Abstract
Pyrethrin is a potent biopesticide, a natural mixture of six compounds (pyrethrin I and II, cinerin I and II, and jasmolin I and II), biosynthesized in plants of Dalmatian pyrethrum (Tanacetum cinerariifolium (Trevir.) Sch. Bip.), a species endemic to the eastern Adriatic coast, but grown worldwide. Not many known natural insecticides encompass such superior qualities as pyrethrin—very high efficacy against a broad spectrum of pests in combination with minor adverse effects on human health and the environment. In previous decades, pyrethrin was largely replaced by its synthetic derivatives, pyrethroids. However, due to their harmful effects on various species and ecosystems, the use of pyrethrin should again take the lead. This review summarizes one century (1920–2020) of research on the properties and use of pyrethrum as a source of pyrethrins. The primary focus is on presenting its current advantages and disadvantages, toxicity on target and non-target species, biosynthesis, factors that influence the pyrethrins content in pyrethrum, comparison of different methods of their extraction and determination; as well as its production potential and development of new products. The final goal is to present possible approaches to improve and enhance the use of this highly effective but still underused phytochemical insecticide with unique properties.
Similar content being viewed by others
Change history
01 October 2021
A Correction to this paper has been published: https://doi.org/10.1007/s11101-021-09778-w
Abbreviations
- MEP:
-
2-C-methyl-d-erithritol 4-phosphate
- IPP:
-
Isopentenyl pyrophosphate
- DMAPP:
-
Dimethylallyl diphosphate
- CDP:
-
Chrysanthemyl diphosphate
- TcLOX1:
-
T. cinerariifolium 13-lipoxygenase
- AOS:
-
Allene oxide synthase
- AOC:
-
Allene oxide cyclase
- TcJMH:
-
T. cinerariifolium jasmone hydroxylase
- TcPYS:
-
T. cinerariifolium pyrethrolone synthase
- TcCDS:
-
T. cinerariifolium chrysanthemyl diphosphate synthase
- TcADH2:
-
T. cinerariifolium alcohol dehydrogenase 2
- TcALDH1:
-
T. cinerariifolium aldehyde dehydrogenase 1
- TcCHH:
-
T. cinerariifolium chrysanthemol 10-hydroxylase
- TcCCMT:
-
T. cinerariifolium 10-carboxychrysanthemic acid 10-methyltransferase
- TcGLIP:
-
T. cinerariifolium GDSL lipase
- OPDA:
-
12-oxo-phytodienoic acid
References
Akhtar Y, Yeoung YR, Isman MB (2008) Comparative bioactivity of selected extracts from Meliaceae and some commercial botanical insecticides against two noctuid caterpillars, Trichoplusia ni and Pseudaletia unipuncta. Phytochem Rev 7:77–88. https://doi.org/10.1007/s11101-006-9048-7
Ambrožič Dolinšek J, Kovač M, Žel J, Camloh M (2007) Pyrethrum (Tanacetum cinerariifolium) from the Northern Adriatic as a potential source of natural insecticide. Ann Ser Hist Nat 17:39–46
Amelia-Yap ZH, Chen CD, Sofian-Azirun M, Low VL (2018) Pyrethroid resistance in the dengue vector Aedes aegypti in Southeast Asia: present situation and prospects for management. Parasit Vectors 11:332. https://doi.org/10.1186/s13071-018-2899-0
Anastassiades M, Lehotay S, Štajnbaher D, Schenck F (2003) Fast and easy multiresidue method employing acetonitrile extraction/partitioning and “dispersive solid-phase extraction” for the determination of pesticide residues in produce. J AOAC Int 86:412–431. https://doi.org/10.1093/jaoac/86.2.412
Andreev R, Kutinkova H, Baltas K (2008) Non-chemical control of some important pests of sweet cherry. J Plant Prot Res 48:503–508. https://doi.org/10.2478/v10045-008-0059-9
Antonious GF, Byers ME, Kerst WC (1997) Residue levels of pyrethrins and piperonyl butoxide in soil and runoff water. J Environ Sci Heal Part B Pestic Food Contam Agric Wastes 32:621–644. https://doi.org/10.1080/03601239709373106
Atkinson BL, Blackman AJ, Faber H (2004) The degradation of the natural pyrethrins in crop storage. J Agric Food Chem 52:280–287. https://doi.org/10.1021/jf0304425
Azab M, Khabour OF, Alzoubi KH et al (2017) Assessment of genotoxicity of pyrethrin in cultured human lymphocytes. Drug Chem Toxicol 40:251–255. https://doi.org/10.1080/01480545.2016.1209679
Babić S, Grdiša M, Periša M et al (2012) Ultrasound-assisted extraction of pyrethrins from pyrethrum flowers. Agrochimica 56:193–206
Baldino L, Della Porta G, Reverchon E (2017) Supercritical CO2 processing strategies for pyrethrins selective extraction. J CO2 Util 20:14–19. https://doi.org/10.1016/j.jcou.2017.04.012
Ban D, Sladonja B, Lukić M et al (2010) Comparison of pyrethrins extraction methods efficiencies. Afr J Biotechnol 9:2702–2708. https://doi.org/10.5897/AJB2010.000-3091
Ban D, Sladonja B, Dudaš S et al (2019) Production potential and economic viability of Croatian pyrethrum ecotypes. J Cent Eur Agric 20:598–608. https://doi.org/10.5513/JCEA01/20.2.2176
Barthel WF (1973) Toxicity of pyrethrum and its constituents to mammals. In: Casida JE (ed) Pyretrum: the natural insecticide. Academic Press, New York, pp 123–142
Beckley VA (1952) Pyrethrum drying. Pyrethrum Post 1:9–11
Bendahou N, Fleche C, Bounias M (1999) Biological and biochemical effects of chronic exposure to very low levels of dietary cypermethrin (Cymbush) on honeybee colonies (Hymenoptera: Apidae). Ecotoxicol Environ Saf 44:147–153. https://doi.org/10.1006/eesa.1999.1812
