{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,19]],"date-time":"2026-02-19T09:37:58Z","timestamp":1771493878358,"version":"3.50.1"},"reference-count":139,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2025,10,28]],"date-time":"2025-10-28T00:00:00Z","timestamp":1761609600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Agron."],"abstract":"<jats:sec>\n                    <jats:title>Background and aims<\/jats:title>\n                    <jats:p>\n                      Climate change is intensifying abiotic stresses in viticulture, particularly through increased drought due to erratic rainfall. Meanwhile, copper (Cu\n                      <jats:sup>2+<\/jats:sup>\n                      ) toxicity, a legacy of phytosanitary treatments, may be aggravated by these environmental shifts. This study evaluated the physiological and ionomic responses of young\n                      <jats:italic>Vitis vinifera<\/jats:italic>\n                      cv. Pinot gris plants, grafted onto three rootstocks (M4, 1103 Paulsen, SO4), under controlled drought, Cu\n                      <jats:sup>2+<\/jats:sup>\n                      toxicity, and their combined effects.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>Plants were grown under greenhouse conditions and subjected to individual and combined stress treatments. Morpho-physiological traits, biomass distribution, and nutrient profiles were assessed to determine genotype-specific responses.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>\n                      Drought markedly reduced gas exchange and photosystem II efficiency (Fv\/Fm), especially in SO4, while M4 maintained better physiological performance. Cu\n                      <jats:sup>2+<\/jats:sup>\n                      toxicity alone had limited physiological impacts but significantly altered root ionomic profiles. Combined stress exacerbated water-state impairment, chlorophyll reduction, and nutrient imbalances, especially in SO4. The PCA analysis of ionomic data revealed clear separation of stress treatments among rootstocks, with M4 exhibiting the most distinct and balanced nutrient profile. In contrast, plants grafted on 1103 Paulsen and SO4 showed less coordinated nutrient responses and reduced recovery capacity.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusions<\/jats:title>\n                    <jats:p>Rootstock genotype strongly affected grapevine resilience under multifactorial stress. M4 emerged as the most tolerant, suggesting its suitability for future viticultural conditions marked by drought and soil contamination. These results emphasize the critical importance of belowground traits in selecting more resilient grapevine plants, integrating physiological and ionomic assessments, to enhance resilience against multifactorial stresses under climate change.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.3389\/fagro.2025.1682753","type":"journal-article","created":{"date-parts":[[2025,10,28]],"date-time":"2025-10-28T06:25:05Z","timestamp":1761632705000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":2,"title":["Double trouble belowground: grapevine rootstocks face drought and copper toxicity"],"prefix":"10.3389","volume":"7","author":[{"given":"R.","family":"Fattorini","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"T. O.","family":"Caretta","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"F.","family":"Benyahia","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"M. Y. A.","family":"Zuluaga","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"S.","family":"Monterisi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"A.","family":"Agostini","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"C.","family":"Andreotti","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"S.","family":"Cesco","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Y.","family":"Pii","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2025,10,28]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2020.00300","article-title":"Manganese in plants: from acquisition to subcellular allocation","volume":"11","author":"Alejandro","year":"2020","journal-title":"Front. Plant Sci."},{"key":"B2","doi-asserted-by":"publisher","first-page":"535","DOI":"10.1016\/j.tree.2004.07.021","article-title":"Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers","volume":"19","author":"Anderson","year":"2004","journal-title":"Trends Ecol. Evol."},{"key":"B3","volume-title":"Ggthemes: Extra Themes, Scales and Geoms for \u201cggplot2\u201d","author":"Arnold","year":"2024"},{"key":"B4","first-page":"181","volume-title":"Combined Stresses in Plants, Physiological, Molecular, and Biochemical Aspects","author":"Atkinson","year":"2014"},{"key":"B5","doi-asserted-by":"publisher","first-page":"3523","DOI":"10.1093\/jxb\/ers100","article-title":"The interaction of plant biotic and abiotic stresses: from genes to the field","volume":"63","author":"Atkinson","year":"2012","journal-title":"J. Exp. Bot."},{"key":"B6","doi-asserted-by":"publisher","first-page":"102","DOI":"10.1016\/j.scienta.2017.09.010","article-title":"Soil-applied phosphorous is an effective tool to mitigate the toxicity of copper excess on grapevine grown in rhizobox","volume":"227","author":"Baldi","year":"2018","journal-title":"Sci. Hortic. Amsterdam"},{"key":"B7","doi-asserted-by":"publisher","first-page":"13804","DOI":"10.1038\/s41598-025-94833-1","article-title":"The combined effect of decreased stomatal density and aperture increases water use efficiency in maize","volume":"15","author":"Barl","year":"2025","journal-title":"Sci. Rep."