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Acyl-CoA oxidase 1 is involved in γ-decalactone release from peach (Prunus persica) fruit

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Abstract

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γ-Decalactone accumulation in peach mesocarp was highly correlated with ACX enzyme activity and natural PpACX1 content. Adding the purified recombinant PpACX1 induced γ-decalactone biosynthesis in cultured mesocarp discs in vitro.

Abstract

Previous gene expression studies have implied that acyl coenzyme A oxidase (ACX) is related to lactones synthesis, the characteristic aroma compounds of peach. Here, we analysed the correlation between γ-decalactone content and ACX enzyme activity in mesocarp of five different types of fully ripe peach varieties. Furthermore, ‘Hu Jing Mi Lu’ (‘HJ’) and ‘Feng Hua Yu Lu’ (‘YL’), which have strong aroma among them, at four ripening stages were selected to study the role of ACX in lactone biosynthesis. The result showed that γ-decalactone was the most abundant lactone compound. γ-Decalactone accumulation was highly correlated with ACX enzyme activity. Mass spectrometry (MS) showed that PpACX1 was the most abundant PpACX protein in fully ripe mesocarp of cv. ‘HJ’. To further elucidate the function of the PpACX1 protein, the PpACX1 gene was heterologously expressed in a bacterial system and characterized in vitro. MS identification gave the molecular weight of the recombinant PpACX1 as 94.44 kDa and the coverage rate of the peptide segments was 47.3%. In cultured mesocarp discs in vitro, adding the purified recombinant PpACX1 and C16-CoA substrate induced the expected γ-decalactone biosynthesis. Using a sandwich ELISA based on mixed mono- and polyclonal antibodies against recombinant PpACX1, PpACX1 content in mesocarp was found to be highly correlated with γ-decalactone accumulation in mesocarp of five fully ripe varieties and four ripening stages of ‘HJ’ and ‘YL’. This study revealed the vital function of PpACX1 in γ-decalactone biosynthesis in peach fruit.

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Abbreviations

ACX:

Acyl coenzyme A oxidase

BSA:

Bovine serum albumin

ELISA:

Enzyme-linked immunosorbent assay

ETH:

Ethephon

FW:

Fresh weight

GC–MS:

Gas chromatography–mass spectrometry

HJ:

Hu Jing Mi Lu

IPTG:

Isopropyl-beta-d-thiogalactopyranoside

LB:

Luria–Bertani

mAbs:

Monoclonal antibodies

MS:

Mass spectrometry

pAbs:

Polyclonal antibodies

qPCR:

Real-time quantitative polymerase chain reaction

RT-PCR:

Reverse transcription PCR

SE:

Standard error

TG:

Tai Gu Rou Tao

TSS:

Total soluble solids

μ HPLC:

Capillary electrophoresis and high performance liquid chromatography

YL:

Feng Hua Yu Lu

ZH:

Zhong Hua Shou Tao

ZN16:

Zhong Nectarine 16

References

  • Aharoni A, Keizer LC, Bouwmeester HJ, Sun Z, Alvarez-Huerta M, Verhoeven HA, Blaas J, van Houwelingen AM, De Vos RC, van der Voet H, Jansen RC, Guis M, Mol J, Davis RW, Schena M, van Tunen AJ, ƠConnell AP (2000) Identification of the SAAT gene involved in strawberry flavor biogenesis by use of DNA microarrays. Plant Cell 12(5):647–662. doi:10.1105/tpc.12.5.647

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Aharoni A, Giri AP, Verstappen FWA, Bertea CM, Sevenier R, Sun Z, Jongsma MA, Schwab W, Bouwmeestera HJ (2004) Gain and loss of fruit flavor compounds produced by wild and cultivated strawberry species. Plant Cell 16:3110–3131. doi:10.1105/tpc.104.023895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Alchihab M, Destain J, Aguedo M, Thonart P (2010) Production d’arômes de type lactone par des levures. Biotechnol Agron Soc Environ 14:681–691

