Genetic diversity of limonene synthase genes in Rongan kumquat (Fortunella crassifolia)
Mengyu Liu
A B , Xiaofeng Liu A B , Junhua Hu A B , Yang Xue A B and Xiaochun Zhao A B C
+ Author Affiliations
- Author Affiliations
A Citrus Research Institute, Southwest University/Chinese Academy of Agricultural Sciences, Beibei, Chongqing, 400712, China.
B National Citrus Engineering Research Center, Beibei, Chongqing, 400712, China.
C Corresponding author. Email: zhaoxiaochun@cric.cn
Functional Plant Biology 47(5) 425-439 https://doi.org/10.1071/FP19051
Submitted: 16 February 2019 Accepted: 8 December 2019 Published: 25 March 2020
Abstract
D-limonene is the main component of citrus essential oils. In the monoterpene biosynthetic pathway, geranyl diphosphate reacts with monoterpenes to form the prenyl-carbocation intermediate to produce d-limonene. In this study, d-limonene synthase (FcLS) genes were first isolated from Rongan kumquat (Fortunella crassifolia Swingle). Sequencing analysis revealed that the open reading frames of 18 FcLS genes contain 12 single nucleotide polymorphisms, which resulted in the variation of FcLS proteins, indicating that the limonene synthase genes are a large family in F. crassifolia. This phenomenon has not been reported in Citrus. The predicted FcLS proteins showed a high amino acid sequence identity with other Citrus limonene synthases and also had the typical structures of limonene synthase protein. FcLS1 was validated to be a functional d-limonene synthase by prokaryotic expression.
Additional keywords: d-limonene synthase, functional analysis, limonene synthase gene family.
References
Ahmad MM, Rehman S, Anjum FM, Bajwa EE (2006) Comparative physical examination of various citrus peel essential oils. International Journal of Agriculture and Biology 8, 186–190.Alquézar B, Rodriguez A, de la Pena M, Pena L (2017) Genomic analysis of terpene synthase family and functional characterization of seven sesquiterpene synthases from Citrus sinensis. Frontiers in Plant Science 8, 1481
| Genomic analysis of terpene synthase family and functional characterization of seven sesquiterpene synthases from Citrus sinensis.Crossref | GoogleScholarGoogle Scholar | 28883829PubMed |
Aubourg S, Lecharny A, Bohlmann J (2002) Genomic analysis of the terpenoid synthase (AtTPS) gene family of Arabidopsis thaliana. Molecular Genetics and Genomics 267, 730–745.
| Genomic analysis of the terpenoid synthase (AtTPS) gene family of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 12207221PubMed |
Audic S, Claverie JM (1997) The significance of digital gene expression profiles. Genome Research 7, 986–995.
| The significance of digital gene expression profiles.Crossref | GoogleScholarGoogle Scholar | 9331369PubMed |
Bohlmann J, Meyer-Gauen G, Croteau R (1998) Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proceedings of the National Academy of Sciences of the United States of America 95, 4126–4133.
| Plant terpenoid synthases: molecular biology and phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar | 9539701PubMed |
Christianson DW (2008) Unearthing the roots of the terpenome. Current Opinion in Chemical Biology 12, 141–150.
| Unearthing the roots of the terpenome.Crossref | GoogleScholarGoogle Scholar | 18249199PubMed |
Demissie ZA, Sarker LS, Mahmoud SS (2011) Cloning and functional characterization of beta-phellandrene synthase from Lavandula angustifolia. Planta 233, 685–696.
| Cloning and functional characterization of beta-phellandrene synthase from Lavandula angustifolia.Crossref | GoogleScholarGoogle Scholar | 21165645PubMed |
Dewick PM (2002) The biosynthesis of C5–C25 terpenoid compounds. Natural Product Reports 19, 181–222.
