Morphological changes to fruit development induced by GA3 application in sweet cherry (Prunus avium L.)Vignati, E., Caccamo, M., Dunwell, J. M. ORCID: https://orcid.org/0000-0003-2147-665X and Simkin, A. J. (2024) Morphological changes to fruit development induced by GA3 application in sweet cherry (Prunus avium L.). Plants, 13 (15). 20252. ISSN 2223-7747
It is advisable to refer to the publisher's version if you intend to cite from this work. See Guidance on citing. To link to this item DOI: 10.3390/plants13152052 Abstract/SummaryCherry (Prunus avium) fruits are important sources of vitamins, minerals, and nutrients in the human diet; however, they contain a large stone, making them inconvenient to eat ‘on the move’ and process. The exogenous application of gibberellic acid (GA3) can induce parthenocarpy in a variety of fruits during development. Here, we showed that the application of GA3 to sweet cherry unpollinated pistils acted as a trigger for fruit set and permitted the normal formation of fruit up to a period of twenty-eight days, indicating that gibberellins are involved in the activation of the cell cycle in the ovary wall cells, leading to fruit initiation. However, after this period, fruit development ceased and developing fruit began to be excised from the branch by 35 days post treatment. This work also showed that additional signals are required for the continued development of fully mature parthenocarpic fruit in sweet cherry.
DownloadsDownloads per month over past year
1. Faust, M.; Surányi, D. Origin and dissemination of cherry. Hortic. Rev. 1997, 19, 263–317.
2. Quero-García, J.; Schuster, M.; López-Ortega, G.; Charlot, G. Sweet cherry Varieties and Improvement; CABI International: Wallingford, UK, 2017; pp. 60–94.
3. Vignati, E.; Lipska, M.; Dunwell, J.M.; Caccamo, M.; Simkin, A.J. Fruit development in sweet cherry. Plants 2022, 11, 1531. https://doi.org/10.3390/plants11121531.
4. Bujdosó, G.; Hrotkó, K. Cherry Production; CABI International: Wallingford, UK, 2017; pp. 1–13.
5. Ganopoulou, M.; Michailidis, M.; Angelis, L.; Ganopoulos, I.; Molassiotis, A.; Xanthopoulou, A.; Moysiadis, T. Could causal discovery in proteogenomics assist in understanding gene-protein relations? A perennial fruit tree case study using sweet cherry as a model. Cells 2022, 11, 92.
6. Kappel, F.; Fisher-Fleming, B.; Hogue, E. Fruit characteristics and sensory attributes of an ideal sweet cherry. HortScience 1996, 31, 443–446. https://doi.org/10.21273/hortsci.31.3.443.
7. Zheng, X.; Yue, C.; Gallardo, K.; McCracken, V.; Luby, J.; McFerson, J. What attributes are consumers looking for in sweet cherries? Evidence from choice experiments. Agric. Resour. Econ. Rev. 2016, 45, 124–142. https://doi.org/10.1017/age.2016.13.
8. Guyer, D.E.; Sinha, N.K.; Chang, T.S.; Cash, J.N. Physiochemical and sensory characteristics of selected Michigan sweet cherry (Prunus avium L.) cultivars. J. Food Qual. 1993, 16, 355–370.
9. Cliff, M.A.; Dever, M.C.; Hall, J.W.; Giraud, B. Development and evaluation of multiple regression models for predicting sweet cherry liking. Food Res. Int. 1996, 28, 583–589.
10. Lyngstad, L.; Sekse, L. Economic aspects of developing a high sweet cherry product in Norway. ActaHortic. 1995, 379, 313–320.
11. Sekse, L.; Lyngstad, L. Strategies for maintaining high quality in sweet cherries during harvesting, handling and marketing. Acta Hortic. 1996, 410, 351–355.
12. Wermund, U.; Fearne, A. Key challenges facing the cherry supply chain in the UK. Acta Hortic. 2000, 536, 613–624.
13. Crisosto, C.H.; Crisosto, G.M.; Metheney, P. Consumer acceptance of ‘Brooks’ and ‘Bing’ cherries is mainly dependent on fruit SSC and visual skin color. Postharvest Biol. Technol. 2003, 28, 159–167. https://doi.org/10.1016/S0925-5214(02)00173-4.
