Abstract
As a result of climate change, temperature patterns are expected to become increasingly irregular with longer and more frequent episodes of unseasonable warm spells during the winter season. Warm spells may promote premature loss of freezing tolerance and bud burst in woody perennials, thereby increasing the risk of tissue damage by subsequent frosts. This study investigated the variation in kinetics of deacclimation and bud break and associated changes in carbohydrate metabolism and water status in floral buds of six blackcurrant (Ribes nigrum) cultivars in response to a simulated warm spell (16/11 °C day/night). In three of the cultivars, the rate of deacclimation showed an almost logarithmic course, whereas the other three cultivars exhibited greater deacclimation resistance and a sigmoid deacclimation pattern. The timing and rate of bud development, and their relationship with deacclimation varied greatly amongst cultivars, indicating genotypic variation in time-dependent responses of freezing tolerance and bud break to warm temperatures. In all six cultivars, deacclimation and growth resumption were strongly associated with rehydration. In contrast, changes in carbohydrate metabolism were mostly associated with deacclimation. Evaluation of phenological responses of the same cultivars under field conditions showed that cultivars which were fast flushing in response to an experimental warm spell also exhibited early bud break under natural conditions, indicating that cultivar differences in phenological responses are consistent under different temperature conditions.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.References
Améglio T, Cochard H, Ewers FW (2001) Stem diameter variations and cold hardiness in walnut trees. J Exp Bot 52(364):2135–2142
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
Arora R, Rowland LJ, Ogden EL, Dhanaraj AL, Marian CO, Ehlenfeldt MK, Vinyard B (2004) Dehardening kinetics, bud development, and dehydrin metabolism in blueberry cultivars during deacclimation at constant, warm temperatures. J Am Soc Hortic Sci 129(5):667–674
Atkinson CJ, Brennan RM, Jones HG (2013) Declining chilling and its impact on temperate perennial crops. Environ Exp Bot 91:48–62
Brennan RM (2006) Currants and gooseberries Ribes species Saxifragaceae. In: Janick J (ed) Encyclopedia of fruit and nut crops. CABI, Cambridge, MA
Castède S, Campoy JA, García JQ, Dantec L, Lafargue M, Barreneche T, Wenden B, Dirlewanger E (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(2):703–715
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(6):763–774
Charrier G, Poirier M, Bonhomme M, Lacointe A, Améglio T (2013) Frost hardiness in walnut trees (Juglans regia L.): How to link physiology and modelling? Tree Physiol 33(11):1229–1241
Cheng L, Fuchigami LH (2002) Growth of young apple trees in relation to reserve nitrogen and carbohydrates. Tree Physiol 22:1297–1303
Chung H, Muraoka H, Nakamura M, Han S, Muller O, Son Y (2013) Experimental warming studies on tree species and forest ecosystems: a literature review. J Plant Res 126(4):447–460
Citadin I, Raseira MC, Herter FG, da Silva JB (2001) Heat requirement for blooming and leafing in peach. HortScience 36(2):305–307
Cox SE, Stushnoff C (2001) Temperature-related shifts in soluble carbohydrate content during dormancy and cold acclimation in Populus tremuloides. Can J Forest Res 31(4):730–737
Crowe JH, Carpenter JF, Crowe LM (1998) The role of vitrification in anhydrobiosis. Annu Rev Physiol 60(1):73–103
Dale A (1987) Some studies in spring frost tolerance in black currants (Ribes nigrum L.). Euphytica 36(3):775–781
Dhuli P, Rohloff J, Strimbeck GR (2014) Metabolite changes in conifer buds and needles during forced bud break in Norway spruce (Picea abies) and European silver fir (Abies alba). Front Plant Sci 5:706
Dinno A (2016) dunn’s.test: Dunn’s test of multiple comparisons using rank sums. R package: version 1.3.2
