Roles of abscisic acid in regulating ripening and quality of strawberry, a model non-climacteric fruit

Abstract

Abscisic acid (ABA) is a dominant regulator of ripening and quality in non-climacteric fruits. Strawberry is regarded as a model non-climacteric fruit due to its extensive genetic studies and proven suitability for transgenic approaches to understanding gene function. Strawberry research has contributed to studies on color, flavor development, and fruit softening, and in recent years ABA has been established as a core regulator of strawberry fruit ripening, whereas ethylene plays this role in climacteric fruits. Despite this major difference, several components of the interacting genetic regulatory network in strawberry, such as MADS-box and NAC transcription factors, are similar to those that operate in climacteric fruit. In this review, we summarize recent advances in understanding the role of ABA biosynthesis and signaling and the regulatory network of transcription factors and other phytohormones in strawberry fruit ripening. In addition to providing an update on its ripening, we discuss how strawberry research has helped generate a broader and more comprehensive understanding of the mechanism of non-climacteric fruit ripening and focus attention on the use of strawberry as a model platform for ripening studies.

References

[1] Cheng J, Niu Q, Zhang B et al. Downregulation of RdDM during strawberry fruit ripening. Genome Biol. 2018; 19: 212.

[2] Fan Z, Hasing T, Johnson TS et al. Strawberry sweetness and consumer preference are enhanced by specific volatile compounds. Hortic Res. 2021; 8: 66.

[3] Fenn MA, Giovannoni JJ . Phytohormones in fruit development and maturation. Plant J. 2021; 105: 446-58.

[4] Bai Q, Huang Y, Shen Y et al. The physiological and molecular mechanism of abscisic acid in regulation of fleshy fruit ripening. Front Plant Sci. 2021; 11: 619953.

[5] Li S, Zhu B, Pirello J et al. Roles of RIN and ethylene in tomato fruit ripening and ripening-associated traits. New Phytol. 2020; 226: 460-75.

[6] Leng P, Yuan B, Guo Y et al. The role of abscisic acid in fruit ripening and responses to abiotic stress. J Exp Bot. 2014; 65: 4577-88.

[7] Kou X, Zhou JQ, Wu CE et al. The interplay between ABA/ethylene and NAC TFs in tomato fruit ripening: a review. Plant Mol Biol. 2021; 106: 223-38.

[8] Kou X, Yang S, Chai L et al. Abscisic acid and fruit ripening: multifaceted analysis of the effect of abscisic acid on fleshy fruit ripening. Sci Hortic. 2021; 281: 109999.

[9] Bianchetti R, De Luca B, de Haro LA et al. Phytochrome-dependent temperature perception modulates isoprenoid metabolism. Plant Physiol. 2020; 183: 869-82.

[10] Tang D, Gallusci P, Lang Z et al. Fruit development and epigenetic modifications. New Phytol. 2020; 228: 839-44.

[11] Brumos J . Gene regulation in climacteric fruit ripening. Curr Opin Plant Biol. 2021; 63: 102042.

[12] Li S, Chen K, Grierson D et al. Molecular and hormonal mechanisms regulating fleshy fruit ripening. Cell. 2021; 10: 1136.

[13] Liu Y, Tang M, Liu M et al. The molecular regulation of ethylene in fruit ripening. Small Methods. 2020; 4: 1900485.

[14] Fan ZQ, Ba LJ, Shan W et al. A banana R2R3-MYB transcription factor MaMYB3 is involved in fruit ripening through modulation of starch degradation by repressing starch degradation-related genes and MabHLH6 . Plant J. 2018; 96: 1191-205.

[15] Guo J, Cao K, Deng C et al. An integrated peach genome structural variation map uncovers genes associated with fruit traits. Genome Biol. 2020; 21: 258.

[16] Shan W, Kuang JF, Wei W et al. MaXB3 modulates MaNAC2, MaACS1, and MaACO1 stability to repress ethylene biosynthesis during banana fruit ripening. Plant Physiol. 2020; 184: 1153-71.

