Non-climacteric ripening in strawberry fruit is linked to ABA, FaNCED2 and FaCYP707A1
Kai Ji A , Pei Chen A , Liang Sun A , Yanping Wang A , Shengjie Dai A , Qian Li A , Ping Li A , Yufei Sun A , Yan Wu A , Chaorui Duan A and Ping Leng A B
+ Author Affiliations
- Author Affiliations
A College of Agriculture and Biotechnology, China Agricultural University, Beijing 100 193, China.
B Corresponding author. Email: [email protected]
Functional Plant Biology 39(4) 351-357 https://doi.org/10.1071/FP11293
Submitted: 25 May 2011 Accepted: 1 February 2012 Published: 22 March 2012
Abstract
To study the role of ABA in development and ripening of strawberry fruit, two ABA key synthetase genes FaNCED1, FaNCED2 and one ABA key degradation enzyme gene FaCYP707A1 were cloned from strawberry cultivar ‘Ablion’. The three genes and putative amino acid sequences, respectively, had high similarities with their homologues in other plants. In strawberry pulp, expression of FaNCED2 rose in two stages that corresponded with increases in ABA levels. The expression of FaNCED1 was much lower and increased continually. The expression of FaCYP707A1 increased as fruit changed from bright green to white, then decreased as it ripened. Auxin reduced expression of these three genes. Analysis of expression of these genes in different organs and tissues showed that FaNCED2 was abundant in mature achenes and the pulp (receptacle) had high expression of FaNCED1 and FaCYP707A1. ABA may play a regulation role in strawberry fruit development and ripening. The content of ABA was regulated by its key synthetase gene NCED2 and degradation gene CYP707A1.
Additional keywords: CYP707A1, Fragaria, fruit development, gene expression, NCED.
References
Archbold DD, Dennis FG (1984) Quantification of free ABA and free and conjugated IAA in strawberry achene and receptacle tissue during fruit development. Journal of the American Society for Horticultural Science 109, 330–335.Benitez-Burraco A, Blanco-Portales R, Redondo-Nevado J, Bellido LM, Moyano E, Caballero JL, Mũnoz-Blanco J (2003) Cloning and characterization of two ripening-related strawberry (Fragaria × ananassa cv. Chandler) pectate lyase genes. Journal of Experimental Botany 54, 633–645.
| Cloning and characterization of two ripening-related strawberry (Fragaria × ananassa cv. Chandler) pectate lyase genes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXit1arur4%3D&md5=43ed5120b0cf9ed308844fd08d73c0d4CAS |
Bianco L, Lopez L, Scalone AG, Di Carli M, Desiderio A, Benvenuto E, Perrotta G (2009) Strawberry proteome characterization and its regulation during fruit ripening and in different genotypes. Journal of Proteomics 72, 586–607.
| Strawberry proteome characterization and its regulation during fruit ripening and in different genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktlylsrg%3D&md5=d12663bbc67df3838fad0a4ced1fd018CAS |
Blanco-Portales R, Lopez-Raez JA, Bellido ML, Moyano E, Dorado G, Gonzalez-Reyes JA, Caballero JL, Munoz-Blanco J (2004) A strawberry fruit-specific and ripening-related gene codes for a HyPRP protein involved in polyphenol anchoring. Plant Molecular Biology 55, 763–780.
| A strawberry fruit-specific and ripening-related gene codes for a HyPRP protein involved in polyphenol anchoring.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtlGmtQ%3D%3D&md5=bd3f19c7fb667c67baf61795a985550eCAS |
Carbone F, Preuss A, de Vos RCH, D’Amico E, Perrotta G, Bovy AG, Martens S, Rosati C (2009) Developmental, genetic and environmental factors affect the expression of flavonoid genes, enzymes and metabolites in strawberry fruits. Plant, Cell & Environment 32, 1117–1131.
| Developmental, genetic and environmental factors affect the expression of flavonoid genes, enzymes and metabolites in strawberry fruits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtValur7P&md5=6ca80ad1d504f3bb598f2369666e3ffbCAS |
Castellarin SD, Pfeiffer A, Sivilotti P, Degan M, Peterlunger E, Di Gaspero G (2007) Transcriptional regulation of anthocyanin biosynthesis in ripening vfruits of grapevine under seasonal water deficit. Plant, Cell & Environment 30, 1381–1399.
