Signal transduction in non-climacteric fruit ripening

Abstract

Fleshy fruit ripening involves changes in numerous cellular processes and metabolic pathways, resulting from the coordinated actions of diverse classes of structural and regulatory proteins. These include enzymes, transporters and complex signal transduction systems. Many aspects of the signaling machinery that orchestrates the ripening of climacteric fruits, such as tomato (Solanum lycopersicum), have been elucidated, but less is known about analogous processes in non-climacteric fruits. The latter include strawberry (Fragaria x ananassa) and grape (Vitis vinifera), both of which are used as non-climacteric fruit experimental model systems, although they originate from different organs: the grape berry is a true fruit derived from the ovary, while strawberry is an accessory fruit that is derived from the floral receptacle. In this article, we summarize insights into the signal transduction events involved in strawberry and grape berry ripening. We highlight the mechanisms underlying non-climacteric fruit ripening, the multiple primary signals and their integrated action, individual signaling components, pathways and their crosstalk, as well as the associated transcription factors and their signaling output.

References

[1] Giovannoni J, Nguyen C, Ampofo B et al. The epigenome and transcriptional dynamics of fruit ripening. Annu Rev Plant Biol. 2017; 68: 61-84.

[2] Giovannoni J. Molecular biology of fruit maturation and ripening. Annu Rev Plant Physiol Plant Mol Biol. 2001; 52: 725-49.

[3] Li S, Chen K, Grierson D . Molecular and hormonal mechanisms regulating fleshy fruit ripening. Cells. 2021; 10: 1136.

[4] Gapper NE, McQuinn RP, Giovannoni JJ . Molecular and genetic regulation of fruit ripening. Plant Mol Biol. 2013; 82: 575-91.

[5] Fray RG, Grierson D . Molecular genetics of tomato fruit ripening. Trends Genet. 1993; 9: 438-43.

[6] Barry CS, Giovannoni JJ . Ethylene and fruit ripening. J Plant Growth Regul. 2007; 26: 143-59.

[7] Alexander L, Grierson D . Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J Exp Bot. 2002; 53: 2039-55.

[8] Moya-León MA, Mattus-Araya E, Herrera R . Molecular events occurring during softening of strawberry fruit. Front Plant Sci. 2019; 10: 615.

[9] Kuhn N, Guan L, Dai ZW et al. Berry ripening: recently heard through the grapevine. J Exp Bot. 2014; 65: 4543-59.

[10] Cherian S, Figueroa CR, Nair H . ’Movers and shakers’ in the regulation of fruit ripening: a cross-dissection of climacteric versus non-climacteric fruit. J Exp Bot. 2014; 65: 4705-22.

[11] Alferez F, de Carvalho DU, Boakye D . Interplay between abscisic acid and gibberellins, as related to ethylene and sugars, in regulating maturation of non-climacteric fruit. Int J Mol Sci. 2021; 22: 669.

[12] Gao R, Bouillet S, Stock AM . Structural basis of response regulator function. Annu Rev Microbiol. 2019; 73: 175-97.

[13] Stepanova AN, Alonso JM . Ethylene signalling and response pathway: a unique signalling cascade with a multitude of inputs and outputs. Physiol Plant. 2005; 123: 195-206.

[14] Etheridge N, Hall BP, Schaller GE . Progress report: ethylene signaling and responses. Planta. 2006; 223: 387-91.

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

[16] Adams-Phillips L, Barry C, Giovannoni J . Signal transduction systems regulating fruit ripening. Trends Plant Sci. 2004; 9: 331-8.

[17] Jia K, Zhang Q, Xing Y et al. A development-associated decrease in osmotic potential contributes to fruit ripening initiation in strawberry (Fragaria ananassa). Front Plant Sci. 2020; 11: 1035.

[18] Verslues PE, Zhu JK . Before and beyond ABA: upstream sensing and internal signals that determine ABA accumulation and response under abiotic stress. Biochem Soc Trans. 2005; 33: 375-9.

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

[20] Zhang WW, Zhao SQ, Zhang LC et al. Changes in the cell wall during fruit development and ripening in Fragaria vesca. Plant Physiol Biochem. 2020; 154: 54-65.

