5,689
Views
1
CrossRef citations to date
0
Altmetric
Review

Research progress in biosynthesis and regulation of plant terpenoids

, , & ORCID Icon
Pages 1799-1808 | Received 05 Aug 2021, Accepted 15 Dec 2021, Published online: 11 Jan 2022

References

  • Christianson DW. Structural and chemical biology of terpenoid cyclases. Chem Rev. 2017;117(17):11570–11648.
  • Gozari M, Alborz M, El-Seedi R, et al. Chemistry, biosynthesis and biological activity of terpenoids and meroterpenoids in bacteria and fungi isolated from different marine habitats. Eur J Med Chem. 2021;210:112957.
  • Zhou F, Pichersky E. More is better: the diversity of terpene metabolism in plants. Curr Opin Plant Biol. 2020;55:1–10.
  • Ashour M, Wink M, Gershenzon J. Biochemistry of terpenoids: monoterpenes, sesquiterpenes and diterpenes. In: Wink M, editor. Biochemistry of plant secondary metabolism. Chapter 5. Oxford: Wiley-Blackwell; 2010. p. 258–303.
  • Lassen LM, Nielsen AZ, Ziersen B, et al. Redirecting photosynthetic electron flow into light-driven synthesis of alternative products including high-value bioactive natural compounds. ACS Synth Biol. 2014;3(1):1–12.
  • Pateraki I, Heskes AM, Hamberger B. Cytochromes P450 for terpene functionalisation and metabolic engineering. Adv Biochem Eng Biotechnol. 2015;148:107–139.
  • Vavitsas K, Fabris M, Vickers CE. Terpenoid metabolic engineering in photosynthetic microorganisms. Genes. 2018;9(11):520.
  • Haba H, Lavaud C, Magid AA, et al. Diterpenoids and triterpenoids from Euphorbia retusa. J Nat Prod. 2009;72(7):1258–1264.
  • Fraser PD, Pinto ME, Holloway E, et al. Technical advance: application of high-performance liquid chromatography with photodiode array detection to the metabolic profiling of plant isoprenoids. Plant J. 2020;24:551–558.
  • Polatolu K, Karako MC. Biologically active essential oils against stored product pests-science direct. Essen Oils Food Preserv. 2016;5:39–59.
  • Xiao H, Zhang Y, Wang M. Discovery and engineering of cytochrome P450s for terpenoid biosynthesis. Trends Biotechnol. 2019;37(6):618–631.
  • Nagegowda DA. Plant volatile terpenoid metabolism: biosynthetic genes, transcriptional regulation and subcellular compartmentation. FEBS Lett. 2010;584(14):2965–2973.
  • Kleine S, Müller C. Drought stress and leaf herbivory affect root terpenoid concentrations and growth of tanacetum vulgare. J Chem Ecol. 2014;40(10):1115–1125.
  • Jonathan G, Natalia D. The function of terpene natural products in the natural world. Nat Chem Biol. 2007;3(7):408–414.
  • Wang GL, Xiong F, Que F, et al. Morphological characteristics, anatomical structure and gene expression: novel insights into gibberellin biosynthesis and perception during carrot growth and development. Hortic Res. 2015;2(1):e0134166.
  • Leng XP, Wang PP, Wang C, et al. Genome-wide identification and characterization of genes involved in carotenoid metabolic in three stages of grapevine fruit development. Sci Rep. 2017;7(1):4216.
  • Zhang T, Sun M, Guo Y, et al. Overexpression of LiDXS and LiDXR from lily (lilium siberia) enhances the terpenoid content in tobacco flowers. Front Plant Sci. 2018;9:909.
  • Li J, Yang Y, Chai M, et al. Gibberellins modulate local auxin biosynthesis and polar auxin transport by negatively affecting flavonoid biosynthesis in the root tips of rice. Plant Sci. 2020;298:110545.
  • Li Q, Li J, Zhang L, et al. Gibberellins are required for dimorphic flower development in Viola philippica. Plant Sci. 2021;303:110749.
  • Byers KJ, Vela JP, Peng F, et al. Floral volatile alleles can contribute to pollinator-mediated reproductive isolation in monkeyflowers (mimulus). Plant J. 2014;80(6):1031–1042.
  • Knudsen JT, Tollsten L. Trends in floral scent chemistry in pollination syndromes: floral scent composition in moth-pollinated taxa. Bot J Linn Soc. 1993;113(3):263–284.