Bhat BK (1995) Breeding methodologies applicable to pyrethrum. In: Casida JE, Quistad GB (eds) Pyrethrum flowers: production, chemistry, toxicology, and uses. Oxford University Press, New York, pp 67–94
Bhat BK, Menary RC (1986) Genotypic and phenotypic correlation in Pyrethrum (Chrysanthemum cinerariaefolium Vis.), and their implication in selection. Pyrethrum Post 16:61–65
Bhat BK, Menary RC, Pandita PN (1985) Population improvement in pyrethrum (Chrysanthemum cinerariaefolium Vis.). Euphytica 34:613–617. https://doi.org/10.1007/BF00035396
Bicchi C, Brunelli C, Galli M, Sironi A (2001) Conventional inner diameter short capillary columns: an approach to speeding up gas chromatographic analysis of medium complexity samples. J Chromatogr A 931:129–140. https://doi.org/10.1016/S0021-9673(01)01169-4
Bigirimana J, Gerard A, Mota-Sanchez D, Gut LJ (2018) Options for managing Antestiopsis thunbergii (Hemiptera: Pentatomidae) and the relationship of bug density to the occurrence of potato taste defect in coffee. Florida Entomol 101:580. https://doi.org/10.1653/024.101.0418
Biošić M, Varga F, Dabić D et al (2020) Matrix solid-phase dispersion optimization for determination of pyrethrin content in Dalmatian pyrethrum (Tanacetum cinerariifolium/Trevir./Sch. Bip.) by liquid chromatography. Ind Crops Prod. https://doi.org/10.1016/j.indcrop.2019.111999
Bojnanský V, Fargašová A (2007) Atlas of seeds and fruits of Central and East-European flora: the Carpathian Mountains Region. Springer, Dordrecht
Boyce WM, Lawler SP, Schultz JM et al (2007) Nontarget effects of the mosquito adulticide pyrethrin applied aerially during a West Nile virus outbreak in an urban California environment. J Am Mosq Control Assoc 23:335–339. https://doi.org/10.2987/8756-971X(2007)23%5b335:NEOTMA%5d2.0.CO;2
BRA (2020) Botanical resources Australia. https://www.botanicalresources.com. Accessed 31 Aug 2020
Brewer JG (1968) Flowering and seed setting in pyrethrum (Chrysanthemum cinerariaefolium Vis.). Pyrethrum Post 9:18–21
Bushway RJ (1985) Normal phase liquid chromatographic determination of pyrethrins in formulations. J Assoc Off Anal Chem 68:1134–1136. https://doi.org/10.1093/jaoac/68.6.1134
Busvine JR (1951) Mechanism of resistance to insecticide in houseflies. Nature 168:193–195. https://doi.org/10.1038/168193a0
Busvine JR (1960a) Use of pyrethrum spraying for malaria control. Bull World Health Organ 22:593–595
Busvine JR (1960b) Resistance to pyrethrins. Bull World Health Organ 22:592–593
Caboni P, Sarais G, Angioni A et al (2005) Fast and versatile multiresidue method for the analysis of botanical insecticides on fruits and vegetables by HPLC/DAD/MS. J Agric Food Chem 53:8644–8649. https://doi.org/10.1021/jf051345+
Caboni P, Minello EV, Cabras M et al (2007) Degradation of pyrethrin residues on stored durum wheat after postharvest treatment. J Agric Food Chem 55:832–835. https://doi.org/10.1021/jf0630973
Camougis G (1973) Mode of action of pyrethrum on arthropod nerves. In: Casida JE (ed) Pyretrum: the natural insecticide. Academic Press, New York, pp 211–222
Camougis G, Davis W (1971) A comparative study of the neuropharmacological basis of action of Pyrethrins. Pyrethrum Post 11:7
Carlson D (2015) New product development with pyrethrins. Acta Hortic 1073:111–112. https://doi.org/10.17660/ActaHortic.2015.1073.15
Casida JE (1973) Biochemistry of the pyrethrins. In: Casida JE (ed) Pyretrum: the natural insecticide. Academic Press, New York, pp 101–120
Casida JE (1980) Pyrethrum flowers and pyrethroid Insecticides. Environ Health Perspect 34:189–202
Casida JE, Quistad GB (eds) (1995) Pyrethrum flowers: production, chemistry, toxicology, and uses. Oxford University Press, New York
Chandre F, Darrier F, Manga L et al (1999) Status of pyrethroid resistance in Anopheles gambiae sensu lato. Bull World Health Organ 77:230–234
Charreton M, Decourtye A, Henry M et al (2015) A locomotor deficit induced by sublethal doses of pyrethroid and neonicotinoid insecticides in the honeybee Apis mellifera. PLoS ONE 10:e0144879. https://doi.org/10.1371/journal.pone.0144879
Chermenskaya TD, Stepanycheva EA, Shchenikova AV, Chakaeva AS (2010) Insectoacaricidal and deterrent activities of extracts of Kyrgyzstan plants against three agricultural pests. Ind Crops Prod 32:157–163. https://doi.org/10.1016/j.indcrop.2010.04.009
Christen V, Fent K (2017) Exposure of honey bees (Apis mellifera) to different classes of insecticides exhibit distinct molecular effect patterns at concentrations that mimic environmental contamination. Environ Pollut 226:48–59. https://doi.org/10.1016/j.envpol.2017.04.003
Coats J (1994) Risks from natural versus synthetic insecticides. Annu Rev Entomol 39:489–515
Crombie L (1995) Chemistry of pyrethrins. In: Casida JE, Quistad GB (eds) Pyrethrum flowers: production, chemistry, toxicology, and uses. Oxford University Press, New York, pp 123–193
Crosby DG (1995) Environmental fate of pyrethrins. In: Casida JE, Quistad GB (eds) Pyrethrum flowers: production, chemistry, toxicology, and uses. Oxford University Press, New York, pp 194–213
Crowley MP, Inglis HS, Snarey M, Thain EM (1961) Biosynthesis of the pyrethrins. Nature 191:281–282. https://doi.org/10.1038/191281a0
Dai P-L, Wang Q, Sun J-H et al (2010) Effects of sublethal concentrations of bifenthrin and deltamethrin on fecundity, growth, and development of the honeybee Apis mellifera ligustica. Environ Toxicol Chem 29:644–649. https://doi.org/10.1002/etc.67
