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Journal of Integrative Agriculture  2021, Vol. 20 Issue (6): 1525-1539    DOI: 10.1016/S2095-3119(20)63481-5
Special Issue: 园艺-分子生物合辑Horticulture — Genetics · Breeding
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Differences of aroma development and metabolic pathway gene expression between Kyoho and 87-1 grapes
JI Xiao-hao, WANG Bao-liang, WANG Xiao-di, WANG Xiao-long, LIU Feng-zhi, WANG Hai-bo
Research Institute of Pomology, Chinese Academy of Agricultural Sciences/Key Laboratory of Biology and Genetic Improvement of Horticultural Crops (Germplasm Resources Utilization), Ministry of Agriculture/Key Laboratory of Mineral Nutrition and Efficient Fertilization for Deciduous Fruits, Liaoning Province, Xingcheng 125100, P.R.China
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摘要  

在本研究中,我们采用固相微萃取SPME结合气相质谱联用技术比较了这两个葡萄品种果实发育过程中香气组分和含量的差异,并通过荧光定量PCR法分析了香气合成途径,比如LOX-HPL、MEP和MVA,酶编码基因的表达差异。结果发现巨峰果实成熟过程中共检测到12种酯类香气物质,并且主要在转色后含量丰富,但87-1葡萄中没有检测到酯类香气物质;87-1葡萄果实中检测到了14种萜烯类香气物质,含量丰富,并以里那醇为主,但在巨峰果实中仅检测到少量的萜烯类香气物质;荧光定量PCR的结果表明醇酰基转移酶编码基因VvAAT的低表达可能是87-1葡萄酯类香气含量低的主要原因,而MEP代谢途径酶编码基因的低表达,特别是里那醇合成酶编码基因VvPNLinNer1的低表达可能是巨峰葡萄中萜烯类香气物质含量低的原因。本研究将有助于对葡萄香气代谢机理认识的加深,并为葡萄香气品质改良提供理论指导。




Abstract  
Aroma is an important quality trait of grapes and often the focus of consumers, viticulturists and grapevine breeders.  Kyoho is a hybrid between Vitis vinifera and Vitis labrusca with a strawberry-like scent, while 87-1 is an early-ripening mutant of Muscat hamburg, belonging to Vitis vinifera, with a rose scent.  In this study, we compared their aroma compositions and concentrations during berry development by headspace-SPME combined with gas chromatography-mass spectrometry (GC-MS), and analyzed the expression differences of enzyme-encoding genes in the LOX-HPL, MEP and MVA metabolic pathways by qRT-PCR.  Twelve esters were detected in Kyoho during the whole berry development and they were abundant after veraison, but no esters were detected in 87-1 berries.  Linalool was the dominant terpene among the 14 terpenes detected in 87-1 berries, while limited amounts of terpenes were detected in Kyoho berries.  qRT-PCR analysis indicated that the low expression of VvAAT might explain the low content of ester volatiles in 87-1 berries, and the low expression of coding genes in the MEP pathway, especially VvPNLinNer1, might be the reason for the low content of volatile terpenes in Kyoho berries.  The results from this work will promote our understanding of aroma metabolic mechanisms of grapes, and offer some suggestions for grape aromatic quality improvement.
Keywords:  grape        Kyoho        87-1        aroma        LOX-HPL        MEP        gene expression  
Received: 20 February 2020   Accepted:
Fund: This work was supported by the National Key R&D Program of China (2018YFD1000200), the Fundamental Research Funds for Central Non-profit Scientific Institution, the Agricultural Science and Technology Innovation Program, Chinese Academy of Agricultural Sciences (CAAS-ASTIP-2015-RIP-04) and the earmarked fund for China Agriculture Research System (CARS-29-zp).
Corresponding Authors:  Correspondence WANG Hai-bo, E-mail: haibo8316@163.com; LIU Feng-zhi, E-mail: liufengzhi6699@126.com   
About author:  JI Xiao-hao, Mobile: +86-13610890936, E-mail: jixiaohao2006@163.com

Cite this article: 

JI Xiao-hao, WANG Bao-liang, WANG Xiao-di, WANG Xiao-long, LIU Feng-zhi, WANG Hai-bo. 2021. Differences of aroma development and metabolic pathway gene expression between Kyoho and 87-1 grapes. Journal of Integrative Agriculture, 20(6): 1525-1539.