  • Dobson HE. Relationship between floral fragrance composition and type of pollinator. In: Dudareva N, Pichersky E, editor. Biology of floral scent. Boca Raton (FL): Taylor and Francis; USA, 2016. p. 147–198.
  • Francesco L, Susanna P, Silvia F, et al. Volatile isoprenoids and their importance for protection against environmental constraints in the mediterranean area. Environ Exp Bot. 2014;103:99–106.
  • Willmer PG, Nuttman CV, Raine NE, et al. Floral volatiles controlling ant behaviour. Funct Ecol. 2009;23(5):888–900.
  • He J, Bouwmeester HJ, Dicke M, et al. Transcriptional and metabolite analysis reveal a shift in direct and indirect defences in response to spider-mite infestation in cucumber (Cucumis sativus). Plant Mol Biol. 2020;103(4-5):489–505.
  • Mumm R, Posthumus MA, Dicke M. Significance of terpenoids in induced indirect plant defence against herbivorous arthropods. Plant Cell Environ. 2008;31(4):575–585.
  • Turlings TC, Tumlinson JH, Lewis WJ. Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science. 1990;250(4985):1251–1253.
  • Nicol RW, Yousef L, Traquair JA, et al. Ginsenosides stimulate the growth of soil-brone pathogens of american ginseng. Phytochemistry. 2003;64(1):257–264.
  • Inderjit KG, Muker JI. Allelochemicals: Biological control of plant pathogens and disease. Vol. 157. Nertherlands: Springer Press; 2006.
  • Nishida N, Tamotsu S, Nagata N, et al. Allelopathic effects of volatile monoterpenoids produced by salvia leucophylla: Inhibition of cell proliferation and DNA synthesis in the root apical meristem of brassica campestris seedlings. J Chem Ecol. 2005;31(5):1187–1203.
  • Jose S, Gillespie AR. Allelopathy in black walnut (Juglans nigra L.) alley cropping: effects of juglone on hydroponically grown corn (Zea mays L.) and soybean (Glycine max L. Merr.) growth and physiology. Plant Soil. 1998;203(2):199–205.
  • Ervin GN, Wetzel RG. Allelochemical autotoxicity in the emergent wetland macrophyte juncus effusus (juncaceae). Am J Bot. 2000;87(6):853–860.
  • Chen TC, Fonseca COD, Schönthal AH. Preclinical development and clinical use of perillyl alcohol for chemoprevention and cancer therapy. Am J Cancer Res. 2015;5(5):1580–1593.
  • Chen F, Li W, Jiang L, et al. Functional characterization of a geraniol synthase-encoding gene from camptotheca acuminata and its application in production of geraniol in Escherichia coli. J Ind Microbiol Biotechnol. 2016;43(9):1281–1292.
  • Akiyama K, Matsuzaki K, Hayashi H. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature. 2005;435(7043):824–827.
  • Wu ZH, Liu D, Proksch P, et al. Punctaporonins H-M: caryophyllene-type sesquiterpenoids from the sponge-associated fungus Hansfordia sinuosae. Mar Drugs. 2014;12(7):3904–3916.
  • Aharoni A, Jongsma MA, Bouwmeester HJ. Volatile science? Metabolic engineering of terpenoids in plants. Trends Plant Sci. 2005;10(12):594–602.
  • George KW, Alonso-Gutierrez J, Keasling JD, et al. Isoprenoid drugs, biofuels, and chemicals-artemisinin, farnesene, and beyond. Adv Biochem Eng Biotechnol. 2015;148:355–398.
  • Fiedor J, Burda K. Potential role of carotenoids as antioxidants in human health and disease. Nutrients. 2014;6(2):466–488.
  • Cheng AC, Hsu YC, Tsai CC. The effects of cucurbitacin E on GADD45β-trigger G2/M arrest and JNK-independent pathway in brain cancer cells. J Cell Mol Med. 2019;23(5):3512–3519.
  • Saeed ME, Boulos JC, Elhaboub G, et al. Cytotoxicity of cucurbitacin E from citrullus colocynthis against multidrug-resistant cancer cells. Phytomedicine. 2019;62:152945.
  • Balkema-Boomstra AG, Zijlstra S, Verstappen FW, et al. Role of cucurbitacin C in reaistance to spider mite (tetranychus urticae) in cucumber (cucumis sativu L.). J Chem Ecol. 2003;29(1):225–235.
  • Kelly C, Jewell C, O’Brien NM. The effect of dietary sup-plementation with the citrus limonoids, lomonin and nomilinon xenobiotic-metabolizing enzymes in the liver and small intestine of the rat. Nutr Res. 2003;23(5):681–690.