},{"key":"B8","doi-asserted-by":"publisher","first-page":"365","DOI":"10.1007\/s11270-009-0259-6","article-title":"Bioaccumulation of copper by zea mays: impact on root, shoot and leaf growth","volume":"210","author":"Benimeli","year":"2010","journal-title":"Water Air Soil pollut."},{"key":"B9","doi-asserted-by":"publisher","DOI":"10.3390\/agronomy13020464","article-title":"Assessing grapevine water status by integrating vine transpiration, leaf gas exchanges, chlorophyll fluorescence and sap flow measurements","volume":"13","author":"Benyahia","year":"2023","journal-title":"Agronomy"},{"key":"B10","doi-asserted-by":"publisher","DOI":"10.1016\/j.scienta.2021.110584","article-title":"Fine-tuning of grapevine xanthophyll-cycle and energy dissipation under Mediterranean conditions by kaolin particle-film","volume":"291","author":"Bernardo","year":"2022","journal-title":"Sci. Hortic."},{"key":"B11","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2019.00225","article-title":"Impact of stomatal density and morphology on water-use efficiency in a changing world","volume":"10","author":"Bertolino","year":"2019","journal-title":"Front. Plant Sci."},{"key":"B12","doi-asserted-by":"publisher","DOI":"10.3390\/plants9101385","article-title":"How do novel M-rootstock (Vitis spp.) genotypes cope with drought","volume":"9","author":"Bianchi","year":"2020","journal-title":"Plants"},{"key":"B13","doi-asserted-by":"publisher","first-page":"91","DOI":"10.1016\/j.agwat.2015.07.016","article-title":"Differences among grapevine cultivars in their stomatal behavior and water use efficiency under progressive water stress","volume":"164","author":"Bota","year":"2016","journal-title":"Agric. Water Manag."},{"key":"B14","article-title":"The Water Requirements of Plants. I. Investigation in the Great Plains in 1910 and 1911. US","volume-title":"Dep., Agr. Bur. Plant Indr. Bull","author":"Briggs","year":"1913"},{"key":"B15","doi-asserted-by":"publisher","first-page":"1088","DOI":"10.1104\/pp.110.162396","article-title":"The dynamics of embolism repair in xylem: in vivo visualizations using high-resolution computed tomography","volume":"154","author":"Brodersen","year":"2010","journal-title":"Plant Physiol."},{"key":"B16","doi-asserted-by":"publisher","first-page":"293","DOI":"10.1016\/j.chemosphere.2016.07.104","article-title":"Copper accumulation in vineyard soils: Rhizosphere processes and agronomic practices to limit its toxicity","volume":"162","author":"Brunetto","year":"2016","journal-title":"Chemosphere"},{"key":"B17","doi-asserted-by":"publisher","first-page":"890","DOI":"10.1007\/s11356-011-0446-z","article-title":"The bioaccumulation and translocation of Fe, Zn, and Cu in species of mushrooms from Russula genus","volume":"18","author":"Busuioc","year":"2011","journal-title":"Environ. Sci. pollut. Res."},{"key":"B18","doi-asserted-by":"publisher","first-page":"6531","DOI":"10.1073\/pnas.95.11.6531","article-title":"Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic acquired resistance","volume":"95","author":"Cao","year":"1998","journal-title":"Proc. Natl. Acad. Sci."},{"key":"B19","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2229-14-183","article-title":"Solar ultraviolet radiation is necessary to enhance grapevine fruit ripening transcriptional and phenolic responses","volume":"14","author":"Carbonell-Bejerano","year":"2014","journal-title":"BMC Plant Biol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"101","DOI":"10.1111\/plb.12410","article-title":"Differential physiological response of the grapevine varieties Touriga Nacional and Trincadeira to combined heat, drought and light stresses","volume":"18","author":"Carvalho","year":"2016","journal-title":"Plant Biol."},{"key":"B21","doi-asserted-by":"publisher","DOI":"10.1016\/j.ijdrr.2024.105015","article-title":"Smart management of emergencies in the agricultural, forestry, and animal production domain: Tackling evolving risks in the climate change era","volume":"114","author":"Cesco","year":"2024","journal-title":"Int. J. Disaster Risk Reduct."},{"key":"B22","doi-asserted-by":"publisher","DOI":"10.3390\/app11030907","article-title":"A smart and sustainable future for viticulture is rooted in soil: how to face cu toxicity","volume":"11","author":"Cesco","year":"2021","journal-title":"Appl. Sci."},{"key":"B23","first-page":"218","article-title":"Nutrient and elemental toxicieties","volume-title":"Soil Constraints on Crop Production","author":"Cesco","year":"2022"},{"key":"B24","doi-asserted-by":"publisher","first-page":"18759","DOI":"10.1038\/s41598-020-75990-x","article-title":"Plasmopara viticola infection affects mineral elements allocation and distribution in Vitis vinifera leaves","volume":"10","author":"Cesco","year":"2020","journal-title":"Sci. Rep. UK"},{"key":"B25","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1023\/a:1019942924985","article-title":"Copper bioavailability and rhizosphere pH changes as affected by nitrogen supply for tomato and oilseed rape cropped on an acidic and a calcareous soil","volume":"243","author":"Chaignon","year":"2002","journal-title":"Plant Soil"},{"key":"B26","doi-asserted-by":"publisher","first-page":"661","DOI":"10.1093\/aob\/mcq030","article-title":"Grapevine under deficit irrigation: hints from physiological and molecular data","volume":"105","author":"Chaves","year":"2010","journal-title":"Ann. Bot."