High-quality simple sequence repeat (SSR) markers are invaluable tools for revealing genetic variability which could be utilized for many purposes, such as breeding new varieties or the identifying current ones, among other applications. Based on the analysis of 3.7 million EST sequences and 15 genomic sequences from bacterial artificial chromosome (BAC) libraries, 200 trinucleotide genic (EST)-SSR and three genomic (gSSR) markers were tested, where 17 of them fulfilled all criteria for quality markers. Moreover, the reproducibility of these new markers was verified by two genetics laboratories, with a mean error rate per allele and per locus equal to 0.17%. These markers were tested on 38 accessions of Papaver somniferum and nine accessions of another five species of the Papaver and Argemone genera. In total, 118 alleles were detected for all accessions (median = 7; three to ten alleles per locus) and 88 alleles (median = 5; three to nine alleles per locus) within P. somniferum alone. Multivariate methods and identity analysis revealed high resolution capabilities of the new markers, where all but three pair accessions (41 out of 47) had a unique profile and opium poppy was distinguished from other species.

Crop Research Institute Division of Crop Genetics and Breeding Drnovská 507 73 6 Ruzyně 16106 Prague Czech Republic

Czech University of Life Sciences FAFNR Department of Agroecology and Crop Production Kamýcká 129 6 Suchdol 16500 Prague Czech Republic

Czech University of Life Sciences Prague FAFNR Department of Genetics and Breeding Kamýcká 129 6 Suchdol 16500 Prague Czech Republic

Zobrazit více v PubMed

Stranska I., Skalicky M., Novak J., Matyasova E., Hejnak V. Analysis of selected poppy (Papaver somniferum L.) cultivars: Pharmaceutically important alkaloids. Ind. Crop. Prod. 2013;41:120–126. doi: 10.1016/j.indcrop.2012.04.018. DOI

Coward F., Shennan S., Colledge S., Conolly J., Collard M. The spread of Neolithic plant economies from the Near East to northwest Europe: A phylogenetic analysis. J. Archaeol. Sci. 2008;35:42–56. doi: 10.1016/j.jas.2007.02.022. DOI

Merlin M.D. Archaeological evidence for the tradition of psychoactive plant use in the old world. Econ. Bot. 2003;57:295–323. doi: 10.1663/0013-0001(2003)057[0295:AEFTTO]2.0.CO;2. DOI

Kabera J.N., Semana E., Mussa A.R., He X. Plant secondary metabolites: Biosynthesis, classification, function and pharmacological properties. J. Pharm. Pharm. 2014;2:377–392.

Winzer T., Gazda V., He Z., Kaminski F., Kern M., Larson T.R., Li Y., Meade F., Teodor R., Vaistij F.E., et al. A Papaver somniferum 10-gene cluster for synthesis of the anticancer alkaloid noscapine. Science. 2012;336:1704–1708. doi: 10.1126/science.1220757. PubMed DOI

Marciano M.A., Panicker S.X., Liddil G.D., Lindgren D., Sweder K.S. Development of a method to extract opium poppy (Papaver somniferum L.) DNA from heroin. Sci. Rep. 2018;8:2590. doi: 10.1038/s41598-018-20996-9. PubMed DOI PMC

Lachenmeier D.W., Sproll C., Musshoff F. Poppy seed foods and opiate drug testing-where are we today? Ther. Drug. Monit. 2010;32:11–18. doi: 10.1097/FTD.0b013e3181c0eee0. PubMed DOI

Jankovičová K., Ulbrich P., Fuknová M. Effect of poppy seed consummation on the positive results of opiates screening in biological samples. Leg. Med. 2009;11:S416–S418. doi: 10.1016/j.legalmed.2009.03.002. PubMed DOI

Lavania U.C., Srivastava S. Quantitative delineation of karyotype variation in Papaver as a measure of phylogenetic differentiation and origin. Curr. Sci. 1999;77:7.

Tétényi P. Opium Poppy (Papaver somniferum): Botany and Horticulture. In: Janick J., editor. Horticultural Reviews. John Wiley & Sons, Inc.; Oxford, UK: 2010. pp. 373–408.