Davies TGE, Field LM, Usherwood PNR, Williamson MS (2007) DDT, pyrethrins, pyrethroids and insect sodium channels. IUBMB Life 59:151–162. https://doi.org/10.1080/15216540701352042
Demok S, Endersby-Harshman N, Vinit R et al (2019) Insecticide resistance status of Aedes aegypti and Aedes albopictus mosquitoes in Papua New Guinea. Parasit Vectors 12:1–8. https://doi.org/10.1186/s13071-019-3585-6
Duchon S, Bonnet J, Marcombe S et al (2009) Pyrethrum: a mixture of natural pyrethrins has potential for malaria vector control. J Med Entomol 46:516–522. https://doi.org/10.1603/033.046.0316
Essig K, Zhao ZJ (2001a) Preparation and characterization of a pyrethrum extract standard. Lc Gc N Am 19:722–730
Essig K, Zhao ZJ (2001b) Method development and validation of a high-performance liquid chromatographic method for pyrethrum extract. J Chromatogr Sci 39:473–480. https://doi.org/10.1093/chromsci/39.11.473
Estep AS, Sanscrainte ND, Waits CM et al (2017) Resistance status and resistance mechanisms in a strain of Aedes aegypti (Diptera: Culicidae) from Puerto Rico. J Med Entomol 54:1643–1648. https://doi.org/10.1093/jme/tjx143
Euro+Med (2006) Euro+Med PlantBase—the information resource for Euro-Mediterranean plant diversity. https://www.emplantbase.org/home.html. Accessed 8 Feb 2020
FAO (2018) Food and Agriculture Organization of the United Nations. Production: crops. http://www.fao.org/faostat/en/#data/QC/visualize. Accessed 8 Feb 2020
Franzosa JA, Osimitz TG, Maibach HI (2007) Cutaneous contact urticaria to pyrethrum-real?, common?, or not documented?: An evidence-based approach. Cutan Ocul Toxicol 26:57–72. https://doi.org/10.1080/15569520601183880
Gallo M, Formato A, Ianniello D et al (2017) Supercritical fluid extraction of pyrethrins from pyrethrum flowers (Chrysanthemum cinerariifolium) compared to traditional maceration and cyclic pressurization extraction. J Supercrit Fluids 119:104–112. https://doi.org/10.1016/j.supflu.2016.09.012
Gerberg EJ (1995) Pyrethrum for control of pests of medical and veterinary importance. In: Casida JE, Quistad GB (eds) Pyrethrum flowers: production, chemistry, toxicology, and uses. Oxford University Press, New York, pp 302–310
Glynne-Jones A (2001) Pyrethrum. Pestic Outlook 12:195–198. https://doi.org/10.1039/b108601b
Gnadinger CB, Corl CS (1930) Studies on pyrethrum flowers. II. The relation between maturity and pyrethrin content. J Am Chem Soc 52:680–684. https://doi.org/10.1021/ja01365a037
Grdiša M, Carović-Stanko K, Kolak I, Šatović Z (2009) Morphological and biochemical diversity of Dalmatian pyrethrum (Tanacetum cinerariifolium (Trevir.) Sch. Bip.). Agric Conspec Sci 74:73–80
Grdiša M, Babić S, Periša M et al (2013) Chemical diversity of the natural populations of Dalmatian pyrethrum (Tanacetum cinerariifolium/Trevir./Sch. Bip.) in Croatia. Chem Biodivers 10:460–472. https://doi.org/10.1002/cbdv.201200015
Grdiša M, Liber Z, Radosavljević I et al (2014) Genetic diversity and structure of Dalmatian pyrethrum (Tanacetum cinerariifolium Trevir./Sch./Bip, Asteraceae) within the Balkan refugium. PLoS ONE. https://doi.org/10.1371/journal.pone.0105265
Greenhill M (2007) Pyrethrum production: Tasmanian success story. Chron Horticult 47:5–8
Gunasekara AS (2004) Environmental fate of pyrethrins. Environmental Monitoring Branch, Department of Pesticide Regulation, Sacramento, CA, pp 1–19
Hata Y, Zimmermann S, Quitschau M et al (2011) Antiplasmodial and antitrypanosomal activity of pyrethrins and pyrethroids. J Agric Food Chem. https://doi.org/10.1021/jf201776z
Head SW (1966) A study of the insecticidal constituents in Tanacetum cinerariifolium. (1) Their development in the flower head. (2) Their distribution in the plant. Pyrethrum Post 8:32–37
Head SW (1973) Composition of pyrethrum extract and analysis of pyrethrins. In: Casida JE (ed) Pyretrum: the natural insecticide. Academic Press, New York, pp 25–53
Henry CW 3rd, Shamsi SA, Warner IM (1999) Separation of natural pyrethrum extracts using micellar electrokinetic chromatography. J Chromatogr A 863:89–103. https://doi.org/10.1016/S0021-9673(99)00884-5
Henry CW 3rd, McCarroll ME, Warner IM (2001) Separation of the insecticidal pyrethrin esters by capillary electrochromatography. J Chromatogr A 905:319–327. https://doi.org/10.1016/s0021-9673(00)01001-3
Hernández-Moreno D, Soffers AEMF, Wiratno et al (2013) Consumer and farmer safety evaluation of application of botanical pesticides in black pepper crop protection. Food Chem Toxicol 56:483–490. https://doi.org/10.1016/j.fct.2013.01.033
Hitmi A, Coudret A, Barthomeuf C (2000) The production of pyrethrins by plant cell and tissue cultures of Tanacetum cinerariifolium and Tagetes species. Crit Rev Biochem Mol Biol 35:317–337. https://doi.org/10.1080/10409230091169230
Ikahu JM, Ngugi CW (1989) Investigations into yield losses of some pyrethrum clones through picking of flowers improper stage of development. Pyrethrum Post 17:56–59
Ismail MF, Mohamed HM (2012) Deltamethrin-induced genotoxicity and testicular injury in rats: comparison with biopesticide. Food Chem Toxicol 50:3421–3425. https://doi.org/10.1016/j.fct.2012.07.060