},{"key":"B27","doi-asserted-by":"publisher","first-page":"1092","DOI":"10.1016\/j.envpol.2008.04.015","article-title":"Factors affecting distribution and mobility of trace elements (Cu, Pb, Zn) in a perennial grapevine (Vitis vinifera L.) in the Champagne region of France","volume":"156","author":"Chopin","year":"2008","journal-title":"Environ. pollut."},{"key":"B28","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2229-13-147","article-title":"Grafting with rootstocks induces extensive transcriptional re-programming in the shoot apical meristem of grapevine","volume":"13","author":"Cookson","year":"2013","journal-title":"BMC Plant Biol."},{"key":"B29","doi-asserted-by":"publisher","first-page":"272","DOI":"10.1111\/nph.16542","article-title":"Differences in grapevine rootstock sensitivity and recovery from drought are linked to fine root cortical lacunae and root tip function","volume":"229","author":"Cuneo","year":"2021","journal-title":"New Phytol."},{"key":"B30","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2164-10-212","article-title":"Water deficit alters differentially metabolic pathways affecting important flavor and quality traits in grape berries of Cabernet Sauvignon and Chardonnay","volume":"10","author":"Deluc","year":"2009","journal-title":"BMC Genomics"},{"key":"B31","doi-asserted-by":"publisher","DOI":"10.32614\/CRAN.package.agricolae","article-title":"Agricolae: Statistical Procedures for Agricultural Research (R package version 1.3-7). Comprehensive R Archive Network (CRAN)","author":"de Mendiburu","year":"2023"},{"key":"B32","doi-asserted-by":"publisher","first-page":"219","DOI":"10.1016\/j.plaphy.2020.06.001","article-title":"Plant response to water stress of native and non-native Oenothera drummondii populations","volume":"154","author":"D\u00edaz-Barradas","year":"2020","journal-title":"Plant Physiol. Biochem."},{"key":"B33","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2023.1154571","article-title":"Detoxifying the heavy metals: a multipronged study of tolerance strategies against heavy metals toxicity in plants","volume":"14","author":"Ejaz","year":"2023","journal-title":"Front. Plant Sci."},{"key":"B34","doi-asserted-by":"publisher","first-page":"185","DOI":"10.1051\/agro:2008021","article-title":"Plant drought stress: effects, mechanisms and management","volume":"29","author":"Farooq","year":"2009","journal-title":"Agron. Sustain. Dev."},{"key":"B35","doi-asserted-by":"publisher","DOI":"10.3390\/agronomy10030450","article-title":"Differential Aquaporin Response to Distinct Effects of Two Zn Concentrations after Foliar Application in Pak Choi (Brassica rapa L.) Plants","volume":"10","author":"Fatemi","year":"2020","journal-title":"Agronomy"},{"key":"B36","doi-asserted-by":"publisher","first-page":"138","DOI":"10.1016\/j.plaphy.2020.10.023","article-title":"Copper toxicity affects phosphorus uptake mechanisms at molecular and physiological levels in Cucumis sativus plants","volume":"157","author":"Feil","year":"2020","journal-title":"Plant Physiol. Bioch."},{"key":"B37","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2022.1034425","article-title":"Copper toxicity compromises root acquisition of nitrate in the high affinity range","volume":"13","author":"Feil","year":"2023","journal-title":"Front. Plant Sci."},{"key":"B38","doi-asserted-by":"publisher","first-page":"186","DOI":"10.1038\/nature10947","article-title":"Emerging fungal threats to animal, plant and ecosystem health","volume":"484","author":"Fisher","year":"2012","journal-title":"Nature"},{"key":"B39","doi-asserted-by":"publisher","first-page":"343","DOI":"10.1111\/j.1399-3054.2006.00621.x","article-title":"Keeping a positive carbon balance under adverse conditions: responses of photosynthesis and respiration to water stress","volume":"127","author":"Flexas","year":"2006","journal-title":"Physiol. Plant"},{"key":"B40","doi-asserted-by":"publisher","first-page":"602","DOI":"10.1111\/j.1365-3040.2007.01757.x","article-title":"Mesophyll conductance to CO2: current knowledge and future prospects","volume":"31","author":"Flexas","year":"2008","journal-title":"Plant Cell Environ."},{"key":"B41","volume-title":"Viticoltura di Qualita: Trattato dell\u2019eccellenza da terroir","author":"Fregoni","year":"2013"},{"key":"B42","first-page":"287","article-title":"Evaluation pr\u00e9coce de la r\u00e9sistance des porte-greffes \u00e0 la secheresse. 2","author":"Fregoni","year":"1978","journal-title":"G\u00e9n\u00e9tique et am\u00e9lioration de la vigne: Comptes rendus du II\u1d49 Symposium International sur l\u2019Am\u00e9lioration de la Vigne (Bordeaux, 12\u201316 septembre 1977)"},{"key":"B43","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1007\/s00271-016-0490-z","article-title":"Gas exchange and water-use efficiency of cv. Sangiovese grafted to rootstocks of varying water-deficit tolerance","volume":"34","author":"Galbignani","year":"2016","journal-title":"Irrig. Sci."