[21] Behnami S, Bonetta D . With an ear up against the wall: an update on Mechanoperception in Arabidopsis. Plants (Basel). 2021; 10: 1587.

[22] Kohorn BD . Cell wall-associated kinases and pectin perception. J Exp Bot. 2016; 67: 489-94.

[23] Novaković L, Guo T, Bacic A et al. Hitting the wall-sensing and signaling pathways involved in plant Cell Wall remodeling in response to abiotic stress. Plants (Basel). 2018; 7: 89.

[24] Ortiz-Morea FA, Liu J, Shan L et al. Malectin-like receptor kinases as protector deities in plant immunity. Nature Plants. 2022; 8: 27-37.

[25] Mohnen D, Hahn MG . Cell wall carbohydrates as signals in plants. Semin Cell Biol. 1993; 4: 93-102.

[26] Ridley BL, O’Neill MA, Mohnen D . Pectins: structure, biosynthesis, and oligogalacturonide-related signaling. Phytochemistry. 2001; 57: 929-67.

[27] Vallarino JG, Osorio S . Signaling role of oligogalacturonides derived during cell wall degradation. Plant Signal Behav. 2012; 7: 1447-9.

[28] Hocking B, Tyerman SD, Burton RA et al. Fruit calcium: transport and physiology. Front Plant Sci. 2016;7:569.

[29] Leclercq J, Ranty B, Sanchez-Ballesta MT et al. Molecular and biochemical characterization of LeCRK1, a ripening-associated tomato CDPK-related kinase. J Exp Bot. 2005; 56: 25-35.

[30] Leszczuk A, Kalaitzis P, Blazakis KN et al. The role of arabinogalactan proteins (AGPs) in fruit ripening-a review. Hortic Res. 2020; 7: 176.

[31] Michailidis M, Karagiannis E, Tanou G et al. Novel insights into the calcium action in cherry fruit development revealed by high-throughput mapping. Plant Mol Biol. 2020; 104: 597-614.

[32] Sriskantharajah K, el Kayal W, Ayyanath MM et al. Preharvest spray Hexanal formulation enhances postharvest quality in ’Honeycrisp’ apples by regulating phospholipase D and calcium sensor proteins genes. Plants (Basel). 2021; 10: 2332.

[33] Xiong T, Tan Q, Li S et al. Interactions between calcium and ABA signaling pathways in the regulation of fruit ripening. J Plant Physiol. 2021; 256: 153309.

[34] Yang T, Peng H, Bauchan GR . Functional analysis of tomato calmodulin gene family during fruit development and ripening. Hortic Res. 2014; 1: 14057.

[35] Yang T, Peng H, Whitaker BD et al. Characterization of a calcium/calmodulin-regulated SR/CAMTA gene family during tomato fruit development and ripening. BMC Plant Biol. 2012; 12: 19.

[36] Chen J, Mao L, Mi H et al. Involvement of three annexin genes in the ripening of strawberry fruit regulated by phytohormone and calcium signal transduction. Plant Cell Rep. 2016; 35: 733-43.

[37] Crane JC, van Overbeek J . Kinin-induced Parthenocarpy in the fig, Ficus carica L. Science. 1965; 147: 1468-9.

[38] Lewis LN, Khalifah RA, Coggins CW . Seasonal changes in citrus auxin and 2 auxin antagonists as related to fruit development. Plant Physiol. 1965; 40: 500-5.

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

[40] Liu DJ, Chen JY, Lu WJ . Expression and regulation of the early auxin-responsive aux/IAA genes during strawberry fruit development. Mol Biol Rep. 2011; 38: 1187-93.

[41] Ziliotto F, Corso M, Rizzini FM et al. Grape berry ripening delay induced by a pre-véraison NAA treatment is paralleled by a shift in the expression pattern of auxin- and ethylene-related genes. BMC Plant Biol. 2012; 12: 185.

[42] Davies C, Nicholson EL, Böttcher C et al. Shiraz wines made from grape berries (Vitis vinifera) delayed in ripening by plant growth regulator treatment have elevated rotundone concentrations and "pepper" flavor and aroma. J Agric Food Chem. 2015; 63: 2137-44.

