Abstract
The rate of global warming varies in magnitude between seasons, with warming being more pronounced in winter and spring than in summer and autumn at high latitudes. Winter warming can have profound effects on dormancy release and spring phenology of perennial fruit crops, but potential follow-on impacts on growth, fruit yield or quality have only rarely been investigated. We studied the effects of mild winter warming on spring phenology, current year shoot growth, cropping performance and fruit quality in four field-grown cultivars of blackcurrant with different chilling requirements. Plants were exposed to ambient or slightly elevated (+ 0.5 °C) temperatures from early October to mid-April the following year. Winter warming had few effects on spring phenology and fruit yield, but caused significant changes in berry contents of phenolic compounds and a reduction in soluble sugars. Increased vegetative growth of warmed plants likely accounts for the changes in berry quality. The results demonstrate a persistent effect of winter warming on shoot growth, which indirectly changes fruit quality.
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References
Andersen UB, Kjaer KH, Erban A, Alpers J, Hincha DK, Kopka J, Zuther E, Pagter M (2017) Impact of seasonal warming on overwintering and spring phenology of blackcurrant. Environ Exp Bot 140:96–109. https://doi.org/10.1016/j.envexpbot.2017.06.005
Atkinson CJ, Brennan RM, Jones HG (2013) Declining chilling and its impact on temperate perennial crops. Environ Exp Bot 91:48–62. https://doi.org/10.1016/j.envexpbot.2013.02.004
Barnuud NN, Zerihun A, Gibberd M, Bates B (2014) Berry composition and climate: Responses and empirical models. Int J Biometeorol 58:1207–1223. https://doi.org/10.1007/s00484-013-0715-2
Blanco V, Blaya-Ros PJ, Torres-Sánchez R, Domingo R (2020) Influence of regulated deficit irrigation and environmental conditions on reproductive response of sweet cherry trees. Plants 9:94. https://doi.org/10.3390/plants9010094
Bonhomme M, Rageau R, Lacointe A, Gendraud M (2005) Influences of cold deprivation during dormancy on carbohydrate contents of vegetative and floral primordia and nearby structures of peach buds (Prunus persica L. Batch). Sci Hortic (amsterdam) 105:223–240. https://doi.org/10.1016/j.scienta.2005.01.015
Brennan R, Graham J (2009) Improving fruit quality in Rubus and Ribes through breeding. Funct Plant Sci Biotechnol 3:22–29
Campoy JA, Darbyshire R, Dirlewanger E et al (2019) Yield potential definition of the chilling requirement reveals likely underestimation of the risk of climate change on winter chill accumulation. Int J Biometeorol 63:183–192. https://doi.org/10.1007/s00484-018-1649-5
Castède S, Campoy JA, García JQ, Le Dantec L, Lafargue M, Barreneche T et al (2014) Genetic determinism of phenological traits highly affected by climate change in Prunus avium: flowering date dissected into chilling and heat requirements. New Phytol 202:703–715. https://doi.org/10.1111/nph.12658
Čereković N, Pagter M, Kristensen HLL, Brennan R, Petersen KK (2014) Effects of deficit irrigation during flower initiation of two blackcurrant (Ribes nigrum L.) cultivars. Sci Hortic (amsterdam) 168:193–201. https://doi.org/10.1016/j.scienta.2014.01.039
Charrier G, Bonhomme M, Lacointe A, Améglio T (2011) Are budburst dates, dormancy and cold acclimation in walnut trees (Juglans regia L.) under mainly genotypic or environmental control? Int J Biometeorol 55:763–774. https://doi.org/10.1007/s00484-011-0470-1
Clarke SJ, Lamont KJ, Pan HY, Barry LA, Hall A, Rogiers SY (2015) Spring root-zone temperature regulates root growth, nutrient uptake and shoot growth dynamics in grapevines. Aust J Grape Wine Res 21:479–489. https://doi.org/10.1111/ajgw.12160
Cleland EE, Chuine I, Menzel A, Mooney HA, Schwartz MD (2007) Shifting plant phenology in response to global change. Trends Ecol Evol 22:357–365. https://doi.org/10.1016/j.tree.2007.04.003
Cortez RE, Gonzalez de Mejia E (2019) Blackcurrants (Ribes nigrum): a review on chemistry, processing, and health benefits. J Food Sci 84:2387–2401. https://doi.org/10.1111/1750-3841.14781
Denisow B (2003) Self-pollination and self-fertility in eight cultivars of black currant (Ribes nigrum L.). Acta Biol Cracov Bot 45:111–114
Ettinger AK, Gee S, Wolkovich EM (2018) Phenological sequences: how early-season events define those that follow. Am J Bot 105:1771–1780. https://doi.org/10.1002/ajb2.1174
Fender AC, Mantilla-Contreras J, Leuschner C (2011) Multiple environmental control of leaf area and its significance for productivity in beech saplings. Trees - Struct Funct 25:847–857. https://doi.org/10.1007/s00468-011-0560-z