    Google Scholar 

  • Arent S, Pye VE, Henriksen A (2008) Structure and function of plant acyl-CoA oxidases. Plant Physiol Biochem 46:292–301. doi:10.1016/j.plaphy.2007.12.014

    Article  CAS  PubMed  Google Scholar 

  • Aubert C, Gunata Z, Ambid C, Baumes R (2003) Changes in physicochemical characteristics and volatile constituents of yellow- and white-fleshed nectarines during maturation and artificial ripening. J Agr Food Chem 51:3083–3091. doi:10.1021/jf026153i

    Article  CAS  Google Scholar 

  • Baker A, Graham IA, Holdsworth M, Smith SM, Theodoulou FL (2006) Chewing the fat: beta-oxidation in signaling and development. Trends Plant Sci 11:124–132. doi:10.1016/j.tplants.2006.01.005

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3

    Article  CAS  PubMed  Google Scholar 

  • De Bellis L, Gonzali S, Alpi A, Hayashi H, Hayashi M, Nishimura M (2000) Purification and characterization of a novel pumpkin short-chain acyl-coenzyme A oxidase with structural similarity to acyl-coenzyme A dehydrogenases. Plant Physiol 123:327–334. doi:10.1104/pp.123.1.327

    Article  PubMed  PubMed Central  Google Scholar 

  • Defilippi BG, Manríquez D, Luengwilai K, González-Agüero M (2009) Aroma volatiles: biosynthesis and mechanisms of modulation during fruit ripening. Adv Bot Res 50:1–37. doi:10.1016/S0065-2296(08)00801-X

    Article  CAS  Google Scholar 

  • Eduardo I, Chietera G, Bassi D, Rossini L, Vecchietti A (2010) Identification of key odor volatile compounds in the essential oil of nine peach accessions. J Sci Food Agr 90:1146–1154. doi:10.1002/jsfa.3932

    Article  CAS  Google Scholar 

  • Eduardo I, Chietera G, Pirona R, Pacheco I, Troggio M, Banchi E, Bassi D, Rossini L, Vecchietti A, Pozzi C (2013) Genetic dissection of aroma volatile compounds from the essential oil of peach fruit: QTL analysis and identification of candidate genes using dense SNP maps. Tree Genet Genomes 9:189–204. doi:10.1007/s11295-012-0546-z

    Article  Google Scholar 

  • Flores F, Yahyaoui FE, Billerbeck G, Romojaro F, Latché A, Bouzayen M, Pech JC, Ambid C (2002) Role of ethylene in the biosynthetic pathway of aliphatic ester aroma volatiles in Charentais Cantaloupe melons. J Exp Bot 53:201–206. doi:10.1093/jexbot/53.367.201

    Article  CAS  PubMed  Google Scholar 

  • Froman BE, Edwards PC, Bursch AG, Dehesh K (2000) ACX3, a novel medium-chain acyl-coenzyme A oxidase from Arabidopsis. Plant Physiol 123:733–742. doi:10.1104/pp.123.2.733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao Z, Ma Y, Zhou X, Yang Z, Jia H, Gao L, Wu S, Han L, Yi X, Wang H, Akkerdaas JH, Ree R (2016) Quantification of peach fruit allergen lipid transfer protein by a double monoclonal antibody-based sandwich ELISA. Food Anal Method 9:823–830. doi:10.1007/s12161-015-0272-x

    Article  Google Scholar 

  • Gorin N, Heidema FT (1976) Peroxidase activity in Golden delicious apples as a possible parameter of senescence. J Agr Food Chem 24:200-201. doi:10.1021/jf60203a043

    Article  CAS  Google Scholar 

  • Groguenin A, Waché Y, Garcia EE, Aguedo M, Husson F, LeDall MT, Nicaud JM, Belin JM (2004) Genetic engineering of the b-oxidation pathway in the yeast Yarrowia lipolytica to increase the production of aroma compounds. J Mol Catal B: Enzym 28:75–79. doi:10.1016/j.molcatb.2004.01.006