  • Lam K, Zhang J. Citrus limoninoid reduction of chemically induced tumorigenesis. Food Technol. 1994;7(11):104–108.
  • Arnason JT, Philogène BJR, Donskov N, et al. Limonoids from the meliaceac and reduce feeding, growth and development of ostrinia nubilalis. Entomol Exp Appl. 1987;43(3):221–226.
  • Sun CD, Chen KS, Chen Y, et al. Contents and antioxi-dant capaeity of limonin and nomilinin different tissues of citrus fruit of four cultivars during fruit growth and maturation. Food Chem. 2005;93(4):599–605.
  • Xu Q, He Y, Yan X, et al. Unraveling a crosstalk regulatory network of temporal aroma accumulation in tea plant (Camellia sinensis) leaves by integration of metabolomics and transcriptomics. Environ Exp Bot. 2018;149:81–94.
  • Zhao H, Feng S, Zhou W, et al. Transcriptomic analysis of postharvest toon buds and key enzymes involved in terpenoid biosynthesis during cold storage. Sci Hortic. 2019;257:108747.
  • Xiao H, Zhong JJ. Production of useful terpenoids by higher-fungus cell factory and synthetic biology approaches. Trends Biotechnol. 2016;34(3):242–255.
  • Lange BM, Croteau R. Isoprenoid biosynthesis via a mevalonate-independent pathway in plants: cloning and heterologous expression of 1-deoxy-D-xylulose-5-phosphate reductoisomerase from peppermint. Arch Biochem Biophys. 1999;365(1):170–174.
  • Vranová E, Coman D, Gruissem W. Network analysis of the MVA and MEP pathways for isoprenoid synthesis. Annu Rev Plant Biol. 2013;64(1):665–700.
  • Dudareva N, Klempien AK, Muhlemann J, et al. Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol. 2013;198(1):16–32.
  • Francesco L, Jörg-Peter S. Abiotic stresses and induced BVOCs. Trends in Plant Sci. 2010;15(3):154–166.
  • Caelles C, Ferrer A, Balcells L, et al. Isolation and structural characterization of a cDNA encoding Arabidopsis thaliana 3-hydroxy-3-methylglutaryl coenzyme a reductase. Plant Mol Biol. 1989;13(6):627–638.
  • Zhang M, Liu H, Wang Q, et al. The 3-hydroxy-3-methylglutaryl-coenzyme a reductase 5 gene from Malus domestica enhances oxidative stress tolerance in Arabidopsis thaliana. Plant Physiol Biochem. 2020;146:269–277.
  • Shen G, Pang Y, Wu W, et al. Cloning and characterization of a root-specific expressing gene encoding 3-hydroxy-3-methylglutaryl coenzyme a reductase from ginkgo biloba. Mol Biol Rep. 2006;33(2):117–127.
  • Bansal S, Narnoliya LK, Mishra B, et al. HMG-CoA reductase from camphor tulsi (ocimum kilimandscharicum) regulated MVA dependent biosynthesis of diverse terpenoids in homologous and heterologous plant systems. Sci Rep. 2018;8(1):3547.
  • Jayashree R, Nazeem PA, Rekha K, et al . Over-expression of 3-hydroxy-3- methylglutaryl-coenzyme A reductase 1 (HMGR1) gene under super-promoter for enhanced latex biosynthesis in rubber tree (Hevea brasiliensis Muell. Arg.). Plant Physiol Biochem. 2018;127:414–424.
  • Battistini MR, Shoji C, Handa S, et al. Mechanistic binding insights for 1-deoxy-D-Xylulose-5-Phosphate synthase, the enzyme catalyzing the first reaction of isoprenoid biosynthesis in the malaria-causing protists, Plasmodium falciparum and Plasmodium vivax. Protein Expr Purif. 2016;120:16–27.
  • Rodriguez-Concepcion M, Boronat A. Breaking new ground in the regulation of the early steps of plant isoprenoid biosynthesis. Curr Opin Plant Biol. 2015;25:17–22.
  • Peebles CA, Sander GW, Hughes EH, et al . The expression of 1-deoxy-D-xylulose synthase and geraniol-10-hydroxylase or anthranilate synthase increases terpenoid indole alkaloid accumulation in Catharanthus roseus hairy roots. Metab Eng. 2011;13(2):234–240.
