Physiology and Photosynthesis. I. Stomatal Regulation and Associated Changes in Endogenous Levels of Abscisic and Phaseic Acids , 1974 .

[125]  David L. Smith,et al.  Expression of three expansin genes during development and maturation of Kyoho grape berries. , 2007, Journal of plant physiology.

[126]  B. Loveys,et al.  Salinity effects on the stomatal behaviour of grapevine. , 1990, The New phytologist.

[127]  P. Guedes de Pinho,et al.  Carotenoid compounds in grapes and their relationship to plant water status. , 2003, Journal of agricultural and food chemistry.

[128]  J. Pereira,et al.  Understanding plant responses to drought - from genes to the whole plant. , 2003, Functional plant biology : FPB.

[129]  Huiqin Ma,et al.  Grape berry plasma membrane proteome analysis and its differential expression during ripening. , 2008, Journal of experimental botany.

[130]  Jaume Flexas,et al.  Effects of drought on photosynthesis in grapevines under field conditions: an evaluation of stomatal and mesophyll limitations. , 2002, Functional plant biology : FPB.

[131]  W. Liu,et al.  Changes in Photosynthesis, Stomatal Resistance and Abscisic Acid ofVitis LabruscanaThrough Drought and Irrigation Cycles , 1978, American Journal of Enology and Viticulture.

[132]  Ernst Steudle,et al.  A hydraulic signal in root-to-shoot signalling of water shortage. , 2007, The Plant journal : for cell and molecular biology.

[133]  C. Ford,et al.  The relationship between the expression of abscisic acid biosynthesis genes, accumulation of abscisic acid and the promotion of Vitis vinifera L. berry ripening by abscisic acid. , 2009 .

[134]  C. R. Souza,et al.  Control of stomatal aperture and carbon uptake by deficit irrigation in two grapevine cultivars , 2005 .

[135]  G. S. Prakash,et al.  Statistical modeling of the effect of physio-biochemical parameters on water use efficiency of grape varieties, rootstocks and their stionic combinations under moisture stress conditions , 2006 .

[136]  P. Dry,et al.  Influence of plant water status on the production of C13-norisoprenoid precursors in Vitis vinifera L. Cv. cabernet sauvignon grape berries. , 2007, Journal of agricultural and food chemistry.

[137]  S. Howitt,et al.  Identification and functional characterisation of aquaporins in the grapevine, Vitis vinifera. , 2009, Functional plant biology : FPB.

[138]  N. Goto-Yamamoto,et al.  Effects of Temperature on Anthocyanin Biosynthesis in Grape Berry Skins , 2006, American Journal of Enology and Viticulture.

[139]  R. Zorer,et al.  Photoinhibition of photosynthesis in water deficit leaves of grapevine (Vitis vinifera L.) plants , 2007, Photosynthetica.

[140]  J. Moutinho-Pereira,et al.  Leaf Gas Exchange and Water Relations of Grapevines Grown in Three Different Conditions , 2004, Photosynthetica.

[141]  M. Chaumont,et al.  Effects of photoinhibitory treatment on CO2 assimilation, the quantum yield of CO2 assimilation, D1 protein, ascorbate, glutathione and xanthophyll contents and the electron transport rate in vine leaves , 1995 .

[142]  Mark A. Matthews,et al.  Fruit Ripening inVitis viniferaL.: Responses to Seasonal Water Deficits , 1988, American Journal of Enology and Viticulture.

[143]  F. Iacono,et al.  Photoinhibition of photosynthesis and photorespiration in Vitis vinifera under field conditions — effects of light climate and leaf position , 1996 .

[144]  R. Stevens,et al.  Grapevine growth of shoots and fruit linearly correlate with water stress indices based on root‐weighted soil matric potential , 1995 .

[145]  P. Hasegawa,et al.  Coordinate accumulation of antifungal proteins and hexoses constitutes a developmentally controlled defense response during fruit ripening in grape. , 1998, Plant Physiology.