[17] Cao X, Wei C, Duan W et al. Transcriptional and epigenetic analysis reveals that NAC transcription factors regulate fruit flavor ester biosynthesis. Plant J. 2021; 106: 785-800.

[18] Xing S, Chen K, Zhu H et al. Fine-tuning sugar content in strawberry. Genome Biol. 2020; 21: 230.

[19] Zeng B, Li T, Wang W et al. An effector-reporter system to study cellular signal transduction in strawberry fruit (Fragaria ananassa) . Hortic Res. 2020; 8: 60.

[20] Cheng J, Wen S, Xiao S et al. Overexpression of the tonoplast sugar transporter CmTST2 in melon fruit increases sugar accumulation. J Exp Bot. 2018; 69: 511-23.

[21] Gaston A, Osorio S, Denoyes B et al. Applying the Solanaceae strategies to strawberry crop improvement. Trends Plant Sci. 2020; 25: 130-40.

[22] Peng Q, Cai Y, Lai E et al. The sucrose transporter MdSUT4.1 participates in the regulation of fruit sugar accumulation in apple. BMC Plant Biol. 2020; 20: 191.

[23] Liston A, Cronn R, Ashman TL et al. Fragaria: a genus with deep historical roots and ripe for evolutionary and ecological insights . Am J Bot. 2014; 101: 1686-99.

[24] Zhou J, Wang G, Liu Z et al. Efficient genome editing of wild strawberry genes, vector development and validation. Plant Biotechnol J. 2018; 16: 1868-77.

[25] Zhou J, Li D, Wang G et al. Application and future perspective of CRISPR/Cas9 genome editing in fruit crops. J Integr Plant Biol. 2020; 62: 269-86.

[26] Fait A, Hanhineva K, Beleggia R et al. Reconfiguration of the achene and receptacle metabolic networks during strawberry fruit development. Plant Physiol. 2008; 148: 730-50.

[27] Gu T, Jia S, Huang X et al. Transcriptome and hormone analyses provide insights into hormonal regulation in strawberry ripening. Planta. 2019; 250: 145-62.

[28] Liao X, Li M, Liu B et al. Interlinked regulatory loops of ABA catabolism and biosynthesis coordinate fruit growth and ripening in woodland strawberry. PNAS Nexus. 2018; 115: E11542-50.

[29] Jia HF, Chai YM, Li CL et al. Abscisic acid plays an important role in the regulation of strawberry fruit ripening. Plant Physiol. 2011; 157: 188-99.

[30] Jia H, Jiu S, Zhang C et al. Abscisic acid and sucrose regulate tomato and strawberry fruit ripening through the abscisic acid-stress-ripening transcription factor. Plant Biotechnol J. 2016; 14: 2045-65.

[31] Tan BC, Joseph LM, Deng WT et al. Molecular characterization of the Arabidopsis 9- cis epoxycarotenoid dioxygenase gene family . Plant J. 2003; 35: 44-56.

[32] Yuan H, Yu H, Huang T et al. The complexity of the Fragaria x ananassa (octoploid) transcriptome by single-molecule long-read sequencing . Hortic Res. 2019; 6: 46.

[33] Kadomura-Ishikawa Y, Miyawaki K, Takahashi A et al. Light and abscisic acid independently regulated FaMYB10 in Fragaria × ananassa fruit . Planta. 2015; 241: 953-65.

[34] Medina-Puche L, Molina-Hidalgo FJ, Boersma M et al. An R2R3-MYB transcription factor regulates eugenol production in ripe strawberry fruit receptacles. Plant Physiol. 2015; 168: 598-614.

[35] Molina-Hidalgo FJ, Puche LM, Gelis S et al. Functional characterization of FaNIP1;1 gene, a ripening-related and receptacle-specific aquaporin in strawberry fruit. Plant Sci. 2015; 238: 198-211.

[36] Chen K, Li GJ, Bressan RA et al. Abscisic acid dynamics, signaling, and functions in plants. J Integr Plant Biol. 2020; 62: 25-54.