Abbas F, Ke Y, Yu R, Yue Y, Amanullah S, Jahangir M M, Fan Y. 2017. Volatile terpenoids: multiple functions, biosynthesis, modulation and manipulation by genetic engineering. Planta, 246, 803–816.
Aharoni A, Keizer L C P, Bouwmeester H J, Sun Z K, Alvarez-Huerta M, Verhoeven H A, Blaas J, van Houwelingen A M M L, De Vos R C H, van der Voet H, Jansen R C, Guis M, Mol J, Davis R W, Schena M, van Tunen A J, O’Connell A P. 2000. Identification of the SAAT gene involved in strawberry flavor biogenesis by use of DNA microarrays. The Plant Cell, 12, 647–661.
Alem H, Rigou P, Schneider R, Ojeda H, Torregrosa L. 2019. Impact of agronomic practices on grape aroma composition: A review. Journal of the Science of Food and Agriculture, 99, 975–985.
Aubert C, Chalot G. 2018. Chemical composition, bioactive compounds, and volatiles of six table grape varieties (Vitis vinifera L.). Food Chemistry, 240, 524–533.
Battilana J, Costantini L, Emanuelli F, Sevini F, Segala C, Moser S, Velasco R, Versini G, Grando M S. 2009. The 1-deoxy-D-xylulose 5-phosphate synthase gene co-localizes with a major QTL affecting monoterpene content in grapevine. Theoretical and Applied Genetics, 118, 653–669.
Battilana J, Emanuelli F, Gambino G, Gribaudo I, Gasperi F, Boss P K, Grando M S. 2011. Functional effect of grapevine 1-deoxy-D-xylulose 5-phosphate synthase substitution K284N on Muscat flavour formation. Journal of Experimental Botany, 62, 5497–5508.
Beekwilder J, Alvarez-Huerta M, Neef E, Verstappen F W A, Bouwmeester H J, Aharoni A. 2004. Functional characterization of enzymes forming volatile esters from strawberry and banana. Plant Physiology, 135, 1865–1878.
Clastre M, Bantignies B, Feron G, Soler E, Ambid C. 1993. Purification and characterization of geranyl diphosphate synthase from Vitis vinifera L. cv. Muscat de Frontignan cell cultures. Plant Physiology, 102, 205–211.
Costa L D, Emanuelli F, Trenti M, Moreno-Sanz P, Lorenzi S, Coller E, Moser S, Slaghenaufi D, Cestaro A, Larcher R, Gribaudo I, Costantini L, Malnoy M, Grando M S. 2018. Induction of terpene biosynthesis in berries of microvine transformed with VvDXS1 alleles. Frontiers in Plant Science, 8, 2244–2257.
Duchêne E, Butterlin G, Claudel P, Dumas V, Jaegli N, Merdinoglu D. 2009. A grapevine (Vitis vinifera L.) deoxy-D-xylulose synthase gene colocates with a major quantitative trait loci for terpenol content. Theoretical and Applied Genetics, 118, 454–552.
Dudareva N, Pichersky E, Gershenzon J. 2004. Biochemistry of plant volatiles. Plant Physiology, 135, 1893–1902.
Eisenreich W, Bacher A, Arigoni D, Rohdich F. 2004. Biosynthesis of isoprenoids via the non-mevalonate pathway. Cellular and Molecular Life Sciences, 61, 1401–1426.
Emanuelli F, Battilana J, Costantini L, Cunff L L, Boursiquot J M, This P, Grando M S. 2010. A candidate gene association study on muscat flavor in grapevine (Vitis vinifera L.). BMC Plant Biology, 10, 241–257.
Feron G, Clastre M, Ambid C. 1990. Prenyltransferase compartmentation in cells of Vitis vinifera cultivated in vitro. FEBS Letters, 271, 236–238.
Gil M, Bottini R, Berli F, Pontin M, Silva M F, Piccoli P. 2013. Volatile organic compounds characterized from grapevine (Vitis vinifera L. cv. Malbec) berries increase at pre-harvest and in response to UV-B radiation. Phytochemistry, 96, 148–157.