[146]  D. Merdinoglu,et al.  Four specific isogenes of the anthocyanin metabolic pathway are systematically co-expressed with the red colour of grape berries , 2006 .

[147]  L. Gény,et al.  Influence of abscisic acid in triggering "véraison" in grape berry skins of Vitis vinifera L. cv. Cabernet-Sauvignon , 2006 .

[148]  E. Gómez‐Plaza,et al.  Is partial root-zone drying an effective irrigation technique to improve water use efficiency and fruit quality in field-grown wine grapes under semiarid conditions? , 2007 .

[149]  V. Sadras Does partial root-zone drying improve irrigation water productivity in the field? A meta-analysis , 2009, Irrigation Science.

[150]  C. Larsson,et al.  The role of aquaporins in cellular and whole plant water balance. , 2000, Biochimica et biophysica acta.

[151]  M. Thomas,et al.  Grapevine (Vitis vinifera L.). , 2006, Methods in molecular biology.

[152]  F. Salamini,et al.  Desiccation- and abscisic acid-responsive genes encoding major intrinsic proteins (MIPs) from the resurrection plant Craterostigma plantagineum , 1998, Plant Molecular Biology.

[153]  H. Schultz,et al.  Resistance to Water Transport in Shoots of Vitis vinifera L. : Relation to Growth at Low Water Potential. , 1988, Plant physiology.

[154]  J. Flexas,et al.  Steady-State and Maximum Chlorophyll Fluorescence Responses to Water Stress in Grapevine Leaves: A New Remote Sensing System , 2000 .

[155]  Mark A. Matthews,et al.  Berry size and vine water deficits as factors in winegrape composition: Anthocyanins and tannins , 2004 .

[156]  N. Ollat,et al.  Identification of grapevine aquaporins and expression analysis in developing berries , 2008, Plant Cell Reports.

[157]  L. Williams,et al.  Relationships among Ambient Temperature and Vapor Pressure Deficit and Leaf and Stem Water Potentials of Fully Irrigated, Field-Grown Grapevines , 2007, American Journal of Enology and Viticulture.

[158]  M. Gullo,et al.  Hydraulic architecture of Vitis vinifera L. and Populus deltoides Bartr. 1-year-old twigs: I-Hydraulic conductivity (LSC) and water potential gradients , 1982 .

[159]  F. Tardieu,et al.  Drought and Abscisic Acid Effects on Aquaporin Content Translate into Changes in Hydraulic Conductivity and Leaf Growth Rate: A Trans-Scale Approach1[W][OA] , 2009, Plant Physiology.

[160]  R. Dewar,et al.  Sink feedback regulation of photosynthesis in vines: measurements and a model. , 2001, Journal of experimental botany.

[161]  D. Smart,et al.  Importance of internal hydraulic redistribution for prolonging the lifespan of roots in dry soil. , 2007, Plant, cell & environment.

[162]  H. Schultz,et al.  A model analysis of the photosynthetic response of Vitis vinifera L. cvs Riesling and Chasselas leaves in the field: I. Interaction of age, light and temperature. , 2000 .

[163]  N. Nedunchezhian,et al.  Photoinhibition and Recovery of photosystem 2 in Grapevine (Vitis vinifera L.) Leaves Grown Under Field Conditions , 2003, Photosynthetica.

[164]  S. Tyerman,et al.  The Role of Plasma Membrane Intrinsic Protein Aquaporins in Water Transport through Roots: Diurnal and Drought Stress Responses Reveal Different Strategies between Isohydric and Anisohydric Cultivars of Grapevine1[OA] , 2008, Plant Physiology.

[165]  H. Bohnert,et al.  Novel Regulation of Aquaporins during Osmotic Stress1 , 2004, Plant Physiology.

[166]  A. Naor,et al.  Gas Exchange and Water Relations in Field-Grown Sauvignon blanc Grapevines , 1994, American Journal of Enology and Viticulture.