Ismail BA, Kafy HT, Sulieman JE et al (2018) Temporal and spatial trends in insecticide resistance in Anopheles arabiensis in Sudan: outcomes from an evaluation of implications of insecticide resistance for malaria vector control. Parasit Vectors 11:1–14. https://doi.org/10.1186/s13071-018-2732-9
Isman MB (2008) Botanical insecticides: for richer, for poorer. Pest Manag Sci 64:8–11. https://doi.org/10.1002/ps.1470
Joffe T, Gunning RV, Allen GR et al (2012) Investigating the potential of selected natural compounds to increase the potency of pyrethrum against houseflies Musca domestica (Diptera: Muscidae). Pest Manag Sci 68:178–184. https://doi.org/10.1002/ps.2241
Jovetić S, De Gooijer CD (1995) The production of pyrethrins by in vitro systems. Crit Rev Biotechnol 15:125–138. https://doi.org/10.3109/07388559509147403
Kalaitzaki A, Papanikolaou NE, Karamaouna F et al (2015) Biocompatible colloidal dispersions as potential formulations of natural pyrethrins: a structural and efficacy study. Langmuir 31:5722–5730. https://doi.org/10.1021/acs.langmuir.5b00246
Kalinović I, Korunić Z, Rožman V, Liška A (2011) Effectiveness of pure diatomaceous earth and different mixtures of diatomaceous earth with pyrethrins. Poljoprivreda 17:13–17
Kasaj D, Rieder A, Krenn L, Kopp B (1999) Separation and quantitative analysis of natural pyrethrins by high-performance liquid chromatography. Chromatographia 50:607–610
Kennedy MK, Hamilton RL (1995) Pyrethrum for control of insects in the home. In: Casida JE, Quistad GB (eds) Pyrethrum flowers: production, chemistry, toxicology, and uses. Oxford University Press, New York, pp 311–327
Khan S, Upadhyay S, Khan F et al (2017) Comparative transcriptome analysis reveals candidate genes for the biosynthesis of natural insecticide in Tanacetum cinerariifolium. BMC Genom 18:1–12. https://doi.org/10.1186/s12864-016-3409-4
Kikuta Y, Ueda H, Nakayama K et al (2011) Specific regulation of pyrethrin biosynthesis in Tanacetum cinerariifolium by a blend of volatiles emitted from artificially damaged conspecific plants. Plant Cell Physiol 52:588–596. https://doi.org/10.1093/pcp/pcr017
Kikuta Y, Ueda H, Takahashi M et al (2012) Identification and characterization of a GDSL lipase-like protein that catalyzes the ester-forming reaction for pyrethrin biosynthesis in Tanacetum cinerariifolium—a new target for plant protection. Plant J 71:183–193. https://doi.org/10.1111/j.1365-313X.2012.04980.x
Kiriamiti HK, Camy S, Gourdon C, Condoret JS (2003) Pyrethrin extraction from pyrethrum flowers using carbon dioxide. J Supercrit Fluids 26:193–200. https://doi.org/10.1016/S0896-8446(02)00165-1
Kumari S, Priya P, Misra G, Yadav G (2013) Structural and biochemical perspectives in plant isoprenoid biosynthesis. Phytochem Rev 12:255–291. https://doi.org/10.1007/s11101-013-9284-6
Lange WH, Akesson NB (1973) Pyrethrum for control of agricultural insects. In: Casida JE (ed) Pyretrum: the natural insecticide. Academic Press, New York, pp 261–279
Levy LW (1981) A large-scale application of tissue culture: the mass propagation of pyrethrum clones in Ecuador. Environ Exp Bot 21:389–395. https://doi.org/10.1016/0098-8472(81)90049-6
Li J, Yin LY, Jongsma MA, Wang CY (2011) Effects of light, hydropriming and abiotic stress on seed germination, and shoot and root growth of pyrethrum (Tanacetum cinerariifolium). Ind Crops Prod 34:1543–1549. https://doi.org/10.1016/j.indcrop.2011.05.012
Li J, Jongsma MA, Wang C-Y (2014) Comparative analysis of pyrethrin content improvement by mass selection, family selection and polycross in pyrethrum (Tanacetum cinerariifolium (Trevir.) Sch.Bip.) populations. Ind Crops Prod 53:268–273. https://doi.org/10.1016/j.indcrop.2013.12.023
Li W, Zhou F, Pichersky E (2018) Jasmone hydroxylase, a key enzyme in the synthesis of the alcohol moiety of pyrethrin insecticides. Plant Physiol 177:1498–1509. https://doi.org/10.1104/pp.18.00748
Li W, Lybrand DB, Zhou F et al (2019) Pyrethrin biosynthesis: the cytochrome P450 oxidoreductase CYP82Q3 converts jasmolone to pyrethrolone. Plant Physiol 181:934–944. https://doi.org/10.1104/pp.19.00499
Liu SQ, Scott IM, Pelletier Y et al (2014) Dillapiol: a pyrethrum synergist for control of the Colorado potato beetle. J Econ Entomol 107:797–805. https://doi.org/10.1603/EC13440
Lu C, Liu X, Dong F et al (2010) Simultaneous determination of pyrethrins residues in teas by ultra-performance liquid chromatography/tandem mass spectrometry. Anal Chim Acta 678:56–62. https://doi.org/10.1016/j.aca.2010.08.015
Lu H, Zhu H, Dong H et al (2020) Purification of pyrethrins from flowers of Chrysanthemum cineraraeflium by high-speed counter-current chromatography based on coordination reaction with silver nitrate. J Chromatogr A 1613:460660. https://doi.org/10.1016/j.chroma.2019.460660
MacDonald WL (1995) Pyrethrum flowers—production in Australia. In: Casida JE, Quistad GB (eds) Pyrethrum flowers: production, chemistry, toxicology, and uses. Oxford University Press, New York, pp 55–66
Maciver DR (1995) Constituents of pyrethrum extract. In: Casida JE, Quistad GB (eds) Pyrethrum flowers: production, chemistry, toxicology, and uses. Oxford University Press, New York, pp 108–122
Marchand PA, Dimier-Vallet C, Vidal R (2018) Biorational substitution of piperonyl butoxide in organic production: effectiveness of vegetable oils as synergists for pyrethrums. Environ Sci Pollut Res 25:29936–29942. https://doi.org/10.1007/s11356-017-1057-0