},{"key":"B44","first-page":"622","volume-title":"General Viticulture","author":"Galet","year":"2000"},{"key":"B45","doi-asserted-by":"publisher","first-page":"4658","DOI":"10.1093\/jxb\/eraa245","article-title":"The physiology of drought stress in grapevine: Towards an integrative definition of drought tolerance Physiological Regulation of Evapotranspiration View project Vineyard ecosystem vulnerability to pathogens and drought in the context of climate change View project","volume":"71","author":"Gambetta","year":"2020","journal-title":"Article J. Exp. Bot"},{"key":"B46","first-page":"3","article-title":"Plasmopara viticola: a review of knowledge on downy mildew of grapevine and effective disease management","volume":"50","author":"Gessler","year":"2011","journal-title":"Phytopathol. Mediterr."},{"key":"B47","doi-asserted-by":"publisher","first-page":"345","DOI":"10.1111\/ajgw.12398","article-title":"Interactive effects of high temperature and water deficit on Malbec grapevines","volume":"25","author":"Giorgi","year":"2019","journal-title":"Aust. J. Grape Wine Res."},{"key":"B48","doi-asserted-by":"publisher","first-page":"215","DOI":"10.1016\/j.chemosphere.2010.10.018","article-title":"Cu fractions, mobility and bioavailability in soil-wheat system after Cu-enriched livestock manure applications","volume":"82","author":"Guan","year":"2011","journal-title":"Chemosphere"},{"key":"B49","doi-asserted-by":"publisher","DOI":"10.3390\/agronomy8030031","article-title":"Potassium: A vital regulator of plant responses and tolerance to abiotic stresses","volume":"8","author":"Hasanuzzaman","year":"2018","journal-title":"Agronomy"},{"key":"B50","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2019.00103","article-title":"Water-use efficiency: advances and challenges in a changing climate","volume":"10","author":"Hatfield","year":"2019","journal-title":"Front. Plant Sci."},{"key":"B51","unstructured":"Horikoshi\n              M.\n            \n            \n              Tang\n              Y.\n            \n          \n          ggfortify: Data Visualization Tools for Statistical Analysis Results\n          \n          2018"},{"key":"B52","doi-asserted-by":"publisher","first-page":"1595","DOI":"10.1093\/jexbot\/51.350.1595","article-title":"Sensitivity of growth of roots versus leaves to water stress: biophysical analysis and relation to water transport","volume":"51","author":"Hsiao","year":"2000","journal-title":"J. Exp. Bot."},{"key":"B53","doi-asserted-by":"publisher","DOI":"10.1080\/15592324.2023.2215025","article-title":"Effects of drought stress on photosynthetic physiological characteristics, leaf microstructure, and related gene expression of yellow horn","volume":"18","author":"Hu","year":"2023","journal-title":"Plant Signal. Behav."},{"key":"B54","doi-asserted-by":"publisher","first-page":"110","DOI":"10.1186\/s12870-023-04109-x","article-title":"Physiological, biochemical and molecular responses associated with drought tolerance in grafted grapevine","volume":"23","author":"Jiao","year":"2023","journal-title":"BMC Plant Biol."},{"key":"B55","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1155\/2014\/789087","article-title":"Moisture and salinity stress induced changes in biochemical constituents and water relations of different grape rootstock cultivars","volume":"2014","author":"Jogaiah","year":"2014","journal-title":"Int. J. Agron."},{"key":"B56","doi-asserted-by":"publisher","DOI":"10.1016\/j.scienta.2021.110076","article-title":"Transcriptome profiling provide new insights into the molecular mechanism of grapevine response to heat, drought, and combined stress","volume":"286","author":"Ju","year":"2021","journal-title":"Sci. Hortic."},{"key":"B57","doi-asserted-by":"publisher","first-page":"501","DOI":"10.1016\/j.plaphy.2018.07.036","article-title":"Physiological, micro-morphological and metabolomic analysis of grapevine (Vitis vinifera L.) leaf of plants under water stress","volume":"130","author":"Ju","year":"2018","journal-title":"Plant Physiol. Biochem."},{"key":"B58","doi-asserted-by":"publisher","first-page":"1315","DOI":"10.1007\/s11356-011-0657-3","article-title":"Copper accumulation, translocation, and toxic effects in grapevine cuttings","volume":"19","author":"Juang","year":"2012","journal-title":"Environ. Sci. pollut. Res."},{"key":"B59","doi-asserted-by":"publisher","first-page":"299","DOI":"10.1007\/bf00335958","article-title":"Influence of heavy metals on the functional diversity of soil microbial communities","volume":"23","author":"Kandeler","year":"1996","journal-title":"Biol. Fert. Soils"},{"key":"B60","doi-asserted-by":"publisher","first-page":"217","DOI":"10.1007\/s10646-017-1888-y","article-title":"Assessment of Cu applications in two contrasting soils\u2014effects on soil microbial activity and the fungal community structure","volume":"27","author":"Keiblinger","year":"2018","journal-title":"Ecotoxicology"},{"key":"B61","first-page":"xi","volume-title":"The science of grapevines","author":"Keller","year":"2020"},{"key":"B62","doi-asserted-by":"publisher","first-page":"2433","DOI":"10.5504\/bbeq.2011.0072","article-title":"The role of dreb transcription factors in abiotic stress tolerance of plants","volume":"25","author":"Khan","year":"2011","journal-title":"Biotechnol. Biotec. Eq."},{"key":"B63","doi-asserted-by":"publisher","DOI":"10.3390\/plants12152861","article-title":"Phosphorus plays key roles in regulating plants\u2019 Physiological responses to abiotic stresses","volume":"12","author":"Khan","year":"2023","journal-title":"Plants"},{"key":"B64","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2014.00207","article-title":"Enhancing crop resilience to combined abiotic and biotic stress through the dissection of physiological and molecular crosstalk","volume":"5","author":"Kissoudis","year":"2014","journal-title":"Front. Plant Sci."