14. Vignati, E.; Lipska, M.; Dunwell, J.M.; Caccamo, M.; Simkin, A.J. Options for the generation of seedless cherry, the ultimate snacking product. Planta 2022, 256, 90. https://doi.org/10.1007/s00425-022-04005-y.
15. Gustafson, F.G. Parthenocarpy: Natural and artificial. Bot. Rev. 1942, 8, 599–654.
16. Picarella, M.E.; Mazzucato, A. The occurrence of seedlessness in higher plants; Insights on roles and mechanisms of parthenocarpy. Front. Plant Sci. 2019, 9, 1997. https://doi.org/10.3389/fpls.2018.01997.
17. Schwabe, W.W.; Mills, J.J. Hormones and parthenocarpic fruit set: A literature survey. Hort. Abstr. 1981, 51, 661–698.
18. Sjut, V.; Bangerth, F. Induced parthenocarpy—A way of changing the levels of endogenous hormones in tomato fruits (Lycopersicon esculentum Mill.) 1. Extractable hormones. Plant Growth Regul. 1982, 1, 243–251. https://doi.org/10.1007/BF00024718.
19. Hedden, P.; Thomas, S.G. Gibberellin biosynthesis and its regulation. Biochem. J. 2012, 444, 11–25.
https://doi.org/10.1042/bj20120245.
20. Hedden, P. Gibberellin biosynthesis in higher plants. Annu. Plant Rev. 2016, 49, 37–72.
21. Hedden, P. The current status of research on gibberellin biosynthesis. Plant Cell Physiol. 2020, 61, 1832–1849.
https://doi.org/10.1093/pcp/pcaa092.
22. Zang, Y.-X.; Chun, I.-J.; Zhang, L.-L.; Hong, S.-B.; Zheng, W.-W.; Xu, K. Effect of gibberellic acid application on plant growth attributes, return bloom, and fruit quality of rabbiteye blueberry. Sci. Hortic. 2016, 200, 13–18. https://doi.org/10.1016/j.scienta.2015.12.057.
23. Garmendia, A.; Beltrán, R.; Zornoza, C.; García-Breijo, F.J.; Reig, J.; Merle, H. Gibberellic acid in Citrus spp. flowering and fruiting: A systematic review. PLoS ONE 2019, 14, e0223147. https://doi.org/10.1371/journal.pone.0223147.
24. Salazar-Cerezo, S.; Martínez-Montiel, N.; García-Sánchez, J.; Pérez, Y.T.R.; Martínez-Contreras, R.D. Gibberellin biosynthesis and metabolism: A convergent route for plants, fungi and bacteria. Microbiol. Res. 2018, 208, 85–98. https://doi.org/10.1016/j.micres.2018.01.010.
25. Yarushnykov, V.V.; Blanke, M.M. Alleviation of frost damage to pear flowers by application of gibberellin. Plant Growth Regul. 2005, 45, 21–27. https://doi.org/10.1007/s10725-004-6893-5.
26. Santos, R.C.d.; Pereira, M.C.T.; Mendes, D.S.; Sobral, R.R.S.; Nietsche, S.; Mizobutsi, G.P.; Santos, B.H.C.d. Gibberellic acid induces parthenocarpy and increases fruit size in the ‘Gefner’ custard apple (‘Annona cherimola’ × ‘Annona squamosa’). Aust. J. Crop Sci. 2016, 10, 314–321.
27. Galimba, K.D.; Bullock, D.G.; Dardick, C.; Liu, Z.; Callahan, A.M. Gibberellic acid induced parthenocarpic ‘Honeycrisp’ apples (Malus domestica) exhibit reduced ovary width and lower acidity. Hortic. Res. 2019, 6, 41. https://doi.org/10.1038/s41438-019-0124-8.
28. Lu, J.; Lamikanra, O.; Leong, S. Induction of seedlessness in ‘triumph’ muscadine grape (Vitis rotundifolia michx.) by applying gibberellic acid. Hortic. Sci. 1997, 32, 89–90. https://doi.org/10.21273/hortsci.32.1.89.
29. Or, E.; Oren, O.; Halaly-Basha, T.; Koilkonda, P.; Shi, Z.; Zheng, C.; Acheampong, A.K. Gibberellin induced shot berry formation in cv. early sweet is a direct consequence of high fruit set. Hortic. Res. 2020, 7, 169. https://doi.org/10.1038/s41438-020-00388-9.