Marcombe S, Carron A, Darriet F et al (2009) Reduced efficacy of pyrethroid space sprays for dengue control in an area of Martinique with pyrethroid resistance. Am J Trop Med Hyg 80:745–751. https://doi.org/10.4269/ajtmh.2009.80.745
Marongiu B, Piras A, Porcedda S et al (2009) Chemical and biological comparisons on supercritical extracts of Tanacetum cinerariifolium (Trevir) Sch. Bip. with three related species of chrysanthemums of Sardinia (Italy). Nat Prod Res 23:190–199. https://doi.org/10.1080/14786410801946221
Martín L, Marqués JL, González-Coloma A et al (2012) Supercritical methodologies applied to the production of biopesticides: a review. Phytochem Rev 11:413–431. https://doi.org/10.1007/s11101-012-9268-y
Matsuda K, Kikuta Y, Haba A et al (2005) Biosynthesis of pyrethrin I in seedlings of Tanacetum cinerariifolium. Phytochemistry 66:1529–1535. https://doi.org/10.1016/j.phytochem.2005.05.005
Matsui R, Takiguchi K, Kuwata N et al (2020) Jasmonic acid is not a biosynthetic intermediate to produce the pyrethrolone moiety in pyrethrin II. Sci Rep 10:1–12. https://doi.org/10.1038/s41598-020-63026-3
McDonnell C, Roark R, Keenan G (1920) Insect powder. US Department of Agriculture Bulletin No. 824:1–100
McEldowney AM, Menary RC (1988) Analysis of pyrethrins in pyrethrum extracts by high-performance liquid chromatography. J Chromatogr A 9673: https://doi.org/10.1016/0021-9673(88)90029-5
Meister M (2016) Head lice—epidemiology, biology, diagnosis, and treatment. Dtsch Arztebl Int 113:763–772. https://doi.org/10.3238/arztebl.2017.0251
Minello EV, Lai F, Zonchello MT et al (2005) Effect of sunscreen and antioxidant on the stability of pyrethrin formulations. J Agric Food Chem 53:8302–8305. https://doi.org/10.1021/jf0510992
Moorman R, Nguyen KT (1997) Identification and quantitation of the six active compounds in a pyrethrin standard. J AOAC Int 80:966–974. https://doi.org/10.1093/jaoac/80.5.966
Morris SE, Davies NW, Brown PH, Groom T (2006) Effect of drying conditions on pyrethrins content. Ind Crops Prod 23:9–14. https://doi.org/10.1016/j.indcrop.2005.01.007
Mouden S, Klinkhamer PGL, Hae Y, Leiss KA (2017) Towards eco-friendly crop protection: natural deep eutectic solvents and defensive secondary metabolites. Phytochem Rev 16:935–951. https://doi.org/10.1007/s11101-017-9502-8
Mužinić V, Želježić D (2018) Non-target toxicity of novel insecticides. Arh Hig Rada Toksikol 69:86–102. https://doi.org/10.2478/aiht-2018-69-3111
Nagar A, Chatterjee A, Ur Rehman L et al (2015) Comparative extraction and enrichment techniques for pyrethrins from flowers of Tanacetum cinerariifolium. Ind Crops Prod 76:955–960. https://doi.org/10.1016/j.indcrop.2015.07.043
Ngugi CW, Ikahu JMK (1990) The effect of drying temperature on pyrethrins content in some pyrethrum clones. Pyrethrum Post 18:18–21
Nikolić T (ed) (2015) Tanacetum cinerariifolium (Trevir.) Sch. Bip. distribution in Croatia. In: Flora Croat. Database. Faculty of Science, University of Zagreb. http://hirc.botanic.hr/fcd. Accessed 8 Feb 2020
O’Brien CD, Hall JE, O’Brien CT et al (2013) Impact of a natural pyrethrin biocide on two amphibians, common toad Bufo bufo and palmate newt Lissotriton helveticus, in Highland, UK. Conserv Evid 10:70–72
Oliveira CR, Domingues CEC, de Melo NFS et al (2019a) Nanopesticide based on botanical insecticide pyrethrum and its potential effects on honeybees. Chemosphere 236:124282. https://doi.org/10.1016/j.chemosphere.2019.07.013
Oliveira CR, Garcia TD, Franco-Belussi L et al (2019b) Pyrethrum extract encapsulated in nanoparticles: toxicity studies based on genotoxic and hematological effects in bullfrog tadpoles. Environ Pollut 253:1009–1020. https://doi.org/10.1016/j.envpol.2019.07.037
Opondo KO, Jawara M, Cham S et al (2019) Status of insecticide resistance in Anopheles gambiae (s.l.) of the Gambia. Parasit Vectors 12:1–8. https://doi.org/10.1186/s13071-019-3538-0
Osimitz TG, Franzosa JA, Maciver DR, Maibach HI (2006) Pyrethrum allergic contact dermatitis in humans—Real?, common?, or not documented? An evidence-based approach. Cutan Ocul Toxicol 25:287–308. https://doi.org/10.1080/15569520601013392
Osimitz TG, Droege W, Kingston R (2017) Safety assessment of pyrethrins based on human experience. Acta Hortic 1169:33–40. https://doi.org/10.17660/ActaHortic.2017.1169.6
Otieno DA, Jondiko IJ, McDowell PG, Kezdy FJ (1982) Quantitative analysis of the pyrethrins by HPLC. J Chromatogr Sci 20:566–570
Ottaro WGW (1977) The relationship between the ploidy level and certain morphological characteristics of Tanacetum cinerariifolium Vis. Pyrethrum Post 14:10–14
Otterbach A, Wenclawiak BW (1999) Ultrasonic/Soxhlet/supercritical fluid extraction kinetics of pyrethrins from flowers and allethrin from paper strips. Fresenius J Anal Chem 365:472–474. https://doi.org/10.1007/s002160051644
Ožanić S (1955) Poljoprivreda Dalmacije u prošlosti (in Croatian). Agronomic society NRH, Društvo agronoma NRH, Podružnica Split, Split, Croatia
Pajnik J, Stamenić M, Radetić M et al (2017) Impregnation of cotton fabric with pyrethrum extract in supercritical carbon dioxide. J Supercrit Fluids 128:66–72. https://doi.org/10.1016/j.supflu.2017.05.006
Pal R (1960) Use of pyrethrum in vector control. Bull World Health Organ 22:595–599