[43] Coombe BG, Hale CR . The hormone content of ripening grape berries and the effects of growth substance treatments. Plant Physiol. 1973; 51: 629-34.

[44] Ttcher CB, Boss PK, Davies C . Delaying Riesling grape berry ripening with a synthetic auxin affects malic acid metabolism and sugar accumulation, and alters wine sensory characters. Funct Plant Biol. 2012; 39: 745-53.

[45] Böttcher C, Harvey K, Forde C et al. Auxin treatment of pre-veraison grape (Vitis vinifera L.) berries both delays ripening and increases the synchronicity of sugar accumulation. Aust J Grape Wine Res. 2011; 17: 1-8.

[46] Dal Santo S, Tucker MR, Tan HT et al. Auxin treatment of grapevine (Vitis vinifera L.) berries delays ripening onset by inhibiting cell expansion. Plant Mol Biol. 2020; 103: 91-111.

[47] Aharoni A, O’Connell AP . Gene expression analysis of strawberry achene and receptacle maturation using DNA microarrays. J Exp Bot. 2002; 53: 2073-87.

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

[49] 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.

[50] 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.

[51] 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.

[52] Encinas-Villarejo S, Maldonado AM, Amil-Ruiz F et al. Evidence for a positive regulatory role of strawberry (Fragaria x ananassa) fa WRKY1 and Arabidopsis at WRKY75 proteins in resistance. J Exp Bot. 2009; 60: 3043-65.

[53] Wei W, Hu Y, Han YT et al. The WRKY transcription factors in the diploid woodland strawberry Fragaria vesca: identification and expression analysis under biotic and abiotic stresses. Plant Physiol Biochem. 2016; 105: 129-44.

[54] Zhou H, Li Y, Zhang Q et al. Genome-wide analysis of the expression of WRKY family genes in different developmental stages of wild strawberry (Fragaria vesca) fruit. PLoS One. 2016; 11: e0154312.

[55] Li D, Mou W, Xia R et al. Integrated analysis of high-throughput sequencing data shows abscisic acid-responsive genes and miRNAs in strawberry receptacle fruit ripening. Hortic Res. 2019; 6: 26.

[56] Jia HF, 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.

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

[58] Zhao Y, Mao W, Chen Y et al. Optimization and standardization of transient expression assays for gene functional analyses in strawberry fruits. Hortic Res. 2019; 6: 53.

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

[60] Li T, Dai Z, Zeng B et al. Autocatalytic biosynthesis of abscisic acid and its synergistic action with auxin to regulate strawberry fruit ripening. Hortic Res. 2022; 9: uhab076.

[61] Zhang R, Wang Y, Li S et al. ABA signaling pathway genes and function during abiotic stress and berry ripening in Vitis vinifera. Gene. 2021; 769: 145226.

[62] Wang J, Wang S, Liu G et al. The synthesis and accumulation of resveratrol are associated with Veraison and abscisic acid concentration in Beihong (Vitis vinifera × Vitis amurensis) berry skin. Front Plant Sci. 2016; 7: 1605.

[63] Koyama K, Sadamatsu K, Goto-Yamamoto N . Abscisic acid stimulated ripening and gene expression in berry skins of the cabernet sauvignon grape. Funct Integr Genomics. 2010; 10: 367-81.

[64] Forlani S, Masiero S, Mizzotti C . Fruit ripening: the role of hormones, cell wall modifications, and their relationship with pathogens. J Exp Bot. 2019; 70: 2993-3006.

[65] Gambetta GA, Matthews MA, Shaghasi TH et al. Sugar and abscisic acid signaling orthologs are activated at the onset of ripening in grape. Planta. 2010; 232: 219-34.

[66] Zhu L, Zhang Y, Zhang W et al. Effects of exogenous abscisic acid on phenolic characteristics of red Vitis vinifera grapes and wines. Food Sci Biotechnol. 2016; 25: 361-70.

[67] Tijero V, Teribia N, Muñoz P et al. Implication of abscisic acid on ripening and quality in sweet cherries: differential effects during pre- and post-harvest. Front Plant Sci. 2016; 7: 602.