    Article  CAS  Google Scholar 

  • Guido CR, Belo I, Ta TMN, Hoang LC, Alchihab M, Gomes N, Thonart P, Teixeira JA, Destain J, Waché Y (2011) Biochemistry of lactone formation in yeast and fungi and its utilisation for the production of flavour and fragrance compounds. Appl Microbiol Biot 89:535–547. doi:10.1007/s00253-010-2945-0

    Article  Google Scholar 

  • Hayashi H, Bellis DL, Yamaguchi K, Kato A (1998) Molecular characterization of a glyoxysomal long chain acyl-CoA oxidase that is synthesized as a precursor of higher molecular mass in pumpkin. J Biochem 273:8301–8307. doi:10.1074/jbc.273.14.8301

    CAS  Google Scholar 

  • Hayashi H, De Bellis L, Ciurli A, Kondo M, Hayashi M, Nishimura M (1999) A novel acyl-CoA oxidase that can oxidize short-chain acyl-CoA in plant peroxisomes. J Biol Chem 274:12715–12721. doi:10.1074/jbc.274.18.12715

    Article  CAS  PubMed  Google Scholar 

  • Hooks MA, Bode K, Couee I (1995) Regulation of Acyl-CoA oxidases in maize seedlings. Phychem 40:657–660. doi:10.1016/0031-9422(95)98169-H

    CAS  Google Scholar 

  • Hooks MA, Bode K, Couee I (1996) Higher-plant medium- and short-chain acyl-CoA oxidases: identification, purification and characterization of two novel enzymes of eukaryotic peroxisomal beta-oxidation. Biochem J 320:607–614. doi:10.1042/bj3200607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hooks MA, Kellas F, Graham IA (1999) Long-chain acyl-CoA oxidases of Arabidopsis. Plant J 20:1–13. doi:10.1046/j.1365-313X.1999.00559.x

    Article  CAS  PubMed  Google Scholar 

  • Husain Q, Hui YH (2010) Chemistry and biochemistry of some vegetable flavors. Handbook of fruit and vegetable flavours. Wiley, Hoboken, pp 575–625

    Google Scholar 

  • Jia HJ, Okamoto G (2001) Distribution of volatile compounds in peach fruit. J Jpn Soc Hortic Sci 70:223–225

    Article  CAS  Google Scholar 

  • Jia HJ, Araki A, Okamoto G (2005) Influence of fruit bagging on aroma volatiles and skin coloration of ‘Hakuho’ peach. Postharvest Biol Tech 35:61–68. doi:10.1016/j.postharvbio.2004.06.004

    Article  CAS  Google Scholar 

  • Kirsch T, Loffler HG, Kindl H (1986) Plant acyl-CoA oxidase: purification, characterization and monomeric apoprotein. J Biochem 18:8570-8575

    Google Scholar 

  • Li XW, Jiang J, Zhang LP, Yu Y, Ye ZW, Wang XM, Zhou JY, Chai ML, Zhang HQ, Arús P, Jia HJ, Gao ZS (2015) Identification of volatile and softening-related genes using digital gene expression profiles in melting peach. Tree Genet Genom 11:71. doi:10.1007/s11295-015-0891-9

    Article  Google Scholar 

  • Liu WL, Jia HJ, Zhang X (2010) The establishment of the methods for detection the activity of acyl coenzyme A oxidase in peach fruits. J Zhejiang Agr Sci 5:1072–1075 (in Chinese)

    Google Scholar 

  • Livak KJ, Schmittgen TD (2001) ∆∆CT method. Methods 25:402–408. doi:10.1006/meth.2001.1262

    Article  CAS  PubMed  Google Scholar 

  • Lurie S, Crisosto CH (2005) Chilling injury in peach and nectarine. Postharvest Biol Technol 37:195–208. doi:10.1016/j.postharvbio.2005.04.012

