1,605
Views
1
CrossRef citations to date
0
Altmetric
Plant Environment Interactions

Proteomic sensing associated with terpenoid biosynthesis of Artemisia annua L. in response to different artificial light spectra

, ORCID Icon, & ORCID Icon
Pages 19-32 | Received 26 Jul 2021, Accepted 17 Nov 2021, Published online: 29 Dec 2021

References

  • Abbas F, Ke Y, Yu R, Yue Y, Amanullah S, Jahangir MM, Fan Y. 2017. Volatile terpenoids: multiple functions, biosynthesis, modulation and manipulation by genetic engineering. Planta. 246:803–816.
  • Abe S, Sado A, Tanaka K, Kisugi T, Asami K, Ota S, Kim HI, Yoneyama K, Xie X, Ohnishi T, et al. 2014. Carlactone is converted to carlactonoic acid by MAX1 in Arabidopsis and its methyl ester can directly interact with AtD14 in vitro. PNAS. 111:18084–18089.
  • Aharoni A, Giri AP, Verstappen FW, Bertea CM, Sevenier R, Sun Z, Jongsma MA, Schwab W, Bouwmeester HJ. 2004. Gain and loss of fruit flavor compounds produced by wild and cultivated strawberry species. Plant Cell. 16:3110–3131.
  • Antonsen S, Skattebøl L, Stenstrøm Y. 2014. Synthesis of Racemic β-Chamigrene, a Spiro[5.5]undecane Sesquiterpene. Molecules. 19:20664–20670.
  • Aracri B, Bartley GE, Scolnik PA, Giuliano G. 1994. Sequence of the phytoene desaturase locus of tomato. Plant Physiol. 106:789.
  • Araki T, Saga Y, Marugami M, Otaka J, Araya H, Saito K, Yamazaki M, Suzuki H, Kushiro T. 2016. Onocerin biosynthesis requires two highly dedicated triterpene cyclases in a fern Lycopodium clavatum. Chembiochem. 17:288–290.
  • Attia M, Kim SU, Ro DK. 2012. Molecular cloning and characterization of (+)-epi-α-bisabolol synthase, catalyzing the first step in the biosynthesis of the natural sweetener, hernandulcin, in Lippia dulcis. Arch. Biochem Biophys. 527:37–44.
  • Attucci S, Aitken SM, Gulick PJ, Ibrahim RK. 1995. Farnesyl pyrophosphate synthase from white lupin: molecular cloning, expression, and purification of the expressed protein. Arch Biochem Biophys. 321:493–500.
  • Aubourg S, Lecharny A, Bohlmann J. 2002. Genomic analysis of the terpenoid synthase (AtTPS) gene family of Arabidopsis thaliana. Mol Genet Genom. 267:730–745.
  • Back K, Chappell J. 1995. Cloning and bacterial expression of a sesquiterpene cyclase from Hyoscyamus muticus and its molecular comparison to related terpene cyclases. J Biol Chem. 270:7375–7381.
  • Barber J, Andersson B. 1992. Too much of a good thing: light can be bad for photosynthesis. Trends Biochem Sci. 17:61–66.
  • Bardou P, Mariette J, Escudié F, Djemiel C, Klopp C. 2014. jvenn: an interactive Venn diagram viewer. BMC Bioinformatics. 15:1.
  • Bartley GE, Scolnik PA. 1993. cDNA cloning, expression during development, and genome mapping of PSY2, a second tomato gene encoding phytoene synthase. J Biol Chem. 268:25718–25721.
  • Basyuni M, Oku H, Tsujimoto E, Kinjo K, Baba S, Takara K. 2007. Triterpene synthases from the Okinawan mangrove tribe, Rhizophoraceae. FEBS. 274:5028–5042.
  • Bertea CM, Schalk M, Karp F, Maffei M, Croteau R. 2001. Demonstration that menthofuran synthase of mint (Mentha) is a cytochrome p450 monooxygenase: cloning, functional expression, and characterization of the responsible gene. Arch Biochem Biophys. 390:279–286.
  • Bhakuni RS, Jain DC, Sharma RP, Kumar S. 2001. Secondary metabolites of Artemisia annua and their biological activity. Curr Sci. 80:35–48.