| Transcriptional regulation of anthocyanin biosynthesis in ripening vfruits of grapevine under seasonal water deficit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1yhsrnO&md5=b9f0176e14006e645215e7c35b02637aCAS |
Chernys JT, Zeevaart JA (2000) Characterization of the 9-cis-epoxycarotenoid dioxygenase gene family and the regulation of abscisic acid biosynthesis in avocado. Plant Physiology 124, 343–354.
| Characterization of the 9-cis-epoxycarotenoid dioxygenase gene family and the regulation of abscisic acid biosynthesis in avocado.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmvVGhtLc%3D&md5=550f1506b44c39d132105ed22a1da93dCAS |
Civello PM, Powell ALT, Sabehat A, Bennett AB (1999) An expansin gene expressed in ripening strawberry fruit. Plant Physiology 121, 1273–1279.
| An expansin gene expressed in ripening strawberry fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXotFyisrg%3D&md5=183d6e9fb354fae7adeb894d918dff2bCAS |
Coombe BG (1976) The development of fleshy fruits. Annual Review of Plant Physiology 27, 207–228.
| The development of fleshy fruits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksF2msL4%3D&md5=efc7ec1b7436b648eb57633ece90c187CAS |
Given NK, Venis MA, Grierson D (1988) Hormonal regulation of ripening in the strawberry, a non-climacteric fruit. Planta 174, 402–406.
| Hormonal regulation of ripening in the strawberry, a non-climacteric fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXksFWrtro%3D&md5=4bc6f53588439cf5f10f504bf8eb83a7CAS |
Griesser M, Hoffmann T, Bellido ML, Rosati C, Fink B, Kurtzer R, Aharoni A, Munoz-Blanco J, Schwab W (2008) Redirection of flavonoid biosynthesis through the down-regulation of an anthocyanidin glucosyltransferase in ripening strawberry fruit. Plant Physiology 146, 1528–1539.
| Redirection of flavonoid biosynthesis through the down-regulation of an anthocyanidin glucosyltransferase in ripening strawberry fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXkvVWjurc%3D&md5=364cbe02ccecf1c1435a2dfaaa63fb27CAS |
Iannetta PPM, Laarhoven LJ, 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. Physiologia Plantarum 127, 247–259.
| Ethylene and carbon dioxide production by developing strawberries show a correlative pattern that is indicative of ripening climacteric fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmtFSrsr8%3D&md5=69d566a53a96d87fb49f65be79ba5edaCAS |
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. The Plant Journal 27, 325–333.
| Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmvFKrtLY%3D&md5=446e81fc996cd5c32d333d2b4e5a2424CAS |
Jia HF, Chai YM, Li CL, Lu D, Luo JJ, Qin L, Shen YY (2011) Abscisic acid plays an important role in the regulation of strawberry fruit ripening. Plant Physiology 157, 188–199.
| Abscisic acid plays an important role in the regulation of strawberry fruit ripening.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Sit7%2FJ&md5=7adac26c878268b0365598327ae49e40CAS |
Jiang Y, Joyce DC (2003) ABA effects on ethylene production, PAL activity, anthocyanin and phenolic contents of strawberry fruit. Plant Growth Regulation 39, 171–174.
| ABA effects on ethylene production, PAL activity, anthocyanin and phenolic contents of strawberry fruit.Crossref | GoogleScholarGoogle Scholar |
John OA, Yamaki S (1994) Sugar content, compartmentation and efflux in strawberry tissue. Journal of the American Society for Horticultural Science 199, 1024–1028.
Kano Y, Asakura T (1981) Roles of cytokinin and abscisic acid in maturing of strawberry fruit. Journal of the Japanese Society for Horticultural Science 50, 31–36.
| Roles of cytokinin and abscisic acid in maturing of strawberry fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXltFWrurY%3D&md5=4d2e01a45e039625981781d7ec48487fCAS |
Lee KH, Piao HL, Kim HY, Choi SM, Jiang F, Hartung W, Hwang I, Kwak JM, Lee IJ, Hwang I (2006) Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid. Cell 126, 1109–1120.
| Activation of glucosidase via stress-induced polymerization rapidly increases active pools of abscisic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVCnsrrL&md5=9aa53dc4aad1f287f24906f5cd114586CAS |
Lefebvre V, North H, Frey A, Sotta B, Seo M, Okamoto M, Nambara E, Marion-poll A (2006) Functional analysis of Arabidopsis NCED6 and NCED9 genes indicates that ABA synthesized in the endosperm is involved in the induction of achene dormancy. The Plant Journal 45, 309–319.