Field SK, Smith JP, Morrison EN, Emery RJN, Holzapfel BP (2020) Soil temperature prior to veraison alters grapevine carbon partitioning, xylem sap hormones, and fruit set. Am J Enol Vitic 71:52–61. https://doi.org/10.5344/ajev.2019.19038
Flynn DFB, Wolkovich EM (2018) Temperature and photoperiod drive spring phenology across all species in a temperate forest community. New Phytol 219:1353–1362. https://doi.org/10.1111/nph.15232
Galat Giorgi E, Keller M, Sadras V, Roig FA, Perez Peña J (2020) High temperature during the budswell phase of grapevines increases shoot water transport capacity. Agric for Meteorol 295:108173. https://doi.org/10.1016/j.agrformet.2020.108173
Ghrab M, Ben Mimoun M, Masmoudi MM, Ben Mechlia N (2014) Chilling trends in a warm production area and their impact on flowering and fruiting of peach trees. Sci Hortic (amsterdam) 178:87–94. https://doi.org/10.1016/j.scienta.2014.08.008
Hatfield JL, Prueger JH (2015) Temperature extremes: effect on plant growth and development. Weather and Climate Extremes 10:4–10. https://doi.org/10.1016/j.wace.2015.08.001
IPCC (2021) Climate Change 2021: the physical science basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge
Jaakola L, Hohtola A (2010) Effect of latitude on flavonoid biosynthesis in plants. Plant, Cell Environ 33:1239–1247. https://doi.org/10.1111/j.1365-3040.2010.02154.x
Jones HG, Hillis RM, Gordon SL, Brennan RM (2013) An approach to the determination of winter chill requirements for different Ribes cultivars. Plant Biol 15:18–27. https://doi.org/10.1111/j.1438-8677.2012.00590.x
Kaldmäe H, Kikas A, Arus L, Libek AV (2013) Genotype and microclimate conditions influence ripening pattern and quality of blackcurrant (Ribes nigrum L.) fruit. Zemdirbyste 100:167–174. https://doi.org/10.13080/z-a.2013.100.021
Keller M, Tarara JM (2010) Warm spring temperatures induce persistent season-long changes in shoot development in grapevines. Ann Bot 106:131–141. https://doi.org/10.1093/aob/mcq091
Keller M, Tarara JM, Mills LJ (2010) Spring temperatures alter reproductive development in grapevines. Aust J Grape Wine Res 16:445–454. https://doi.org/10.1111/j.1755-0238.2010.00105.x
Koltowski Z, Pluta S, Jablonski B, Szklanowska K (1999) Pollination requirements of eight cultivars of black currant (Ribes nigrum L.). J Hortic Sci Biotechnol 74:472–474. https://doi.org/10.1080/14620316.1999.11511139
Körner C (2015) Paradigm shift in plant growth control. Curr Opin Plant Biol 25:107–114. https://doi.org/10.1016/j.pbi.2015.05.003
Kreyling J, Grant K, Hammerl V, Arfin-Khan MAS, Malyshev AV, Peñuelas J et al (2019) Winter warming is ecologically more relevant than summer warming in a cool-temperate grassland. Sci Rep 9:14632. https://doi.org/10.1038/s41598-019-51221-w
Liu Y, Mu J, Niklas KJ, Li G, Sun S (2012) Global warming reduces plant reproductive output for temperate multi-inflorescence species on the Tibetan plateau. New Phytol 195:427–436. https://doi.org/10.1111/j.1469-8137.2012.04178.x
Luedeling E, Girvetz EH, Semenov MA, Brown PH (2011) Climate change affects winter chill for temperate fruit and nut trees. PLoS ONE 6:e20155. https://doi.org/10.1371/journal.pone.0020155
Luedeling E, Kunz A, Blanke MM (2013) Identification of chilling and heat requirements of cherry trees – a statistical approach. Int J Biometeorol 57:679–689. https://doi.org/10.1007/s00484-012-0594-y
Pagter M, Andersen UB, Andersen L (2015) Winter warming delays dormancy release, advances budburst, alters carbohydrate metabolism and reduces yield in a temperate shrub. AoB Plants 7:24. https://doi.org/10.1093/aobpla/plv024
Pagter M, Yde CC, Kjær KH (2017) Metabolic fingerprinting of dormant and active flower primordia of Ribes nigrum using high-resolution magic angle spinning NMR. J Agric Food Chem 65:10123–10130. https://doi.org/10.1021/acs.jafc.7b03788
Pedersen HL (2008) Juice quality and yield capacity of black currant cultivars in Denmark. Acta Hortic 777:510–516. https://doi.org/10.17660/ActaHortic.2008.777.78
Poorter H, Fiorani F, Pieruschka R, Wojciechowski T, van der Putten WH, Kleyer M et al (2016) Pampered inside, pestered outside? Differences and similarities between plants growing in controlled conditions and in the field. New Phytol 212:838–855. https://doi.org/10.1111/nph.14243
Preedy K, Brennan R, Jones H, Gordon S (2020) Improved models of the effects of winter chilling on blackcurrant (Ribes nigrum L.) show cultivar specific sensitivity to warm winters. Agric For Meteorol 280:107777. https://doi.org/10.1016/j.agrformet.2019.107777