},{"key":"B65","doi-asserted-by":"publisher","first-page":"138","DOI":"10.1016\/j.envint.2009.10.005","article-title":"Contamination of vineyard soils with fungicides: A review of environmental and toxicological aspects","volume":"36","author":"Kom\u00e1rek","year":"2010","journal-title":"Environ. Int."},{"key":"B66","doi-asserted-by":"publisher","first-page":"287","DOI":"10.1007\/s11104-005-1578-z","article-title":"Effect of cu toxicity on growth of cowpea (Vigna unguiculata)","volume":"279","author":"Kopittke","year":"2006","journal-title":"Plant Soil"},{"key":"B67","doi-asserted-by":"publisher","first-page":"258","DOI":"10.1002\/cbin.11503","article-title":"Molecular mechanisms of plant adaptive responses to heavy metals stress","volume":"45","author":"Kosakivska","year":"2021","journal-title":"Cell Biol. Int."},{"key":"B68","doi-asserted-by":"publisher","first-page":"1360","DOI":"10.1126\/science.1166453","article-title":"A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat","volume":"323","author":"Krattinger","year":"2009","journal-title":"Science"},{"key":"B69","doi-asserted-by":"publisher","first-page":"601","DOI":"10.1111\/j.1747-0765.2010.00494.x","article-title":"Copper concentrations in grapevines and vineyard soils in central Taiwan","volume":"56","author":"Lai","year":"2010","journal-title":"Soil Sci. Plant Nutr."},{"key":"B70","doi-asserted-by":"publisher","first-page":"121","DOI":"10.20870\/oeno-one.2009.43.3.798","article-title":"Vine water status is a key factor in grape ripening and vintage quality for red Bordeaux wine. How can it be assessed for vineyard management purposes","volume":"43","author":"Leeuwen","year":"2009","journal-title":"Oeno One"},{"key":"B71","doi-asserted-by":"publisher","first-page":"197","DOI":"10.5073\/vitis.2008.47.197-200","article-title":"Root dynamics and pattern of \u2018Riesling\u2019on 5C rootstock using minirhizotrons","volume":"47","author":"Lehnart","year":"2008","journal-title":"Vitis"},{"key":"B72","doi-asserted-by":"publisher","first-page":"905","DOI":"10.1111\/pce.12349","article-title":"UV\u2010B\u2010induced gene expression","volume":"38","author":"Liu","year":"2015","journal-title":"Plant Cell Environ."},{"key":"B73","doi-asserted-by":"publisher","first-page":"98","DOI":"10.1071\/fp09191","article-title":"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","volume":"37","author":"Lovisolo","year":"2010","journal-title":"Funct. Plant Biol."},{"key":"B74","doi-asserted-by":"publisher","DOI":"10.1016\/j.plantsci.2020.110600","article-title":"Molecular basis of rootstock-related tolerance to water deficit in Vitis vinifera L. cv. Sangiovese: A physiological and metabolomic combined approach","volume":"299","author":"Lucini","year":"2020","journal-title":"Plant Sci."},{"key":"B75","doi-asserted-by":"publisher","first-page":"563","DOI":"10.1016\/j.chemosphere.2018.09.127","article-title":"Synergism and antagonisms between nutrients induced by copper toxicity in grapevine rootstocks: Monocropping vs. intercropping","volume":"214","author":"Marastoni","year":"2019","journal-title":"Chemosphere"},{"key":"B76","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2019.00946","article-title":"Morphological root responses and molecular regulation of cation transporters are differently affected by copper toxicity and cropping system depending on the grapevine rootstock genotype","volume":"10","author":"Marastoni","year":"2019","journal-title":"Front. Plant Sci."},{"key":"B77","doi-asserted-by":"publisher","DOI":"10.1016\/j.ecoenv.2019.109430","article-title":"The potential of two different Avena sativa L. cultivars to alleviate Cu toxicity","volume":"182","author":"Marastoni","year":"2019","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"B78","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1016\/j.scienta.2017.12.027","article-title":"Photosynthetic response of bottle gourd [Lagenaria siceraria (Molina) Standl.] to drought stress: Relationship between cucurbitacins accumulation and drought tolerance","volume":"231","author":"Mashilo","year":"2018","journal-title":"Sci. Hortic."},{"key":"B79","unstructured":"Global Warming of 1.5\u00b0C: IPCC special report on impacts of global warming of 1.5\u00b0C above pre-industrial levels in context of strengthening response to climate change, sustainable development, and efforts to eradicate poverty\n          \n          43\n          50\n          \n            \n              Masson-Delmotte\n              V.\n            \n            \n              Zhai\n              P.\n            \n            \n              P\u00f6rtner\n              H.-O.\n            \n            \n              Roberts\n              D.\n            \n            \n              Skea\n              J.\n            \n            \n              Shukla\n              P. R.\n            \n          \n          Cambridge, UK\n          Cambridge University Press\n          An IPCC Special Report on the impacts of global warming of\n          \n          2022"},{"key":"B80","doi-asserted-by":"publisher","first-page":"607","DOI":"10.1071\/fp02110","article-title":"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","volume":"30","author":"Medrano","year":"2003","journal-title":"Funct. Plant Biol."