Investigating properties of sweet cherry (Prunus avium) flower buds that help promote freezing avoidance by supercooling.
Cold hardiness
Prunus
differential thermal analysis
extra‐organ freezing
low temperature survival
reproductive buds
Journal
Plant biology (Stuttgart, Germany)
ISSN: 1438-8677
Titre abrégé: Plant Biol (Stuttg)
Pays: England
ID NLM: 101148926
Informations de publication
Date de publication:
21 Aug 2024
21 Aug 2024
Historique:
received:
04
04
2024
accepted:
27
06
2024
medline:
21
8
2024
pubmed:
21
8
2024
entrez:
21
8
2024
Statut:
aheadofprint
Résumé
Mechanisms involved in the supercooling of plant tissues as a means of low temperature survival are still not fully understood. We investigated properties that may promote supercooling in overwintering sweet cherry (Prunus avium) flower buds. We conducted experiments on sweet cherry flower buds using differential thermal analysis (DTA) and observed locations of ice formation in the bud structure. We also used anatomical development and water-soluble dye uptake throughout the overwintering period to identify changes that correlate with gain and loss of supercooling capacity. Our results revealed barriers to ice propagation are likely unique to each primordium, as inferred from exotherms produced from buds subjected to DTA, although multiple primordia may freeze simultaneously. Ice is accommodated between the bud scales and within the bud axis; however, full expression of supercooling was not dependent on the presence of scales. Anatomical and DTA studies revealed a correlation between vascular differentiation in primordia and loss of supercooling in the spring; these observations were at a higher temporal resolution than previously described for Prunus. Furthermore, disturbing tissues subtending the primordia interfered with typical patterns of supercooling, indicated more erratic and numerous exotherms produced during DTA. In summary, sweet cherry flower buds undergo extra-organ freezing. In winter, a barrier to ice propagation in the region directly subtending primordia protects the flower from freezing damage, but in the spring xylem differentiation in primordia provides a conduit for ice propagation that compromises supercooling.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Agriculture and Agri-Food Canada
Organisme : Natural Sciences and Engineering Research Council of Canada (NSERC)
ID : 9576
Organisme : Canadian Agricultural Partnership delivered by the Investment Agriculture Foundation of BC
Informations de copyright
© 2024 His Majesty the King in Right of Canada and The Author(s). Plant Biology published by John Wiley & Sons Ltd on behalf of German Society for Plant Sciences, Royal Botanical Society of the Netherlands. Reproduced with the permission of the Minister of Agriculture and Agri‐Food Canada.
Références
Andreini L., Viti R., Bartolini S., Ruiz D., Egea J., Campoy J.A. (2012) The relationship between xylem differentiation and dormancy evolution in apricot flower buds (Prunus armeniaca L.): the influence of environmental conditions in two Mediterranean areas. Trees, 26, 919–928.