  • Bleeker PM, Spyropoulou EA, Diergaarde PJ, Volpin H, De Both MT, Zerbe P, Bohlmann J, Falara V, Matsuba Y, Pichersky E, et al. 2011. RNA-seq discovery, functional characterization, and comparison of sesquiterpene synthases from Solanum lycopersicum and Solanum habrochaites trichomes. Plant Mol. Biol. 77:323–336.
  • Block AK, Vaughan MM, Schmelz EA, Christensen SA. 2019. Biosynthesis and function of terpenoid defense compounds in maize (Zea mays). Planta. 249:21–30.
  • Bohlmann J, Keeling CI. 2008. Terpenoid biomaterials. Plant J. 54:656–669.
  • Bohlmann J, Stauber EJ, Krock B, Oldham NJ, Gershenzon J, Baldwin IT. 2002. Gene expression of 5-epi-aristolochene synthase and formation of capsidiol in roots of Nicotiana attenuata and N. sylvestris. Phytochemistry. 60:109–116.
  • Bohlmann J, Steele CL, Croteau R. 1997. Monoterpene synthases from grand fir (Abies grandis). cDNA isolation, characterization, and functional expression of myrcene synthase, (-)-(4S)-limonene synthase, and (-)-(1S,5S)-pinene synthase. J. Biol. Chem. 272:21784–21792.
  • Bonk M, Hoffmann B, Von Lintig J, Schledz M, Al-Babili S, Hobeika E, Kleinig H, Beyer P. 1997. Chloroplast import of four carotenoid biosynthetic enzymes in vitro reveals differential fates prior to membrane binding and oligomeric assembly. FEBS. 247:942–950.
  • Bradford MM. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 72:248–254.
  • Breitenbach J, Kuntz M, Takaichi S, Sandmann G. 1999. Catalytic properties of an expressed and purified higher plant type zeta-carotene desaturase from Capsicum annuum. FEBS. 265:376–383.
  • Breitenbach J, Sandmann G. 2005. zeta-carotene cis isomers as products and substrates in the plant poly-cis carotenoid biosynthetic pathway to lycopene. Planta. 220:785–793.
  • Bryant L, Patole C, Cramer R. 2016. Proteomic analysis of the medicinal plant Artemisia annua: data from leaf and trichome extracts. Data Brief. 7:325–331.
  • Cai Y, Luo Q, Sun M, Corke H. 2004. Antioxidant activity and phenolic compounds of 112 traditional Chinese medicinal plants associated with anticancer. Life Sci. 74:2157–2184.
  • Chang Z. 2016. The discovery of Qinghaosu (artemisinin) as an effective anti-malaria drug: a unique China story. Sci China Life Sci. 59:81–88.
  • Cheng CY, Krishnakumar V, Chan AP, Thibaud-Nissen F, Schobel S, Town CD. 2017. Araport11: a complete reannotation of the Arabidopsis thaliana reference genome. Plant J. 89:789–804.
  • Chi YH, Koo SS, Oh HT, Lee ES, Park JH, Phan KAT, Wi SD, Bae SB, Paeng SK, Chae HB, et al. 2019. The physiological functions of universal stress proteins and their molecular mechanism to protect plants from environmental stresses. Front Plant Sci. 10:750.
  • Chiou CY, Pan HA, Chuang YN, Yeh KW. 2010. Differential expression of carotenoid-related genes determines diversified carotenoid coloration in floral tissues of Oncidium cultivars. Planta. 232:937–948.
  • Choi D, Ward BL, Bostock RM. 1992. Differential induction and suppression of potato 3-hydroxy-3-methylglutaryl coenzyme A reductase genes in response to Phytophthora infestans and to its elicitor arachidonic acid. Plant Cell. 4:1333–1344.
  • Chye ML, Tan CT, Chua NH. 1992. Three genes encode 3-hydroxy-3-methylglutaryl-coenzyme A reductase in Hevea brasiliensis: hmg1 and hmg3 are differentially expressed. Plant Mol Biol. 19:473–484.