Harada M, Ueda Y, Iwata T. 1985. Purification and some properties of alcohol acetyltransferase from banana fruit. Plant Cell Physiology, 26, 1067–1074.
Jaillon O, Aury J M, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyère C, Billault A, Segurens B, et al. 2007. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature, 449, 463–468.
Ji X H, Wang B L, Wang X D, Shi X B, Liu P P, Liu F Z, Wang H B. 2019. Effects of different color paper bags on aroma development of Kyoho grape berries. Journal of Integrative Agriculture, 18, 70–82.
Lee B, Lin P C, Cha H S, Luo J, Chen F. 2016. Characterization of volatile compounds in Cowart muscadine grape (Vitis rotundifolia) during ripening stages using GC-MS combined with principal component analysis. Food Science and Biotechnology, 25, 1319–1326.
Lee K R, Kim S H, Go Y S, Jung S M, Roh K H, Kim J B, Suh M C, Lee S, Kim H U. 2012. Molecular cloning and functional analysis of two FAD2 genes from american grape (Vitis labrusca L.). Gene, 509, 189–194.
Li D P, Xu Y F, Xu G M, Gu L K, Li D Q, Shu H R. 2006. Molecular cloning and expression of a gene encoding alcohol acyltransferase (MdAAT2) from apple (cv. Golden Delicious). Phytochemistry, 67, 658–667.
Lin J, Massonnet M, Cantu D. 2019. The genetic basis of grape and wine aroma. Horticulture Research, 6, 81–104.
Luan F, Wüst M. 2002. Differential incorporation of 1-deoxy-D-xylulose into (3S)-linalool and geraniol in grape berry exocarp and mesocarp. Phytochemistry, 60, 451–459.
Maffei M E, Gertsch J, Appendino G. 2011. Plant volatiles: Production, function and pharmacology. Natural Product Reports, 28, 1359–1380.
Martin D M, Aubourg S, Schouwey M B, Daviet L, Schalk M, Toub O, Lund S T, Bohlmann J. 2010. Functional annotation, genome organization and phylogeny of the grapevine (Vitis vinifera) terpene synthase gene family based on genome assembly, flcDNA cloning, and enzyme assays. BMC Plant Biology, 10, 226–247.
Mateo J J, Jiménez M. 2000. Monoterpenes in grape juice and wines. Journal of Chromatography (A), 881, 557–567.
May B, Lange B M, Wüst M. 2013. Biosynthesis of sesquiterpenes in grape berry exocarp of Vitis vinifera L.: Evidence for a transport of farnesyl diphosphate precursors from plastids to the cytosol. Phytochemistry, 95, 135–144.
McGarvey D J, Croteau R. 1995. Terpenoid metabolism. The Plant Cell, 7, 1015–1026.
Pazouki L, Niinemets Ü. 2016. Multi-substrate terpene synthases: Their occurrence and physiological significance. Frontiers in Plant Science, 7, 1019–1034.
Pérez A G, Olías R, Ríos J J, Olías J M. 1996. Evolution of strawberry alcohol acytransferase activity during fruit development and storage. Journal of Agricultural and Food Chemistry, 44, 3286–3290.
Pérez A G, Sanz C, Olías J M. 1993. Partial purification and some properties of alcohol acyltransferase from strawberry fruits. Journal of Agricultural and Food Chemistry, 41, 1462–1466.
Podolyan A, White J, Jordan B, Winefield C. 2010. Identification of the lipoxygenase gene family from Vitis vinifera and biochemical characterisation of two 13-lipoxygenases expressed in grape berries of Sauvignon Blanc. Functional Plant Biology, 37, 767–784.
Schwab W, Davidovich-Rikanati R, Lewinsohn. 2008. Biosynthesis of plant-derived flavor compounds. The Plant Journal, 54, 712–732.
Shalit M, Katzir N, Tadmor Y, Larkov O, Burger Y, Shalekhet F, Lastochkin E, Ravid U, Amar O, Edelstein M, Karchi Z, Lewinsohn E. 2001. Acetyl-CoA: alcohol acetyltransferase activity and aroma formation in ripening melon fruits. Journal of Agricultural and Food Chemistry, 49, 794–799.