Ferguson JC, Tarara JM, Mills LJ, Grove GG, Keller M (2011) Dynamic thermal time model of cold hardiness for dormant grapevine buds. Ann Bot Lond 107(3):389–396
Fox J, Weisberg S, Adler D, Bates D, Baud-Bovy G, Ellison S, Firth D, Friendly M, Gorjanc G, Graves S, Heiberger R, Laboissiere R, Monette G (2016) car: companion to applied regression. R package: version 2.1-4. R-Core
Fu YH, Campioli M, Deckmyn G, Janssens IA (2012) The impact of winter and spring temperatures on temperate tree budburst dates: results from an experimental climate manipulation. PLoS ONE 7(10):e47324
Gu L, Hanson PJ, Mac Post W, Kaiser DP, Yang B, Nemani R, Pallardy SG, Meyers T (2008) The 2007 eastern US spring freeze: increased cold damage in a warming world? Bioscience 58(3):253–262
Harrell FE (2016) Hmisc: Harrel miscellaneous. R package: version 4.0-1
Hedley PE, Russell JR, Jorgensen L, Gordon S, Morris JA, Hackett CA, Cardle L, Brennan R (2010) Candidate genes associated with bud dormancy release in blackcurrant (Ribes nigrum L.). BMC Plant Biol 10(1):202
Hothorn T, Bretz F, Westfall P, Heiberger R, Schuezenmeister A, Scheibe S (2016) multcorp: simultaneous inference in general parametric models. R package: version 1.4-6
Jones KS, Paroschy J, McKersie BD, Bowley SR (1999) Carbohydrate composition and freezing tolerance of canes and buds in Vitis vinifera. J Plant Physiol 155:101–106
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(1):18–27
Jones HG, Gordon SL, Brennan RM (2015) Chilling requirement of Ribes cultivars. Front Plant Sci 5:767
Jönsson AM, Bärring L (2011) Ensemble analysis of frost damage on vegetation caused by spring backlashes in a warmer Europe. Nat Hazard Earth Syst 11(2):401–418
Kalberer SR, Wisniewski M, Arora R (2006) Deacclimation and reacclimation of cold-hardy plants: current understanding and emerging concepts. Plant Sci 171:3–16
Kalberer SR, Arora R, Leyva-Estrada N, Krebs SL (2007) Cold hardiness of floral buds of deciduous azaleas: dehardening, rehardening, and endodormancy in late winter. J Am Soc Hortic Sci 132(1):73–79
Kjaer KH, Poiré R, Ottosen CO, Walter A (2012) Rapid adjustment in chrysanthemum carbohydrate turnover and growth activity to a change in time-of-day application of light and daylength. Funct Plant Biol 39(8):639–649
Leinonen L, Repo T, Hanninen H (1997) Changing environmental effects on frost hardiness of Scots pine during dehardening. Ann Bot 79(2):133–137
Lenz A, Hoch G, Vitasse Y, Körner C (2013) European deciduous trees exhibit similar safety margins against damage by spring freeze events along elevational gradients. New Phytol 200(4):1166–1175
Mackėla I, Kraujalis P, Baranauskienė R, Venskutonis PR (2015) Biorefining of blackcurrant (Ribes nigrum L.) buds into high value aroma and antioxidant fractions by supercritical carbon dioxide and pressurized liquid extraction. J Supercrit Fluids 104:291–300
Mahfoozi S, Limin AE, Fowler DB (2001) Developmental regulation of low-temperature tolerance in winter wheat. Ann Bot 87(6):751–757
Muffler L, Beierkuhnlein C, Aas G, Jentsch A, Schweiger AH, Zohner C, Kreyling J (2016) Distribution ranges and spring phenology explain late frost sensitivity in 170 woody plants from the Northern Hemisphere. Global Ecol Biogeogr 25(9):1061–1071
Ögren E (2001) Effects of climatic warming on cold hardiness of some northern woody plants assessed from simulation experiments. Physiol Plantarum 112(1):71–77
Pagter M, Arora R (2013) Winter survival and deacclimation of perennials under warming climate: physiological perspectives. Physiol Plantarum 147(1):75–87
Pagter M, Hausman JF, Arora R (2011a) Deacclimation kinetics and carbohydrate changes in stem tissues of Hydrangea in response to an experimental warm spell. Plant Sci 180:140–148
Pagter M, Lefèvre I, Arora R, Hausman JF (2011b) Quantitative and qualitative changes in carbohydrates associated with spring deacclimation in contrasting Hydrangea species. Environ Exp Bot 72(3):358–367