  • Colby SM, Crock J, Dowdle-Rizzo B, Lemaux PG, Croteau R. 1998. Germacrene c synthase from Lycopersicon esculentum cv. VFNT cherry tomato: cDNA isolation, characterization, and bacterial expression of the multiple product sesquiterpene cyclase. PNAS. 95:2216–2221.
  • Cordier H, Karst F, Bergès T. 1999. Heterologous expression in Saccharomyces cerevisiae of an Arabidopsis thaliana cDNA encoding mevalonate diphosphate decarboxylase. Plant Mol Biol. 39:953–967.
  • Czechowski T, Larson TR, Catania TM, Harvey D, Wei C, Essome M, Brown GD, Graham IA. 2018. Detailed phytochemical analysis of high- and low artemisinin-producing chemotypes of Artemisia annua. Front Plant Sci. 9:641–641.
  • Deguerry F, Pastore L, Wu S, Clark A, Chappell J, Schalk M. 2006. The diverse sesquiterpene profile of patchouli, Pogostemon cablin, is correlated with a limited number of sesquiterpene synthases. Arch Biochem Biophys. 454:123–136.
  • Dias T, Brito I, Moujir L, Paiz N, Darias J, Cueto M. 2005. Cytotoxic sesquiterpenes from Aplysia dactylomela. J Nat Prod. 68:1677–1679.
  • Dinakar C, Djilianov D, Bartels D. 2012. Photosynthesis in desiccation tolerant plants: energy metabolism and antioxidative stress defense. Plant Sci. 182:29–41.
  • Dondorp AM, Nosten F, Yi P, Das D, Phyo AP, Tarning J, Lwin KM, Ariey F, Hanpithakpong W, Lee SJ, et al. 2009. Artemisinin resistance in Plasmodium falciparum malaria. N Engl J Med. 361:455–467.
  • Dudareva N, Martin D, Kish CM, Kolosova N, Gorenstein N, Fäldt J, Miller B, Bohlmann J. 2003. (E)-beta-ocimene and myrcene synthase genes of floral scent biosynthesis in snapdragon: function and expression of three terpene synthase genes of a new terpene synthase subfamily. Plant Cell. 15:1227–1241.
  • Efferth T, Dunstan H, Sauerbrey A, Miyachi H, Chitambar C. 2001. The anti-malarial artesunate is also active against cancer. Int J Oncol. 18:767–773.
  • Fitzpatrick AH, Bhandari J, Crowell DN. 2011. Farnesol kinase is involved in farnesol metabolism, ABA signaling and flower development in Arabidopsis. Plant J. 66:1078–1088.
  • Fuglevand G, Jackson JA, Jenkins GI. 1996. UV-B, UV-A, and blue light signal transduction pathways interact synergistically to regulate chalcone synthase gene expression in Arabidopsis. Plant Cell. 8:2347–2357.
  • Genschik P, Criqui MC, Parmentier Y, Marbach J, Durr A, Fleck J, Jamet E. 1992. Isolation and characterization of a cDNA encoding a 3-hydroxy-3-methylglutaryl coenzyme A reductase from Nicotiana sylvestris. Plant Mol. Biol. 20:337–341.
  • Gomez SK, Cox MM, Bede JC, Inoue K, Alborn HT, Tumlinson JH, Korth KL. 2005. Lepidopteran herbivory and oral factors induce transcripts encoding novel terpene synthases in Medicago truncatula. Arch. Insect Biochem. Physiol. 58:114–127.
  • Graziose R, Lila MA, Raskin I. 2010. Merging traditional Chinese medicine with modern drug discovery technologies to find novel drugs and functional foods. Curr Drug Discov Technol. 7:2–12.
  • Hall DE, Robert JA, Keeling CI, Domanski D, Quesada AL, Jancsik S, Kuzyk MA, Hamberger B, Borchers CH, Bohlmann J. 2011. An integrated genomic, proteomic and biochemical analysis of (+)-3-carene biosynthesis in Sitka spruce (Picea sitchensis) genotypes that are resistant or susceptible to white pine weevil. Plant J. 65:936–948.
  • Hayashi H, Huang P, Inoue K, Hiraoka N, Ikeshiro Y, Yazaki K, Tanaka S, Kushiro T, Shibuya M, Ebizuka Y. 2001. Molecular cloning and characterization of isomultiflorenol synthase, a new triterpene synthase from Luffa cylindrica, involved in biosynthesis of bryonolic acid. FEBS. 268:6311–6317.
