Abstract
Key message
Comparison of five sweet cherry cultivars—over 3 years—shows an asynchronous early and late flower development, but a consistent, specific flower developmental stage for dormancy.
Abstract
In temperate woody deciduous perennials, dormancy is a survival strategy to persist winter temperatures; but chilling is also required for the release of flower bud dormancy and for the completion of flower development. This was noticed over 100 years ago, but the biological mechanisms underlying cold regulated dormancy and its release remain poorly understood. That chilling is required for the completion of flower development led us to hypothesize that a particular stage of flower development may be consistently associated with the dormant phase of flower bud development. Flower development of five sweet cherry cultivars was examined weekly under stereoscopic and optical microscopes over 3 years. Chilling requirements for each cultivar were determined by placing weekly shoots in forcing conditions. The establishment of a flower developmental scale showed that early and late flower development, in the autumn and spring, were asynchronous among cultivars and years. However, in all circumstances, dormancy occurred at the same stage of flower development, characterized by the presence of all flower whorls, with the anthers clearly differentiated in the four locules, and the pistil showing an incipient ovary, style and stigma. The length of time flower buds remained at this stage differed between cultivars and was related to their chilling requirements and date of flowering. The observation that a particular stage of flower development, common to the five cultivars examined, exists during the combined rest period provides a framework for further studies on the physiology and cellular biology of dormancy.
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References
Beauvieux R, Wenden B, Dirlewanger E (2018) Bud dormancy in perennial fruit tree species: a pivotal role for oxidative cues. Front Plant Sci 9:1–13. https://doi.org/10.3389/fpls.2018.00657
Brown DS, Kotob FA (1957) Growth of flower buds of apricot, peach, and pear during the rest period. Proc Am Soc Hortic Sci 69:158–164
Brukhin V, Hernould M, Gonzalez N, Chevalier C (2003) Flower development schedule in tomato Lycopersicon esculentum cv. sweet cherry. Sex Plant Reprod 15:311–320. https://doi.org/10.1007/s00497-003-0167-7
Campoy JA, Ruiz D, Egea J (2011) Dormancy in temperate fruit trees in a global warming context: a review. Sci Hortic (Amsterdam) 130:357–372. https://doi.org/10.1016/j.scienta.2011.07.011
Castède S, Campoy JA, García JQ 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
Considine MJ, Considine JA (2016) On the language and physiology of dormancy and quiescence in plants. J Exp Bot 67:3189–3203. https://doi.org/10.1093/jxb/erw138
Cooke JEK, Eriksson ME, Junttila O (2012) The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms. Plant Cell Environ 35:1707–1728. https://doi.org/10.1111/j.1365-3040.2012.02552.x
Coville FV (1920) The influence of cold in stimulating the growth of plants. Proc Natl Acad Sci 6:434–735. https://doi.org/10.1073/pnas.6.7.434
Del Cueto J, Ionescu IA, Pičmanová M et al (2017) Cyanogenic glucosides and derivatives in almond and sweet cherry flower buds from dormancy to flowering. Front Plant Sci 8:1–16. https://doi.org/10.3389/fpls.2017.00800
Dennis FG (2003) Problems in standardizing methods for evaluating the chilling requirements for the breaking of dormancy in buds of woody plants. HortScience 38:347–350
Diaz DH, Rasmussen HP, Dennis FG (1981) Scanning electron microscope examination of flower bud differentiation in sour cherry. J Am Soc Hortic Sci 4:513–515
Fadón E, Rodrigo J (2018) Unveiling winter dormancy through empirical experiments. Environ Exp Bot 152:28–36. https://doi.org/10.1016/j.envexpbot.2017.11.006
Fadón E, Herrero M, Rodrigo J (2015a) Flower bud dormancy in Prunus species. In: Anderson JV (ed) Advances in plant dormancy. Springer, Switzerland, pp 123–135
Fadón E, Herrero M, Rodrigo J (2015b) Flower development in sweet cherry framed in the BBCH scale. Sci Hortic (Amsterdam) 192:141–147. https://doi.org/10.1016/j.scienta.2015.05.027