[167]  D. Hukin,et al.  Cavitation vulnerability in roots and shoots: does Populus euphratica Oliv., a poplar from arid areas of Central Asia, differ from other poplar species? , 2005, Journal of experimental botany.

[168]  M. Keller Deficit Irrigation and Vine Mineral Nutrition , 2005, American Journal of Enology and Viticulture.

[169]  J. Flexas,et al.  Effects of drought on light-energy dissipation mechanisms in high-light-acclimated, field-grown grapevines. , 2002, Functional plant biology : FPB.

[170]  P. Baeza,et al.  Variation in stomatal behaviour and gas exchange between mid-morning and mid-afternoon of north–south oriented grapevines (Vitis vinifera L. cv. Tempranillo) at different levels of soil water availability , 2006 .

[171]  J. Flexas,et al.  Mercurial inhibition of root hydraulic conductance in Vitis spp. rootstocks under water stress , 2008 .

[172]  S. Poni,et al.  Response of “Sangiovese” grapevines to partial root-zone drying: Gas-exchange, growth and grape composition , 2007 .

[173]  S. Komatsu,et al.  Aquaporin isoforms responsive to salt and water stresses and phytohormones in radish seedlings. , 2002, Plant & cell physiology.

[174]  Pablo J. Zarco-Tejada,et al.  Simple reflectance indices track heat and water stress-induced changes in steady-state chlorophyll fluorescence at the canopy scale , 2005 .

[175]  S. Robinson,et al.  Differential screening indicates a dramatic change in mRNA profiles during grape berry ripening. Cloning and characterization of cDNAs encoding putative cell wall and stress response proteins. , 2000, Plant physiology.

[176]  L. Zulini,et al.  Effect of water deficit on photosynthetic and other physiological responses in grapevine (Vitis vinifera L. cv. Riesling) plants , 2006, Photosynthetica.

[177]  M. Thomas,et al.  A molecular genetic perspective of reproductive development in grapevine. , 2008, Journal of experimental botany.

[178]  Stefanos Koundouras,et al.  Influence of vineyard location and vine water status on fruit maturation of nonirrigated cv. Agiorgitiko (Vitis vinifera L.). Effects on wine phenolic and aroma components. , 2006, Journal of agricultural and food chemistry.

[179]  C. Lovisolo,et al.  Effects of water stress on vessel size and xylem hydraulic conductivity in Vitis vinifera L. , 1998 .

[180]  S. Zhao,et al.  Photoprotective Function of Photorespiration in Several Grapevine Cultivars Under Drought Stress , 2004, Photosynthetica.

[181]  B. Loveys,et al.  Non‐uniform stomatal closure induced by water stress causes putative non‐stomatal inhibition of photosynthesis , 1988 .

[182]  Hans R. Schultz,et al.  Differences in hydraulic architecture account for near‐isohydric and anisohydric behaviour of two field‐grown Vitis vinifera L. cultivars during drought , 2003 .

[183]  B. Holzapfel,et al.  Vascular function in berries of Vitis vinifera (L.) cv.Shiraz , 2001 .

[184]  N. Ollat,et al.  Carbon isotope composition of sugars in grapevine, an integrated indicator of vineyard water status. , 2002, Journal of experimental botany.

[185]  J. Schiefelbein,et al.  Molecular identification of proline-rich protein genes induced during root formation in grape ( Vitis vinifera L.) stem cuttings , 2003 .

[186]  E. Steudle,et al.  Gating of water channels (aquaporins) in cortical cells of young corn roots by mechanical stimuli (pressure pulses): effects of ABA and of HgCl2. , 2004, Journal of experimental botany.

[187]  S. Lund,et al.  An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development , 2006, BMC Plant Biology.

[188]  J. Gamon,et al.  Photoinhibition in Vitis californica: The Role of Temperature during High-Light Treatment. , 1990, Plant physiology.