},{"key":"B81","doi-asserted-by":"publisher","first-page":"310","DOI":"10.1111\/ajgw.12071","article-title":"Biochemical and physiological responses of two grapevine rootstock genotypes to drought and salt treatments","volume":"20","author":"Meggio","year":"2014","journal-title":"Aust. J. Grape Wine R"},{"key":"B82","doi-asserted-by":"publisher","first-page":"749","DOI":"10.1071\/sr01084","article-title":"The potential impact of long-term copper fungicide usage on soil microbial biomass and microbial activity in an avocado orchard","volume":"40","author":"Merrington","year":"2002","journal-title":"Soil Res."},{"key":"B83","volume-title":"ggpattern: \u201cggplot2\u201d Pattern Geoms","author":"Mike","year":"2025"},{"key":"B84","doi-asserted-by":"publisher","first-page":"125","DOI":"10.1007\/s00425-024-04548-2","article-title":"Plant membrane transporters function under abiotic stresses: a review","volume":"260","author":"Mishra","year":"2024","journal-title":"Planta"},{"key":"B85","first-page":"10.35248","article-title":"Breeding for drought tolerance by monitoring chlorophyll content","volume":"10","author":"Monteoliva","year":"2021","journal-title":"Gene Technol."},{"key":"B86","doi-asserted-by":"publisher","first-page":"3983","DOI":"10.1093\/jxb\/ert208","article-title":"Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications","volume":"64","author":"Murchie","year":"2013","journal-title":"J. Exp. Bot."},{"key":"B87","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1007\/s001280094","article-title":"Copper and Zinc Uptake by Spring Wheat (Triticum aestivum L.) and Corn (Zea mays L.) Grown in Baiyin Region","volume":"67","author":"Nan","year":"2001","journal-title":"Bull. Environ. Contam. Toxicol."},{"key":"B88","first-page":"183","article-title":"Role of Rootstocks in Fruit Production-A Review Crop regulation and source sink relation studies in Annona View project Organic farming practices for sustainable horticulture Vol 3 View project Role of Rootstocks in Fruit Production-A Review","volume":"3","author":"Nimbolkar","year":"2016","journal-title":"J. Agric. Eng. Food Technol."},{"key":"B89","unstructured":"STATE OF THE WORLD VINE AND WINE SECTOR 2021- April 2022\n          \n          2022"},{"key":"B90","unstructured":"2024"},{"key":"B91","doi-asserted-by":"publisher","first-page":"11","DOI":"10.17660\/ActaHortic.2016.1136.2","article-title":"Grapevine rootstocks: origins and perspectives","volume":"1136","author":"Ollat","year":"2016","journal-title":"Acta Horticulturae"},{"key":"B92","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/978-3-642-67637-6_1","article-title":"Physiological processes in plant ecology, toward a synthesis with atriplex","author":"Osmond","year":"1980","journal-title":"Ecol. Stud."},{"key":"B93","doi-asserted-by":"publisher","first-page":"5191","DOI":"10.1093\/jxb\/erx314","article-title":"Stomatal conductance, mesophyll conductance, and transpiration efficiency in relation to leaf anatomy in rice and wheat genotypes under drought","volume":"68","author":"Ouyang","year":"2017","journal-title":"J. Exp. Bot."},{"key":"B94","doi-asserted-by":"publisher","first-page":"84","DOI":"10.1016\/j.jplph.2015.07.007","article-title":"Physiological parameters and protective energy dissipation mechanisms expressed in the leaves of two Vitis vinifera L. genotypes under multiple summer stresses","volume":"185","author":"Palliotti","year":"2015","journal-title":"J. Plant Physiol."},{"key":"B95","doi-asserted-by":"publisher","first-page":"43","DOI":"10.1016\/j.scienta.2014.07.039","article-title":"Changes in vineyard establishment and canopy management urged by earlier climate-related grape ripening: A review","volume":"178","author":"Palliotti","year":"2014","journal-title":"Sci. Hortic."},{"key":"B96","doi-asserted-by":"publisher","DOI":"10.32614\/cran.package.patchwork","article-title":"patchwork: the composer of plots (R package version 1.3.0). CRAN","author":"Pedersen","year":"2024"},{"key":"B97","doi-asserted-by":"publisher","first-page":"326","DOI":"10.1007\/s11270-024-07166-6","article-title":"Distribution and bioavailability of copper in the soil of a young steep vineyard applying different extraction procedures and pseudo-total digestion","volume":"235","author":"Pham","year":"2024","journal-title":"Water Air Soil pollut."},{"key":"B98","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1016\/j.geoderma.2004.01.005","article-title":"Copper accumulation, distribution and fractionation in vineyard soils of Victoria, Australia","volume":"122","author":"Pietrzak","year":"2004","journal-title":"Geoderma"},{"key":"B99","doi-asserted-by":"publisher","first-page":"445","DOI":"10.1016\/j.scienta.2017.12.035","article-title":"Grapevine quality: A multiple choice issue","volume":"234","author":"Poni","year":"2018","journal-title":"Sci. Hortic."