| Functional analysis of Arabidopsis NCED6 and NCED9 genes indicates that ABA synthesized in the endosperm is involved in the induction of achene dormancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsFansbY%3D&md5=e55c811b37d4f1210040d327465f941bCAS |
Li Q, Li P, Sun L, Wang YP, Ji K, Sun YF, Dai SJ, Chen P, Duan CR, Leng P (2011) Expression analysis of β-glucosidase genes that regulate abscisic acid homeostasis during watermelon (Citrullus lanatus) development and under stress conditions. Journal of Plant Physiology 169, 78–85.
| Expression analysis of β-glucosidase genes that regulate abscisic acid homeostasis during watermelon (Citrullus lanatus) development and under stress conditions.Crossref | GoogleScholarGoogle Scholar |
Liu DJ, Chen J, Lu W (2011) Expression and regulation of the early auxin-responsive Aux/IAA genes during strawberry fruit development. Molecular Biology Reports 38, 1187–1193.
| Expression and regulation of the early auxin-responsive Aux/IAA genes during strawberry fruit development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXovVamsA%3D%3D&md5=c001ac86d1f21d1d1e9f400f2b5fe98aCAS |
Luchi 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. The Plant Journal 27, 325–333.
| Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Manning K (1994) Changes in gene expression during strawberry fruit ripening and their regulation by auxin. Planta 194, 62–68.
| Changes in gene expression during strawberry fruit ripening and their regulation by auxin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXktlWht78%3D&md5=108154aa82578df5eda9c742fbbe4d04CAS |
Nambara E, Marion-Poll M (2005) Abscisic acid biosynthesis and catabolism. Annual Review of Plant Biology 56, 165–185.
| Abscisic acid biosynthesis and catabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmtVaru7o%3D&md5=ae702566bb531c871287a0e4e06e066dCAS |
Ofosu-Anim J, Kanayama Y, Yamaki S (1996) Sugar uptake into strawberry fruit is stimulated by abscisic acid and indoleacetic acid. Physiologia Plantarum 97, 169–174.
| Sugar uptake into strawberry fruit is stimulated by abscisic acid and indoleacetic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjtFOrtbY%3D&md5=8b8e5dd0659c675aa5f705ed8a282e12CAS |
Owen SJ, Lafond MD, Bowen P, Bogdanoff C, Usher K, Abrams SR (2009) Profiles of abscisic acid and its catabolites in developing Merlot grape (Vitis vinifera) berries. American Journal of Enology and Viticulture 60, 277–284.
Perkins-Veazie P (1995) Growth and ripening of strawberry fruit. Horticultural Reviews 17, 287–297.
| Growth and ripening of strawberry fruit.Crossref | GoogleScholarGoogle Scholar |
Prasanna V, Prabha TN, Tharanathan RN (2007) Fruit ripening phenomena-an overview. Critical Reviews in Food Science and Nutrition 47, 1–19.
| Fruit ripening phenomena-an overview.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsFahtb0%3D&md5=117b27241a9ef6c695e0a8cb3e94a2cdCAS |
Qin X, Zeevaart JAD (1999) The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proceedings of the National Academy of Sciences of the United States of America 96, 15354–15361.
| The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhtFehug%3D%3D&md5=3958132f4c75335fb7f56f052671015aCAS |
Qin XQ, 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 Physiology 128, 544–551.
| Overexpression of a 9-cis-epoxycarotenoid dioxygenase gene in Nicotiana plumbaginifolia increases abscisic acid and phaseic acid levels and enhances drought tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhsVSru7c%3D&md5=5082b297961645dcc6e8e9b11e8e2c1dCAS |
Quesada MA, Blanco-Portales R, Posé S, García-Gago JA, Jiménez-Bermúdez S, Muñoz-serrano A, Caballero JL, Pliego-Alfaro F, Mercado JA, Muñoz-Blanco J (2009) Antisense down-regulation of the FaPG1 gene reveals an unexpected central role for polygalacturonase in strawberry fruit softening. Plant Physiology 150, 1022–1032.
| Antisense down-regulation of the FaPG1 gene reveals an unexpected central role for polygalacturonase in strawberry fruit softening.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnsleiurs%3D&md5=26d0ac4deaceddb6e129ab4ad8525efeCAS |
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. Journal of Plant Physiology 167, 1486–1493.