  • Heijde M, Ulm R. 2012. UV-B photoreceptor-mediated signalling in plants. Trends Plant Sci. 17:230–237.
  • Hemm MR, Rider SD, Ogas J, Murry DJ, Chapple C. 2004. Light induces phenylpropanoid metabolism in Arabidopsis roots. Plant J. 38:765–778.
  • Hemmerlin A, Hoeffler JF, Meyer O, Tritsch D, Kagan IA, Grosdemange-Billiard C, Rohmer M, Bach TJ. 2003. Cross-talk between the cytosolic mevalonate and the plastidial methylerythritol phosphate pathways in tobacco bright yellow-2 cells. J Biol Chem. 278:26666–26676.
  • Henry LK, Gutensohn M, Thomas ST, Noel JP, Dudareva N. 2015. Orthologs of the archaeal isopentenyl phosphate kinase regulate terpenoid production in plants. PNAS. 112:10050–10055.
  • Hieber AD, Mudalige-Jayawickrama RG, Kuehnle AR. 2006. Color genes in the orchid Oncidium Gower Ramsey: identification, expression, and potential genetic instability in an interspecific cross. Planta. 223:521–531.
  • Huang H, Ullah F, Zhou D-X, Yi M, Zhao Y. 2019. Mechanisms of ROS regulation of Plant development and stress responses. Front Plant Sci. 10:800.
  • Huang R, Wang Y, Wang P, Li C, Xiao F, Chen N, Li N, Li C, Sun C, Li L, et al. 2018. A single nucleotide mutation of IspF gene involved in the MEP pathway for isoprenoid biosynthesis causes yellow-Green leaf phenotype in rice. Plant Mol Biol. 96:5–16.
  • Husselstein-Muller T, Schaller H, Benveniste P. 2001. Molecular cloning and expression in yeast of 2,3-oxidosqualene-triterpenoid cyclases from Arabidopsis thaliana. Plant Mol. Biol. 45:75–92.
  • Iijima Y, Davidovich-Rikanati R, Fridman E, Gang DR, Bar E, Lewinsohn E, Pichersky E. 2004. The biochemical and molecular basis for the divergent patterns in the biosynthesis of terpenes and phenylpropenes in the peltate glands of three cultivars of basil. Plant Physio. 136:3724–3736.
  • Irmisch S, Krause ST, Kunert G, Gershenzon J, Degenhardt J, Köllner TG. 2012. The organ-specific expression of terpene synthase genes contributes to the terpene hydrocarbon composition of chamomile essential oils. BMC Plant Biol. 12:84.
  • Jenkins GI. 2014. The UV-B photoreceptor UVR8: from structure to physiology. Plant Cell. 26:21–37.
  • Jones CG, Moniodis J, Zulak KG, Scaffidi A, Plummer JA, Ghisalberti EL, Barbour EL, Bohlmann J. 2011. Sandalwood fragrance biosynthesis involves sesquiterpene synthases of both the terpene synthase (TPS)-a and TPS-b subfamilies, including santalene synthases. J Biol Chem. 286:17445–17454.
  • Kajiwara S, Kakizono T, Saito T, Kondo K, Ohtani T, Nishio N, Nagai S, Misawa N. 1995. Isolation and functional identification of a novel cDNA for astaxanthin biosynthesis from Haematococcus pluvialis, and astaxanthin synthesis in Escherichia coli. Plant Mol. Biol. 29:343–352.
  • Karaket N, Wiyakrutta S, Lacaille-Dubois MA, Supaibulwatana K. 2014. T-DNA insertion alters the terpenoid content composition and bioactivity of transgenic Artemisia annua. Nat Prod Commun. 9:363–366.
  • Karvouni Z, John I, Taylor JE, Watson CF, Turner AJ, Grierson D. 1995. Isolation and characterisation of a melon cDNA clone encoding phytoene synthase. Plant Mol Biol. 27:1153–1162.
  • Keller Y, Bouvier F, d’Harlingue A, Camara B. 1998. Metabolic compartmentation of plastid prenyl lipid biosynthesis-evidence for the involvement of a multifunctional geranylgeranyl reductase. FEBS. 251:413–417.