Reyes F, DeJong T, Franceschi P, Tagliavini M, Gianelle D (2016) Maximum growth potential and periods of resource limitation in apple tree. Front Plant Sci 7:233. https://doi.org/10.3389/fpls.2016.00233
Rohde A, Bhalerao RP (2007) Plant dormancy in the perennial context. Trends Plant Sci 12:217–223. https://doi.org/10.1016/j.tplants.2007.03.012
Ruttink T, Arend M, Morreel K et al (2007) A molecular timetable for apical bud formation and dormancy induction in poplar. Plant Cell 19:2370–2390. https://doi.org/10.1105/tpc.107.052811
Sandell M, Laaksonen O, Ja R, Rostiala N, Pohjanheimo T, Tiitinen K et al (2009) Orosensory profiles and chemical composition of black currant (Ribes nigrum) juice and fractions of press residue. J Agric Food Chem 57:3718–3728. https://doi.org/10.1021/jf803884y
Sønsteby A, Heide OM (2011) Elevated autumn temperature promotes growth cessation and flower formation in black currant cultivars (Ribes nigrum L.). J Hortic Sci Biotechnol 86:120–127. https://doi.org/10.1080/14620316.2011.11512736
Sønsteby A, Heide OM (2014) Chilling requirements of contrasting black currant (Ribes nigrum L.) cultivars and the induction of secondary bud dormancy. Sci Hortic (amsterdam) 179:256–265. https://doi.org/10.1016/j.scienta.2014.09.038
Tian Y, Laaksonen O, Haikonen H, Vanag A, Ejaz H, Linderborg K et al (2019) Compositional diversity among blackcurrant (Ribes nigrum) cultivars originating from European countries. J Agric Food Chem 67:5621–5633. https://doi.org/10.1021/acs.jafc.9b00033
Vagiri M, Ekholm A, Öberg E, Johansson E, Andersson SC, Rumpunen K (2013) Phenols and ascorbic acid in black currants (Ribes nigrum L.): variation due to genotype, location, and year. J Agric Food Chem 61:9298–9306. https://doi.org/10.1021/jf402891s
Winde J, Andersen UB, Kjaer KH, Pagter M (2017) Variation in freezing tolerance, water content and carbohydrate metabolism of floral buds during deacclimation of contrasting blackcurrant cultivars. Acta Physiol Plant 39:201. https://doi.org/10.1007/s11738-017-2503-9
Woznicki TL, Aaby K, Sønsteby A, Heide OM, Wold AB, Remberg SF (2016) Influence of controlled postflowering temperature and daylength on individual phenolic compounds in four black currant cultivars. J Agric Food Chem 64:752–61. 64(4):752–761. https://doi.org/10.1021/acs.jafc.5b05966
Woznicki TL, Heide OM, Sønsteby A, Wold AB, Remberg SF (2015) Effects of controlled post-flowering temperature and daylength on chemical composition of four black currant (Ribes nigrum L.) cultivars of contrasting origin. Sci Hortic (amsterdam) 197:627–636. https://doi.org/10.1016/j.scienta.2015.10.026
Wrolstad RE (1976) Color and pigment analyses in fruit products. In Station Bulletin 624 (Corvallis): Agricultural Experiment Station, Oregon State University, Corvallis
Xia J, Chen J, Piao S, Ciais P, Luo Y, Wan S (2014) Terrestrial carbon cycle affected by non-uniform climate warming. Nat Geosci 7:173–180. https://doi.org/10.1038/ngeo2093
Zheng J, Yang B, Ruusunen V, Laaksonen O, Tahvonen R, Hellsten J et al (2012) Compositional differences of phenolic compounds between black currant (Ribes nigrum L.) cultivars and their response to latitude and weather conditions. J Agric Food Chem 60:6581–6593. https://doi.org/10.1021/jf3012739
Zohner CM, Renner SS (2014) Common garden comparison of the leaf-out phenology of woody species from different native climates, combined with herbarium records, forecasts long-term change. Ecol Lett 17:1016–1025. https://doi.org/10.1111/ele.12308
Acknowledgements
We thank Connie Krogh Damgaard, Finn Kristiansen and Elisabeth Kjemtrup for the outstanding technical assistance and Kwaku Bonsu and Michael Rajeev Vagiri for the analyses of monomeric anthocyanins.
Funding
This work was supported by the Danish Council for Independent Research | Technology and Production Sciences (Grant No. DFF-1335–00182 to MP).
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Conceived and designed the study: M.P., K.H.K.; carried out the experiment: K.H.K., M.P.; analyzed the data: M.P.; writing—original draft preparation: M.P.; writing—review and editing: M.P., K.H.K.; funding acquisition – M.P.
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Pagter, M., Kjær, K.H. Winter warming stimulates vegetative growth and alters fruit quality of blackcurrant (Ribes nigrum). Int J Biometeorol 66, 1391–1401 (2022). https://doi.org/10.1007/s00484-022-02284-4
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DOI: https://doi.org/10.1007/s00484-022-02284-4