[37] Xu ZJ, Nakajima M, Suzuki Y et al. Cloning and characterization of the abscisic acid-specific glucosyltransferase gene from adzuki bean seedlings. Plant Physiol. 2002; 129: 1285-95.

[38] Lee KH, Piao HL, Kim HY et al. Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell. 2006; 126: 1109-20.

[39] Okamoto M, Kuwahara A, Seo M et al. CYP707A1 and CYP707A2, which encode abscisic acid 8′-hydroxylases, are indispensable for proper control of seed dormancy and germination in Arabidopsis . Plant Physiol. 2006; 141: 97-107.

[40] Figueroa NE, Hoffman T, Olbricht K et al. Contrasting dynamics in abscisic acid metabolism in different Fragaria spp. during fruit ripening and identification of the enzymes involved. J Exp Bot. 2021; 72: 1245-59.

[41] Kim J, Lee JG, Hong Y et al. Analysis of eight phytohormone concentrations, expression levels of ABA biosynthesis genes, and ripening-related transcription factors during fruit development in strawberry. J Plant Physiol. 2019; 239: 52-60.

[42] Zhang SH, Sun JH, Dong YH et al. Enzymatic and functional analysis of β-glucosidase FaBG1 during strawberry fruit ripening. J Hortic Sci Biotechnol. 2014; 89: 733-9.

[43] Li Q, Ji K, Sun Y et al. The role of FaBG3 in fruit ripening and B. cinerea fungal infection of strawberry . Plant J. 2013; 76: 24-35.

[44] Castillejo C, Waurich V, Wagner H et al. Allelic variation of MYB10 is the major force controlling natural variation in skin and flesh color in strawberry (Fragaria spp.) fruit. Plant Cell. 2020; 32: 3723-49.

[45] Zhang Z, Shi Y, Ma Y et al. The strawberry transcription factor FaRAV1 positively regulates anthocyanin accumulation by activation of FaMYB10 and anthocyanin pathway genes. Plant Biotechnol J. 2020; 18: 2267-79.

[46] Medina-Puche L, Cumplido-Laso G, Amil-Ruiz F et al. MYB10 plays a major role in the regulation of flavonoid/phenylpropanoid metabolism during ripening of Fragaria × ananassa fruits . J Exp Bot. 2014; 65: 401-17.

[47] Li D, Li L, Luo Z et al. Comparative transcriptome analysis reveals the influence of abscisic acid on the metabolism of pigments, ascorbic acid and folic acid during strawberry fruit ripening. PLoS One. 2015; 10: e0130037.

[48] Liu HT, Ji Y, Liu Y et al. The sugar transporter system of strawberry: genome-wide identification and expression correlation with fruit soluble sugar-related traits in a Fragaria × ananassa germplasm collection . Hortic Res. 2020; 7: 132.

[49] Ma QJ, Sun MH, Liu YJ et al. Molecular cloning and functional characterization of the apple sucrose transporter gene MdSUT2. Plant Physiol Biochem. 2016; 109: 442-51.

[50] Chen JY, Liu DJ, Jiang YM et al. Molecular characterization of a strawberry FaASR gene in relation to fruit ripening. PLoS One. 2011; 6: e24649.

[51] Luo Y, Ge C, Yang M et al. Cytosolic/plastid glyceraldehyde-3-phosphate dehydrogenase is a negative regulator of strawberry fruit ripening. Genes. 2020; 11: 580.

[52] Raab T, Lopez-Raez JA, Klein D et al. FaQR, required for the biosynthesis of the strawberry flavor compound 4-hydroxy-2,5-dimethyl-3(2H)-furanone, encodes an enone oxidoreductase . Plant Cell. 2006; 18: 1023-37.

[53] Han Y, Dang R, Li J et al. SUCROSE NONFERMENTING1-RELATED PROTEIN KINASE2.6, an ortholog of OPEN STOMATA1, is a negative regulator of strawberry fruit development and ripening. Plant Physiol. 2015; 167: 915-30.