Labanca F., Ovesnà J., Milella L. Papaver somniferum L. taxonomy, uses and new insight in poppy alkaloid pathways. Phytochem. Rev. 2018;17:853–871. doi: 10.1007/s11101-018-9563-3. DOI

Choe S., Kim S., Lee C., Yang W., Park Y., Choi H., Chung H., Lee D., Hwang B.Y. Species identification of Papaver by metabolite profiling. Forensic Sci. Int. 2011;211:51–60. doi: 10.1016/j.forsciint.2011.04.015. PubMed DOI

Schulz H., Baranska M., Quilitzsch R., Schütze W. Determination of alkaloids in capsules, milk and ethanolic extracts of poppy (Papaver somniferum L.) by ATR-FT-IR and FT-Raman spectroscopy. Analyst. 2004;129:917–920. doi: 10.1039/B408930H. PubMed DOI

Odell L.R., Skopec J., McCluskey A. Isolation and identification of unique marker compounds from the Tasmanian poppy Papaver somniferum N. Forensic Sci. Int. 2008;175:202–208. doi: 10.1016/j.forsciint.2007.07.002. PubMed DOI

Németh-Zámbori É., Jászberényi C., Rajhárt P., Bernáth J. Evaluation of alkaloid profiles in hybrid generations of different poppy (Papaver somniferum L.) genotypes. Ind. Crop. Prod. 2011;33:690–696. doi: 10.1016/j.indcrop.2011.01.013. DOI

Gümüşçü A., Arslan N., Sarıhan E.O. Evaluation of selected poppy (Papaver somniferum L.) lines by their morphine and other alkaloids contents. Eur. Food Res. Technol. 2008;226:1213–1220. doi: 10.1007/s00217-007-0739-0. DOI

Dittbrenner A., Mock H.P., Börner A., Lohwasser U. Variability of alkaloid content in Papaver somniferum L. J. Appl. Bot. Food Qual. 2009;82:103–107.

Ziegler J., Facchini P.J., Geißler R., Schmidt J., Ammer C., Kramell R., Voigtländer S., Gesell A., Pienkny S., Brandt W. Evolution of morphine biosynthesis in opium poppy. Phytochemistry. 2009;70:1696–1707. doi: 10.1016/j.phytochem.2009.07.006. PubMed DOI

Güçlü G.B., Gürkök T., Koyuncu M., Arslan N., Parmaksız İ. Genetic characterization of Turkish commercial opium poppy (Papaver somniferum L.) cultivars using ISSR and SSR markers. J. New Results Sci. 2014;3:48–57.

Parmaksiz İ., Özcan S. Morphological, chemical, and molecular analyses of Turkish papaver accessions (Sect. Oxytona) Turk. J. Bot. 2011;35:1–16.

Acharya H.S., Sharma V. Molecular characterization of opium poppy (Papaver somniferum) germplasm. Am. J. Infect. Dis. 2009;5:155–160. doi: 10.3844/ajidsp.2009.148.153. DOI

Saunders J.A., Pedroni M.J., Penrose L.D.J., Fist A.J. AFLP analysis of opium poppy. Crop. Sci. 2001;41:1596. doi: 10.2135/cropsci2001.4151596x. DOI

Mičianová V., Ondreičková K., Muchová D., Klčová L., Hudcovicová M., Havrlentová M., Mihálik D., Kraic J. Forensic application of EST-derived STR markers in opium poppy. Biologia. 2017;72:587–594. doi: 10.1515/biolog-2017-0076. DOI

Celik I., Gultekin V., Allmer J., Doganlar S., Frary A. Development of genomic simple sequence repeat markers in opium poppy by next-generation sequencing. Mol. Breed. 2014;34:323–334. doi: 10.1007/s11032-014-0036-0. DOI

Şelale H., Çelik I., Gültekin V., Allmer J., Doğanlar S., Frary A. Development of EST-SSR markers for diversity and breeding studies in opium poppy. Plant. Breed. 2013;132:344–351. doi: 10.1111/pbr.12059. DOI

Lee E.J., Jin G.N., Lee K.L., Han M.S., Lee Y.H., Yang M.S. Exploiting expressed sequence tag databases for the development and characterization of gene-derived simple sequence repeat markers in the opium poppy (Papaver somniferum L.) for forensic applications. J. Forensic Sci. 2011;56:1131–1135. doi: 10.1111/j.1556-4029.2011.01810.x. PubMed DOI

Richard G.-F., Kerrest A., Dujon B. Comparative Genomics and Molecular Dynamics of DNA Repeats in Eukaryotes. Microbiol. Mol. Biol. Rev. 2008;72:686–727. doi: 10.1128/MMBR.00011-08. PubMed DOI PMC

Ellegren H. Microsatellites: Simple sequences with complex evolution. Nat. Rev. Genet. 2004;5:435–445. doi: 10.1038/nrg1348. PubMed DOI