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
Palonen P (1999) Relationship of seasonal changes in carbohydrates and cold hardiness in canes and buds of three red raspberry cultivars. J Am Soc Hortic Sci 124(5):507–513
Pinheiro J, Bates D, DebRoy S, Sarkar D (2016) nlme: linear and nonlinear mixed effects models. R package: version 3.1-117. R-Core. http://cran.r-project.org/package=nlme
Rapacz M (2002) Cold-deacclimation of Oilseed Rape (Brassica napus var. oleifera) in response to fluctuating temperatures and photoperiod. Ann Bot 89(5):543–549
Renaut J, Lutts S, Hoffmann L, Hausman JF (2004) Responses of poplar to chilling temperatures: proteomic and physiological aspects. Plant Biol 7(1):81–90
Rodrigo J (2000) Spring frosts in deciduous fruit trees—morphological damage and flower hardiness. Sci Hortic 85(3):155–173
Rohde A, Bhalerao RP (2007) Plant dormancy in the perennial context. Trends Plant Sci 12(5):217–223
Rowland LJ, Ogden EL, Ehlenfeldt MK, Vinyard B (2005) Cold hardiness, deacclimation kinetics, and bud development among 12 diverse blueberry genotypes under field conditions. J Am Soc Hortic Sci 130(4):508–514
Saxe H, Cannell MG, Johnsen Ø, Ryan MG, Vourlitis G (2001) Tree and forest functioning in response to global warming. New Phytol 149(3):369–399
Sønsteby A, Heide OM (2014) Chilling requirements of contrasting black currant (Ribes nigrum L.) cultivars and the induction of secondary bud dormancy. Sci Hortic 179:256–265
Steponkus PL, Lanphear FO (1967) Refinement of the triphenyl tetrazolium chloride method of determining cold injury. Plant Physiol 42(10):1423–1426
Stocker TF, Qin D, Plttner G, Tignor MMB, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (2013) IPCC. Climate change 2013: the physical science basis. Contribution of working group I to the fifth assessment report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge and New York
Stone W, Idle DB, Brennan RM (1993) Freezing events within overwintering buds of blackcurrant (Ribes nigrum L.). Ann Bot 72(6):613–617
Suojala T, Lindén L (1997) Frost hardiness of Philadelphus and Hydrangea clones during ecodormancy. Acta Agric Scand B S P 47(1):58–63
Takeda F, Arora R, Wisniewski ME, Davis GA, Warmund MR (1993) Assessment of freeze injury in ‘Boskoop Giant’ black currant buds. HortScience 28(6):652–654
Tinklin IG, Wilkinson EH, Schwabe WW (1970) Factors affecting flower initiation in the black currant Ribes nigrum (L.). J Hortic Sci Biotech 45:275–282
Vitasse Y, Basler D (2014) Is the use of cuttings a good proxy to explore phenological responses of temperate forests in warming and photoperiod experiments? Tree Physiol 34(2):174–183
Vitasse Y, Lenz A, Hoch G, Körner C (2014) Earlier leaf-out rather than difference in freezing resistance puts juvenile trees at greater risk of damage than adult trees. J Ecol 102(4):981–988
Wei T, Simko V (2016) Corrplot: visualization of a correlation matrix. R package: version 0.77
Welling A, Moritz T, Palva ET, Junttila O (2002) Independent activation of cold acclimation by low temperature and short photoperiod in hybrid aspen. Plant Physiol 129(4):1633–1641
Acknowledgements
We thank Elin Marianne Rosenstrøm, Karin Henriksen, Ruth Nielsen and Annette Steen Brandsholm for excellent technical assistance. This study was supported by the Danish Council for Independent Research | Technology and Production Sciences (Project No. DFF-1335-00182).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by L. Bavaresco.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Winde, J., Andersen, U.B., Kjaer, K.H. et al. Variation in freezing tolerance, water content and carbohydrate metabolism of floral buds during deacclimation of contrasting blackcurrant cultivars. Acta Physiol Plant 39, 201 (2017). https://doi.org/10.1007/s11738-017-2503-9
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-017-2503-9