Abstract
The purpose of this study was to investigate the role of abscisic acid (ABA) in the pre- and postharvest maturation of the nonclimacteric sweet cherry. It was found that ABA content increased rapidly at the straw-colored stage and reached its highest level 4 days before commercial harvest time. The increase in ABA level was paralleled by an increase in the expression of a gene involved in ABA synthesis [9-cis-epoxycarotenoid dioxygenase (PacNCED1)]. Well before the ABA increase, the expression of a gene involved in ABA catabolism (PacCYP707A2) was downregulated. During the straw-colored stage, the application of exogenous ABA induced ABA accumulation, anthocyanin biosynthesis, and an increase in the maturity index (SSC/TA), thereby promoting fruit ripening. ABA treatment stimulated the expression of PacNCED1 and of genes involved in anthocyanin biosynthesis (PacCHS, PacF3H, PacCHI, PacDFR, and PacUFGT). The application of NiCl2 inhibited the release of ethylene and the expression of PacACO1 encoded 1-aminocyclopropane-1-carboxylic acid oxidase, of which the effect on fruit ripening was opposite that of ABA. Ethephon and nordihydroguaiaretic acid treatments, however, had no effect on fruit ripening. For postharvest fruit, the pedicel was a major route for water loss, and dehydration induced the transcription of PacNCED1 and the accumulation of ABA. Followed by ethylene release, the start of postharvest fruit senescence is triggered. In conclusion, endogenous ABA triggered the ripening of fruit via the modulation of ripening-related metabolism pathways such as anthocyanin accumulation. ABA also induced postharvest fruit senescence through stimulation of ethylene release in cherry fruit.
Similar content being viewed by others
References
Aneja M, Gianfagna T, Ng E (1999) The roles of abscisic acid and ethylene in the abscission and senescence of cocoa flowers. Plant Growth Regul 27:149–155
Barry CS, Blume B, Bouzayen M, Cooper W, Hamillton AJ, Grierson D (1996) Differential expression of the 1-aminocyclopropane-1-carboxylate oxidase gene family of tomato. Plant J 9:525–535
Barthe P, Garello G, Bianco-Trinchant J, Ie Page-Degivry MT (2000) Oxygen availability and ABA metabolism in Fagus sylvatica seeds. Plant Growth Regul 30:185–191
Beruter J (1983) Effect of abscisic acid on sorbitol uptake in growing apple fruits. J Exp Bot 34:737–743
Burbidge A, Grieve TM, Jackson A, Thompson A, McCarty DR, Taylor IB (1999) Characterization of the ABA-deficient tomato mutant notabilis and its relationship with maize Vp14. Plant J 17:427–431
Cakir B, Agasse A, Gaillard C, Saumonneau A, Delrot S, Atanassova R (2003) A grape ASR protein involved in sugar and abscisic acid signaling. Plant Cell 15:2165–2180
Chernys J, Zeevaart JAD (2000) Characterization of the 9-cis-epoxycarotenoid dioxygenase gene family and the regulation of abscisic acid biosynthesis in avocado. Plant Physiol 124:343–353
Chervin C, Deluc L (2010) Ethylene signalling receptors and transcription factors over the grape berry development: gene expression profiling. Vitis 49:129–136
Chervin C, El-Kereamy A, Roustana JP, Latchéa A, Lamona J, Bouzayena M (2004) Ethylene seems required for the berry development and ripening in grape, a non-climacteric fruit. Plant Sci 167:1301–1305
Chervin C, Tira-Umphon A, Terrier N, Zouine M, Dany Severac D, Roustan JP (2008) Stimulation of the grape berry expansion by ethylene and effects on related gene transcripts, over the ripening phase. Physiol Plant 134:534–546