  • Henriquez MA, Soliman A, Li G, et al. Molecular cloning, functional characterization and expression of potato (Solanum tuberosum) 1-deoxy-D-xylulose 5-phosphate synthase 1 (StDXS1) in response to Phytophthora infestans. Plant Sci. 2016;243:71–83.
  • Yang J, Adhikari MN, Liu H, et al. Characterization and functional analysis of the genes encoding 1-deoxy-D-xylulose-5-phosphate reductoisomerase and 1-deoxy-D-xylulose-5-phosphate synthase, the two enzymes in the MEP pathway, from Amomum villosum lour. Mol Biol Rep. 2012;39(8):8287–8296.
  • Burke C, Croteau R . Geranyl diphosphate synthase from Abies grandis: cDNA isolation, functional expression, and characterization. Arch Biochem Biophys. 2002;405(1):130–136.
  • Han JL, Liu BY, Ye HC, et al. Effects of overexpression of the endogenous farnesyl diphosphate synthase on the artemisinin content in artemisia annua L. J Integr Plant Biol. 2006;48(4):482–487.
  • Okada K, Saito T, Nakagawa T, et al. Five geranylgeranyl diphosphate synthases expressed in different organs are localized into three subcellular compartments in arabidopsis. Plant Physiol. 2000;122(4):1045–1056.
  • Ament K, Schie VC, Bouwmeester HJ, et al. Induction of a leaf specific geranylgeranyl pyrophosphate synthase and emission of (E,E)-4,8,12-trimethyltrideca-1,3,7,11-tetraene in tomato are dependent on both jasmonic acid and salicylic acid signaling pathways. Planta. 2006;224(5):1197–1208.
  • Degenhardt J, Köllner TG, Gershenzon J. Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry. 2009;70(15-16):1621–1637.
  • Muchlinski A, Ibdah M, Ellison S, et al. Diversity and function of terpene synthases in the production of carrot aroma and flavor compounds. Sci Rep. 2020;10(1):9989.
  • Ashaari NS, Rahim MH, Sabri S, et al. Functional characterization of a new terpene synthase from Plectranthus amboinicus. PLoS One. 2020;15(7):e0235416.
  • Li MY, Feng K, Hou XL, et al. The genome sequence of celery (Apium graveolens L.), an important leaf vegetable crop rich in apigenin in the apiaceae family. Hortic Res. 2020;7:9.
  • Chen X, Chen H, Yuan JS, et al. The rice terpene synthase gene OsTPS19 functions as an (S)-limonene synthase in planta, and its overexpression leads to enhanced resistance to the blast fungus Magnaporthe oryzae. Plant Biotechnol J. 2018;16(10):1778–1787.
  • Kampranis SC, Ioannidis D, Purvis A, et al. Rational conversion of substrate and product specificity in a salvia monoterpene synthase: structural insights into the evolution of terpene synthase function. Plant Cell. 2007;19(6):1994–2005.
  • Green S, Baker EN, Laing W. A non-synonymous nucleotide substitution can account for one evolutionary route to sesquiterpene synthase activity in the TPS-b subgroup. FEBS Lett. 2011;585(12):1841–1846.
  • Shimada T, Endo T, Ana R, et al. Isolation and characterization of germacrene a synthases gene in citrus unshiu marc. Sci Hortic. 2012;145:102–108.
  • Cui MY. Expression, purification and characterization of four sesquiterpene synthases from salvia miltiorrhiza [PhD dissertation]. Harbin: Northeast Forestry University; 2016.
  • Tan H, Xiao L, Gao S, et al. TRICHOME and ARTEMISININ REGULATOR 1 is required for trichome development and artemisinin biosynthesis in artemisia annua. Mol Plant. 2015;8(9):1396–1411.
  • Broun P. Transcription factors as tools for metabolic engineering in plants. Curr Opin Plant Biol. 2004;7(2):202–209.
  • Xu YH, Wang JW, Wang S, et al . Characterization of GaWRKY1, a cotton transcription factor that regulates the sesquiterpene synthase gene (+)-delta-cadinene synthase-A. Plant Physiol. 2004;135(1):507–515.
  • He XY, Wang H, Yang JF, et al. RNA sequencing on Amomum villosum lour. induced by MeJA identifies the genes of WRKY and terpene synthases involved in terpene biosynthesis. Genome. 2018;61(2):91–102.
  • Mahjoub A, Hernould M, Joubes J, et al. Overexpression of a grapevine R2R3-MYB factor in tomato affects vegetative development, flower morphology and flavonoid and terpenoid metabolism. Plant Physiol Biochem. 2009;47(7):551–561.