    Article  Google Scholar 

  • Montero-Prado P, Bentayeb K, Nerín C (2013) Pattern recognition of peach cultivars (Prunus persica L.) from their volatile components. Food Chem 138:724–731. doi:10.1016/j.foodchem.2012.10.145

    PubMed  Google Scholar 

  • Nieuwenhuizen NJ, Wang MY, Matich AJ, Green SA, Chen X, Yauk Y-K, Beuning LL, Nagegowda DA, Dudareva N, Atkinson RG (2009) Two terpene synthases are responsible for the major sesquiterpenes emitted from the flowers of kiwifruit (Actinidia deliciosa). J Exp Bot 60:3203–3219. doi:10.1093/jxb/erp162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ouyang J, Rong D, Hao XZ, Chen YT (2002) Purification and characterization of acyl coenzyme a oxidase (ACO) from Candida tropicalis. Acta Microbiol Sin 42:713–719 (in Chinese)

    CAS  Google Scholar 

  • Pafricia B, Pelegini S (2006) Structure and enzyme properties of Zabrotes subfasciatus a-amylase. Arch Insect Biochem 61:77–86. doi:10.1002/arch.20099

    Article  Google Scholar 

  • Qi YJ, Zhang X, Yang X, Gao ZS, Jia HJ (2012) Molecular cloning and sequence analysis of Acyl-CoA oxidase gene from ‘Hujingmilu’ peach fruit. Sci Agri Sin 45:1758–1765 (in Chinese)

    CAS  Google Scholar 

  • Sánchez G, Venegas-Calerón M, Salas JJ, Monforte A, Badenes ML, Granell A (2013) An integrative “omics” approach identifies new candidate genes to impact aroma volatiles in peach fruit. BMC Genom 14:343. doi:10.1186/1471-2164-14-343

    Article  Google Scholar 

  • Sanz C, Pérez AG (2010) Plant metabolic pathways and flavor biosynthesis. In: Hui YH (ed) Handbook of fruit and vegetable flavors. Wiley, Hoboken, pp 129–130. doi:10.1002/9780470622834.ch9

    Chapter  Google Scholar 

  • Schwab W, Davidovich-Rikanati R, Lewinsohn E (2008) Biosynthesis of plant-derived flavor compounds. Plant J 54:712–732. doi:10.1111/j.1365-313X.2008.03446.x

    Article  CAS  PubMed  Google Scholar 

  • Tong Z, Gao Z, Wang F, Zhou J, Zhang Z (2009) Selection of reliable reference genes for gene expression studies in peach using real-time PCR. BMC Mol Biol 10:71. doi:10.1186/1471-2199-10-71

    Article  PubMed  PubMed Central  Google Scholar 

  • Visai C, Vanoli M (1997) Volatile compound production during growth and ripening of peaches and nectarines. Sci Hortic 70:15–24. doi:10.1016/S0304-4238(97)00032-0

    Article  CAS  Google Scholar 

  • Waché Y, Pagot Y, Nicaud JM, Belin JM (1998) Acyl-CoA oxidase, a key step for lactone production by Yarrowia lipolytica. J Mol Catal B Enzym 5:165–169. doi:10.1016/S1381-1177(98)00027-7

    Article  Google Scholar 

  • Waché Y, Laroche C, Bergmark K, Charlotte MA, Aguedo M, Dall MT, Wang HJ, Nicaud JM, Belin JM (2000) Involvement of acyl coenzyme A oxidase isozymes in biotransformation of methyl ricinoleate into g-decalactone by Yarrowia lipolytica. Appl Environ Microb 66:1233–1236. doi:10.1128/AEM.66.3.1233-1236.2000