[54] Han SY, Kitahata N, Saito T et al. A new lead compound for abscisic acid biosynthesis inhibitors targeting 9- cis-epoxycarotenoid dioxygenase . Bioorg Med Chem Lett. 2004; 14: 3033-6.

[55] Molina-Hidalgo FJ, Medina-Puche L, Cañete-Gomez C et al. The fruit-specific transcription factor FaDOF2 regulates the production of eugenol in ripe fruit receptacles. J Exp Bot. 2017; 68: 4529-43.

[56] Morales-Quintana L, Ramos P . Chilean strawberry (Fragaria chiloensis): an integrative and comprehensive review . Food Res Int. 2019; 119: 769-76.

[57] Molina-Hidalgo FJ, Franco AR, Villatoro C et al. The strawberry (Fragaria × ananassa) fruit-specific rhamnogalacturonate lyase 1 (FaRGLyase1) gene encodes an enzyme involved in the degradation of cell-wall middle lamellae . J Exp Bot. 2013; 64: 1471-83.

[58] Paniagua C, Blanco-Portales R, Barcelo-Muñoz M et al. Antisense down-regulation of the strawberry β-galactosidase gene FaβGal4 increases cell wall galactose levels and reduces fruit softening. J Exp Bot. 2016; 67: 619-31.

[59] Bustamante CA, Civello PM, Martinez GA et al. Cloning of the promoter region of β-xylosidase (FaXyl1) gene and effect of plant growth regulators on the expression of FaXyl1 in strawberry fruit. Plant Sci. 2009; 177: 49-56.

[60] Opazo MC, Lizana R, Pimentel P et al. Changes in the mRNA abundance of FcXTH1 and FcXTH2 promoted by hormonal treatments of Fragaria chiloensis fruit . Postharvest Biol Technol. 2013; 77: 28-34.

[61] Nardi CF, Villarreal N, Opazo C et al. Expression of FaXTH1 and FaXTH2 genes in strawberry fruit. Cloning of promoter regions and effect of plant growth regulators . Sci Hortic. 2014; 165: 111-22.

[62] Nardi CF, Villarreal NM, Dotto MC et al. Influence of plant growth regulators on Expansin2 expression in strawberry fruit. Cloning and functional analysis of FaEXP2 promoter region . Postharvest Biol Technol. 2016; 114: 17-28.

[63] Daminato M, Guzzo F, Casador G et al. A SHATTERPROOF-like gene controls ripening in non-climacteric strawberries, and auxin and abscisic acid antagonistically affect its expression. J Exp Bot. 2013; 64: 3775-86.

[64] Lu W, Chen J, Ren X et al. One novel strawberry MADS-box transcription factor FaMADS1a acts as a negative regulator in fruit ripening. Sci Hortic. 2018; 227: 124-31.

[65] Martín-Pizarro C, Vallarino JG, Osorio S et al. The NAC transcription factor FaRIF controls fruit ripening in strawberry. Plant Cell. 2021; 33: 1574-93.

[66] Moyano E, Martinez-Rivas FJ, Blanco-Portaes R et al. Genome-wide analysis of the NAC transcription factor family and their expression during the development and ripening of the Fragaria × ananassa fruits . PLoS One. 2018; 13: e0196953.

[67] Symons GM, Chua YJ, Ross JJ et al. Hormonal changes during non-climacteric ripening in strawberry. J Exp Bot. 2012; 63: 4741-50.

[68] Luo Y, Ge C, Ling Y et al. ABA and sucrose co-regulate strawberry fruit ripening and show inhibition of glycolysis. Mol Gen Genomics. 2020; 295: 421-38.

[69] Yoshida T, Fernie AR, Shimozaki K et al. Long-distance stress and developmental signals associated with abscisic acid signaling in environmental responses. Plant J. 2021; 105: 477-88.

[70] Fujii H, Chinnusamy V, Rodrigues A et al. In vitro reconstitution of an abscisic acid signalling pathway . Nature. 2009; 462: 660-4.