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

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

[70] Garrido-Bigotes A, Figueroa NE, Figueroa PM et al. Jasmonate signalling pathway in strawberry: genome-wide identification, molecular characterization and expression of JAZs and MYCs during fruit development and ripening. PLoS One. 2018; 13: e0197118.

[71] Delgado LD, Zúñiga 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.

[72] 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.

[73] Moreno Fde L, Blanch GP, Flores G et al. Impact of postharvest methyl jasmonate treatment on the volatile composition and flavonol content of strawberries. J Sci Food Agric. 2010; 90: 989-94.

[74] Paladines-Quezada DF, Fernández-Fernández JI, Moreno-Olivares JD et al. Application of elicitors in two ripening periods of Vitis vinifera L. cv Monastrell: influence on anthocyanin concentration of grapes and wines. Molecules. 2021; 26: 1689.

[75] Jia H, Zhang C, Pervaiz T et al. Jasmonic acid involves in grape fruit ripening and resistant against Botrytis cinerea. Funct Integr Genomics. 2016; 16: 79-94.

[76] Ruiz-García Y, Romero-Cascales I, Gil-Muñoz R et al. Improving grape phenolic content and wine chromatic characteristics through the use of two different elicitors: methyl jasmonate versus benzothiadiazole. J Agric Food Chem. 2012; 60: 1283-90.

[77] Ruiz-García Y, Gil-Muñoz R, López-Roca JM et al. Increasing the phenolic compound content of grapes by preharvest application of abcisic acid and a combination of methyl jasmonate and benzothiadiazole. J Agric Food Chem. 2013; 61: 3978-83.

[78] Rocio G. Improving phenolic and chromatic characteristics of Monastrell, merlot and Syrah wines by using methyl jasmonate and benzothiadiazole. Oeno One. 2017; 51: 1814.

[79] Vezzulli S, Civardi S, Ferrari F et al. Methyl jasmonate treatment as a trigger of resveratrol synthesis in cultivated grapevine. Am J Enol Vitic. 2007; 58: 530-3.

[80] 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.

[81] Fukano Y, Tachiki Y . Evolutionary ecology of climacteric and non-climacteric fruits. Biol Lett. 2021; 17: 20210352.

[82] Mondoni A, Probert RJ, Rossi G et al. Seeds of alpine plants are short lived: implications for long-term conservation. Ann Bot. 2011; 107: 171-9.

[83] Frenkel C, Hartman TG . Decrease in fruit moisture content heralds and might launch the onset of ripening processes. J Food Sci. 2012; 77: S365-76.

[84] Jiang W, Li N, Zhang D et al. Elevated temperature and drought stress significantly affect fruit quality and activity of anthocyanin-related enzymes in jujube (Ziziphus jujuba mill. cv. ’Lingwuchangzao’). PLoS One. 2020; 15: e0241491.

[85] Zhu JK . Abiotic stress signaling and responses in plants. Cell. 2016; 167: 313-24.

[86] 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.

[87] Liu J, Hasanuzzaman M, Wen H et al. High temperature and drought stress cause abscisic acid and reactive oxygen species accumulation and suppress seed germination growth in rice. Protoplasma. 2019; 256: 1217-27.

[88] Wang ZY, Gehring C, Zhu J et al. The Arabidopsis vacuolar sorting Receptor1 is required for osmotic stress-induced abscisic acid biosynthesis. Plant Physiol. 2015; 167: 137-52.

[89] 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.

[90] Lin-Wang K, McGhie TK, Wang M et al. Engineering the anthocyanin regulatory complex of strawberry (Fragaria vesca). Front Plant Sci. 2014; 5: 651.

[91] Lin-Wang K, Bolitho K, Grafton K et al. An R2R3 MYB transcription factor associated with regulation of the anthocyanin biosynthetic pathway in Rosaceae. BMC Plant Biol. 2010; 10: 50.

[92] 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.

[93] 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.

[94] Deluc L, Bogs J, Walker AR et al. The transcription factor VvMYB5b contributes to the regulation of anthocyanin and proanthocyanidin biosynthesis in developing grape berries. Plant Physiol. 2008; 147: 2041-53.