    Article  Google Scholar 

  • Waché Y, Aguedo M, Choquet A, Gatfield IL, Nicaud JM, Belin JM (2001) Role of beta-oxidation enzymes in gamma-decalactone production by the yeast Yarrowia lipolytica. Appl Environ Microb 67:5700–5704. doi:10.1128/AEM.67.12.5700-5704.2001

    Article  Google Scholar 

  • Waché Y, Aguedo M, LeDall MT, Nicaud JM, Belin JM (2002) Optimization of Yarrowia lipolytica’s b-oxidation pathway for g-decalactone production. J Mol Catal B Enzym 19–20:347–351

    Article  Google Scholar 

  • Waché Y, Aguedo M, Nicaud JM, Belin JM (2003) Catabolism of hydroxyacids and biotechnological production of lactones by Yarrowia lipolytica. Appl Microbiol Biot 61:393–404. doi:10.1007/s00253-002-1207-1

    Article  Google Scholar 

  • Waché Y, Husson F, Feron G (2006) Yeast as an efficient biocatalyst for the production of lipid-derived flavours and fragrances. Antouie van Leeuwenhoek 89:405–416. doi:10.1007/s10482-005-9049-3

    Article  Google Scholar 

  • Wang LR, Zhu GR et al (2005) Descriptors and data standard for peach (Prunus persica L.). Series books of technical standard for crop germplasm resources (5–4), China Agriculture Press, p 47 (in Chinese)

  • Xi WP, Zhang B, Liang L, Shen JY, Wei WW, Xu CJ, Allan AC, Ferguson IB, Chen KS (2012) Postharvest temperature influences volatile lactone production via regulation of acyl-CoA oxidases in peach fruit. Plant Cell Environ 35:534–545. doi:10.1111/j.1365-3040.2011.02433.x

    Article  CAS  PubMed  Google Scholar 

  • Yang Z, Ohlrogge JB (2009) Turnover of fatty acids during natural senescence of Arabidopsis, Brachypodium, and switchgrass and in Arabidopsis b-oxidation mutants. Plant Physiol 150:1981–1989. doi:10.1104/pp.109.140491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang B, Shen JY, Wei WW, Xi WP, Xu CJ, Ferguson I, Chen K (2010) Expression of genes associated with aroma formation derived from the fatty acid pathway during peach fruit ripening. J Agr Food Chem 58:6157–6165. doi:10.1021/jf100172e

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was funded by the National Science Foundation of China (31372040, 31401833), the State Ministry of Science and Technology of China (International Cooperation 1114), the Key Project for New Agricultural Cultivar Breeding in Zhejiang Province, China (2016C02052-5) and the Chinese Postdoctoral Science Foundation (2014M551753).

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Authors and Affiliations

  1. Key Laboratory of Horticultural Plant Growth, Development and Quality improvement, Ministry of Agriculture, Department of Horticulture, Zhejiang University, Hangzhou, 310058, China

    Liping Zhang, Haiyan Li, Ling Gao, Yujie Qi, Wanyi Fu, Xiongwei Li, Xiang Zhou, Zhongshan Gao & Huijuan Jia

  2. Forest and Fruit Tree Institute, Shanghai Academy of Agricultural Sciences, Shanghai, 201403, China

    Xiongwei Li

  3. Bio-Macromolecules Analysis Lab, Analysis Center of Agrobiology, Environmental Sciences of Zhejiang University, Hangzhou, 310058, China

    Qikang Gao

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  1. Liping Zhang
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  2. Haiyan Li
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  3. Ling Gao
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  4. Yujie Qi
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  5. Wanyi Fu
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  9. Zhongshan Gao
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  10. Huijuan Jia
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Correspondence to Zhongshan Gao.

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Communicated by Kathryn K. Kamo.

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Zhang, L., Li, H., Gao, L. et al. Acyl-CoA oxidase 1 is involved in γ-decalactone release from peach (Prunus persica) fruit. Plant Cell Rep 36, 829–842 (2017). https://doi.org/10.1007/s00299-017-2113-4

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