[71] Melcher K, Ng LM, Zhou XE et al. A gate-latch-lock mechanism for hormone signaling by abscisic acid receptors. Nature. 2009; 462: 602-8.

[72] Nakashima K, Fujita Y, Kanamori N et al. Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant Cell Physiol. 2009; 50: 1345-63.

[73] Umezawa T, Sugiyama N, Mizoguchi M et al. Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis . PNAS Nexus. 2009; 106: 17588-93.

[74] Shinozawa A, Otake R, Takezawa D et al. SnRK2 protein kinases represent an ancient system in plants for adaptation to a terrestrial environment. Commun Biol. 2019; 2: 30.

[75] Shang Y, Yan L, Liu ZQ et al. The Mg-chelatase H subunit of Arabidopsis antagonizes a group of WRKY transcription repressors to relieve ABA-responsive genes of inhibition. Plant Cell. 2010; 22: 1909-35.

[76] Li C, Jia H, Chai Y et al. Abscisic acid perception and signaling transduction in strawberry: a model for non-climacteric fruit ripening. Plant Signal Behav. 2011; 6: 1950-3.

[77] Chai YM, Jia HF, Li CL et al. FaPYR1 is involved in strawberry fruit ripening. J Exp Bot. 2011; 62: 5079-89.

[78] Jia H, Lu D, Sun JH et al. Type 2C protein phosphatase ABI1 is a negative regulator of strawberry fruit ripening. J Exp Bot. 2013; 64: 1677-87.

[79] Hou BZ, Chen XH, Shen YY et al. Interactions between strawberry ABA receptor PYR/PYLs and protein phosphatase PP2Cs on basis of transcriptome and yeast two-hybrid analyses. J Plant Growth Regul. 2021; 40: 594-602.

[80] Jia M, Ding N, Zhang Q et al. A FERONIA-like receptor kinase regulates strawberry (Fragaria × ananassa) fruit ripening and quality formation. Front Plant Sci. 2017; 8: 1099.

[81] Zhang S . Sigma factor FaSigE positively regulates strawberry fruit ripening by ABA. Plant Growth Regul. 2017; 83: 417-27.

[82] Hou BZ, Xu C, Shen YY et al. A leu-rich repeat receptor-like protein kinase, FaRIPK1, interacts with the ABA receptor, FaABAR, to regulate fruit ripening in strawberry. J Exp Bot. 2018; 69: 1569-82.

[83] Chai L, Shen YY . FaABI4 is involved in strawberry fruit ripening. Sci Hortic. 2016; 210: 34-40.

[84] Vallarino JG, Osorio S, Bombarely A et al. Central role of FaGAMYB in the transition of the strawberry receptacle from development to ripening. New Phytol. 2015; 208: 482-96.

[85] Concha CM, Figueroa NE, Poblete LA et al. Methyl jasmonate treatment induces changes in fruit ripening by modifying the expression of several ripening genes in Fragaria chiloensis fruit. Plant Physiol Biochem. 2013; 70: 433-44.

[86] Li Z, Wang Z, Wang K et al. Co-expression network analysis uncovers key candidate genes related to the regulation of volatile esters accumulation in woodland strawberry. Planta. 2020; 252: 55.

[87] Li S, Chen K, Grierson D . A critical evaluation of the role of ethylene and MADS transcription factors in the network controlling fleshy fruit ripening. New Phytol. 2019; 221: 1724-41.

[88] Seymour GB, Ryder CD, Cevik V et al. A SEPALLATA gene is involved in the development and ripening of strawberry (Fragaria × ananassa Duch.) fruit, a non-climacteric tissue . J Exp Bot. 2011; 62: 1179-88.

[89] Vrebalov J, Ruezinksy D, Padmanabhan V et al. A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (Rin) locus. Science. 2002; 296: 343-6.

[90] Qi X, Liu C, Song L et al. PaMADS7, a MADS-box transcription factor, regulates sweet cherry fruit ripening and softening. Plant Sci. 2020; 301: 110634.