30. Gultom, T.; Silitonga, D.Y. Effect of hormones gibberelin (GA 3) to produce parthenocarpy fruit on tomato tree (Solanum betaceum, Cav). IOP Conf. Ser. Mater. Sci. Eng. 2018, 420, 012074. https://doi.org/10.1088/1757-899X/420/1/012074.
31. Mesejo, C.; Yuste, R.; Reig, C.; Martínez-Fuentes, A.; Iglesias, D.J.; Muñoz-Fambuena, N.; Bermejo, A.; Germanà, M.A.; Primo-Millo, E.; Agustí, M. Gibberellin reactivates and maintains ovary-wall cell division causing fruit set in parthenocarpic Citrus species. Plant Sci. 2016, 247, 13–24. https://doi.org/10.1016/j.plantsci.2016.02.018.
32. Qian, C.; Ren, N.; Wang, J.; Xu, Q.; Chen, X.; Qi, X. Effects of exogenous application of CPPU, NAA and GA(4+7 ) on parthenocarpy and fruit quality in cucumber (Cucumis sativus L.). Food Chem. 2018, 243, 410–413. https://doi.org/10.1016/j.foodchem.2017.09.150.
33. Liu, L.; Wang, Z.; Liu, J.; Liu, F.; Zhai, R.; Zhu, C.; Wang, H.; Ma, F.; Xu, L. Histological, hormonal and transcriptomic reveal the changes upon gibberellin-induced parthenocarpy in pear fruit. Hortic. Res. 2018, 5, 1. https://doi.org/10.1038/s41438-017-0012-z.
34. Niu, Q.; Wang, T.; Li, J.; Yang, Q.; Qian, M.; Teng, Y. Effects of exogenous application of GA4+7 and N-(2-chloro-4-pyridyl)-N′-phenylurea on induced parthenocarpy and fruit quality in Pyrus pyrifolia ‘Cuiguan’. Plant Growth Regul. 2015, 76, 251–258.
https://doi.org/10.1007/s10725-014-9995-8.
35. Crane, J.C.; Primer, P.E.; Campbell, R.C. Gibberellin induced parthenocarpy in Prunus. Proc. Am. Soc. Hortic. Sci. 1960, 75, 129–137.
36. Wen, B.; Song, W.; Sun, M.; Chen, M.; Mu, Q.; Zhang, X.; Wu, Q.; Chen, X.; Gao, D.; Wu, H. Identification and characterization of cherry (Cerasus pseudocerasus G. Don) genes responding to parthenocarpy induced by GA3 through transcriptome analysis. BMC Genet. 2019, 20, 65. https://doi.org/10.1186/s12863-019-0746-8.
37. Tukey, H.B.; Young, J.O. Histological study of the developing fruit of the sour cherry. Bot. Gaz. 1939, 100, 723–749.
38. Singh, D.P.; Jermakow, A.M.; Swain, S.M. Gibberellins are required for seed development and pollen tube growth in Arabidopsis. Plant Cell 2002, 14, 3133–3147. https://doi.org/10.1105/tpc.003046.
39. Swain, S.M.; Reid, J.B.; Kamiya, Y. Gibberellins are required for embryo growth and seed development in pea. Plant J. 1997, 12, 1329–1338.
40. Tukey, H.B. Growth of the embryo, seed, and pericarp of the sour cherry (Prunus cerasus) in relation to season of fruit ripening. Proc. Am. Soc. Hortic. Sci. 1934, 31, 125–144.
41. Lilleland, O.; Newsome, L. A growth study of the cherry fruit. Proc. Am. Soc. Hortic. Sci. 1934, 32, 291–299.
42. Lilleland, O. Growth study of the peach fruit. Proc. Am. Soc. Hortic. Sci. 1935, 33, 269–279.
43. Lilleland, O. Growth study of the plum fruit-I. The growth and changes in chemical composition of the climax plum. Proc. Am. Soc. Hortic. Sci. 1933, 30, 203–208.
44. Varoquaux, F.; Blanvillain, R.; Delseny, M.; Gallois, P. Less is better: New approaches for seedless fruit production. Trends Biotechnol. 2000, 18, 233–242. https://doi.org/10.1016/s0167-7799(00)01448-7.
45. Gillaspy, G.; Ben-David, H.; Gruissem, W. Fruits: A developmental perspective. Plant Cell 1993, 5, 1439–1451.
https://doi.org/10.1105/tpc.5.10.1439.
