Advertisement

Phytochemistry Reviews

, Volume 17, Issue 4, pp 853–871 | Cite as

Papaver somniferum L. taxonomy, uses and new insight in poppy alkaloid pathways

  • Fabiana Labanca
  • Jaroslava Ovesnà
  • Luigi MilellaEmail author
Article
  • 362 Downloads

Abstract

Since ancient times, opium poppy (Papaver somniferum L.) is known for its medicinal properties, related to its secondary metabolite content. Its most important secondary metabolites, called benzylisoquinoline alkaloids (BIAs), are still essential in pharmaceutical field. Few of them, like morphine, have specific clinical application but also effects on CNS. Not all poppy cultivars are able to biosynthesize morphine in high amount, making this plant useful for other purposes like food uses. For this reason it is crucial to deeply understand the origin of poppy, its possible use and have a deep knowledge of the BIA biosynthesis. These aspects are crucial for the final use of P. somniferum. This review aims to summarize the state-of-the-art on its taxonomy and origin beside its uses and BIA biosynthetic pathways, its most important metabolites. The review focuses on conflicting or unsolved questions about enzymatic localization, role of different plant organs in the biosynthesis, and storage and external conditions that influence the alkaloid production, highlighting the significant involvement of transcription factors. Behind this review, there is the firm belief that only a deep knowledge of alkaloid biosynthetic processes could lead to the characterization of undefined step and to the development of engineering cultivars optimizing the potential uses of P. somniferum. The goal is answer in more sustainable way to ever-increasing worldwide request of such products, in particular morphine and derivates, obtaining high morphine content cultivars useful for pharmaceutical market or no morphine producing cultivars appreciated as food. Devising cultivars with different BIA content could lead to decrease, or even avoid, illicit use and illegal extraction, confining only low alkaloid content cultivars to consumers market.

Keywords

Benzylisoquinoline alkaloid BIAs Biosynthesis Poppy Phylogenetic Transcription factors 