| The biosynthesis of C5–C25 terpenoid compounds.Crossref | GoogleScholarGoogle Scholar | 12013278PubMed |
Dudareva N, Andersson S, Orlova I, Gatto N, Reichelt M, Rhodes D, Boland W, Gershenzon J (2005) The nonmevalonate pathway supports both monoterpene and sesquiterpene formation in snapdragon flowers. Proceedings of the National Academy of Sciences of the United States of America 102, 933–938.
| The nonmevalonate pathway supports both monoterpene and sesquiterpene formation in snapdragon flowers.Crossref | GoogleScholarGoogle Scholar | 15630092PubMed |
Goldstein JL, Brown MS (1990) Regulation of the mevalonate pathway. Nature 343, 425–430.
| Regulation of the mevalonate pathway.Crossref | GoogleScholarGoogle Scholar | 1967820PubMed |
Güney M, Oz AT, Kafkas E (2015) Comparison of lipids, fatty acids and volatile compounds of various kumquat species using HS/GC/MS/FID techniques. Journal of the Science of Food and Agriculture 95, 1268–1273.
| Comparison of lipids, fatty acids and volatile compounds of various kumquat species using HS/GC/MS/FID techniques.Crossref | GoogleScholarGoogle Scholar | 25044361PubMed |
Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y (2007) KEGG for linking genomes to life and the environment. Nucleic Acids Research 36, D480–D484.
| KEGG for linking genomes to life and the environment.Crossref | GoogleScholarGoogle Scholar | 18077471PubMed |
Li R, Yu C, Li Y, Lam TW, Yiu SM, Kristiansen K, Wang J (2009) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25, 1966–1967.
| SOAP2: an improved ultrafast tool for short read alignment.Crossref | GoogleScholarGoogle Scholar | 19497933PubMed |
Lücker J, El Tamer MK, Schwab W, Verstappen FW, van der Plas LH, Bouwmeester HJ, Verhoeven HA (2002) Monoterpene biosynthesis in lemon (Citrus limon) cDNA isolation and functional analysis of four monoterpene synthases. European Journal of Biochemistry 269, 3160–3171.
| Monoterpene biosynthesis in lemon (Citrus limon) cDNA isolation and functional analysis of four monoterpene synthases.Crossref | GoogleScholarGoogle Scholar | 12084056PubMed |
Martin VJ, Pitera DJ, Withers ST, Newman JD, Keasling JD (2003) Engineering a mevalonate pathway in Escherichia coli for production of terpenoids. Nature Biotechnology 21, 796–802.
| Engineering a mevalonate pathway in Escherichia coli for production of terpenoids.Crossref | GoogleScholarGoogle Scholar | 12778056PubMed |
Martin DM, Aubourg S, Schouwey MB, Daviet L, Schalk M, Toub O, Lund ST, 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
| Functional annotation, genome organization and phylogeny of the grapevine (Vitis vinifera) terpene synthase gene family based on genome assembly, FLcDNA cloning, and enzyme assays.Crossref | GoogleScholarGoogle Scholar | 20964856PubMed |
Morehouse BR, Kumar RP, Matos JO, Olsen SN, Entova S, Oprian DD (2017) Functional and structural characterization of a (+)-limonene synthase from Citrus sinensis. Biochemistry 56, 1706–1715.
| Functional and structural characterization of a (+)-limonene synthase from Citrus sinensis.Crossref | GoogleScholarGoogle Scholar | 28272875PubMed |
Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nature Methods 5, 621–628.
| Mapping and quantifying mammalian transcriptomes by RNA-Seq.Crossref | GoogleScholarGoogle Scholar | 18516045PubMed |
Pandreka A, Dandekar DS, Haldar S, Uttara V, Vijayshree SG, Mulani FA, Aarthy T, Thulasiram HV (2015) Triterpenoid profiling and functional characterization of the initial genes involved in isoprenoid biosynthesis in neem (Azadirachta indica). BMC Plant Biology 15, 214
| Triterpenoid profiling and functional characterization of the initial genes involved in isoprenoid biosynthesis in neem (Azadirachta indica).Crossref | GoogleScholarGoogle Scholar | 26335498PubMed |
Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF Chimera – a visualization system for exploratory research and analysis. Journal of Computational Chemistry 25, 1605–1612.