46. Figueiredo, D.D.; Köhler, C. Bridging the generation gap: Communication between maternal sporophyte, female gametophyte and fertilization products. Curr. Opin. Plant Biol. 2016, 29, 16–20. https://doi.org/10.1016/j.pbi.2015.10.008.
47. Ingram, G.C. Family life at close quarters: Communication and constraint in angiosperm seed development. Protoplasma 2010, 247, 195–214. https://doi.org/10.1007/s00709-010-0184-y.
48. Chmielewski, F.-M.; Götz, K.-P. Performance of models for the beginning of sweet cherry blossom under current and changed climate conditions. Agric. For. Meteorol. 2016, 218–219, 85–91. https://doi.org/10.1016/j.agrformet.2015.11.022.
49. Carrera, E.; Ruiz-Rivero, O.; Peres, L.E.; Atares, A.; Garcia-Martinez, J.L. Characterization of the procera tomato mutant shows novel functions of the SlDELLA protein in the control of flower morphology, cell division and expansion, and the auxin-signaling pathway during fruit-set and development. Plant Physiol. 2012, 160, 1581–1596. https://doi.org/10.1104/pp.112.204552.
50. Martí, C.; Orzáez, D.; Ellul, P.; Moreno, V.; Carbonell, J.; Granell, A. Silencing of DELLA induces facultative parthenocarpy in tomato fruits. Plant J. 2007, 52, 865–876. https://doi.org/10.1111/j.1365-313X.2007.03282.x.
51. Livne, S.; Lor, V.S.; Nir, I.; Eliaz, N.; Aharoni, A.; Olszewski, N.E.; Eshed, Y.; Weiss, D. Uncovering DELLA-independent gibberellin responses by characterizing new tomato procera mutants. Plant Cell 2015, 27, 1579–1594.
https://doi.org/10.1105/tpc.114.132795.
52. Klap, C.; Yeshayahou, E.; Bolger, A.M.; Arazi, T.; Gupta, S.K.; Shabtai, S.; Usadel, B.; Salts, Y.; Barg, R. Tomato facultative parthenocarpy results from SlAGAMOUS-LIKE 6 loss of function. Plant Biotechnol. J. 2017, 15, 634–647.
https://doi.org/10.1111/pbi.12662.
53. Takisawa, R.; Nakazaki, T.; Nunome, T.; Fukuoka, H.; Kataoka, K.; Saito, H.; Habu, T.; Kitajima, A. The parthenocarpic gene Pat-k is generated by a natural mutation of SlAGL6 affecting fruit development in tomato (Solanum lycopersicum L.). BMC Plant Biol. 2018, 18, 72. https://doi.org/10.1186/s12870-018-1285-6.
54. Hu, J.; Israeli, A.; Ori, N.; Sun, T.-p. The interaction between DELLA and ARF/IAA mediates crosstalk between gibberellin and auxin signaling to control fruit initiation in tomato. Plant Cell 2018, 30, 1710–1728. https://doi.org/10.1105/tpc.18.00363.
55. Zhang, J.; Chen, R.; Xiao, J.; Qian, C.; Wang, T.; Li, H.; Ouyang, B.; Ye, Z. A single-base deletion mutation in SlIAA9 gene causes tomato (Solanum lycopersicum) entire mutant. J. Plant Res. 2007, 120, 671–678. https://doi.org/10.1007/s10265-007-0109-9.
56. Royo, C.; Torres-Pérez, R.; Mauri, N.; Diestro, N.; Cabezas, J.A.; Marchal, C.; Lacombe, T.; Ibáñez, J.; Tornel, M.; Carreño, J.; et al. The major origin of seedless grapes Is associated with a missense mutation in the MADS-Box gene VviAGL11. Plant Physiol. 2018, 177, 1234–1253. https://doi.org/10.1104/pp.18.00259.
57. Yao, J.-L.; Dong, Y.-H.; Morris, B.A.M. Parthenocarpic apple fruit production conferred by transposon insertion mutations in a MADS-box transcription factor. Proc. Natl. Acad. Sci. USA 2001, 98, 1306–1311. https://doi.org/10.1073/pnas.98.3.1306.
58. Ocarez, N.; Mejía, N. Suppression of the D-class MADS-box AGL11 gene triggers seedlessness in fleshy fruits. Plant Cell Rep. 2016, 35, 239–254. https://doi.org/10.1007/s00299-015-1882-x.