},{"key":"B100","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1111\/j.1399-3054.2008.01138.x","article-title":"Adjustments of water use efficiency by stomatal regulation during drought and recovery in the drought\u2010adapted Vitis hybrid Richter\u2010110 (V. berlandieri \u00d7 V. rupestris)","volume":"134","author":"Pou","year":"2008","journal-title":"Physiol. Plant"},{"key":"B101","first-page":"47","article-title":"To the problem of depth of root system penetration of grapevine","volume":"2","author":"Pourtchev","year":"2003","journal-title":"Soil Science, Agrochemistry and Ecology (Sofia)"},{"key":"B102","doi-asserted-by":"publisher","DOI":"10.3390\/agronomy11020289","article-title":"Grapevine rootstocks differently affect physiological and molecular responses of the scion under water deficit condition","volume":"11","author":"Prinsi","year":"2021","journal-title":"Agronomy"},{"key":"B103","doi-asserted-by":"publisher","first-page":"76","DOI":"10.1111\/j.1467-7652.2009.00467.x","article-title":"Expression of pigeonpea hybrid\u2010proline\u2010rich protein encoding gene (CcHyPRP) in yeast and Arabidopsis affords multiple abiotic stress tolerance","volume":"8","author":"Priyanka","year":"2010","journal-title":"Plant Biotechnol. J."},{"key":"B104","doi-asserted-by":"publisher","first-page":"428","DOI":"10.1016\/j.bbrc.2015.06.128","article-title":"A wheat salinity-induced WRKY transcription factor TaWRKY93 confers multiple abiotic stress tolerance in Arabidopsis thaliana","volume":"464","author":"Qin","year":"2015","journal-title":"Biochem. Bioph. Res. Co"},{"key":"B105","first-page":"117","volume-title":"Grape Rootstocks and Related Species","author":"Rahemi","year":"2022"},{"key":"B106","doi-asserted-by":"publisher","first-page":"1634","DOI":"10.1104\/pp.114.248203","article-title":"Rice Growt under Drought Kinase is Required for Drought Tolerance and Grain Yield under Normal and Drought Stress Conditions","volume":"166","author":"Ramegowda","year":"2014","journal-title":"Plant Physiol."},{"key":"B107","doi-asserted-by":"publisher","first-page":"9148","DOI":"10.1038\/s41598-017-09542-1","article-title":"GBF3 transcription factor imparts drought tolerance in Arabidopsis thaliana","volume":"7","author":"Ramegowda","year":"2017","journal-title":"Sci. Rep. UK"},{"key":"B108","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1016\/j.jplph.2014.11.008","article-title":"The interactive effects of simultaneous biotic and abiotic stresses on plants: Mechanistic understanding from drought and pathogen combination","volume":"176","author":"Ramegowda","year":"2015","journal-title":"J. Plant Physiol."},{"key":"B109","doi-asserted-by":"publisher","first-page":"e40397","DOI":"10.1371\/journal.pone.0040397","article-title":"Expression of a finger millet transcription factor, ecNAC1, in tobacco confers abiotic stress-tolerance","volume":"7","author":"Ramegowda","year":"2012","journal-title":"PloS One"},{"key":"B110","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2021.717223","article-title":"Modifications of grapevine berry composition induced by main viral and fungal pathogens in a climate change scenario","volume":"12","author":"Rienth","year":"2021","journal-title":"Front. Plant Sci."},{"key":"B111","doi-asserted-by":"crossref","first-page":"i","DOI":"10.1094\/9780890546383.fm","volume-title":"Emerging Plant Diseases and Global Food Security","author":"Ristaino","year":"2020"},{"key":"B112","doi-asserted-by":"publisher","first-page":"1143","DOI":"10.1104\/pp.006858","article-title":"The combined effect of drought stress and heat shock on gene expression in tobacco","volume":"130","author":"Rizhsky","year":"2002","journal-title":"Plant Physiol."},{"key":"B113","doi-asserted-by":"publisher","first-page":"1683","DOI":"10.1104\/pp.103.033431","article-title":"When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress","volume":"134","author":"Rizhsky","year":"2004","journal-title":"Plant Physiol."},{"key":"B114","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2020.608813","article-title":"Nitrate uptake and transport properties of two grapevine rootstocks with varying vigor","volume":"11","author":"Rossdeutsch","year":"2021","journal-title":"Front. Plant Sci."},{"key":"B115","doi-asserted-by":"publisher","DOI":"10.3390\/plants10020419","article-title":"Potassium control of plant functions: ecological and agricultural implications","volume":"10","author":"Sardans","year":"2021","journal-title":"Plants"},{"key":"B116","doi-asserted-by":"publisher","first-page":"1393","DOI":"10.1046\/j.1365-3040.2003.01064.x","article-title":"Differences in hydraulic architecture account for near\u2010isohydric and anisohydric behaviour of two field\u2010grown Vitis vinifera L. cultivars during drought","volume":"26","author":"Schultz","year":"2003","journal-title":"Plant Cell Environ."},{"key":"B117","doi-asserted-by":"publisher","DOI":"10.3390\/ijms24032430","article-title":"Phytochelatins: sulfur-containing metal(loid)-chelating ligands in plants","volume":"24","author":"Seregin","year":"2023","journal-title":"Int. J. Mol. Sci."},{"key":"B118","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1111\/ajgw.12054","article-title":"Review: the interaction between rootstocks and cultivars (Vitis vinifera L.) to enhance drought tolerance in grapevine","volume":"20","author":"Serra","year":"2014","journal-title":"Aust. J. Grape Wine Res."},{"key":"B119","doi-asserted-by":"publisher","first-page":"537","DOI":"10.1007\/s11104-024-06536-7","article-title":"Soil water availability modulates the response of grapevine leaf gas exchange and PSII traits to a simulated heat wave","volume":"501","author":"Shtai","year":"2024","journal-title":"Plant Soil"},{"key":"B120","doi-asserted-by":"publisher","DOI":"10.1016\/j.agsy.2024.104034","article-title":"European vineyards and their cultural landscapes exposed to record drought and heat","volume":"219","author":"Straffelini","year":"2024","journal-title":"Agric. Syst."