Fadón E, Herrero M, Rodrigo J (2018) Dormant flower buds actively accumulate starch over winter in sweet cherry. Front Plant Sci. https://doi.org/10.3389/fpls.2018.00171
Felker FC, Robitaille HA, Hess FD (1983) Morphological and ultrastructural development and starch accumulation during chilling of sour cherry flower buds. Am J Bot 70:376–386
Foster T, Johnston R, Seleznyova A (2003) A morphological and quantitative characterization of early floral development in apple (Malus × domestica Borkh.). Ann Bot 92:199–206. https://doi.org/10.1093/aob/mcg120
Gella R, Fustero R, Rodrigo J (2001) Variedades de cerezo (CD). Diputación General de Aragón, Zaragoza
Gibson PJ, Diggle PK (1997) Structural analysis of female and hermaphroditic flowers of a gynodioecious tree, Ocotea tenera (Laureaceae). Am J Bot 84:298–307
Guimond CM, Andrews PK, Lang GA (1998) Scanning electron microscopy of floral initiation in sweet cherry. J Am Soc Hortic Sci 123:509–512
Hedhly A, Hormaza JI, Herrero M (2007) Warm temperatures at bloom reduce fruit set in sweet cherry. J Appl Bot Food Qual 81:158–164
Heide OM (2008) Interaction of photoperiod and temperature in the control of growth and dormancy of Prunus species. Sci Hortic (Amsterdam) 115:309–314. https://doi.org/10.1016/j.scienta.2007.10.005
Herrero M, Rodrigo J, Wunsch A (2017) Flowering, fruit set and development. In: Quero-Garcia J, Iezzoni A, Lang G, Pulawska J (eds) Cherries: botany, production and uses. CAB International, Boston, pp 14–35
Hughes J, McCully ME (1975) The use of an optical brightener in the study of plant structures. Stain Technol 50:319–329
Ionescu IA, López-Ortega G, Burow M et al (2017) Transcriptome and metabolite changes during hydrogen cyanamide-induced floral bud break in sweet cherry. Front Plant Sci 8:1–17. https://doi.org/10.3389/fpls.2017.01233
Jansson S, Douglas CJ (2007) Populus: a model system for plant biology. Annu Rev Plant Biol 58:435–458. https://doi.org/10.1146/annurev.arplant.58.032806.103956
Julian C, Herrero M, Rodrigo J (2010) Flower bud differentiation and development in fruiting and non-fruiting shoots in relation to fruit set in apricot (Prunus armeniaca L.). Trees 24:833–841. https://doi.org/10.1007/s00468-010-0453-6
Julian C, Rodrigo J, Herrero M (2011) Stamen development and winter dormancy in apricot (Prunus armeniaca). Ann Bot 108:617–625. https://doi.org/10.1093/aob/mcr056
Julian C, Herrero M, Rodrigo J (2014) Anther meiosis time is related to winter cold temperatures in apricot (Prunus armeniaca L.). Environ Exp Bot 100:20–25. https://doi.org/10.1016/j.envexpbot.2013.12.002
Kaufmann H, Blanke M (2017) Changes in carbohydrate levels and relative water content (RWC) to distinguish dormancy phases in sweet cherry. J Plant Physiol 218:1–5. https://doi.org/10.1016/j.jplph.2017.07.004
Knight TA (1801) Account of some experiments on the ascent of the sap in trees. Philos Trans R Soc Lond 91:333–353. https://doi.org/10.1098/rstl.1801.0017
Koltunow AM, Truettner J, Cox KH, Wallroth M, Goldberg RB (1990) Different temporal and spatial gene expression patterns occur during anther development. Plant Cell 2:1201–1224. https://doi.org/10.1105/tpc.2.12.1201
Kuhn BF (2006) Determination of starch in ovules of the sour cherry cv. “Stevnsbaer”. Eur J Hortic Sci 71:120–124
Kurokura T, Mimida N, Battey NH, Hytönen T (2013) The regulation of seasonal flowering in the Rosaceae. J Exp Bot 64:4131–4141. https://doi.org/10.1093/jxb/ert233
Lamp BM, Connell JH, Duncan RA et al (2001) Almond flower development: floral initiation and organogenesis. J Am Soc Hortic Sci 126:689–696
Lang GA, Early JD, Martin GC, Darnell RL (1987) Endodormancy, paradormancy, and ecodormancy—physiological terminology and classification for dormancy research. HortScience 22:371–377
Liu Z, Zhu H, Abbott A (2015) Dormancy behaviors and underlying regulatory mechanisms: from perspective of pathways to epigenetic regulation. In: Anderson J (ed) Advances in plant dormancy. Springer, Fargo, USA, pp 35–47
Losada JM, Herrero M (2012) Arabinogalactan-protein secretion is associated with the acquisition of stigmatic receptivity in the apple flower. Ann Bot 110:573–584. https://doi.org/10.1093/aob/mcs116
Luna V, Reinoso H, Lorenzo E et al (1991) Dormancy in peach (Prunus persica L.) flower buds. II. Comparative morphology and phenology in floral and vegetative buds, and the effect of chilling and gibberellin A3. Trees 5:244–246