Pan WHT, Chang CC, Su TT et al (1995) Preparative supercritical fluid extraction of pyrethrin I and II from pyrethrum flower. Talanta 42:1745–1749. https://doi.org/10.1016/0039-9140(95)01657-0
Pan L, Feng X, Zhang H (2017) Dissipation and residues of pyrethrins in leaf lettuce under greenhouse and open field conditions. Int J Environ Res Public Health 14:822. https://doi.org/10.3390/ijerph14070822
Pandita PN, Bhat BK (1986) Correlations in phenotypic traits of Pyrethrum (Tanacetum cinerariifolium Vis). Pyrethrum Post 16:93–94
Pandita PN, Sharma SD (1990) Pyrethrin content and dry-flower yield of some strains of Dalmatian pyrethrum (Tanacetum cinerariifolium). Indian J Sci 60:693
Parlevliet J (1974) The genetic variability of the yield components in the Kenyan pyrethrum populations. Euphytica 23:377–384
Parlevliet J (1975) Breeding pyrethrum in Kenya. Pyrethrum Post 13:47–54
Parlevliet JE, Contant RB (1970) Selection for combining ability in Pyrethrum, Tanacetum cinerariifolium Vis. Euphytica 19:4–11. https://doi.org/10.1007/BF01904659
Parlevliet JE, Brewer JG, Ottaro WGM (1979) Collecting pyrethrum, Chrisanthemum cinerariaefolium Vis. in Yugoslavia for Kenya. In: Proceedings conference broadening genetic base crops. Pudoc, Wageningen 1978, pp 91–96
Pattenden G (1970) Some studies on the biosynthesis of the pyrethrins. Pyrethrum Post 10:2–5
Peruga A, Hidalgo C, Sancho JV, Hernández F (2013) Development of a fast analytical method for the individual determination of pyrethrins residues in fruits and vegetables by liquid chromatography-tandem mass spectrometry. J Chromatogr A 1307:126–134. https://doi.org/10.1016/j.chroma.2013.07.090
Pillmore RE (1973) Toxicity of pyrethrum to fish and wildlife. In: Casida JE (ed) Pyrethrum the natural insecticide. Academic Press, New York, pp 160–164
Pimentel D, Edwards CA (1982) Pesticides and ecosystems. Bioscience 32:595–600. https://doi.org/10.2307/1308603
Prestes OD, Padilla-Sánchez JA, Romero-González R et al (2012) Comparison of several extraction procedures for the determination of biopesticides in soil samples by ultrahigh pressure LC-MS/MS. J Sep Sci 35:861–868. https://doi.org/10.1002/jssc.201101057
Pwalia R, Joannides J, Iddrisu A et al (2019) High insecticide resistance intensity of Anopheles gambiae (s.l.) and low efficacy of pyrethroid LLINs in Accra, Ghana. Parasit Vectors 12:1–9. https://doi.org/10.1186/s13071-019-3556-y
Qi S, Niu X, Wang DH et al (2020) Flumethrin at sublethal concentrations induces stresses in adult honey bees (Apis mellifera L.). Sci Total Environ 700:134500. https://doi.org/10.1016/j.scitotenv.2019.134500
Ramirez AM, Stoopen G, Menzel TR et al (2012) Bidirectional secretions from glandular trichomes of pyrethrum enable immunization of seedlings. Plant Cell 24:4252–4265. https://doi.org/10.1105/tpc.112.105031
Rauf S, Teixeira da Silva J, Khan A, Naveed A (2010) Consequences of plant breeding on genetic diversity. Int J Plant Breed 4:1–21
Rawn DFK, Judge J, Roscoe V (2010) Application of the QuEChERS method for the analysis of pyrethrins and pyrethroids in fish tissues. Anal Bioanal Chem 397:2525–2531. https://doi.org/10.1007/s00216-010-3786-5
Rehman H, Aziz AT, Saggu S et al (2014) Systematic review on pyrethroid toxicity with special reference to deltamethrin. J Entomol Zool Stud JEZS 2:60–70
Rivera SB, Swedlund BD, King GJ et al (2001) Chrysanthemyl diphosphate synthase: isolation of the gene and characterization of the recombinant non-head-to-tail monoterpene synthase from Tanacetum cinerariifolium. Proc Natl Acad Sci USA 98:4373–4378. https://doi.org/10.1073/pnas.071543598
Romdhane M, Gourdon C (2002) Investigation in solid–liquid extraction: influence of ultrasound. Chem Eng J 87:11–19. https://doi.org/10.1016/S1385-8947(01)00206-6
Romero-González R, Garrido Frenich A, Martínez Vidal JL et al (2011) Simultaneous determination of pesticides, biopesticides and mycotoxins in organic products applying a quick, easy, cheap, effective, rugged and safe extraction procedure and ultra-high performance liquid chromatography-tandem mass spectrometry. J Chromatogr A 1218:1477–1485. https://doi.org/10.1016/j.chroma.2011.01.034
Rončević S, Svedružić LP, Nemet I (2014) Elemental composition and chemometric characterization of pyrethrum plant materials and insecticidal flower extracts. Anal Lett 47:627–640. https://doi.org/10.1080/00032719.2013.845898
Ruiz I, Morales A, Oliva J, Barba A (2011) Validation of an analytical method for the quantification of pyrethrins on lemons and apricots using high-performance liquid chromatography/mass spectrometry. J Environ Sci Heal - Part B Pestic Food Contam Agric Wastes 46:530–534. https://doi.org/10.1080/03601234.2011.583874
Ryan RF, Greenhill M, Chung B (2015) Pyrethrum: the natural choice in pest control. Acta Hortic 1073:131–135. https://doi.org/10.17660/ActaHortic.2015.1073.19
Sakamori K, Ono N, Ihara M et al (2016) Selective regulation of pyrethrin biosynthesis by the specific blend of wound induced volatiles in Tanacetum cinerariifolium. Plant Signal Behav 11:1–6. https://doi.org/10.1080/15592324.2016.1149675
Sanford MT (2011) Protecting honey bees from pesticides. Institute of Food and Agricultural Sciences, University of Florida, pp 1–13
Sawicki RM, Thain EM (1962) Insecticidal activity of pyrethrum extract and its four insecticidal constituents against house flies. IV.—Knock-down activities of the four constituents. J Sci Food Agric 13:292–297. https://doi.org/10.1002/jsfa.2740130504