[95] Chen G, Xu P, Pan J et al. Inhibition of FvMYB10 transcriptional activity promotes color loss in strawberry fruit. Plant Sci. 2020; 298: 110578.

[96] 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.

[97] 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.

[98] Wei L, Mao W, Jia M et al. FaMYB44.2, a transcriptional repressor, negatively regulates sucrose accumulation in strawberry receptacles through interplay with FaMYB10. J Exp Bot. 2018; 69: 4805-20.

[99] Xie YG, Ma YY, Bi PP et al. Transcription factor FvTCP9 promotes strawberry fruit ripening by regulating the biosynthesis of abscisic acid and anthocyanins. Plant Physiol Biochem. 2020; 146: 374-83.

[100] Sheng L, Ma C, Chen Y et al. Genome-wide screening of AP2 transcription factors involving in fruit color and aroma regulation of cultivated strawberry. Genes. 2021; 12: 530.

[101] Li Y, Xu P, Chen G et al. FvbHLH9 functions as a positive regulator of anthocyanin biosynthesis by forming a HY5-bHLH9 transcription complex in strawberry fruits. Plant Cell Physiol. 2020; 61: 826-37.

[102] Jiu S, Guan L, Leng X et al. The role of VvMYBA2r and VvMYBA2w alleles of the MYBA2 locus in the regulation of anthocyanin biosynthesis for molecular breeding of grape (Vitis spp.) skin coloration. Plant Biotechnol J. 2021; 19: 1216-39.

[103] Huang YF, Vialet S, Guiraud JL et al. A negative MYB regulator of proanthocyanidin accumulation, identified through expression quantitative locus mapping in the grape berry. New Phytol. 2014; 201: 795-809.

[104] Cheng J, Yu K, Shi Y et al. Transcription factor VviMYB86 oppositely regulates Proanthocyanidin and anthocyanin biosynthesis in grape berries. Front Plant Sci. 2020; 11: 613677.

[105] Bogs J, Jaffé FW, Takos AM et al. The grapevine transcription factor VvMYBPA1 regulates proanthocyanidin synthesis during fruit development. Plant Physiol. 2007; 143: 1347-61.

[106] Zhang Y, Yin X, Xiao Y et al. An ETHYLENE RESPONSE FACTOR-MYB transcription complex regulates Furaneol biosynthesis by activating QUINONE OXIDOREDUCTASE expression in strawberry. Plant Physiol. 2018; 178: 189-201.

[107] 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 x ananassa fruits. J Exp Bot. 2014; 65: 401-17.

[108] Czemmel S, Stracke R, Weisshaar B et al. The grapevine R2R3-MYB transcription factor VvMYBF1 regulates flavonol synthesis in developing grape berries. Plant Physiol. 2009; 151: 1513-30.

[109] Yu Y, Guo D, Li G et al. The grapevine R2R3-type MYB transcription factor VdMYB1 positively regulates defense responses by activating the stilbene synthase gene 2 (VdSTS2). BMC Plant Biol. 2019; 19: 478.

[110] Wong DCJ, Schlechter R, Vannozzi A et al. A systems-oriented analysis of the grapevine R2R3-MYB transcription factor family uncovers new insights into the regulation of stilbene accumulation. DNA Res. 2016; 23: 451-66.

[111] Molina-Hidalgo FJ, Medina-Puche L, Cañete-Gómez 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.

[112] 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.

[113] Daminato M, Guzzo F, Casadoro G . 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.

[114] Carrasco-Orellana C, Stappung Y, Mendez-Yañez A et al. Characterization of a ripening-related transcription factor FcNAC1 from Fragaria chiloensis fruit. Sci Rep. 2018; 8: 10524.

[115] Amato A, Cavallini E, Zenoni S et al. A grapevine TTG2-like WRKY transcription factor is involved in regulating vacuolar transport and flavonoid biosynthesis. Front Plant Sci. 2016; 7: 1979.

[116] Moyano E, Martínez-Rivas FJ, Blanco-Portales 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.