  • Chuang YC, Hung YC, Tsai WC, et al. PbbHLH4 regulates floral monoterpene biosynthesis in phalaenopsis orchids. J Exp Bot. 2018;69(18):4363–4377.
  • Li X, Xu Y, Shen S, et al. Transcription factor CitERF71 activates the terpene synthase gene CitTPS16 involved in the synthesis of E-geraniol in sweet orange fruit. J Exp Bot. 2017;68(17):4929–4938.
  • Lu S, Xu R, Jia J, et al. Cloning and functional characterization of a beta-pinene synthase from Artemisia annua that shows a circadian pattern of expression. Plant Physiol. 2002;130(1):477–486.
  • Zheng R, Liu C, Wang Y, et al. Expression of MEP pathway genes and non-volatile sequestration are associated with circadian rhythm of dominant terpenoids emission in Osmanthus fragrans lour. Front Plant Sci. 2017;8:1869.
  • Chuang L, Wen CH, Lee YR, et al. Identification, functional characterization, and seasonal expression patterns of five sesquiterpene synthases in Liquidambar formosana. J Nat Prod. 2018;81(5):1162–1172.
  • Christensen LP, Kai G. Effect of development stage at harvest on the composition and yield of essential oils from thyme and oregano. Develop Food Sci. 2005;43(25):261–264.
  • Pandeló D, Melo TD, Singulani JL, et al. Oil production at different stages of leaf development in Lippia Alba. Rev Bras Farmacogn. 2012;22(3):497–501.
  • Zhou HC, Shamala LF, Yi XK, et al. Analysis of terpene synthase family genes in camellia sinensis with an emphasis on abiotic stress conditions. Sci Rep. 2020;10(1):933.
  • Fäldt J, Martin D, Miller B, et al. Traumatic resin defense in Norway spruce (picea abies): methyl jasmonate-induced terpene synthase gene expression, and cDNA cloning and functional characterization of (+)-3-carene synthase. Plant Mol Biol. 2003;51(1):119–133.
  • D’Onofrio C, Matarese F, Cuzzola A. Effect of methyl jasmonate on the aroma of sangiovese grapes and wines. Food Chem. 2018;242:352–361.
  • Shrivastava G, Ownley BH, Augé RM, et al. Colonization by arbuscular mycorrhizal and endophytic fungi enhanced terpene production in tomato plants and their defense against a herbivorous insect. Symbiosis. 2015;65(2):65–74.
  • Yoon SJ, Sukweenadhi J, Khorolragchaa A, et al. Overexpression of panax ginseng sesquiterpene synthase gene confers tolerance against Pseudomonas syringae pv. tomato in Arabidopsis thaliana. Physiol Mol Biol Plants. 2016;22(4):485–495.
  • Riedlmeier M, Ghirardo A, Wenig M, et al. Monoterpenes support systemic acquired resistance within and between plants. Plant Cell. 2017;29(6):1440–1459.
  • Van Poecke RM, Posthumus MA, Dicke M. Herbivore-induced volatile production by Arabidopsis thaliana leads to attraction of the parasitoid cotesia rubecula: chemical, behavioral, and gene-expression analysis. J Chem Ecol. 2001;27(10):1911–1928.
  • Hartikainen K, Riikonen J, Nerg A-M, et al. Impact of elevated temperature and ozone on the emission of volatile organic compounds and gas exchange of silver birch (Betula pendula roth). Environ Exp Bot. 2012;84:33–43.
  • Vanhatalo A, Ghirardo A, Juurola E, et al. Long-term dynamics of monoterpene synthase activities, monoterpene storage pools and emissions in boreal scots pine. Biogeosciences. 2018;15(16):5047–5060.
  • Duan Q, Kleiber A, Jansen K, et al. Effects of elevated growth temperature and enhanced atmospheric vapour pressure deficit on needle and root terpenoid contents of two douglas fir provenances. Environ Exp Bot. 2019;166:103819.
  • Lee GW, Lee S, Chung MS, et al. Rice terpene synthase 20 (OsTPS20) plays an important role in producing terpene volatiles in response to abiotic stresses. Protoplasma. 2015;252(4):997–1007.
  • Liao P, Wang H, Wang M, et al. Transgenic tobacco overexpressing brassica juncea HMG-CoA synthase 1 shows increased plant growth, pod size and seed yield. PLoS One. 2014;9(5):e98264.