Sawicki RM, Elliott M, Gower JC et al (1962) Insecticidal activity of pyrethrum extract and its four insecticidal constituents against house flies. I.—Preparation and relative toxicity of the pure constituents; Statistical analysis of the action of mixtures of these components. J Sci Food Agric 13:172–185. https://doi.org/10.1002/jsfa.2740130307
Sheppard D, Swedlund B (2000) Toxicity of individual pyrethrin esters to house flies (Diptera: Muscidae). J Entomol Sci 35:279–282. https://doi.org/10.18474/0749-8004-35.3.279
Silcox CA, Roth ES (1995) Pyrethrum for control of pests of agricultural and stored products. In: Casida JE, Quistad GB (eds) Pyrethrum flowers: production, chemistry, toxicology, and uses. Oxford University Press, New York, pp 287–301
Singh SP, Rajeswara RBR, Sharma JR, Sharma S (1987) Genetic improvement of pyrethrum I. Assesment of genetic variability and clonal selection. Pyrethrum Post 16:120–124
Singh SP, Sharma JR, Rajeswara Rao BR, Sharma SK (1988) Genetic improvement of pyrethrum. II. Parent-offspring correlation and progeny performance. Pyrethrum Post 17:8–11
Sitango K, Lindsay E, Gracie A et al (2015) Pyrethrum research in the high altitude highlands of Papua New Guinea. Acta Hortic 1073:49–51. https://doi.org/10.17660/ActaHortic.2015.1073.5
Smith LB, Kasai S, Scott JG (2016) Pyrethroid resistance in Aedes aegypti and Aedes albopictus: important mosquito vectors of human diseases. Pestic Biochem Physiol 133:1–12. https://doi.org/10.1016/j.pestbp.2016.03.005
Soderlund DM (1995) Mode of action of pyrethrins and pyrethroids. In: Casida JE, Quistad GB (eds) Pyrethrum flowers: production, chemistry, toxicology, and uses. Oxford University Press, New York, pp 217–230
Soderlund DM, Knipple DC (1999) Knockdown resistance to DDT and pyrethroids in the house fly (Diptera: Muscidae): from genetic trait to molecular mechanism. Ann Entomol Soc Am 92:909–915. https://doi.org/10.1093/aesa/92.6.909
Stanley J, Sah K, Jain SK et al (2015) Evaluation of pesticide toxicity at their field recommended doses to honeybees, Apis cerana and A. mellifera through laboratory, semi-field and field studies. Chemosphere 119:668–674. https://doi.org/10.1016/j.chemosphere.2014.07.039
Suraweera DD, Groom T, Nicolas ME (2017a) Pattern of pyrethrin accumulation, achene and trichome development in relation to pattern of flower development in pyrethrum. Acta Hortic 1169:93–100. https://doi.org/10.17660/ActaHortic.2017.1169.15
Suraweera DD, Groom T, Taylor PWJ et al (2017b) Dynamics of flower, achene and trichome development governs the accumulation of pyrethrins in pyrethrum (Tanacetum cinerariifolium) under irrigated and dryland conditions. Ind Crops Prod 109:123–133. https://doi.org/10.1016/j.indcrop.2017.07.042
Tisch M, Faulde MK, Maier H (2005) Genotoxic effects of pentachlorophenol, lindane, transfluthrin, cyfluthrin, and natural pyrethrum on human mucosal cells of the inferior and middle nasal conchae. Am J Rhinol 19:141–151
Toma M, Vinatoru M, Paniwnyk L, Mason TJ (2001) Investigation of the effects of ultrasound on vegetal tissues during solvent extraction. Ultrason Sonochem 8:137–142. https://doi.org/10.1016/S1350-4177(00)00033-X
Ueda H, Matsuda K (2011) VOC-mediated within-plant communications and nonvolatile systemic signals upregulate pyrethrin biosynthesis in wounded seedlings of Tanacetum cinerariifolium. J Plant Interact 6:89–91. https://doi.org/10.1080/17429145.2011.555566
Vayias B, Christos G, Athanassiou C et al (2006) Persistence and efficacy of two diatomaceous earth formulations and a mixture of diatomaceous earth with natural pyrethrum against Tribolium confusum Jacquelin du Val (Coleoptera: Tenebrionidae) on wheat and maize. Pest Manag Sci 62:456–464. https://doi.org/10.1002/ps.1185
Wainaina JMG (1995) Pyrethrum flowers—production in Africa. In: Casida JE, Quistad GB (eds) Pyrethrum flowers: production, chemistry, toxicology, and uses. Oxford University Press, New York, pp 49–53
Wandahwa P, Van Ranst E, Van Damme P (1996) Pyrethrum (Chrysanthemum cinerariaefolium Vis.) cultivation in West Kenya: origin, ecological conditions and management. Ind Crops Prod 5:307–322. https://doi.org/10.1016/S0926-6690(96)00032-5
Wang I-H, Subramanian V, Moorman R et al (1997) Direct determination of pyrethrins in pyrethrum extracts by reversed-phase high-performance liquid chromatography with diode-array detection. J Chromatogr A 766:277–281. https://doi.org/10.1016/S0021-9673(96)00969-7
Wang Q, Diao Q, Dai P et al (2017) Exploring poisonous mechanism of honeybee, Apis mellifera ligustica Spinola, caused by pyrethroids. Pestic Biochem Physiol 135:1–8. https://doi.org/10.1016/j.pestbp.2016.07.005
Wei D, Li Z, Wang G et al (2006) Separation and purification of natural pyrethrins by reversed phase high performance liquid chromatography. Chin J Anal Chem 34:1776–1779. https://doi.org/10.1016/S1872-2040(07)60021-8
Wenclawiak B, Otterbach A, Krappe M (1998) Capillary supercritical fluid chromatography of pyrethrins and pyrethroids with positive pressure and negative temperature gradients. J Chromatogr A 799:265–273. https://doi.org/10.1016/S0021-9673(97)01236-3