  • Khoury M, El Beyrouthy M, Ouaini N, Iriti M, Eparvier V, Stien D. 2014. Chemical composition and antimicrobial activity of the essential oil of Juniperus excelsa M. Bieb. Growing Wild in Lebanon. Chem Biodivers. 11:825–830.
  • Klayman DL. 1985. Qinghaosu (artemisinin): an antimalarial drug from China. Science. 228:1049–1055.
  • Köllner TG, Gershenzon J, Degenhardt J. 2009. Molecular and biochemical evolution of maize terpene synthase 10, an enzyme of indirect defense. Phytochemistry. 70:1139–1145.
  • Köllner TG, Schnee C, Li S, Svatos A, Schneider B, Gershenzon J, Degenhardt J. 2008. Protonation of a neutral (S)-beta-bisabolene intermediate is involved in (S)-beta-macrocarpene formation by the maize sesquiterpene synthases TPS6 and TPS11. J Biol Chem. 283:20779–20788.
  • Kong SG, Okajima K. 2016. Diverse photoreceptors and light responses in plants. J Plant Res. 129:111–114.
  • Korth KL, Stermer BA, Bhattacharyya MK, Dixon RA. 1997. HMG-CoA reductase gene families that differentially accumulate transcripts in potato tubers are developmentally expressed in floral tissues. Plant Mol. Biol. 33:545–551.
  • Koschmieder J, Fehling-Kaschek M, Schaub P, Ghisla S, Brausemann A, Timmer J, Beyer P. 2017. Plant-type phytoene desaturase: functional evaluation of structural implications. PloS one. 12:e0187628.
  • Kranz-Finger S, Mahmoud O, Ricklefs E, Ditz N, Bakkes PJ, Urlacher VB. 2018. Insights into the functional properties of the marneral oxidase CYP71A16 from Arabidopsis thaliana. Biochim Biophys Acta. 1866:2–10.
  • Lange BM, Croteau R. 1999. Isopentenyl diphosphate biosynthesis via a mevalonate-independent pathway: Isopentenyl monophosphate kinase catalyzes the terminal enzymatic step. PNAS. 96:13714–13719.
  • Laule O, Fürholz A, Chang H-S, Zhu T, Wang X, Heifetz PB, Gruissem W, Lange M. 2003. Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. PNAS. 100:6866–6871.
  • Lee S, Chappell J. 2008. Biochemical and genomic characterization of terpene synthases in Magnolia grandiflora. Plant Physiol. 147:1017–1033.
  • Legris M, Ince YÇ, Fankhauser C. 2019. Molecular mechanisms underlying phytochrome-controlled morphogenesis in plants. Nat Commun. 10:5219.
  • Li G, Köllner TG, Yin Y, Jiang Y, Chen H, Xu Y, Gershenzon J, Pichersky E, Chen F. 2012. Nonseed plant Selaginella moellendorffi has both seed plant and microbial types of terpene synthases. PNAS. 109:14711–14715.
  • Li Y. 2012. Qinghaosu (artemisinin): chemistry and pharmacology. Acta Pharmacol Sin. 33:1141–1146.
  • Li Z, Wakao S, Fischer BB, Niyogi KK. 2009. Sensing and responding to excess light. Annu Rev Plant Biol. 60:239–260.
  • Li ZH, Matthews PD, Burr B, Wurtzel ET. 1996. Cloning and characterization of a maize cDNA encoding phytoene desaturase, an enzyme of the carotenoid biosynthetic pathway. Plant Mol Biol. 30:269–279.
  • Lin C. 2002. Blue light receptors and signal transduction. Plant Cell. 14(Suppl):207–225.
  • Lluch MA, Masferrer A, Arró M, Boronat A, Ferrer A. 2000. Molecular cloning and expression analysis of the mevalonate kinase gene from Arabidopsis thaliana. Plant Mol Biol. 42:365–376.
  • Loizzo MR, Tundis R, Menichini F, Saab AM, Statti GA, Menichini F. 2008. Antiproliferative effects of essential oils and their major constituents in human renal adenocarcinoma and amelanotic melanoma cells. Cell Prolif. 41:1002–1012.