Abbreviations

3′OHase

3′-Hydroxylase

3′OMT

3′-O-methyltransferase

3OHase

Tyrosine/tyramine 3-hydroxylase

4′OMT

3′-hydroxyl-N-methylcoclaurine 4′-O-methyltransferase

4HPAA

4 Hydroxyphenylacetic acid

4HPPDC

4-Hydroxyphenylpuruvate decarboxylase

6OMT

Norcoclaurine 6-O-methyltransferase

7OMT

Reticuline 7-O-methyltransferase

AC

Adenylyl cyclase

AFLP

Amplified fragment length polymorphism

AMP

Adenosine monophosphate

AMPc

Adenosine monophosphate cyclic

BBE

Berberine bridge enzyme

BIAs

Benzylisoquinoline alkaloids

CAS

Canadine synthase

CFS

Cheilanthifoline synthase

CNMT

Coclaurine N-methyltransferase

CNS

Central nervous system

CODM

Codeine O-demethylase

CoOMT

Columbamine O-methyltransferase

COR

Codeinone reductase

CPVO

Community Plant Variety Office

CYP

Cytochrome P450 enzyme family

CYP82Y1

N-methylcanadine 1-hydroxylase

CYP80B

(S)-N-methylcoclaurine 3′-hydroxylase isozyme

Cys

Cysteine

DA

Dopamine

DBOX

Dihydrosanguinarine oxidase

EFSA

European Food Safety Authority

ER

Endoplasmic reticulum

EST

Expressed sequence tag

FT–ICR–MS

Fourier-transform–ion-cyclotron resonance–mass spectrometry

GC

Gas chromatography

GPCR

G protein–coupled receptors

HPLC

High performance liquid chromatography

MeJa

Methyl jasmonate

MIA

Monoterpenoid indole alkaloid

MLP15

Major latex proteins

MSH

N-methylstylopine 14-hydroxylase

N7OMT

Norreticuline 7-O-methyltransferase

NAc

Nucleus accumbens

NCS

Norcoclaurine synthase

NMCH

N-methylcoclaurine 3′-hydroxylase

NOS

Noscapine synthase

Nuclear factor-κB

Nuclear factor kappa-light-chain-enhancer of activated B cells

OR receptors

Receptors for endogenous opiates

ORL1

Opioid receptor-like

P6H

Protopine 6-hydroxylase

PKA

Protein kinase A

PKC

Protein kinase C

PPH

Protopine-6-hydroxylase

RAPD

Random amplified polymorphic DNA

RFLP

Restriction fragment length polymorphism

ROS

Reactive oxygen species

RSP

Restriction site polymorphism

RVM

Rostral ventromedial medulla

SalAT

Salutaridinol 7-O-acetyltransferase

SalR

Salutaridine reductase

SanR

Sanguinarine reductase

SAT

(7S)-salutaridinol 7-O-acetyltransferase

SNPs

Single nucleotide polymorphism

SOMT1

Scoulerine 9-O-methyltransferase

SOR

7-Oxidoreductase

SPS

Stylopine synthase

STOX

(S)-tetrahydroxyprotoberberineoxidase

STRs

Short tandem repeat

STS

Salutaridine synthase

StySyn

Sstylopine synthase

T6ODM

Thebaine 6-O-demethylase

TFBSs

Transcription factor binding bites

TFs

Transcription factors

TNMT

Tetrahydroprotoberberine N-methyltransferase

TYDC

Tyrosine/DOPA decarboxylase

UHPLC–ESI–QTOF–MS

Ultra high performance liquid chromatography–electrospray ionization–quadrupole time-of-flight–mass spectrometry

VNTRs

Variable number of tandem repeat or minisatellites

Notes

Acknowledgements

Authors would like to thank the Czech Minstry of Agriculture, Projects NAZV QK1720263 and RO0417 for the support.