Kalia R.K., Rai M.K., Kalia S., Singh R., Dhawan A.K. Microsatellite markers: An overview of the recent progress in plants. Euphytica. 2011;177:309–334. doi: 10.1007/s10681-010-0286-9. DOI

Buschiazzo E., Gemmell N.J. The rise, fall and renaissance of microsatellites in eukaryotic genomes. Bioessays. 2006;28:1040–1050. doi: 10.1002/bies.20470. PubMed DOI

Guichoux E., Lagache L., Wagner S., Chaumeil P., Léger P., Lepais O., Lepoittevin C., Malausa T., Revardel E., Salin F., et al. Current trends in microsatellite genotyping. Mol. Ecol. Resour. 2011;11:591–611. doi: 10.1111/j.1755-0998.2011.03014.x. PubMed DOI

Parida S.K., Kalia S.K., Kaul S., Dalal V., Hemaprabha G., Selvi A., Pandit A., Singh A., Gaikwad K., Sharma T.R., et al. Informative genomic microsatellite markers for efficient genotyping applications in sugarcane. Theor. Appl. Genet. 2009;118:327–338. doi: 10.1007/s00122-008-0902-4. PubMed DOI

Varshney R.K., Graner A., Sorrells M.E. Genic microsatellite markers in plants: Features and applications. Trends Biotechnol. 2005;23:48–55. doi: 10.1016/j.tibtech.2004.11.005. PubMed DOI

Vieira M.L.C., Santini L., Diniz A.L., Munhoz C.D.F. Microsatellite markers: What they mean and why they are so useful. Genet. Mol. Biol. 2016;39:312–328. doi: 10.1590/1678-4685-GMB-2016-0027. PubMed DOI PMC

Hayward A.C., Tollenaere R., Dalton-Morgan J., Batley J. Molecular Marker Applications in Plants. In: Batley J., editor. Plant Genotyping. Volume 1245. Springer; New York, NY, USA: 2015. pp. 13–27. PubMed

Meyer L., Causse R., Pernin F., Scalone R., Bailly G., Chauvel B., Délye C., Le Corre V. New gSSR and EST-SSR markers reveal high genetic diversity in the invasive plant Ambrosia artemisiifolia L. and can be transferred to other invasive Ambrosia species. PLoS ONE. 2017;12:e0176197. doi: 10.1371/journal.pone.0176197. PubMed DOI PMC

Chen H., Wang L., Liu X., Hu L., Wang S., Cheng X. De novo transcriptomic analysis of cowpea (Vigna unguiculata L. Walp.) for genic SSR marker development. BMC Genet. 2017;18:65. doi: 10.1186/s12863-017-0531-5. PubMed DOI PMC

El-Esawi M.A., Germaine K., Bourke P., Malone R. Genetic diversity and population structure of Brassica oleracea germplasm in Ireland using SSR markers. C. R. Biol. 2016;339:133–140. doi: 10.1016/j.crvi.2016.02.002. PubMed DOI

Kishine M., Tsutsumi K., Kitta K. A set of tetra-nucleotide core motif SSR markers for efficient identification of potato (Solanum tuberosum) cultivars. Breed. Sci. 2017;67:544–547. doi: 10.1270/jsbbs.17066. PubMed DOI PMC

Bora A., Choudhury P.R., Pande V., Mandal A.B. Assessment of genetic purity in rice (Oryza sativa L.) hybrids using microsatellite markers. 3 Biotech. 2016;6:50. doi: 10.1007/s13205-015-0337-y. PubMed DOI PMC

Subirana J.A., Messeguer X. Structural families of genomic microsatellites. Gene. 2008;408:124–132. doi: 10.1016/j.gene.2007.10.025. PubMed DOI

Lai Y., Sun F. The relationship between microsatellite slippage mutation rate and the number of repeat units. Mol. Biol. Evol. 2003;20:2123–2131. doi: 10.1093/molbev/msg228. PubMed DOI

Levinson G., Gutman G. Slipped-strand mispairing: A major mechanism for DNA sequence evolution. Mol. Biol. Evol. 1987;4:203–221. PubMed

Van de Peer Y., Fawcett J.A., Proost S., Sterck L., Vandepoele K. The flowering world: A tale of duplications. Trends Plant. Sci. 2009;14:680–688. doi: 10.1016/j.tplants.2009.09.001. PubMed DOI

Ramsey J., Schemske D.W. Pathway, mechanisms, and rates of polyploid formation in flowering plants. Annu. Rev. Ecol. Syst. 1998;29:467–501. doi: 10.1146/annurev.ecolsys.29.1.467. DOI