  • Lopes EM, Guimarães-Dias F, Gama TdSS, Macedo AL, Valverde AL, de Moraes MC, de Aguiar-Dias ACA, Bizzo HR, Alves-Ferreira M, Tavares ES, et al. 2020. Artemisia annua L. and photoresponse: from artemisinin accumulation, volatile profile and anatomical modifications to gene expression. Plant Cell Rep. 39:101–117.
  • Martin DM, Fäldt J, Bohlmann J. 2004. Functional characterization of nine Norway Spruce TPS genes and evolution of gymnosperm terpene synthases of the TPS-d subfamily. Plant Physiol. 135:1908–1927.
  • Mawphlang OIL, Kharshiing EV. 2017. Photoreceptor mediated plant growth responses: implications for photoreceptor engineering toward improved performance in crops. Front Plant Sci. 8:1181.
  • Mishra SK, Bae YS, Lee Y-M, Kim J-S, Oh SH, Kim HM. 2021. Sesquiterpene alcohol cedrol chemosensitizes human cancer cells and suppresses cell proliferation by destabilizing plasma membrane lipid rafts. Front Cell Dev. 8.
  • Montamat F, Guilloton M, Karst F, Delrot S. 1995. Isolation and characterization of a cDNA encoding Arabidopsis thaliana 3-hydroxy-3-methylglutaryl-coenzyme A synthase. Gene. 167:197–201.
  • Morita M, Shibuya M, Kushiro T, Masuda K, Ebizuka Y. 2000. Molecular cloning and functional expression of triterpene synthases from pea (Pisum sativum) new alpha-amyrin-producing enzyme is a multifunctional triterpene synthase. FEBS. 267:3453–3460.
  • Muhlemann JK, Klempien A, Dudareva N. 2014. Floral volatiles: from biosynthesis to function. Plant Cell Environ. 37:1936–1949.
  • Murashige T, Skoog F. 1962. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant. 15:473–497.
  • Nguyen DT, Göpfert JC, Ikezawa N, Macnevin G, Kathiresan M, Conrad J, Spring O, Ro DK. 2010. Biochemical conservation and evolution of germacrene A oxidase in Asteraceae. J Biol Chem. 285:16588–16598.
  • Niehaus TD, Okada S, Devarenne TP, Watt DS, Sviripa V, Chappell J. 2011. Identification of unique mechanisms for triterpene biosynthesis in Botryococcus braunii. PNAS. 108:12260–12265.
  • Okada A, Shimizu T, Okada K, Kuzuyama T, Koga J, Shibuya N, Nojiri H, Yamane H. 2007. Elicitor induced activation of the methylerythritol phosphate pathway toward phytoalexins biosynthesis in rice. Plant Mol Biol. 65:177–187.
  • Okuda S, Watanabe Y, Moriya Y, Kawano S, Yamamoto T, Matsumoto M, Takami T, Kobayashi D, Araki N, Yoshizawa AC, et al. 2016. jPOSTrepo: an international standard data repository for proteomes. Nucl Acids Res. 45:1107–1111.
  • Opitz S, Nes WD, Gershenzon J. 2014. Both methylerythritol phosphate and mevalonate pathways contribute to biosynthesis of each of the major isoprenoid classes in young cotton seedlings. Phytochemistry. 98:110–119.
  • Otomo K, Kenmoku H, Oikawa H, König WA, Toshima H, Mitsuhashi W, Yamane H, Sassa T, Toyomasu T. 2004. Biological functions of ent- and syn-copalyl diphosphate synthases in rice: key enzymes for the branch point of gibberellin and phytoalexin biosynthesis. Plant J. 39:886–893.
  • Peters RJ. 2006. Uncovering the complex metabolic network underlying diterpenoid phytoalexin biosynthesis in rice and other cereal crop plants. Phytochemistry. 67:2307–2317.
  • Phillips MA, Wildung MR, Williams DC, Hyatt DC, Croteau R. 2003. cDNA isolation, functional expression, and characterization of (+)-alpha-pinene synthase and (-)-alpha-pinene synthase from loblolly pine (Pinus taeda): stereocontrol in pinene biosynthesis. Arch Biochem Biophys. 411:267–276.