References

  1. Acheson RM, Harper JL, Mcnaughton IH (1956) Distribution of anthocyanin pigments in poppies. Nature 178:1283–1284CrossRefGoogle Scholar
  2. Acheson RM, Jenkins CL, Harper JL et al (2006) Floral pigments in papaver and their significance in the systematics of the genus. New Phytol 61(3):256–260CrossRefGoogle Scholar
  3. Agarwal PS, Lakhwani D et al (2016) Comparative analysis of transcription factor gene families from Papaver somniferum: identification of regulatory factors involved in benzylisoquinoline alkaloid biosynthesis. Protoplasma 253(3):857–871CrossRefPubMedGoogle Scholar
  4. Bajpai S, Gupta AP, Gupta MM et al (2000) Inter-relation between descriptors and morphine yield in Asian germplasm of opium poppy Papaver somniferum. Genet Resour Crop Evol 47(3):315–322CrossRefGoogle Scholar
  5. Batterham RL, Cowley MA, Small CJ et al (2004) Physiology: does gut hormone PYY3-36 decrease food intake in rodents? Nature 430(6996):413–414Google Scholar
  6. Beaudoin GA, Facchini JP (2014) Benzylisoquinoline alkaloid biosynthesis in opium poppy. Planta 240(1):19–32CrossRefPubMedGoogle Scholar
  7. Bird DA, Franceschi VR, Facchini PJ (2003) A tale of three cell types: alkaloid biosynthesis is localized to sieve elements in opium poppy. The Plant Cell 15:2626–2635CrossRefPubMedPubMedCentralGoogle Scholar
  8. Celik I, Gultekin V, Allmer J et al (2014) Development of genomic simple sequence repeat markers in opium poppy by next-generation sequencing. Mol Breed 34(2):323–334CrossRefGoogle Scholar
  9. Danert S (1958) Zur Systematik von Papaver somniferum L. Kulturpflanze 6:61–88CrossRefGoogle Scholar
  10. Dang TT, Onoyovwi A, Farrow SC et al (2012) Biochemical genomics for gene discovery in benzylisoquinoline alkaloid biosynthesis in opium poppy and related species. Methods Enzymol 515:231–266CrossRefPubMedGoogle Scholar
  11. Darokar MP, Dhawan SS, Shukla AK et al (2014) Assessment of genetic relatedness among selected cultivars of opium poppy (Papaver somniferum L.) through DNA profiling. Acta Hortic 1036:21–28CrossRefGoogle Scholar
  12. Desgagné-Penix I, Khan MF, Schremier DC et al (2010) Integration of deep transcriptome and proteome analyses reveals the components of alkaloid metabolism in opium poppy cell cultures. BMC Plant Biol 10(1):252CrossRefPubMedPubMedCentralGoogle Scholar
  13. Desgagné-Penix I, Farrow SC, Cram D et al (2012) Integration of deep transcript and targeted metabolite profiles for eight cultivars of opium poppy. Plant Mol Biol 79(3):295–313CrossRefPubMedGoogle Scholar
  14. Dittbrenner A, Lohwasser U, Mock HP et al (2008) Molecular and phytochemical studies of Papaver somniferum in the context of infraspecific classification. Acta Hortic 799:81–88CrossRefGoogle Scholar
  15. Duarte DF (2005) Uma breve história do ópio e dos opióides. Rev Bras Anestesiol 55(1):135–146PubMedGoogle Scholar
  16. Egan PA, Pendry CA, Shresth S (2011) Flora of Nepal Papaveraceae. Royal Botanic Gardens, MelbourneGoogle Scholar
  17. El Nehir S, Karakaya S (2004) Radical scavenging and iron-chelating activities of some greens used as traditional dishes in mediterranean diet. Int J Food Sci Nutr 55(1):67–74CrossRefGoogle Scholar
  18. Eryilmaz T, Yesilyurt MK, Cesur C et al (2016) Biodiesel production potential from oil seeds in Turkey. Renew Sustain Energy Rev 58:842–851CrossRefGoogle Scholar
  19. European Food Safety Authority (EFSA) (2011) Scientific opinion on the risks for public health related to the presence of opium alkaloids in poppy seeds. EFSA J 9(11):1–150Google Scholar
  20. Facchini PJ (2001) Alkaloid biosynthesis in plants: biochemistry, cell biology, molecular regulation, and metabolic engineering applications. Annu Rev Plant Biol 52(1):29–66CrossRefGoogle Scholar
  21. Facchini PJ, De Luca V (2008) Opium poppy and Madagascar periwinkle: model non-model systems to investigate alkaloid biosynthesis in plants. Plant Journal 54(4):763–784CrossRefPubMedGoogle Scholar