Kati V., Le Corre V., Michel S., Jaffrelo L., Poncet C., Délye C. Isolation and characterisation of 11 polymorphic microsatellite markers in Papaver rhoeas L. (corn poppy), a major annual plant species from cultivated areas. Int. J. Mol. Sci. 2012;14:470–479. doi: 10.3390/ijms14010470. PubMed DOI PMC

Pompanon F., Bonin A., Bellemain E., Taberlet P. Genotyping errors: Causes, consequences and solutions. Nat. Rev. Genet. 2005;6:847–859. doi: 10.1038/nrg1707. PubMed DOI

Baldoni L., Cultrera N.G., Mariotti R., Ricciolini C., Arcioni S., Vendramin G.G., Buonamici A., Porceddu A., Sarri V., Ojeda M.A., et al. A consensus list of microsatellite markers for olive genotyping. Mol. Breed. 2009;24:213–231. doi: 10.1007/s11032-009-9285-8. DOI

Drašnarová A., Krak K., Vít P., Doudová J., Douda J., Hadincová V., Zákravský P., Mandák B. Cross-amplification and multiplexing of SSR markers for Alnus glutinosa and A. incana. Tree Genet. Genomes. 2014;10:865–873. doi: 10.1007/s11295-014-0727-z. DOI

Kameníková L., Vrbovský V. White-seeded poppy varieties Orel and Racek. Czech. J. Genet. Plant. Breed. 2009;45:37–38. doi: 10.17221/5/2009-CJGPB. DOI

Butler J.M. Advanced Topics in Forensic DNA Typing: Interpretation. Academic Press; Cambridge, MA, USA: 2015.

Waits L.P., Luikart G., Taberlet P. Estimating the probability of identity among genotypes in natural populations: Cautions and guidelines. Mol. Ecol. 2001;10:249–256. doi: 10.1046/j.1365-294X.2001.01185.x. PubMed DOI

Meier U. BBCH-Monograph: Growth Stages of Mono-and Dicotyledonous Plants. Blackwell Wissenschafts-Verlag; Berlin, Germany: 1997.

Masoudi-Nejad A., Tonomura K., Kawashima S., Moriya Y., Suzuki M., Itoh M., Kanehisa M., Endo T., Goto S. EGassembler: Online bioinformatics service for large-scale processing, clustering and assembling ESTs and genomic DNA fragments. Nucleic Acids Res. 2006;34:W459–W462. doi: 10.1093/nar/gkl066. PubMed DOI PMC

Wang X., Wang L. GMATA: An integrated software package for genome-scale SSR mining, marker development and viewing. Front. Plant. Sci. 2016;7:1350. doi: 10.3389/fpls.2016.01350. PubMed DOI PMC

Untergasser A., Cutcutache I., Koressaar T., Ye J., Faircloth B.C., Remm M., Rozen S.G. Primer3—new capabilities and interfaces. Nucleic Acids Res. 2012;40:e115. doi: 10.1093/nar/gks596. PubMed DOI PMC

Koressaar T., Remm M. Enhancements and modifications of primer design program Primer3. Bioinformatics. 2007;23:1289–1291. doi: 10.1093/bioinformatics/btm091. PubMed DOI

Hall T.A. Proceedings of the Nucleic Acids Symposium Series. Volume 41. Information Retrieval Ltd.; London, UK: 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT; pp. 95–98.

Edgar R.C. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792–1797. doi: 10.1093/nar/gkh340. PubMed DOI PMC

Kalinowski S.T., Taper M.L., Marshall T.C. Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol. Ecol. 2007;16:1099–1106. doi: 10.1111/j.1365-294X.2007.03089.x. PubMed DOI

TIBCO Statistica. [(accessed on 28 December 2019)]; Available online: https://www.tibco.com/resources/product-download/tibco-statistica-trial-download-windows.

Perrier X., Jacquemoud-Collet J.P. DARwin Software. [(accessed on 26 April 2019)]; Available online: http://darwin.cirad.fr/darwin.

Dice L.R. Measures of the amount of ecologic association between species. Ecology. 1945;26:297–302. doi: 10.2307/1932409. DOI

Hintze J. NCSS. NCSS; Kaysville, UT, USA: 2001.

Production and properties of particleboard and paper from waste poppy straw

cor1 Gene: A Suitable Marker for Identification of Opium Poppy (Papaver somniferum L.)

OpiumPlex is a novel microsatellite system for profiling opium poppy (Papaver somniferum L.)