Daniel M, Benes C, Danielová V, Kríz B (2011) Sixty years of research of tick-borne encephalitis—a basis of the current knowledge of the epidemiological situation in Central Europe. Epidemiol Mikrobiol Imunol 60(4):135–155
Deluc LG, Grimplet J, Wheatley MD, Tillett RL, Quilici DR, Osborne C, Schooley DA, Schlauch KA, Cushman JC, Cramer GR (2007) Transcriptomic and metabolite analyses of Cabernet Sauvignon grape berry development. BMC Genomics 8:429–471
Deluc LG, Quilici DR, Decendit A, Grimplet J, Wheatley MD, Schlauch KA, Merillon JM, Cushman JC, Cramer GR (2009) Water deficit alters differentially metabolic pathways affecting important flavor and quality traits in grape berries of Cabernet Sauvignon and Chardonnay. BMC Genomics 10:212
Fincher GB (1989) Molecular and cellular biology associated with endosperm mobilization in germinating cereal grains. Annu Rev Plant Physiol Plant Mol Biol 40:305–346
Gambetta GA, Matthews MA, Shaghasi TH, McElrone AJ, Castellarin SD (2010) Sugar and abscisic acid signaling orthologs are activated at the onset of ripening in grape. Planta 232:219–234
Iannetta PPM, Laarhoven L-J, Medina-Escobar N, James EK, McManus MT, Davies HV, Harren FJM (2006) Ethylene and carbon dioxide production by developing strawberries show a correlative pattern that is indicative of ripening climacteric fruit. Physiol Plant 127:247–259
Ishiguro T, Yamaguchi M, Nishimura K, Satoh I (1993) Changes of fruit characteristics and respiration in sweet cherry (Prunus avium L.) during ripening. J Jpn Soc Hortic Sci 62(Suppl 2):146–147
Iuchi S, Kobayashi M, Taji T, Naramoto M, Seki M, Kato T, Tabata S, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (2001) Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J 27:325–333
Jia HF, Chai YM, Li CL et al (2011) Abscisic acid plays an important role in the regulation of strawberry fruit ripening. Plant Physiol 157:188–199
Jia HF, Lu D, Sun JH, Li CL, Xing Y, Qin L, Shen YY (2013) Type 2C protein phosphatase ABI1 is a negative regulator of strawberry fruit ripening. J Exp Biol 64(6):1677–1687
Kondo S, Gemma H (1993) Relationship between abscisic acid (ABA) content and maturation of the sweet cherry. J Jpn Soc Hortic Sci 62:63–68
Kondo S, Inoue K (1997) Abscisic acid and 1-aminocyclopropane-1-carboxylic acid (ACC) content during growth of ‘Satohnishiki’ cherry fruit, and the effect of ABA and ethepnon application on fruit quality. J Hortic Sci 72:221–227
Krochko JE, Abrams GD, Loewen MK, Abrams SR, Cutler AJ (1998) (+)-Abscisic acid 8′-hydroxylase is a cytochrome P450 monooxygenase. Plant Physiol 118:849–860
Lara I, Vendrell M (2000a) Changes in abscisic acid levels, ethylene biosynthesis and protein patterns during fruit maturation of apples. J Am Soc Hortic Sci 125:183–189
Lara I, Vendrell M (2000b) Development of ethylene-synthesizing capacity in preclimacteric apples: interaction between abscisic acid and ethylene. J Am Soc Hortic Sci 125:505–512
Leng P, Zhang GL, Li XX, Wang LH, Zheng ZM (2009) Cloning of 9-cis-epoxycarotenoid dioxygenase (NCED) gene encoding a key enzyme during abscisic acid (ABA) biosynthesis and ABA-regulated ethylene production in detached young persimmon calyx. Chinese Sci Bull 54:2830–2838
Leung J, Giraudat J (1998) Abscisic acid signal transduction. Annu Rev Plant Physiol Plant Mol Biol 49:199–222
Li Q, Li P, Sun L, Wang YP, Ji K, Sun YF, Dai SJ, Chen P, Duan CR, Leng P (2012) Expression analysis of β-glucosidase genes that regulate abscisic acid homeostasis during watermelon (Citrullus lanatus) development and under stress conditions. J Plant Physiol 169:78–85