WHO (2000) Pesticide residues in food: toxicological evaluations/Joint Meeting of the FAO Panel of Experts on Pesticides Residues in Food and the Environment and the WHO Core Assessment Group, 1999. Pyrethrum extract (Pyrethrins) (addendum). World Health Organization, Rome, Italy
WHO (2010) The WHO recommended classification of pesticides by hazard and guidelines to classification 2009. World Health Organization
Wolansky MJ, Harrill JA (2008) Neurobehavioral toxicology of pyrethroid insecticides in adult animals: a critical review. Neurotoxicol Teratol 30:55–78. https://doi.org/10.1016/j.ntt.2007.10.005
Wong A, Glinski JA (2017) Efficient, baseline separation of pyrethrins by centrifugal partition chromatography. J Chromatogr Sep Tech 8:362. https://doi.org/10.4172/2157-7064.1000362
Woudneh MB, Oros DR (2006) Pyrethroids, pyrethrins, and piperonyl butoxide in sediments by high-resolution gas chromatography/high-resolution mass spectrometry. J Chromatogr A 1135:71–77. https://doi.org/10.1016/j.chroma.2006.09.017
Xu H, Moghe GD, Wiegert-Rininger K et al (2018) Coexpression analysis identifies two oxidoreductases involved in the biosynthesis of the monoterpene acid moiety of natural pyrethrin insecticides in Tanacetum cinerariifolium. Plant Physiol 176:524–537. https://doi.org/10.1104/pp.17.01330
Xu H, Li W, Schilmiller AL et al (2019) Pyrethric acid of natural pyrethrin insecticide: complete pathway elucidation and reconstitution in Nicotiana benthamiana. New Phytol 223:751–765. https://doi.org/10.1111/nph.15821
Yamashiro T, Shiraishi A, Satake H, Nakayama K (2019) Draft genome of Tanacetum cinerariifolium, the natural source of mosquito coil. Sci Rep 9:1–17. https://doi.org/10.1038/s41598-019-54815-6
Yan S, Hu Q, Li J et al (2019) A star polycation acts as a drug nanocarrier to improve the toxicity and persistence of botanical pesticides. ACS Sustain Chem Eng 7:17406–17413. https://doi.org/10.1021/acssuschemeng.9b04567
Yang T, Stoopen G, Wiegers G et al (2012) Pyrethrins protect pyrethrum leaves against attack by western flower thrips, Frankliniella occidentalis. J Chem Ecol 38:370–377. https://doi.org/10.1007/s10886-012-0097-7
Yang T, Gao L, Hu H et al (2014) Chrysanthemyl diphosphate synthase operates in planta as a bifunctional enzyme with chrysanthemol synthase activity. J Biol Chem 289:36325–36335. https://doi.org/10.1074/jbc.M114.623348
Yang L, Norris EJ, Jiang S et al (2020) Reduced effectiveness of repellents in a pyrethroid-resistant strain of Aedes aegypti (Diptera: Culicidae) and its correlation with olfactory sensitivity. Pest Manag Sci 76:118–124. https://doi.org/10.1002/ps.5562
Zang X, Fukuda EK, Rosen JD (1998) Multiresidue analytical procedure for insecticides used by organic farmers. J Agric Food Chem 46:2206–2210. https://doi.org/10.1021/jf980332b
Zhang X-X, Gao S-L, Gao Y-L et al (2008) Analyses on pyrethrins content and agronomic traits of autotetraploid lines of Pyrethrum cinerariifolium in flowering stage. J Plant Resour Environ 17:67–72
Zito WS, Tio CD (1990) Constituents of Tanacetum cinerariifolium in leaves, regenerated plantlets and callus. Phytochemistry 29:2533–2534. https://doi.org/10.1016/0031-9422(90)85182-F
Zito SW, Zieg RG, Staba EJ (1983) Distribution of pyrethrins in oil glands and leaf tissue of Chrysanthemum cinerariaefolium. Planta Med 47:205–207. https://doi.org/10.1055/s-2007-969986
Acknowledgements
This work has been fully supported by the Croatian Science Foundation under the project ‘Genetic background of Dalmatian pyrethrum (Tanacetum cinerariifolium/Trevir./Sch. Bip.) insecticidal potential’—(PyrDiv) (IP-06-2016-9034). Authors are thankful to reviewers for their valuable comments.
Funding
This work has been fully supported by the Croatian Science Foundation under the project ‘Genetic background of Dalmatian pyrethrum (Tanacetum cinerariifolium/Trevir./Sch. Bip.) insecticidal potential’—(PyrDiv) (IP-06-2016-9034).
Author information
Authors and Affiliations
Contributions
NJ: Conceptualization, Writing—original draft, Writing—review & editing. MG: Conceptualization, Writing—original draft, Writing—review & editing, Supervision, Project administration, Funding acquisition. FV: Writing—original draft, Writing—review & editing. ZŠ: Writing—review & editing. ZL: Writing—review & editing. DD—Construction of biosynthetic pathway (Fig. 1). MB: Conceptualization, Writing—original draft, Writing—review & editing.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Consent for publication
The manuscript has been approved by all authors. This manuscript has not been published and it is not under consideration for publication elsewhere.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The original online version of this article was revised: In the original publication, the plant name has been published incorrectly as “Tanacetum cinerariifolium/Trevir./Sch. Bip.” in the article title and abstract. The correct name should read as “Tanacetum cinerariifolium (Trevir.) Sch. Bip.”
Rights and permissions
About this article
Cite this article
Jeran, N., Grdiša, M., Varga, F. et al. Pyrethrin from Dalmatian pyrethrum (Tanacetum cinerariifolium (Trevir.) Sch. Bip.): biosynthesis, biological activity, methods of extraction and determination. Phytochem Rev 20, 875–905 (2021). https://doi.org/10.1007/s11101-020-09724-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11101-020-09724-2