  22. Fernández EC, Rajchl A, Lachman J et al (2013) Impact of yacon landraces cultivated in the Czech Republic and their ploidy on the short- and long-chain fructooligosaccharides content in tuberous roots. LWT Food Sci Technol 54(1):80–86CrossRefGoogle Scholar
  23. Froede R (1972) Drugs of abuse: legal and illegal. Hum Pathol 3(1):23–36CrossRefPubMedGoogle Scholar
  24. Gurkok T, Turktas M, Parmaksiz I et al (2015) Transcriptome profiling of alkaloid biosynthesis in elicitor induced opium poppy. Plant Mol Biol Rep 33(3):673–688CrossRefGoogle Scholar
  25. Hagel JM, Facchini PJ (2013) Benzylisoquinoline alkaloid metabolism: a century of discovery and a brave new world. Plant Cell Physiol 54(5):647–672CrossRefPubMedGoogle Scholar
  26. Hammer K (1981) Problems of Papaver somniferum classification and some remarks on recently collected European poppy land-races. Genet Resour Crop Evol 29:287–296Google Scholar
  27. Hao D, Xiao JG, Pei GX (2015) Medicinal plant: chemistry, biology and omics. Woodhead Publishing, CambridgeGoogle Scholar
  28. Hofman PJ, Menary RC (1985) Alkaloid losses from the capsules of Papaver Somniferum L. during kiln drying and storage under commercial conditions in Tasmania. J Stored Prod Res 21(3):135–139CrossRefGoogle Scholar
  29. Inukai S, Hong Kock K, Bulyk ML (2017) Transcription factor-DNA binding: beyond binding site motifs. Curr Opin Genet Dev 43:110–119.  https://doi.org/10.1016/j.gde.2017.02.007 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Jablonická V, Mansfeld J, Heilmann I et al (2016) Identification of a secretory phospholipase A2 from Papaver somniferum L. that transforms membrane phospholipids. Phytochemistry 129:4–13CrossRefPubMedGoogle Scholar
  31. Jia L, Clegg MT, Jiang T (2004) Evolutionary dynamics of the DNA-binding domains in putative R2R3-MYB genes identified from rice subspecies indica and japonica genomes. Plant Physiol 134(2):575–585CrossRefPubMedPubMedCentralGoogle Scholar
  32. Kadereit JW (1988) Sectional affinities and geographical distribution in the genus Papaver L. (Papaveraceae). Beitrage zur Biologie der Pflanzen 63:139–156Google Scholar
  33. Kakeshpour T, Nayebi S, Rashidi Monfared S et al (2015) Identification and expression analyses of MYB and WRKY transcription factor genes in Papaver somniferum L. Physiol Mol Biol Plants 21(4):465–478CrossRefPubMedPubMedCentralGoogle Scholar
  34. Kreek MJ (2007) Opioids, dopamine, stress, and the addictions. Dialog Clin Neurosci 9(4):363–378Google Scholar
  35. Kutchan TM, Weid M, Ziegler J (2004) The roles of latex and the vascular bundle in morphine biosynthesis in the opium poppy, Papaver somniferum. Proc Natl Acad Sci USA 101(38):13957–13962CrossRefPubMedGoogle Scholar
  36. Li Q, Zhang H (2017) Research progress on the synthesis of morphine alkaloids. Chin J Organ Chem 37(7):1629–1652CrossRefGoogle Scholar
  37. Liscombe DK, Facchini PJ (2008) Evolutionary and cellular webs in benzylisoquinoline alkaloid biosynthesis. Curr Opin Biotechnol 19(2):173–180CrossRefPubMedGoogle Scholar
  38. Marciano MA, Panicker SX et al (2018) Development of a method to extract opium poppy (Papaver somniferum L.) DNA from heroin. Sci Rep 8:2590.  https://doi.org/10.1038/s41598-018-20996-9 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Meos A, Saks L, Raal A (2017) Content of alkaloids in ornamental Papaver somniferum L. cultivars growing in estonia. Proc Est Acad Sci 66(1):34–39CrossRefGoogle Scholar
  40. Mishra S, Triptahi V, Singh S, Phukan UJ, Gupta MM, Shanker K, Shukla RK (2013) Wound induced tanscriptional regulation of benzylisoquinoline pathway and characterization of wound inducible PsWRKY transcription factor from Papaver somniferum. PLoS ONE 8(1):e52784.  https://doi.org/10.1371/journal.pone.0052784 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Mitrová K, Svoboda P, Milella L et al (2018) Alliinase and cysteine synthase transcription in developing garlic (Allium sativum L.) over time. Food Chem 15(251):103–109.  https://doi.org/10.1016/j.foodchem.2017.12.090 CrossRefGoogle Scholar