Martínez-Madrid MC, Serrano M, Riquelme F, Romojaro F (1996) Polyamines, abscisic acid and ethylene production in tomato fruit. Phytochemistry 43:323–326
McCarty DR (1995) Genetic control and integration of maturation and germination pathways in seed development. Annu Rev Plant Physiol Plant Mol Biol 46:71–79
Mozetic B, Trebse P, Simcic M, Hribar J (2004) Changes of anthocyanins and hydroxycinnamic acid affecting the skin colour during maturation of sweet cherries (Prunus avium L.). Lebensm Wiss Technol 37:123–128
Nakatsuka A, Murachi S, Okunishi H, Shiomi S, Nakano R, Kubo Y, Inaba A (1998) Differential expression and internal feedback regulation of 1-aminocyclopropane-1-carboxylate synthase, 1-aminocyclopropane-1-carboxylate oxidase and ethylene receptor genes in tomato fruit during development and ripening. Plant Physiol 118:1295–1305
Nambara E, Marion-Poll A (2005) Abscisic acid biosynthesis and catabolism. Ann Rev Plant Biol 56:165–185
Qin X, Zeevaart JAD (1999) The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proc Natl Acad Sci USA 96:15354–15361
Qin X, Zeevaart JAD (2002) Overexpression of a 9-cis-epoxycarotenoid dioxygenase gene in Nicotiana plumbaginifolia increases abscisic acid and phaseic acid levels and enhances drought tolerance. Plant Physiol 128:544–551
Rabino I, Mancinelli AL (1986) Light, temperature and anthocyanin production. Plant Physiol 81:922–924
Ren J, Sun L, Wu JF, Zhao SL, Wang CL, Wang YP, Ji K, Leng P (2010) Cloning and expression analysis of cDNAs for ABA 8′-hydroxylase during sweet cherry fruit maturation and under stress conditions. J Plant Physiol 167:1486–1493
Ren J, Chen P, Dai SJ, Li P, Li Q, Ji K, Wang YP, Leng P (2011a) Role of abscisic acid and ethylene in sweet cherry fruit maturation: molecular aspects. New Zeal J Crop Hort Sci 39:161–174
Ren J, Sun L, Wu JF, Zhao SL, Wang CL, Wang YP, Ji K, Leng P (2011b) Expression analysis of the cDNA for Magnesium Chelatase H Subunit (CHLH) during sweet cherry fruit ripening and under stress conditions. Plant Growth Regul 63:301–307
Rodrigo MJ, Alquezar B, Zacarias L (2006) Cloning and characterization of two 9-cis-epoxycarotenoid dioxygenase genes, differentially regulated during fruit maturation and under stress conditions, from orange (Citrus sinensis L. Osbeck). J Exp Bot 57:633–643
Romero P, Lafuente MT, Rodrigo MJ (2012) The citrus ABA signalosome: identification and transcriptional regulation during sweet orange fruit ripening and leaf dehydration. J Exp Bot 63:4931–4945
Sagee O, Goren R, Riov J (1980) Abscission of citrus leaf explants: interrelationships of abscisic acid, ethylene, and hydrolytic enzymes. Plant Physiol 66:750–753
Setha S, Kondo S, Hirai N, Ohigashi H (2005) Quantification of ABA and its metabolites in sweet cherries using deuterium-labeled internal standards. Plant Growth Regul 45:183–188
Sun L, Zhang M, Ren J, Qi JX, Zhang GJ, Leng P (2010) Reciprocity between abscisic acid and ethylene at the onset of berry ripening and after harvest. BMC Plant Biol 10:257
Sun L, Sun YF, Zhang M, Wang L, Ren J, Cui MM, Wang YP, Ji K, Li P, Li Q, Chen P, Dai SJ, Duan CR, Wu Y, Leng P (2012a) Suppression of 9-cis-epoxycarotenoid dioxygenase (NCED), which encodes a key enzyme in abscisic acid biosynthesis, alters fruit texture in transgenic tomatoes. Plant Physiol 158:283–298