  • Rai R, Meena RP, Smita SS, Shukla A, Rai SK, Pandey-Rai S. 2011. UV-B and UV-C pre-treatments induce physiological changes and artemisinin biosynthesis in Artemisia annua L. – An antimalarial plant. J Photochem Photobiol. B. 105:216–225.
  • Ringer KL, McConkey ME, Davis EM, Rushing GW, Croteau R. 2003. Monoterpene double-bond reductases of the (-)-menthol biosynthetic pathway: isolation and characterization of cDNAs encoding (-)-isopiperitenone reductase and (+)-pulegone reductase of peppermint. Arch Biochem Biophys. 418:80–92.
  • Riou C, Tourte Y, Lacroute F, Karst F. 1994. Isolation and characterization of a cDNA encoding Arabidopsis thaliana mevalonate kinase by genetic complementation in yeast. Gene. 148:293–297.
  • Rivera SB, Swedlund BD, King GJ, Bell RN, Hussey CE, Shattuck-Eidens DM, Wrobel WM, Peiser GD, Poulter CD. 2001. Chrysanthemyl diphosphate synthase: isolation of the gene and characterization of the recombinant non-head-to-tail monoterpene synthase from Chrysanthemum cinerariaefolium. PNAS. 98:4373–4378.
  • Rohdich F, Wungsintaweekul J, Luttgen H, Fischer M, Eisenreich W, Schuhr CA, Fellermeier M, Schramek N, Zenk MH, Bacher A. 2000. Biosynthesis of terpenoids: 4-diphosphocytidyl-2-C-methyl-D-erythritol kinase from tomato. PNAS. 97:8251–8256.
  • Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, et al. 2003. TM4: a free, open-source system for microarray data management and analysis. BioTechniques. 34:374–378.
  • Sasaki K, Ohara K, Yazaki K. 2005. Gene expression and characterization of isoprene synthase from Populus alba. FEBS Lett. 579:2514–2518.
  • International Rice Genome Sequencing Project, Sasaki T. 2005. The map-based sequence of the rice genome. Nature. 436:793. (1476–4687).
  • Sawai S, Uchiyama H, Mizuno S, Aoki T, Akashi T, Ayabe S, Takahashi T. 2011. Molecular characterization of an oxidosqualene cyclase that yields shionone, a unique tetracyclic triterpene ketone of Aster tataricus. FEBS Lett. 585:1031–1036.
  • Schäfer UA, Reed DW, Hunter DG, Yao K, Weninger AM, Tsang EW, Reaney MJ, MacKenzie SL, Covello PS. 1999. An example of intron junctional sliding in the gene families encoding squalene monooxygenase homologues in Arabidopsis thaliana and Brassica napus. Plant Mol Biol. 39:721–728.
  • Schepmann HG, Pang J, Matsuda SP. 2001. Cloning and characterization of Ginkgo biloba levopimaradiene synthase which catalyzes the first committed step in ginkgolide biosynthesis. Arch Biochem Biophys. 392:263–269.
  • Sharopov FS, Salimov A, Numonov S, Safomuddin A, Bakri M, Salimov T, Setzer WN, Habasi M. 2020. Chemical composition, antioxidant, and antimicrobial activities of the essential oils from Аrtemisia annua L. growing wild in Tajikistan. Nat Prod Commun. 15:1934578X20927814.
  • Sharrock RA. 2008. The phytochrome red/far-red photoreceptor superfamily. Genome Biol. 9:230.
  • Supaibulwatana K, Banyai W, Cheewasakulyong P, Kirdmanee C, Kamchonwongpaisan S, Yuthavong Y. 2004. Effect of culture conditions, elicitation and induced mutagenesis on plant growth and productions of antimalarial agents in Artemisia annua L. In: Jonas R, Pandy A, Tharun G, editors. Proceedings of the biotechnological advances and application in bioconversion of renewable raw materials; Braunschweig, Germany. p. 240–249.
  • Swaminathan S, Morrone D, Wang Q, Fulton DB, Peters RJ. 2009. CYP76M7 is an ent-cassadiene C11alpha-hydroxylase defining a second multifunctional diterpenoid biosynthetic gene cluster in rice. Plant Cell. 21:3315–3325.