[117] Gupta S, Malviya N, Kushwaha H et al. Insights into structural and functional diversity of Dof (DNA binding with one finger) transcription factor. Planta. 2015; 241: 549-62.

[118] Tello J, Torres-Pérez R, Grimplet J et al. Polymorphisms and minihaplotypes in the VvNAC26 gene associate with berry size variation in grapevine. BMC Plant Biol. 2015; 15: 253.

[119] Nicolas P, Lecourieux D, Gomès E et al. The grape berry-specific basic helix-loop-helix transcription factor VvCEB1 affects cell size. J Exp Bot. 2013; 64: 991-1003.

[120] Leida C, Dal Rì A, Dalla Costa L et al. Insights into the role of the berry-specific ethylene responsive factor VviERF045. Front Plant Sci. 2016; 7: 1793.

[121] Huang T, Yu D, Wang X . VvWRKY22 transcription factor interacts with VvSnRK1.1/VvSnRK1.2 and regulates sugar accumulation in grape. Biochem Biophys Res Commun. 2021; 554: 193-8.

[122] 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.

[123] 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.

[124] Li B, Yan J, Jia W . FERONIA/FER-like receptor kinases integrate and modulate multiple signaling pathways in fruit development and ripening. Plant Signal Behav. 2017; 12: e1366397.

[125] 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.

[126] Llop-Tous I, Domínguez-Puigjaner E, Vendrell M . Characterization of a strawberry cDNA clone homologous to calcium-dependent protein kinases that is expressed during fruit ripening and affected by low temperature. J Exp Bot. 2002; 53: 2283-5.

[127] Crizel RL, Perin EC, Vighi IL et al. Genome-wide identification, and characterization of the CDPK gene family reveal their involvement in abiotic stress response in Fragaria x ananassa. Sci Rep. 2020; 10: 11040.

[128] Zhou H, Ren S, Han Y et al. Identification and analysis of mitogen-activated protein kinase (MAPK) cascades in Fragaria vesca. Int J Mol Sci. 2017; 18: 1766.

[129] Zhang Q, Jia M, Xing Y et al. Genome-wide identification and expression analysis of MRLK family genes associated with strawberry (Fragaria vesca) fruit ripening and abiotic stress responses. PLoS One. 2016; 11: e0163647.

[130] Li D, Mou W, Luo Z et al. Developmental and stress regulation on expression of a novel miRNA, fan-miR73, and its target ABI5 in strawberry. Sci Rep. 2016; 6: 28385.

[131] Tang Y, Qu Z, Lei J et al. The long noncoding RNA FRILAIR regulates strawberry fruit ripening by functioning as a non-canonical target mimic. PLoS Genet. 2021; 17: e1009461.

[132] Gao Z, Li Q, Li J et al. Characterization of the ABA receptor VlPYL1 that regulates anthocyanin accumulation in grape berry skin. Front Plant Sci. 2018; 9: 592.

[133] Wang XQ, Zheng LL, Lin H et al. Grape hexokinases are involved in the expression regulation of sucrose synthase- and cell wall invertase-encoding genes by glucose and ABA. Plant Mol Biol. 2017; 94: 61-78.

[134] Zeng J, Haider MS, Huang J et al. Functional characterization of VvSK gene family in grapevine (Vitis vinifera L.) revealing their role in berry ripening. Int J Mol Sci. 2020; 21: 4336.

[135] Yu Y, Meng X, Guo D et al. Grapevine U-box E3 ubiquitin ligase VlPUB38 negatively regulates fruit ripening by facilitating abscisic-aldehyde oxidase degradation. Plant Cell Physiol. 2021; 61: 2043-54.

[136] Morris ER, Walker JC . Receptor-like protein kinases: the keys to response. Curr Opin Plant Biol. 2003; 6: 339-42.

[137] Hewitt S, Dhingra A . Beyond ethylene: new insights regarding the role of alternative oxidase in the respiratory climacteric. Front Plant Sci. 2020; 11: 543958.

[138] Woodson WR, Lawton KA . Ethylene-induced gene expression in carnation petals: relationship to autocatalytic ethylene production and senescence. Plant Physiol. 1988; 87: 498-503.

[139] 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.