Souleyre E J F, Chagne D, Chen X, Tomes S, Turner R M, Wang M Y, Maddumage R, Hunt M B, Winz R A, Wiedow C, Hamiaux C, Gardiner S E, Rowan D D, Atkinson R G. 2014. The AAT1 locus is critical for the biosynthesis of esters contributing to ‘ripe apple’ flavour in ‘Royal Gala’ and ‘Granny Smith’ apples. The Plant Journal, 78, 903–915.
Souleyre E J F, Greenwood D R, Friel E N, Karunairetnam S, Newcomb R D. 2005. An alcohol acyl transferase from apple (cv. Royal Gala), MpAAT1, produces esters involved in apple fruit flavor. FEBS Journal, 272, 3132–3144.
Tesnière C, Davies C, Sreekantan L, Bogs J, Thomas M, Torregrosa L. 2006. Analysis of the transcript levels of VvAdh1, VvAdh2 and VvGrip4, three genes highly expressed during Vitis vinifera L. berry development. Vitis, 45, 75–79.
Tesnière C, Verriès C. 2000. Molecular cloning and expression of cDNAs encoding alcohol dehydrogenases from Vitis vinifera L. during berry development. Plant Science, 157, 77–88.
Vilanova M, Genisheva Z, Bescansa L, Masa A, Oliveira J M. 2012. Changes in free and bound fractions of aroma compounds of four Vitis vinifera cultivars at the last ripening stages. Phytochemistry, 74, 196–205.
Vranová E, Coman D, Gruissem W. 2013. Network analysis of the MVA and MEP pathways of isoprenoid synthesis. Annual Review of Plant Biology, 64, 665–700.
Wang C, Xing J, Chin C K, Ho C T, Martin C E. 2001. Modification of fatty acids changes the flavor volatiles in tomato leaves. Phytochemistry, 58, 227–232.
Wang D, Cai J, Zhu B Q, Wu G F, Duan C Q, Chen G, Shi Y. 2015. Study of free and glycosidically bound volatile compounds in air-dried raisins from three seedless grape varieties using HS-SPME with GC-MS. Food Chemistry, 177, 346–353.
Wang J, Luca V D. 2005. The biosynthesis and regulation of biosynthesis of Concord grape fruit esters, including ‘foxy’ methylanthranilate. Plant Journal, 44, 606–619.
Wu Y S, Duan S Y, Zhao L P, Gao Z, Luo M, Song S R, Xu W P, Zhang C X, Ma C, Wang S P. 2016. Aroma characterization based on aromatic series analysis in table grapes. Scientific Reportes, 6, 31116.
Xu X Q, Cheng G, Duan L L, Jiang R, Pan Q H, Duan C Q, Wang J. 2015. Effect of training systems on fatty acids and their derived volatiles in Cabernet Sauvignon grapes and wines of the north foot of Mt. Tianshan. Food Chemistry, 181, 198–206.
Yahyaoui F E L, Wongs-Aree C, Latche A, Hackett R, Grierson D, Pech J C. 2002. Molecular and biochemical characteristics of a gene encoding an alcohol acyl-transferase involved in the generation of aroma volatile esters during melon ripening. European Journal of Biochemistry, 269, 2359–2366.
Yang C X, Wang Y J, Liang Z C, Fan P G, Wu B H, Yang L, Wang Y N, Li S H. 2009. Volatiles of grape berries evaluated at the germplasm level by headspace-SPME with GC-MS. Food Chemistry, 114, 1106–1114.
Yang C X, Wang Y J, Wu B H, Fang J B, Li S H. 2011. Volatile compounds evolution of three table grapes with different flavour during and after maturation. Food Chemistry, 128, 823–830.
Zhang E P, Chai F M, Zhang H H, Li S H, Liang Z C, Fan P G. 2017. Effects of sunlight exclusion on the profiles of monoterpene biosynthesis and accumulation in grape exocarp and mesocarp. Food Chemistry, 237, 379–389.
Zhu B Q, Xu X Q, Wu Y W, Duan C Q, Pan Q H. 2012. Isolation and characterization of two hydroperoxide lyase genes from grape berries. Molecular Biology Reports, 39, 7443–7455.
 
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