Andrews P.K., Proebsting E.L. (1986) Development of deep supercooling in acclimating sweet cherry and peach flower buds. HortScience, 21, 99–100. https://doi.org/10.21273/HORTSCI.21.1.99
Andrews P.K., Proebsting E.L. (1987) Effects of temperature on the deep supercooling characteristics of dormant and deacclimating sweet cherry flower buds. Journal of the American Society for Horticultural Science, 112, 334–340. https://doi.org/10.21273/JASHS.112.2.334
Andrews P.K., Proebsting E.L., Gross D.C. (1986) Ice nucleation and supercooling in freeze‐sensitive peach and sweet cherry tissues. Journal of the American Society for Horticultural Science, 111, 232–236. https://doi.org/10.21273/JASHS.111.2.232
Ashworth E.N. (1982) Properties of peach flower buds which facilitate supercooling. Plant Physiology, 70, 1475–1479. https://doi.org/10.1104/pp.70.5.1475
Ashworth E.N. (1984) Xylem development in Prunus flower buds and the relationship to deep supercooling. Plant Physiology, 74, 862–865. https://doi.org/10.1104/pp.74.4.862
Ashworth E.N. (1990) The formation and distribution of ice within forsythia flower buds. Plant Physiology, 92, 718–725. https://doi.org/10.1104/pp.92.3.718
Ashworth E.N. (1992) Formation and spread of ice in plant tissues. Horticultural Reviews, 13, 215–255. https://doi.org/10.1002/9780470650509.ch6
Ashworth E.N., Davis G.A., Wisniewski M.E. (1989) The formation and distribution of ice within dormant and deacclimated peach flower buds. Plant, Cell & Environment, 12, 521–528. https://doi.org/10.1111/j.1365‐3040.1989.tb02125.x
Ashworth E.N., Rowse D.J. (1982) Vascular development in dormant Prunus flower buds and its relationship to supercooling. HortScience, 17, 790–791. https://doi.org/10.21273/HORTSCI.17.5.790
Ashworth E.N., Willard T.J., Malone S.R. (1992) The relationship between vascular differentiation and the distribution of ice within Forsythia flower buds. Plant, Cell & Environment, 15, 607–612. https://doi.org/10.1111/j.1365‐3040.1992.tb01495.x
Bartolini S., Giorgelli F. (1995) Observations on development of vascular connections in two apricot cultivars. Advances in Horticultural Science, 8, 91–100.
Callan N.W. (1990) Dormancy effects on supercooling in deacclimated “Meteor” tart cherry flower buds. Journal of the American Society for Horticultural Science, 115, 982–986. https://doi.org/10.21273/jashs.115.6.982
Charrier G., Ngao J., Saudreau M., Améglio T. (2015) Effects of environmental factors and management practices on microclimate, winter physiology, and frost resistance in trees. Frontiers in Plant Science, 6, 259. https://doi.org/10.3389/fpls.2015.00259
Endoh K., Kuwabara C., Arakawa K., Fujikawa S. (2014) Consideration of the reasons why dormant buds of trees have evolved extraorgan freezing as an adaptation for winter survival. Environmental and Experimental Botany, 106, 52–59. https://doi.org/10.1016/j.envexpbot.2014.02.008
Government of Canada (2023) Historical data. Available from https://climate.weather.gc.ca/historical_data/search_historic_data_e.html (accessed 1 April 2023).
Houghton E., Hannam K., Neilsen D., Nelson L.M. (2023a) Factors that influence measurements of sweet cherry (Prunus avium) flower bud cold hardiness obtained using differential thermal analysis. Canadian Journal of Plant Science, 103, 204–216. https://doi.org/10.1139/CJPS‐2023‐008
Houghton E., Noonan M.J., Hannam K., Nelson L.M., Neilsen D. (2023b) Models for estimating the cold hardiness of sweet cherry (Prunus avium cv. ‘Sweetheart’ and ‘Lapins’) in cold climate regions. HortScience, 58, 963–973. https://doi.org/10.21273/HORTSCI17128‐23
Ishikawa M., Ide H., Price Y., Arata T., Nakamura T., Kishimoto T. (2009) Freezing behaviours in plant tissue. In: Gusta L.V., Wisniewski M.E., Tanino K.K. (Eds), Plant cold hardiness: from the laboratory to the field. CABI, Oxfordshire, UK, pp 1–11.
Ishikawa M., Sakai A. (1981) Freezing avoidance mechanisms by supercooling in some Rhododendron flower buds with reference to water relations. Plant and Cell Physiology, 22, 953–967. https://doi.org/10.1093/oxfordjournals.pcp.a076259
Ishikawa M., Sakai A. (1982) Characteristics of freezing avoidance in comparison with freezing tolerance: a demonstration of extraorgan freezing. In: Li P.H., Sakai A. (Eds), Plant cold hardiness and freezing stress: mechanisms and crop implications. 2. Academic Press, New York, NY, pp 325–340.
