Abstract
The ripening pattern of strawberry (Fragaria × ananassa) is different from other fruits, primarily because plant hormones affect the fruit’s quality in a different way than in other fruits. However, most studies on strawberries have focused on cultivation methods, control of pests and diseases, and breeding, and considerably less research has been done on hormones that determine strawberry internal quality. Even though strawberries have good indicators for gauging external quality, there is not enough data to for it to be related to internal quality. As such, we sought to better understand quality as strawberry fruit in specific six progressive developmental stages: flower buds, flowering, green fruits (GF), white fruits, pink fruits, and red fruits (RF). The internal quality and hormonal changes of ‘Seolhyang’ and ‘Maehyang’ cultivars were investigated on the basis of these developmental stages. This report highlights the changes in plant hormones that affect fruit ripening of ‘Seolhyang’ and ‘Maehyang’ cultivars. ABA, cytokinin, JA, and SA content increased gradually with maturity from the GF to the RF stage, while auxin content decreased gradually from GF to RF. Meanwhile, cytokinin and GA3 content exhibited fluctuations and differences between ‘Seolhyang’ and ‘Maehyang’ cultivars. The quality of strawberries was highest at the sixth (RF) stage in the both cultivars. Our results reveal that plant hormones play a role in the maturation of strawberry fruits and provide a foundation for their agricultural use in controlling the maturity of fruits.
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References
Adams-Phillips L, Barry C, Giovannoni J (2004) Signal transduction systems regulating fruit ripening. Trends Plant Sci 9:331–338. https://doi.org/10.1016/j.tplants.2004.05.004
AOAC (2000) Official methods of analysis, 17th edn. Washington, DC: Association of Analytical Chemists. Method no. 981.12 and 942.15
Archbold D, Dennis FJ (1984) Quantification of free ABA and free and conjugated IAA in strawberry achene and receptacle tissue during fruit development. J Am Soc Hortic Sci 109:330–335
Barry CS, McQuinn RP, Thompson AJ, Seymour GB, Grierson D, Giovannoni JJ (2005) Ethylene insensitivity conferred by the Green-ripe and Never-ripe 2 ripening mutants of tomato. Plant Physiol 138:267–275. https://doi.org/10.1104/pp.104.057745
Beril TJ, Fanzone M, Piccill P, Botany R (2011) Solar UV-B and ABA are involved in phenol metabolism of Vitis vinfera L. increasing biosynthesis of berry skin polyphenols. J Agric Food Chem 59:4874–4884. https://doi.org/10.1021/jf200040z
Chai YM, Jia HF, Li CL, Dong QH, Shen YY (2011) FaPYR1 is involved in strawberry fruit ripening. J Exp Bot 62:5079–5089. https://doi.org/10.1093/jxb/err207
Chou CM, Kao CH (1992) Methyl jasmonate, calcium, and leaf senscence in rice. Plant Physiol 99:1693–1694
Concha CM, Figueroa NE, Poblete LA, Oñate FA, Schwab W, Figueroa CR (2013) Methyl jasmonate treatment induces changes in fruit ripening by modifying the expression of several ripening genes in Fragaria chiloensis fruit. Plant Physiol Biochem 70:433–444. https://doi.org/10.1016/j.plaphy.2013.06.008
Eshghi S, Tafazoli E (2007) Possible role of cytokinins in flower induction in strawberry. Am J Plant Physiol 2:167–174. https://doi.org/10.3923/ajpp.2007.167.174
Frenkel C (1972) Involvement of peroxidase and indole-3-acetic acid oxidase isozyme from pear, tomato and blueberry fruits in ripening. Plant Physiol 49:757–763. https://doi.org/10.1104/pp.49.5.757