| UCSF Chimera – a visualization system for exploratory research and analysis.Crossref | GoogleScholarGoogle Scholar | 15264254PubMed |
Rohmer M (1999) The discovery of a mevalonate-independent pathway for isoprenoid biosynthesis in bacteria, algae and higher plants. Natural Product Reports 16, 565–574.
| The discovery of a mevalonate-independent pathway for isoprenoid biosynthesis in bacteria, algae and higher plants.Crossref | GoogleScholarGoogle Scholar | 10584331PubMed |
Ruberto G (2002) Analysis of volatile components of Citrus fruit essential oils. In ‘Analysis of taste and aroma. Vol. 21.’ (Ed. JF Jackson, HF Linskens) pp. 123–157. (Springer: Berlin, Heidelberg)
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406
Shimada T, Endo T, Fujii H, Hara M, Ueda T, Kita M, Omura M (2004) Molecular cloning and functional characterization of four monoterpene synthase genes from Citrus unshiu Marc. Plant Science 166, 49–58.
| Molecular cloning and functional characterization of four monoterpene synthase genes from Citrus unshiu Marc.Crossref | GoogleScholarGoogle Scholar |
Shimada T, Endo T, Fujii H, Hara M, Omura M (2005a) Isolation and characterization of (E)-beta-ocimene and 1,8 cineole synthases in Citrus unshiu Marc. Plant Science 168, 987–995.
| Isolation and characterization of (E)-beta-ocimene and 1,8 cineole synthases in Citrus unshiu Marc.Crossref | GoogleScholarGoogle Scholar |
Shimada T, Endo T, Fujii H, Omura M (2005b) Isolation and characterization of a new d-limonene synthase gene with a different expression pattern in Citrus unshiu Marc. Scientia Horticulturae 105, 507–512.
| Isolation and characterization of a new d-limonene synthase gene with a different expression pattern in Citrus unshiu Marc.Crossref | GoogleScholarGoogle Scholar |
Shimada T, Endo T, Fujii H, Rodriguez A, Pena L, Omura M (2014) Characterization of three linalool synthase genes from Citrus unshiu Marc. and analysis of linalool-mediated resistance against Xanthomonas citri subsp. citri and Penicilium italicum in citrus leaves and fruits. Plant Science 229, 154–166.
| Characterization of three linalool synthase genes from Citrus unshiu Marc. and analysis of linalool-mediated resistance against Xanthomonas citri subsp. citri and Penicilium italicum in citrus leaves and fruits.Crossref | GoogleScholarGoogle Scholar | 25443842PubMed |
Tholl D (2006) Terpene synthases and the regulation, diversity and biological roles of terpene metabolism. Current Opinion in Plant Biology 9, 297–304.
| Terpene synthases and the regulation, diversity and biological roles of terpene metabolism.Crossref | GoogleScholarGoogle Scholar | 16600670PubMed |
Vranová E, Coman D, Gruissem W (2013) Network analysis of the MVA and MEP pathways for isoprenoid synthesis. Annual Review of Plant Biology 64, 665–700.
| Network analysis of the MVA and MEP pathways for isoprenoid synthesis.Crossref | GoogleScholarGoogle Scholar | 23451776PubMed |
Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L, Wang J (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Research 34, W293–W297.
| WEGO: a web tool for plotting GO annotations.Crossref | GoogleScholarGoogle Scholar | 16845012PubMed |
Zhang H, Xie Y, Liu C, Chen S, Hu S, Xie Z, Deng X, Xu J (2017) Comprehensive comparative analysis of volatile compounds in citrus fruits of different species. Food Chemistry 230, 316–326.
| Comprehensive comparative analysis of volatile compounds in citrus fruits of different species.Crossref | GoogleScholarGoogle Scholar | 28407917PubMed |