[91] Fu CC, Chen HJ, Gao HY et al. Papaya CpMADS4 and CpNAC3 cooperatively regulate ethylene signal genes CpERF9 and CpEIL5 during fruit ripening . Postharvest Biol Technol. 2021; 175: 111485.

[92] Vallarino JG, Merchante C, Sanchez-Sevilla JF et al. Characterizing the involvement of FaMADS9 in the regulation of strawberry fruit receptacle development. Plant Biotechnol J. 2020; 18: 929-43.

[93] Lang Z, Wang Y, Tang K et al. Critical roles of DNA demethylation in the activation of ripening-induced genes and inhibition of ripening-repressed genes in tomato fruit. PNAS Nexus. 2017; 114: E4511-9.

[94] Zhou L, Tian S, Qin G et al. RNA methylomes reveal the m⁶A-mediated regulation of DNA demethylase gene SlDML2 in tomato fruit ripening. Genome Biol. 2019; 20: 156.

[95] Zhou L, Tang R, Li X et al. N⁶-methyladenosine RNA modification regulates strawberry fruit ripening in an ABA-dependent manner . Genome Biol. 2021; 22: 168.

[96] Pan J, Hu Y, Wang H et al. Molecular mechanism underlying the synergetic effect of jasmonate on abscisic acid signaling during seed germination in Arabidopsis . Plant Cell. 2020; 32: 3846-65.

[97] Aerts N, Mendes MP, Van Wees SCM et al. Multiple levels of crosstalk in hormone networks regulating plant defense. Plant J. 2021; 105: 489-504.

[98] Xie Q . Abscisic acid regulates the root growth trajectory by reducing auxin transporter PIN2 protein levels in Arabidopsis thaliana . Front Plant Sci. 2021; 12: 632676.

[99] Kang C, Darwish O, Geretz A et al. Genome-scale transcriptomic insights into early-stage fruit development in woodland strawberry Fragaria vesca . Plant Cell. 2013; 25: 1960-78.

[100] Estrada-Johnson E, Csukasi F, Pizarro CM et al. Transcriptomic analysis in strawberry fruits reveals active auxin biosynthesis and signaling in the ripe receptacle. Front Plant Sci. 2017; 8: 889.

[101] Zhou J, Sittman J, Guo L et al. Gibberellin and auxin signaling genes RGA1 and ARF8 repress accessory fruit initiation in diploid strawberry . Plant Physiol. 2021; 185: 1059-75.

[102] Perkins-Veazie P. Growth and ripening of strawberry fruit. In: Janick J, ed. Horticultural Reviews, Vol. 17.John Wiley & Sons, 1995.

[103] Medina-Puche L, Blanco-Portales R, Molina-Hidalgo FJ et al. Extensive transcriptomic studies on the roles played by abscisic acid and auxins in the development and ripening of strawberry fruits. Funct Integr Genomics. 2016; 16: 671-92.

[104] Aharoni A, Keizer LCP, Van Den Broeck HC et al. Novel insight into vascular, stress, and auxin-dependent and -independent gene expression programs in strawberry, a non-climacteric fruit. Plant Physiol. 2002; 129: 1019-31.

[105] Figueroa RC, Pimentel P, Dotto M et al. Expression of five expansin genes during softening of Fragaria chiloensis fruit: effect of auxin treatment. Postharvest Biol Technol. 2009; 53: 51-7.

[106] Barbez E, Kubes M, Rolcik J et al. A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants. Nature. 2012; 485: 119-22.

[107] Given NK, Venis MA, Gierson D et al. Hormonal regulation of ripening in the strawberry, a non-climacteric fruit. Planta. 1988; 174: 402-6.

[108] Manning K. Changes in gene expression during strawberry fruit ripening and their regulation by auxin. Planta. 1994; 194: 62-8.

[109] Feng J, Dai C, Luo H et al. Reporter gene expression reveals precise auxin synthesis sites during fruit and root development in wild strawberry. J Exp Bot. 2019; 70: 563-74.