Malagi G, Sachet MR, Citadin I et al (2015) The comparison of dormancy dynamics in apple trees grown under temperate and mild winter climates imposes a renewal of classical approaches. Trees 29:1365–1380. https://doi.org/10.1007/s00468-015-1214-3
Pacini E, Bellani LM, Lozzi R (1986) Pollen, tapetum and anther development in two cultivars of sweet cherry (Prunus avium). Phytomorphology 36:197–210
Perry TO (1971) Dormancy of trees in winter. Science 171:29–36. https://doi.org/10.1126/science.171.3966.29
Reinoso H, Luna V, Pharis RP, Bottini R (2002) Dormancy in peach (Prunus persica) flower buds. V. Anatomy of bud development in relation to phenological stage. Can J Bot 80:656–663. https://doi.org/10.1139/b02-052
Richardson EA, Seeley SD, Walker DR (1974) A model for estimating the completion of rest for “Redhaven” and “Elberta” peach trees. HortScience 9:331–332
Richardson EA, Seeley SD, Walker DR et al (1975) Pheno-climatography of spring peach bud development. HortScience 10:236–237
Rinne PLH, Welling A, van der Schoot C (2010) Perennial life style of Populus: dormancy cycling and overwintering. In: Jansson S, Bhalerao R, Groover A (eds) Genetics and genomics of Populus. Springer, New York, pp 171–200
Rodrigo J, Hormaza JI, Herrero M (2000) Ovary starch reserves and flower development in apricot (Prunus armeniaca). Physiol Plant 108:35–41. https://doi.org/10.1034/j.1399-3054.2000.108001035.x
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 Online 19:2370–2390. https://doi.org/10.1105/tpc.107.052811
Saito T, Tuan P, Katsumi-Horigane A et al (2015) Development of flower buds in the Japanese pear (Pyrus pyrifolia) from late autumn to early spring. Tree Physiol 35:653–662. https://doi.org/10.1093/treephys/tpv043
Sánchez Martín-Fontecha E, Tarancón C, Cubas P (2017) To grow or not to grow, a power-saving program induced in dormant buds. Curr Opin Plant Biol 41:102–109. https://doi.org/10.1016/j.pbi.2017.10.001
Sasaki R, Yamane H, Ooka T et al (2011) Functional and expressional analyses of PmDAM genes associated with endodormancy in Japanese apricot. Plant Physiol 157:485–497
Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767. https://doi.org/10.1105/tpc.2.8.755
Tarancón C, González-Grandío E, Oliveros JC et al (2017) A conserved carbon starvation response underlies bud dormancy in woody and herbaceous species. Front Plant Sci 8:1–21. https://doi.org/10.3389/fpls.2017.00788
Thompson M (1996) Flowering, pollination and fruit set. In: Webster A, Looney N (eds) Cherries: crop physiology, production and uses. CAB International, Wallingford, pp 223–241
Tufts WP, Morrow EB (1925) Fruit bud differentiation in deciduous fruits. Hilgardia 1:1–14
Vanstraelen M, Benková E (2012) Hormonal interactions in the regulation of plant development. Annu Rev Cell Dev Biol 28:463–487. https://doi.org/10.1146/annurev-cellbio-101011-155741
Velappan Y, Signorelli S, Considine MJ (2017) Cell cycle arrest in plants: what distinguishes quiescence, dormancy and differentiated G1? Ann Bot 120:495–509. https://doi.org/10.1093/aob/mcx082
Williams JHW, Friedman WEF, Arnold MLA (1999) Developmental selection within the angiosperm style: using gamete DNA to visualize interspecific pollen competition. Proc Natl Acad Sci 96:9201–9206
Yamane H, Kashiwa Y, Kakehi E et al (2006) Differential expression of dehydrin in flower buds of two Japanese apricot cultivars requiring different chilling requirements for bud break. Tree Physiol 26:1559–1563
Acknowledgements
This work was supported by the Ministerio de Economía y Competitividad—European Regional Development Fund, European Union (Grant Numbers AGL2012-40239, BES-2010–037992 to EF); Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (Grant Numbers RFP2015-00015-00, RTA2014-00085-00, RTA2017-00003-00); and Gobierno de Aragón—European Social Fund, European Union (Grupo Consolidado A12_17R).
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Fadón, E., Rodrigo, J. & Herrero, M. Is there a specific stage to rest? Morphological changes in flower primordia in relation to endodormancy in sweet cherry (Prunus avium L.). Trees 32, 1583–1594 (2018). https://doi.org/10.1007/s00468-018-1735-7
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DOI: https://doi.org/10.1007/s00468-018-1735-7