Ishikawa M., Sakai A. (1985) Extraorgan freezing in wintering flower buds of Cornus officinalis Sieb. et Zucc. Plant, Cell and Environment, 8, 333–338. https://doi.org/10.1111/j.1365‐3040.1985.tb01407.x
Julian C., Herrero M., Rodrigo J. (2007) Flower bud drop and pre‐blossom frost damage in apricot (Prunus armeniaca L.). Journal of Applied Botany and Food Quality, 81, 21–25.
Kader S.A., Proebsting E.L. (1992) Freezing behavior of Prunus, subgenus Padus, flower buds. Journal of the American Society for Horticultural Science, 117, 955–960. https://doi.org/10.21273/JASHS.117.6.955
Kadir S.A., Proebsting E.L. (1993) Dead Prunus flower‐bud primordia retain deep‐supercooling properties. HortScience, 28, 831–832. https://doi.org/10.21273/HORTSCI.28.8.831
Kadir S.A., Proebsting E.L. (1994) Various freezing strategies of flower‐bud hardiness in Prunus. Journal of the American Society for Horticultural Science, 119, 584–588. https://doi.org/10.21273/JASHS.119.3.584
Kang S.K., Motosugi H., Yonemori K., Sugiura A. (1998) Supercooling characteristics of some deciduous fruit trees as related to water movement within the bud. The Journal of Horticultural Science and Biotechnology, 73, 165–172. https://doi.org/10.1080/14620316.1998.11510960
Kaya O., Kose C., Donderalp V., Gecim T., Taskın S. (2020) Last updates on cell death point, bud death time and exothermic characteristics of flower buds for deciduous fruit species by using differential thermal analysis. Scientia Horticulturae, 270, 1–12. https://doi.org/10.1016/j.scienta.2020.109403
Kaya O., Kose C., Gecim T. (2018) An exothermic process involved in the late spring frost injury to flower buds of some apricot cultivars (Prunus armenica L.). Scientia Horticulturae, 241, 322–328. https://doi.org/10.1016/j.scienta.2018.07.019
Keates S.E., Draper D.A., Hawkins C.D. (1990) FRDA Report 104: techniques for preparing plant tissues for optical and scanning electron microscopy. Forestry Canada and the British Columbia Ministry of Forests, BC, Canada. Available form https://a100.gov.bc.ca/pub/eirs/finishDownloadDocument.do;jsessionid=5F42EFBC1B31C763B0D317E83C1E0CAF?subdocumentId=12776. (accessed 21 June 2022)
Kovaleski A.P. (2022) Woody species do not differ in dormancy progression: differences in time to budbreak due to forcing and cold hardiness. Proceedings of the National Academy of Sciences of the United States of America, 119, e2112250119. https://doi.org/10.1073/pnas.2112250119
Kuprian E., Munkler C., Resnyak A., Zimmermann S., Tuong T.D., Gierlinger N., Müller T., Livingston D.P., 3rd, Neuner G. (2017) Complex bud architecture and cell‐specific chemical patterns enable supercooling of Picea abies bud primordia. Plant, Cell & Environment, 40, 3101–3112. https://doi.org/10.1111/pce.13078
Kuprian E., Tuong T.D., Pfaller K., Wagner J., Livingston D.P., Neuner G. (2016) Persistent supercooling of reproductive shoots is enabled by structural ice barriers being active despite an intact xylem connection. PLoS One, 11, e0163160. https://doi.org/10.1371/journal.pone.0163160
Liu J., Lindstrom O.M., Chavez D.J. (2019) Differential thermal analysis of ‘Elberta’ and ‘Flavorich’ peach flower buds to predict cold hardiness in Georgia. HortScience, 54, 676–683. https://doi.org/10.21273/HORTSCI13518‐18
Mathers H.M. (2004) Supercooling and cold hardiness in sour cherry germplasm: flower buds. Journal of the American Society for Horticultural Science, 129, 675–681. https://doi.org/10.21273/JASHS.129.5.0675