[110] Thompson PA . The effect of applied growth substances on development of the strawberry fruit. II. Interactions of auxins and gibberellins. J Exp Bot. 1969; 20: 629-47.

[111] Csukasi F, Osorio S, Gutierrez JR et al. Gibberellin biosynthesis and signalling during development of the strawberry receptacle. New Phytol. 2011; 191: 376-90.

[112] Martínez GA, Chaves AR, Añon MC et al. Effect of exogenous application of gibberellic acid on color change and phenylalanine ammonia-lyase, chlorophyllase, and peroxidase activities during ripening of strawberry fruit (Fragaria × ananassa Duch.) . J Plant Growth Regul. 1996; 15: 139-46.

[113] Csukasi F, Donaire L, Casañal A et al. Two strawberry miR159 family members display developmental-specific expression patterns in the fruit receptacle and cooperatively regulate FaGAMYB . New Phytol. 2012; 195: 47-57.

[114] Lü P, Yu S, Zhu N et al. Genome encode analyses reveal the basis of convergent evolution of fleshy fruit ripening. Nat Plants. 2018; 4: 784-91.

[115] Jiang Y, Joyce DC . ABA effects on ethylene production, PAL activity, anthocyanin and phenolic contents of strawberry fruit. Plant Growth Regul. 2003; 39: 171-4.

[116] Villarreal NM, Bustamante CA, Civello PM et al. Effect of ethylene and 1-MCP treatments on strawberry fruit ripening. J Sci Food Agric. 2010; 90: 683-9.

[117] Merchante C, Vallarino JG, Osorio S et al. Ethylene is involved in strawberry fruit ripening in an organ-specific manner. J Exp Bot. 2013; 64: 4421-39.

[118] Sun JH, Figueroa CR, Nair H et al. New evidence for the role of ethylene in strawberry fruit ripening. J Plant Growth Regul. 2013; 32: 461-70.

[119] Elmi F, Pradas I, Tosetti R et al. Effect of ethylene on postharvest strawberry fruit tissue biochemistry. Acta Hortic. 2017; 1156: 667-72.

[120] Guo J, Wang S, Yu X et al. Polyamines regulate strawberry fruit ripening by abscisic acid, auxin, and ethylene. Plant Physiol. 2018; 177: 339-51.

[121] Figueroa NE, Gatica-Melendez C, Figueroa CR et al. Ethylene application at the immature stage of Fragaria chiloensis fruit represses the anthocyanin biosynthesis with a concomitant accumulation of lignin. Food Chem. 2021; 358: 129913.

[122] Luo Y, Lin Y, Mo F et al. Sucrose promotes strawberry fruit ripening and affects ripening-related processes. Int J Genomics. 2019; 2019: 9203057.

[123] Reis L, Forney CF, Jordan M et al. Metabolic profile of strawberry fruit ripened on the plant following treatment with an ethylene elicitor or inhibitor. Front Plant Sci. 2020; 11: 995.

[124] Tosetti R, Elmi F, Pradas I et al. Continuous exposure to ethylene differentially affects senescence in receptacle and achene tissues in strawberry fruit. Front Plant Sci. 2020; 11: 174.

[125] Pérez AG, Sanz C, Olias R et al. Effect of methyl jasmonate on in vitro strawberry ripening. J Agric Food Chem. 1997; 45: 3733-7.

[126] Delgado LD, Zuñiga PE, Figueroa NE et al. Application of a JA-Ile biosynthesis inhibitor to methyl jasmonate-treated strawberry fruit induces upregulation of specific MBW complex-related genes and accumulation of proanthocyanidins. Molecules. 2018; 23: 1433.

[127] Han Y, Chen C, Yan Z et al. The methyl jasmonate accelerates the strawberry fruits ripening process. Sci Hortic. 2019; 249: 250-6.