Sun L, Yuan B, Zhang M, Wang L, Cui MM, Wang Q, Leng P (2012b) Fruit-specific RNAi-mediated suppression of SlNCED1 increases both lycopene and β-carotene contents in tomato fruit. J Exp Bot 63:3097–3108
Tan BC, Schwartz SH, Zeevaart JAD, McCarty DR (1997) Genetic control of abscisic acid biosynthesis in maize. Proc Natl Acad Sci USA 94:12235–12240
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
Usenik V, Fabcic J, Stampar F (2008) Sugars, organic acid, phenolic composition and antioxidant activity of sweet cherry (Prunus avium L.). Food Chem 37:123–128
Valero D, Huertas M, Diaz-Mula, Zapata PJ, Castillo S, Guillen F, Domingo MR, Serrano M (2011) Postharvest treatments with salicylic acid, acetylsalicylic acid or oxalic acid delayed ripening and enhanced bioactive compounds and antioxidant capacity in sweet cherry. Agric Food Chem 59:5483–5489
Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R, Schuch W, Giovannoni J (2002) A MADS-box gene necessary for fruit ripening at tomato ripening-inhibitor (rin) locus. Science 296:343–346
Wan CY, Wilkins TA (1994) A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). Anal Biochem 223:7–12
Wheeler S, Loveys B, Ford C, Davies C (2009) The relationship between the expression of abscisic acid biosynthesis genes, accumulation of abscisic acid and the promotion of Vitis vinifera L. berry ripening by abscisic acid. Aust J Grape Wine Res 15:195–204
Yoo SD, Gao Z, Cantini C, Loescher WH, Nocker SV (2003) Fruit ripening in sour cherry: changes in expression of genes encoding expansins and other cell-wall-modifying enzymes. J Am Soc Hort Sci 128:16–22
Zeevaart JAD (1999) Abscisic acid metabolism and its regulation. In: Biochemistry and molecular biology of plant hormones. New York: Elsevier Science, pp 189–207
Zhang M, Yuan B, Leng P (2009a) The role of ABA in triggering ethylene biosynthesis and ripening of tomato fruit. J Exp Bot 60:1579–1588
Zhang M, Leng P, Zhang GL, Li XX (2009b) Cloning and functional analysis of 9-cis-epoxycarotenoid dioxygenase (NCED) gene encoding a key enzyme during abscisic acid biosynthesis from peach and grape fruits. J Plant Physiol 166:1241–1252
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
344_2013_9388_MOESM1_ESM.tif
Fig.S1. Process of ABA, NDGA, ethephon and NiCl2 application on cherry fruits. a Thirty fruits in each treatment were soaked in water (as control) or ABA or NDGA or ethephon or NiCl2 respectively for 30 min. b, c. The solution was washed from the fruit surface by water and fruits were kept in plastic cups with film covers. (TIFF 4,624 kb)
344_2013_9388_MOESM2_ESM.tif
Fig. S2. The effects of exogenous ABA, NDGA, NiCl2 and ethephon application on the maturation of the cherry fruit detached from tree. a Control fruits (treated by water); b At 4 days after treatments; c At five DAT. Line a Control; b ABA treatment; c NDGA treatment; d, Ethephon treatment; e, NiCl2 treatment. (TIFF 2,908 kb)
344_2013_9388_MOESM3_ESM.tif
Fig. S3. The effects of exogenous ABA, NDGA, NiCl2 and ethephon application on the maturation of the cherry fruit attached to the tree. a, f At zero days and seven days for control fruits on the tree. b–e At 7 days after treatment with ABA or NDGA or ethephon or NiCl2 on the tree. (TIFF 1,922 kb)
Rights and permissions
About this article
Cite this article
Luo, H., Dai, S., Ren, J. et al. The Role of ABA in the Maturation and Postharvest Life of a Nonclimacteric Sweet Cherry Fruit. J Plant Growth Regul 33, 373–383 (2014). https://doi.org/10.1007/s00344-013-9388-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-013-9388-7