Giovannoni J (2001) Molecular biology of fruit maturation and ripening. Ann Rev Plant Physiol Plant Mol Biol 52:725–749. https://doi.org/10.1146/annurev.arplant.52.1.725
Given NK, Venis MA, Gierson D (1988) Hormonal regulation of ripening in the strawberry, a non-climacteric fruit. Planta 174:402–406. https://doi.org/10.1007/BF00959527
Griesser M, Vitzthum F, Fink B, Bellido ML, Raasch C, Munoz-Blanco J, Schwab W (2008) Multi-substrate flavonol O-glucosyltransferases from strawberry (Fragaria x ananassa) achene and receptacle. J Exp Bot 59:2611–2625. https://doi.org/10.1093/jxb/ern117
Gu T, Jia S, Huang X, Wang L, Fu W, Huo G, Gan L, Ding J, Li Y (2019) Transcriptome and hormone analyses provide insights into hormonal regulation in strawberry ripening. Planta. https://doi.org/10.1007/s00425-019-03155-w
Herde O, Pena-Cortes H, Willmitzer L, Fisahn J (1997) Stomatal responses to jasmonic acid, linolenic acid and abscisic acid in wild-type and ABA-deficient tomato plants. Plant, Cell Environ 20:136–141. https://doi.org/10.1046/j.1365-3040.1997.d01-11.x
Hong SJ, Lee SK (1996) Effects of cytokinin and gibberellin on ripening of tomato fruit. J Kor Soc Hortic Sci 37:374–379
Jia HF, Chai YM, Li CL, Lu D, Luo JJ, Qin L (2011) Abscisic acid plays an important role in the regulation of strawberry fruit ripening. Plant Physiol 157:183–199. https://doi.org/10.1104/pp.111.177311
Kang C, Darwish O, Geretz A, Shahan R, Alkharouf N, Liu Z (2013) Genome-scale transcriptomic insights into early-stage fruit development in woodland strawberry Fragaria vesca. Plant Cell 25:1960–1978. https://doi.org/10.1105/tpc.113.111732
Kim SK, Bae RN, Na HY, Ko KD, Chun CH (2013) Changes in physicochemical characteristics during fruit development in June-bearing strawberry cultivars. Hortic Environ Biotechnol 54:44–51. https://doi.org/10.1007/s13580-013-0166-z
Liao X, Li M, Liu B, Yan M, Yu X, Zi H, Liu R, Yamamuro C (2018) Interlinked regulatory loops of ABA catabolism and biosynthesis coordinate fruit growth and ripening in woodland strawberry. Proc Natl Acad Sci USA 115:E11542–E11550. https://doi.org/10.1073/pnas.1812575115
Meir S, Philosoph-Hadas S, Lurie S, Droby S, Akorman M, Zauberman G, Shapiro B, Cohen E, Fuchs L (1996) Reduction of chilling injury in stored avocado, grapefruit, and bell pepper by methyl jasmonate. Can J Bot 74:870–874. https://doi.org/10.1139/b96-108
Mukkun L, Singh Z (2009) Methyl jasmonate plays a role in fruit ripening of ‘Pajaro’ strawberry through stimulation of ethylene biosynthesis. Sci Hortic 123:5–10. https://doi.org/10.1016/j.scienta.2009.07.006
Nitsch JP (1950) Growth and morphogenesis of the strawberry as related to auxin. Am J Bot 37:211–215. https://doi.org/10.1002/j.1537-2197.1950.tb12183.x
Oh HD (2017) Abscisic acid stimulates softening and pigmentation of ‘Jersey’ highbush blueberry fruits during ripening. Master dissertation, Seoul National University. http://hdl.handle.net/10371/125614
Oh HD, Yu DJ, Chung SW, Chea S, Lee HJ (2018) Abscisic acid stimulates anthocyanin accumulation in ‘Jersey’ highbush blueberry fruits during ripening. Food Chem 244:403–407. https://doi.org/10.1016/j.foodchem.2017.10.051
Pan X, Welti R, Wang X (2010) Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography-mass spectrometry. Nat Protoc 5:986–992. https://doi.org/10.1038/nprot.2010.37
Park IK, Jang KS, Kim MK, Kim SD (1994) Circulation state of strawberry and quality changes during ripening. Kor J Post-Harvest Sci Technol Agri Products 1:45–53