  • Takaya A, Zhang YW, Asawatreratanakul K, Wititsuwannakul D, Wititsuwannakul R, Takahashi S, Koyama T. 2003. Cloning, expression and characterization of a functional cDNA clone encoding geranylgeranyl diphosphate synthase of Hevea brasiliensis. Biochim Biophys Acta. 1625:214–220.
  • Wang G, Tian L, Aziz N, Broun P, Dai X, He J, King A, Zhao PX, Dixon RA. 2008. Terpene biosynthesis in glandular trichomes of hop. Plant Physiol. 148:1254–1266.
  • Wang J-w, Chen S-s, Zhang Y-m, Guan J, Su G-Y, Ding M, Li W, Zhao Y-Q. 2019. Anti-inflammatory and analgesic activity based on polymorphism of cedrol in mice. Environ Toxicol Pharmacol. 68:13–18.
  • Wang Q, Jia M, Huh JH, Muchlinski A, Peters RJ, Tholl D. 2016. Identification of a Dolabellane type Diterpene synthase and other root-expressed Diterpene synthases in Arabidopsis. Front Plant Sci. 7:1761.
  • Wang Z, Yeats T, Han H, Jetter R. 2010. Cloning and characterization of oxidosqualene cyclases from Kalanchoe daigremontiana: enzymes catalyzing up to 10 rearrangement steps yielding friedelin and other triterpenoids. J Biol Chem. 285:29703–29712.
  • Wu Y, Wang Q, Hillwig ML, Peters RJ. 2013. Picking sides: distinct roles for CYP76M6 and CYP76M8 in rice oryzalexin biosynthesis. Biochem J. 454:209–216.
  • Xie H-T, Wan Z-Y, Li S, Zhang Y. 2014. Spatiotemporal production of reactive oxygen species by NADPH oxidase is critical for tapetal programmed cell death and pollen development in arabidopsis. Plant Cell. 26:2007–2023.
  • Xie X, Kirby J, Keasling JD. 2012. Functional characterization of four sesquiterpene synthases from Ricinus communis (castor bean). Phytochemistry. 78:20–28.
  • Xu M, Wilderman PR, Morrone D, Xu J, Roy A, Margis-Pinheiro M, Upadhyaya NM, Coates RM, Peters RJ. 2007. Functional characterization of the rice kaurene synthase-like gene family. Phytochemistry. 68:312–326.
  • Yasumoto S, Fukushima EO, Seki H, Muranaka T. 2016. Novel triterpene oxidizing activity of Arabidopsis thaliana CYP716A subfamily enzymes. FEBS Lett. 590:533–540.
  • Yazaki K, Arimura G-i, Ohnishi T. 2017. ‘Hidden’ terpenoids in plants: their biosynthesis, localization and ecological roles. Plant Cell Physiol. 58:1615–1621.
  • Yu B, Liu Y, Pan Y, Liu J, Wang H, Tang Z. 2018. Light enhanced the biosynthesis of terpenoid indole alkaloids to meet the opening of cotyledons in process of photomorphogenesis of Catharanthus roseus. Plant Growth Regul. 84:617–626.
  • Yu J, Wang J, Lin W, Li S, Li H, Zhou J, Ni P, Dong W, Hu S, Zeng C, et al. 2005. The genomes of Oryza sativa: a history of duplications. PLoS Biol. 3:e38.
  • Zhang D, Sun W, Shi Y, Wu L, Zhang T, Xiang L. 2018. Red and blue light promote the accumulation of artemisinin in Artemisia annua L. Molecules. 23:1329.
  • Zhou X, Welsch R, Yang Y, Álvarez D, Riediger M, Yuan H, Fish T, Liu J, Thannhauser TW, Li L. 2015. Arabidopsis OR proteins are the major posttranscriptional regulators of phytoene synthase in controlling carotenoid biosynthesis. PNAS. 112:3558–3563.
  • Zhu C, Yamamura S, Nishihara M, Koiwa H, Sandmann G. 2003. cDNAs for the synthesis of cyclic carotenoids in petals of Gentiana lutea and their regulation during flower development. Biochim Biophys Acta. 1625:305–308.