59. Fernandez, L.; Chaïb, J.; Martinez-Zapater, J.M.; Thomas, M.R.; Torregrosa, L. Mis-expression of a PISTILLATA-like MADS box gene prevents fruit development in grapevine. Plant J. 2013, 73, 918–928. https://doi.org/10.1111/tpj.12083.
60. IPCC. Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Inter-governmental Panel on Climate Change; Cambridge University Press: Cambridge, UK; New York, NY, USA, 2007.
61. IPCC. Summary for Policymakers. In Climate Change and Land: An IPCC Special Report on Climate Change, Desertifcation, Land Degradation, Sustainableland Management, Food Security, and Greenhouse Gas Fuxes in Terrestrial Ecosystems; Cambridge University Press: Cambridge, UK; New York, NY, USA., 2019.
62. Le Quéré, C.; Raupach, M.R.; Canadell, J.G.; Marland, G.; Bopp, L.; Ciais, P.; Conway, T.J.; Doney, S.C.; Feely, R.A.; Foster, P.; et al. Trends in the sources and sinks of carbon dioxide. Nat. Geosci. 2009, 2, 831–836. https://doi.org/10.1038/ngeo689.
63. Meinshausen, M.; Smith, S.J.; Calvin, K.; Daniel, J.S.; Kainuma, M.L.T.; Lamarque, J.F.; Matsumoto, K.; Montzka, S.A.; Raper, S.C.B.; Riahi, K.; et al. The RCP greenhouse gas concentrations and their extensions from 1765 to 2300. Clim. Change 2011, 109, 213. https://doi.org/10.1007/s10584-011-0156-z.
64. NASA. Global Climate Change: Vital Signs of the Planet. Available online: https://climate.nasa.gov/413ppmquotes (accessed on 1 June 2022).
65. IPCC. IPCC: Climate Change 2023: Synthesis Report. Contribution of Working Groups I, II and III to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change; IPCC: Geneva, Switzerland, 2023; pp. 35–115.
66. Doddrell, N.H.; Lawson, T.; Raines, C.A.; Wagstaff, C.; Simkin, A.J. Feeding the world: Impacts of elevated [CO2] on nutrient content of greenhouse grown fruit crops and options for future yield gains. Hortic. Res. 2023, 10, uhad026. https://doi.org/10.1093/hr/uhad026.
67. Herrero, M.; Rodrigo, J.; Wünsch, A. Flowering, Fruit Set and Development; CABI International: Wallingford, UK, 2017; pp. 14–35.
68. Rutkowski, K.; Łysiak, G.P. Weather conditions, orchard age and nitrogen fertilization influences yield and quality of ‘Łutówka’ Sour cherry fruit. Agriculture 2022, 12, 2008.
69. Gou, C.; Zhu, P.; Meng, Y.; Yang, F.; Xu, Y.; Xia, P.; Chen, J.; Li, J. Evaluation and genetic analysis of parthenocarpic germplasms in cucumber. Genes 2022, 13, 225.
70. Eeraerts, M.; Borremans, L.; Smagghe, G.; Meeus, I. A growers’ perspective on crop pollination and measures to manage the pollination service of wild pollinators in sweet cherry cultivation. Insects 2020, 11, 372.
71. Eeraerts, M.; Smsagghe, G.; Meeus, I. Pollinator diversity, floral resources and semi-natural habitat, instead of honey bees and intensive agriculture, enhance pollination service to sweet cherry. Agric. Ecosyst. Environ. 2019, 284, 106586.
https://doi.org/10.1016/j.agee.2019.106586.
72. Cong, L.; Yue, R.; Wang, H.; Liu, J.; Zhai, R.; Yang, J.; Wu, M.; Si, M.; Zhang, H.; Yang, C.; et al. 2,4-D-induced parthenocarpy in pear is mediated by enhancement of GA 4 biosynthesis. Physiol. Plant. 2019, 166, 812–820. https://doi.org/10.1111/ppl.12835.
73. Akšić, M.F.; Colić, S.; Meland, M.; Natić, M. Sugar and polyphenolic diversity in floral nectar of cherry. In Co-Evolution of Secondary Metabolites; Mérillon, J.-M., Ramawat, K.G., Eds.; Springer International Publishing: Cham, Switzerland, 2020; pp. 755–773. University Staff: Request a correction | Centaur Editors: Update this record |