[128] Garrido-Bigotes A, Figueroa PM, Figueroa CR et al. Jasmonate metabolism and its relationship with abscisic acid during strawberry fruit development and ripening. J Plant Growth Regul. 2018; 37: 101-13.

[129] Jia H, Wang Y, Sun M et al. Sucrose functions as a signal involved in the regulation of strawberry fruit development and ripening. New Phytol. 2013; 198: 453-65.

[130] Pál M, Szalai G, Gondor OK et al. Unfinished story of polyamines: role of conjugation, transport and light-related regulation in the polyamine metabolism in plants. Plant Sci. 2021; 308: 110923.

[131] Mo A, Xu T, Bai Q et al. FaPAO5 regulates Spm/Spd levels as a signaling during strawberry fruit ripening. Plant Direct. 2020; 4: e00217.

[132] Perin E, da Silva Messias R, Borowski JM et al. ABA-dependent salt and drought stress improve strawberry fruit quality. Food Chem. 2019; 271: 516-26.

[133] Galli V, Perin EC, da Silva Messias R et al. Mild salt stress improves strawberry fruit quality. LWT. 2016; 73: 693-9.

[134] Seymour GB, Granell A . Fruit development and ripening. Annu Rev Plant Biol. 2013; 64: 219-41.

[135] Qi WY, Wang H, Zhou Z et al. Ethylene emission as a potential indicator of Fuji apple flavor quality evaluation under low temperature. Hortic Plant J. 2020; 6: 231-9.

[136] Khaleghnezhad V, Yousefi AR, Tavakoli A et al. Interactive effects of abscisic acid and temperature on rosmarinic acid, total phenolic compounds, anthocyanin, carotenoid and flavonoid content of dragonhead (Dracocephalum moldavica L.) . Sci Hortic. 2019; 250: 302-9.

[137] Wang QH, Zhao C, Zhang M et al. Transcriptome analysis around the onset of strawberry fruit ripening uncovers an important role of oxidative phosphorylation in ripening. Sci Rep. 2017; 7: 41477.

[138] Chen T, Britzi M, Zakin V et al. Advances and strategies for controlling the quality and safety of postharvest fruit. Engineering. 2021; 7: 1177-84.

[139] Yan J, Luo Z, Ban Z et al. The effect of the layer-by-layer (LBL) edible coating on strawberry quality and metabolites during storage. Postharvest Biol Technol. 2019; 147: 29-38.

[140] Chen J, Mi H, Zhao Y et al. Detachment-accelerated ripening and senescence of strawberry (Fragaria × ananassa Duch. cv. Akihime) fruit and the regulation role of multiple phytohormones. Acta Physiol Plant. 2014; 36: 2441-51.

[141] Chen J, Mao L, Lu W et al. Transcriptome profiling of postharvest strawberry fruit in response to exogenous auxin and abscisic acid. Planta. 2016; 243: 183-97.

[142] Siebeneichler TJ, Crizel RL, Comozatto GH et al. The postharvest ripening of strawberry fruits induced by abscisic acid and sucrose differs from their in vivo ripening. Food Chem. 2020; 317: 126407.

[143] Chen J, Mao L, Mi H et al. Involvement of abscisic acid in postharvest water-deficit stress associated with the accumulation of anthocyanins in strawberry fruit. Postharvest Biol Technol. 2016; 111: 99-105.

[144] Gaston A, Potier A, Alonso M et al. The FveFT2 florigen/ FveTFL1 antiflorigen balance is critical for the control of seasonal flowering in strawberry while FveFT3 modulates axillary meristem fate and yield . New Phytol. 2021; 232: 372-87.

[145] Gao Q, Luo H, Li Y et al. Genetic modulation of RAP alters fruit coloration in both wild and cultivated strawberry. Plant Biotechnol J. 2020; 18: 1550-61.

[146] Mao W, Han Y, Chen Y et al. Low temperature inhibits anthocyanin accumulation in strawberry fruit by activating FvMAPK3-induced phosphorylation of FvMYB10 and degradation of chalcone synthase 1. Plant Cell. 2022; 34: 1226-49.