Mills L.J., Ferguson J.C., Keller M. (2006) Cold‐hardiness evaluation of grapevine buds and cane tissues. American Journal of Enology and Viticulture, 57, 194–200. https://doi.org/10.5344/ajev.2006.57.2.194
Neuner G., Hacker J. (2012) Ice formation and propagation in alpine plants, Plants in alpine regions. Springer, Vienna, Austria, pp 163–174. https://doi.org/10.1007/978‐3‐7091‐0136‐0_12
Pramsohler M., Neuner G. (2013) Dehydration and osmotic adjustment in apple stem tissue during winter as it relates to the frost resistance of buds. Tree Physiology, 33, 807–816. https://doi.org/10.1093/treephys/tpt057
Quamme H.A. (1978) Mechanism of supercooling in overwintering peach flower buds. Journal of the American Society for Horticultural Science, 103, 57–61. https://doi.org/10.21273/JASHS.103.1.57
Quamme H.A. (1983) Relationship of air temperature to water content and supercooling of overwintering peach flower buds. Journal of the American Society for Horticultural Science, 108, 697–701. https://doi.org/10.21273/JASHS.108.5.697
Quamme H.A. (1995) Deep supercooling in buds of woody plants. In: Lee R., Warren C., Gusta L. (Eds), Biological ice nucleation and its applications. APS Press, St. Paul, USA, pp 184–199.
Quamme H.A., Gusta L.V. (1987) Relationship of ice nucleation and water status to freezing patterns in dormant peach flower buds. HortScience, 22, 465–467.
Quamme H.A., Su W.A., Veto L.J. (1995) Anatomical features facilitating supercooling of the flower within the dormant peach flower bud. Journal of the American Society for Horticultural Science, 120, 814–822. https://doi.org/10.21273/JASHS.120.5.814
R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R‐project.org/ (accessed 1 September 2022)
Rossi S., Anfodillo T., Menardi R. (2006) Trephor: a new tool for sampling microcores from tree stems. IAWA Journal, 27, 89–97. https://doi.org/10.1163/22941932‐90000139
Sakai A. (1982) Extraorgan freezing of primordial shoots of winter buds of conifer. In: Li P.H., Sakai A. (Eds), Plant cold hardiness and freezing stress. Academic Press, New York, USA, pp 199–209. https://doi.org/10.1016/B978‐0‐12‐447602‐8.50020‐9
Savage J.A., Chuine I. (2021) Coordination of spring vascular and organ phenology in deciduous angiosperms growing in seasonally cold climates. New Phytologist, 230, 1700–1715. https://doi.org/10.1111/nph.17289
Sterle D.G., Caspari H.W., Minas I.S. (2023) Optimized differential thermal analysis sheds light on the effect of temperature on peach floral bud cold hardiness and transition from endo‐ to ecodormancy. Plant Science, 335, 111791. https://doi.org/10.1016/j.plantsci.2023.111791
Stone W., Idle D.B., Brennan R.M. (1993) Freezing events within overwintering buds of blackcurrant (Ribes nigrum L.). Annals of Botany, 72, 613–617. https://doi.org/10.1006/anbo.1993.1152
Wisniewski M., Gusta L., Neuner G. (2014) Adaptive mechanisms of freeze avoidance in plants: a brief update. Environmental and Experimental Botany, 99, 133–140. https://doi.org/10.1016/j.envexpbot.2013.11.011
Wisniewski M.E., Gusta L.V., Fuller M.P., Karlson D. (2009) Ice nucleation, propagation and deep supercooling: the lost tribes of freezing studies. In: Gusta L.V., Wisniewski M.E., Tanino K.K. (Eds), Plant cold hardiness: from the laboratory to the field. CABI, Oxfordshire, UK, pp 1–11.
Wittenbach V.A., Bukovac M.J. (1972) An anatomical and histochemical study of abscission in maturing sweet cherry fruit. Journal of the American Society for Horticultural Science, 97, 214–219. https://doi.org/10.21273/JASHS.97.2.214