| Cloning and expression analysis of cDNAs for ABA 8′-hydroxylase during sweet cherry fruit maturation and under stress conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlSjt73F&md5=23d39aee71919e72aa6b49145e55e668CAS |
Ren J, Chen P, Dai SJ, Li P, Li Q, Ji K, Wang YP, Leng P (2011) Role of abscisic acid and ethylene in sweet cherry fruit maturation: molecular aspects. New Zealand Journal of Crop and Horticultural Science 39, 1–14.
| Role of abscisic acid and ethylene in sweet cherry fruit maturation: molecular aspects.Crossref | GoogleScholarGoogle Scholar |
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). Journal of Experimental Botany 57, 633–643.
| 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).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XovVCrtQ%3D%3D&md5=46ca45a886912b253d507130ccea5cdbCAS |
Seo M, Koshiba T (2002) Complex regulation of ABA biosynthesis in plants. Trends in Plant Science 7, 41–48.
| Complex regulation of ABA biosynthesis in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xntl2nsg%3D%3D&md5=708920de93679ee929d274eb4fa0f0afCAS |
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 Biology 10, 257
| Reciprocity between abscisic acid and ethylene at the onset of berry ripening and after harvest.Crossref | GoogleScholarGoogle Scholar |
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 (2012) Suppression of 9-cis-epoxycarotenoid dioxygenase (NCED), which encodes a key enzyme in abscisic acid biosynthesis, alters fruit texture in transgenic tomatoes. Plant Physiology 158, 283–298.
| Suppression of 9-cis-epoxycarotenoid dioxygenase (NCED), which encodes a key enzyme in abscisic acid biosynthesis, alters fruit texture in transgenic tomatoes.Crossref | GoogleScholarGoogle Scholar |
Tan BC, Joseph LM, Deng WT, Liu L, Li QB, Cline K, McCarty DR (2003) Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. The Plant Journal 35, 44–56.
| Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmt12hu7Y%3D&md5=dc09c58a190cdde84d7ef00ee25887cfCAS |
Taylor IB, Burbidge A, Thompson AJ (2000) Control of abscisic acid synthesis. Journal of Experimental Botany 51, 1563–1574.
| Control of abscisic acid synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnt12jurc%3D&md5=ca519e42553bad35f68a9328b4051893CAS |
Wan CY, Wilkins TA (1994) A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). Analytical Biochemistry 223, 7–12.
| A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXit1Cksrs%3D&md5=95570c398d12f74c3d5ce8fb9c717773CAS |
Yang SH, Choi D (2006) Characterization of genes encoding ABA 8′-hydroxylase in ethylene-induced stem growth of deepwater rice (Oryza sativa L.). Biochemical and Biophysical Research Communications 350, 685–690.
| Characterization of genes encoding ABA 8′-hydroxylase in ethylene-induced stem growth of deepwater rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVyisbjF&md5=196a4e85422a49fce4f568c6f6e918e3CAS |
Yang SH, Zeevaar JAD (2006) Expression of ABA 8′-hydroxylases in relation to leaf water relations and achene development in bean. The Plant Journal 47, 675–686.
| Expression of ABA 8′-hydroxylases in relation to leaf water relations and achene development in bean.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpvVKgu70%3D&md5=7ff998859443408961141f0f278b413aCAS |
Zhang M, Yuan B, Leng P (2009a) The role of ABA in triggering ethylene biosynthesis and ripening of tomato fruit. Journal of Experimental Botany 60, 1579–1588.
| The role of ABA in triggering ethylene biosynthesis and ripening of tomato fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltFWhs7k%3D&md5=e3b2d2b15121a9feafeaa1257f1724abCAS |
Zhang M, Leng P, Zhang GL, Li XX (2009b) Cloning and functional analysis of 9-cis-epoxycarotenoid dioxygenase (NCED) genes encoding a key enzyme during abscisic acid biosynthesis from peach and grape fruits. Journal of Plant Physiology 166, 1241–1252.
| Cloning and functional analysis of 9-cis-epoxycarotenoid dioxygenase (NCED) genes encoding a key enzyme during abscisic acid biosynthesis from peach and grape fruits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpvVyltrY%3D&md5=a6f175f12b37b281467cb547021d2773CAS |
Zhong XH, Ma DW, Huang YF (2004) Content variation of endogenous hormone during fruit developing period of strawberry. Acta Agriculturae Universitatis Jiangxiensis 26, 107–111.