Shen X, Zhao K, Liu L, Zhang K, Yuan H, Liao X (2014) A role for PacMYBA in ABA-regulated anthocyanin biosynthesis in red-coloured sweet cherry cv. Hong Deng (Prunus avium L.). Plant Cell Physiol 55:862–880. https://doi.org/10.1093/pcp/pcu013
Sohn EY, Kim YH, Kim JT, Jang SW, Lee IJ (2011) Changes in endogenous abscisic acid, jasmonic acid and sucrose content during bulb development in the cold-type cultivar of garlic (Allium sativum L.) of korea. Korean J Hortic Sci Technol 29:1–9
Symons GM, Chua YJ, Ross JJ, Quittenden LJ, Davies NW, Reid JB (2012) Hormonal changes during non-climacteric ripening in strawberry. J Exp Bot 63:4741–4750. https://doi.org/10.1093/jxb/ers147
Trainotti L, Pavanello A, Casadoro G (2005) Different ethylene receptors show an increased expression during the ripening of strawberries: does such an increment imply a role for ethylene in the ripening of these non-climacteric fruits? J Exp Bot 56:2037–2046. https://doi.org/10.1093/jxb/eri202
Tucker GA (1993) Introduction. In: Seymour GB, Taylor JE, Tucker GA (eds) Biochemistry of fruit ripening. Chapman and Hall, London, pp 1–52
Yamasaki A, Yamashita M (1993) Changes in endogenous cytokinins during flower induction of strawberry. Acta Hortic 345:93–99. https://doi.org/10.17660/ActaHortic.1993.345.12
Zhang XR, Luo GG, Wang RH, Wang J, Himelrick DG (2003) Growth the developmental responses of seeded and seedless grape berries to shoot girdling. J Am Soci Hortic Sci 128:316–323. https://doi.org/10.21273/JASHS.128.3.0316
Acknowledgements
This study was financially supported by the Korea Institute of Planning and Evaluation for Technology in Food, Agriculture, Forestry, and Fisheries (IPET) through the Agri-Bio Industry Technology Development Program funded by the Ministry of Agriculture, Food, and Rural Affairs (MAFRA) (315004-05-1-HD030). This work was supported by Pusan National University Research Grant, 201803330001. Thank you for funding for the research.
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GBL contributed to the Conception, Design, Analysis, Investigation, Methodology, and Drafting. JEL contributed to the Design, Analysis, Investigation, Methodology, and Drafting. JHL contributed to the Conception and Drafting. YJL contributed to the Conception, Design, and Methodology. YHP contributed to the Conception, Design, and Methodology. YWC contributed to the Conception, Design, and Methodology. BGS contributed to the Conception, Design, and Methodology. NJK contributed to the Design, Analysis, Investigation, and Methodology. BIJ contributed to the Conception, Design, Data curation, Analysis, Supervision, Funding acquisition, Investigation, Interpretation, Drafting, Revising, Agreement to be accountable for all aspects of the work, and Final approval. JSK contributed to the Conception, Design, Data curation, Analysis, Supervision, Funding acquisition, Investigation, Methodology, Interpretation, Drafting, Revising, Agreement to be accountable for all aspects of the work, and Final approval.
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Gyu-Bin Lee and Byoung Il Je share the first authorship.
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Lee, GB., Lee, JE., Lee, JH. et al. Phytohormone profiles of ‘Seolhyang’ and ‘Maehyang’ strawberry fruits during ripening. Hortic. Environ. Biotechnol. 61, 229–239 (2020). https://doi.org/10.1007/s13580-019-00213-w
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DOI: https://doi.org/10.1007/s13580-019-00213-w