},{"key":"B121","doi-asserted-by":"publisher","first-page":"621","DOI":"10.1007\/s00299-020-02519-x","article-title":"The transcription factor VaNAC17 from grapevine (Vitis amurensis) enhances drought tolerance by modulating jasmonic acid biosynthesis in transgenic Arabidopsis","volume":"39","author":"Su","year":"2020","journal-title":"Plant Cell Rep."},{"key":"B122","doi-asserted-by":"publisher","first-page":"17934","DOI":"10.1038\/s41598-023-45103-5","article-title":"Physiological and biochemical mechanisms of grain yield loss in fumitory (Fumaria parviflora Lam.) exposed to copper and drought stress","volume":"13","author":"Tashakorizadeh","year":"2023","journal-title":"Sci. Rep."},{"key":"B123","unstructured":"R: A Language and Environment for Statistical Computing\n          \n          2025"},{"key":"B124","doi-asserted-by":"publisher","first-page":"85","DOI":"10.1111\/j.1755-0238.2008.00040.x","article-title":"Response of potted grapevines to increasing soil copper concentration","volume":"15","author":"Toselli","year":"2009","journal-title":"Aust. J. Grape Wine R"},{"key":"B125","doi-asserted-by":"publisher","DOI":"10.3390\/horticulturae10080883","article-title":"Identifying grapevine rootstocks tolerant to copper excess","volume":"10","author":"Trentin","year":"2024","journal-title":"Horticulturae"},{"key":"B126","doi-asserted-by":"publisher","first-page":"82844","DOI":"10.1007\/s11356-022-21515-0","article-title":"The tolerance of grapevine rootstocks to copper excess and to the use of calcium and phosphorus to mitigate its phytotoxicity","volume":"29","author":"Trentin","year":"2022","journal-title":"Environ. Sci. pollut. Res."},{"key":"B127","doi-asserted-by":"publisher","DOI":"10.3390\/agronomy10020249","article-title":"Adaptive response of a native Mediterranean grapevine cultivar upon short-term exposure to drought and heat stress in the context of climate change","volume":"10","author":"Tzortzakis","year":"2020","journal-title":"Agronomy"},{"key":"B128","doi-asserted-by":"publisher","DOI":"10.3390\/agriculture13091768","article-title":"Patterns of copper bioaccumulation and translocation in grapevine grafts depending on rootstocks","volume":"13","author":"Vr\u0161i\u010d","year":"2023","journal-title":"Agriculture"},{"key":"B129","doi-asserted-by":"publisher","first-page":"1439","DOI":"10.1105\/tpc.10.9.1439","article-title":"A mutation within the leucine-rich repeat domain of the Arabidopsis disease resistance gene RPS5 partially suppresses multiple bacterial and downy mildew resistance genes","volume":"10","author":"Warren","year":"1998","journal-title":"Plant Cell"},{"key":"B130","doi-asserted-by":"publisher","first-page":"251","DOI":"10.1007\/s11248-007-9098-7","article-title":"Over-expression of the apple spermidine synthase gene in pear confers multiple abiotic stress tolerance by altering polyamine titers","volume":"17","author":"Wen","year":"2008","journal-title":"Transgenic Res."},{"key":"B131","doi-asserted-by":"crossref","first-page":"1","DOI":"10.18637\/jss.v040.i01","article-title":"The split-apply-combine strategy for data analysis","volume":"40","author":"Wickham","year":"2011","journal-title":"J. Stat. Softw."},{"key":"B132","doi-asserted-by":"crossref","unstructured":"Wickham\n              H.\n            \n          \n          ggplot2: Elegant Graphics for Data Analysis\n          \n          2016","DOI":"10.1007\/978-3-319-24277-4_9"},{"key":"B133","volume-title":"stringr: Simple, Consistent Wrappers for Common String Operations","author":"Wickham","year":"2023"},{"key":"B134","volume-title":"readxl: Read Excel Files","author":"Wickham","year":"2025"},{"key":"B135","volume-title":"dplyr: A Grammar of Data Manipulation","author":"Wickham","year":"2023"},{"key":"B136","volume-title":"tidyr: Tidy Messy Data","author":"Wickham","year":"2024"},{"key":"B137","doi-asserted-by":"publisher","first-page":"111","DOI":"10.1016\/j.fcr.2005.08.018","article-title":"Role of ABA in integrating plant responses to drought and salt stresses","volume":"97","author":"Zhang","year":"2006","journal-title":"Field Crop Res."},{"key":"B138","doi-asserted-by":"publisher","first-page":"143","DOI":"10.1007\/s40626-016-0070-x","article-title":"The influence of grapevine rootstocks on scion growth and drought resistance","volume":"28","author":"Zhang","year":"2016","journal-title":"Theor. Exp. Plant Phys."},{"key":"B139","doi-asserted-by":"publisher","DOI":"10.3390\/f14071343","article-title":"Effects of drought and flooding on growth and physiology of Cinnamomum camphora seedlings","volume":"14","author":"Zhao","year":"2023","journal-title":"Forests"}],"container-title":["Frontiers in Agronomy"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fagro.2025.1682753\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,28]],"date-time":"2025-10-28T06:25:12Z","timestamp":1761632712000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fagro.2025.1682753\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,10,28]]},"references-count":139,"alternative-id":["10.3389\/fagro.2025.1682753"],"URL":"https:\/\/doi.org\/10.3389\/fagro.2025.1682753","relation":{},"ISSN":["2673-3218"],"issn-type":[{"value":"2673-3218","type":"electronic"}],"subject":[],"published":{"date-parts":[[2025,10,28]]},"article-number":"1682753"}}