  42. Moloney MG (2016) Natural products as a source for novel antibiotics. Trends Pharmacol Sci 37(8):689–701CrossRefPubMedGoogle Scholar
  43. Onoyovwe A, Hagel JM, Chen X et al (2013) Morphine biosynthesis in opium poppy involves two cell types: sieve elements and laticifers. Plant Cell 25(10):4110–4122CrossRefPubMedPubMedCentralGoogle Scholar
  44. Ovesná J, Kučera L, Vaculová K et al (2013) Analysis of the genetic structure of a barley collection using DNA diversity array technology (DArT). Plant Mol Bio Rep 31(2):280–288CrossRefGoogle Scholar
  45. Pathak S, Lakhwani D, Gupta P et al (2013) Comparative transcriptome analysis using high papaverine mutant of Papaver Somniferum reveals pathway and uncharacterized steps of papaverine biosynthesis. PLoS ONE 8(5):e65622.  https://doi.org/10.1371/journal.pone.0065622 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Prajapati S, Bajpai S, Singh D et al (2002) Alkaloid profiles of the Indian land races of the opium poppy Papaver somniferum L. Genet Resour Crop Evol 49(2):183–188CrossRefGoogle Scholar
  47. Prescha A, Grajzer M, Dedyk M et al (2014) The Antioxidant activity and oxidative stability of cold-pressed oils. J Am Oil Chem Soc 91(8):1291–1301CrossRefPubMedPubMedCentralGoogle Scholar
  48. Russo D, Valentão P, Andrade PB et al (2015) Evaluation of antioxidant, antidiabetic and anticholinesterase activities of Smallanthus sonchifolius landraces and correlation with their phytochemical profiles. Int J Mol Sci 16(8):17696–17718CrossRefPubMedPubMedCentralGoogle Scholar
  49. Saunders JM, Pedroni MJ, Penrose LDJ et al (2000) AFLP analysis of opium poppy. Crop Sci 41(5):1596–1601CrossRefGoogle Scholar
  50. Şelale H, Çelik I, Visam Gü V et al (2013) Development of EST-SSR markers for diversity and breeding studies in opium poppy. Plant Breed 132(3):344–351CrossRefGoogle Scholar
  51. Singh M, Chaturvedi N, Shasany AK et al (2014) Impact of promising genotypes of Papaver somniferum L. developed for beneficial uses. Acta Hortic 1036:29–41CrossRefGoogle Scholar
  52. Sofo A, Milella L, Tataranni G (2010) Effects of Trichoderma harzianum strain T-22 on the growth of two Prunus rootstocks during the rooting phase. J Hortic Sci Biotechnol 85(6):497–502CrossRefGoogle Scholar
  53. Solanki G, Dodiya NS, Kunwar R et al (2017) Character Association and path coefficient analysis for seed yield and latex yield in opium poppy (Papaver somniferum L.). Int J Cur Microbiol Appl Sci 6(8):1116–1123CrossRefGoogle Scholar
  54. Stefano GB, Pilonis N, Ptacek R et al (2017) Reciprocal evolution of opiate science from medical and cultural perspectives. Med Sci Monit 23:2890–2896CrossRefPubMedPubMedCentralGoogle Scholar
  55. Tavakkoli Z, Assadi M (2016) Evaluation of seed and leaf epidermis characters in the taxonomy of some annual species of the genus papaver (Papaveraceae). Nord J Bot 34(3):302–321CrossRefGoogle Scholar
  56. Tétényi P (1997) Opium botany and horticulture. In: Janick J (ed) Horticultural reviews, vol 19. Wiley, New York, pp 375–382Google Scholar
  57. Wang H, Wang H, Shao H et al (2016) Recent advances in utilizing transcription factors to improve plant abiotic stress tolerance by transgenic technology. Front Plant Sci 7:1–13PubMedPubMedCentralGoogle Scholar
  58. Winzer T, Gazda V, Zhesi H et al (2012) A papaver somniferum 10-gene cluster for synthesis of the anticancer alkaloid noscapine. Science 336(6089):1704–1708CrossRefPubMedGoogle Scholar
  59. Ziegler J, Facchini PJ, Rene G et al (2009) Evolution of morphine biosynthesis in opium poppy. Phytochemistry 70(15–16):1696–1707CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of ScienceUniversity of BasilicataPotenzaItaly
  2. 2.Plant Genetics and Breeding Methods, Division of Crop Genetics and BreedingCrop Research InstitutePrague 6Czech Republic

Personalised recommendations