Taxonomic investigation of the Xanthium strumarium L. complex (Asteraceae) distributed in Iran inferred from morphological, palynological and molecular data
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Abstract. Noedoost F, Vaezi J, Nikzat Siahkolaee S. 2021. Taxonomic investigation of the Xanthium strumarium L. complex (Asteraceae) distributed in Iran inferred from morphological, palynological and molecular data. Biodiversitas 22: 1961-1974. Unclear species boundaries due to high morphological similarities lead to different opinions on Xanthium classification. To solve this problem, we conducted investigation on morphological, palynological and molecular (ITS sequencing) of three species of Xanthium (i.e., X. strumarium, X. sibiricum, and X. brasilicum) forming Xanthium strumarium complex in Iran. We randomly collected 110 plant individuals of the Xanthium strumarium complex as well as X. spinosum from 30 geographical populations in eight provinces of Iran. Pollen grains of 19 populations were studied by scanning electron microscope (SEM). Results obtained from the analysis of morphological characters showed that the three species, X. strumarium, X. brasilicum and X. sibiricum were placed nearly together specially X. strumarium and X. brasilicum are obviously overlapped. Palynological results indicated the pollen grains of section Acanthoxanthium (i.e., X. spinosum) and Xanthium (i.e., X. strumarium, X. sibiricum, and X. brasilicum) are clearly differing by their LM and SEM characters. However, no significant difference found between the pollen of X. strumarium and X. brasilicum. The Bayesian phylogenetic tree of the ITS region of rDNA sequences revealed that X. strumarium, X. sibiricum and X. brasilicum could not be discriminated as independent species. Overall, the morphological, palynological and molecular data provided evidence to synonymize X. brasilicum and X. strumarium with X. orientale and X. sibiricum with X. strumarium.
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References
Alam SS, Sukur MB, Zaman MY. 2011. Karyotype analysis in 2 morphological forms of Xanthium strumarium L. Cytologia 76(4):483-488.
Alorfi HS, Alshehry AA, Ghandourah MA, Bawakid NO, Elfaky MA, Ali AM, Alarif WM. 2020. Cytotoxic isoprenoids from Xanthium strumarium linn. Phcog Mag 16(70): 391-395.
Baldoni G, Viggiani P, Bonetti A, Dinelli G, Catizone P. 2000. Classification of Italian Xanthium strumarium complex based on biological traits, electrophoretic analysis and response to maize interference. Weed Res 40: 191-204.
Barth OM, Melhem TS. 1988. Glossário ilustrado de Palinologia. Editora Unicamp, Campinas.
Bentham G. 1873. Notes on the classification, history and geographical distribution of the Compositae. Botanical Journal of the Linnean Society 13: 335–557.
Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K, Ingram KK, Das I. 2007. Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22: 148–155.
Blackmore S, Wortley AH, Skvarla JJ, Gabarayeva NI, Rowley JJ. 2010. Developmental origins of structural diversity in pollen walls of Compositae. Plant Syst Evol 284(1–2): 17–32.
Blais PA, Lechowicz MJ. 1989. Variation among populations of Xanthium strumarium (Compositae) from natural and ruderal habitats. Amer J Bot 76: 901-908.
Bordbar F, Mirtadzadini M. 2015. Palynological study of Jurinea (Asteraceae) and related genera from flora of Iran. Plant Syst Evol 301(1): 151–162.
Caius JF. 1986. Medicinal and poisonous plants of India. Pbl Sci Publ Jodhpur India 1: 375-376.
Chandel S, Bagai U, Vashishat N. 2012. Antiplasmodial activity of Xanthium strumarium against Plasmodium berghei-infected BALB/c mice. Parasitol Res 110(3):1179-1183.
Cole RJ, Stuart BP, Lansden JA, Cox Rh. 1980. Isolation and redefinition of the toxic agent from cocklebur (Xanthium strumarium). J Agric Food Chem 28(6): 1330-1332.
Coutinho AP, Silveira P, Pita C, Santos MJ, Saraiva C, Perpétuo NC. 2020. Pollen morphology of Xanthium L. (sl) (Asteraceae, Asteroideae, Heliantheae, Ambrosiinae) in the Iberian Peninsula-a palynotaxonomic approach to a poisonous, allergenic and invasive genus. Grana 17: 1-22.
Davis PH. 1975. Flora of Turkey and the East Aegean Island, Vol. 5. Edinburgh University Press: Edinburgh.
Dinelli G, Bonetti A, Viggiani P. 2003. Genetic Structure and Mating System of Italian Xanthium strumarium Complex. Weed Sci 51(1): 69-77.
Dittrich M. 1989. Compositae VII. In: K. H. Rechinger (eds) Flora Iranica, no. 164, pp 125, 83tab, Graz-Austria.
Doyle JJ, Doyle JL. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19: 11–15.
Erdtman G. 1963. Palynology. In Advances in botanical research (Vol. 1). Academic Press.
Gautam R, Saklani A, Jachak SM. 2007. Indian medicinal plants as a source of antimycobacterial agents. J Ethnopharmacol 110(2): 200-34.
Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98.
Hammer O, Harper DAT, Ryan PD. 2009. Past version 1.91: Paleontological Statical Software package for education and data analysis. Palaeontol Electron 4: 4.
Hare JD. 1980. Variation in fruit size and susceptibility to seed predation among and within populations of the cocklebur, Xanthium strumarium L. Oecol 46: 217-222.
Hicks JA. 1971. Systematic studies of Xanthium (compositae: Ambrosieae): The cockleburs of Tazewell country: Illionois [Dissertation]. Urbana-champaign: University Illinois.
Hind DJN. 1993. Heliantheae. In: D.J.N. Hind, C. Jeffrey, & A. J. Scott, Flore des Mascareignes: La Rénion, Maurice, Rodrigues. 109. Composées. The Sugar Industry Research Institute, Mauritius; L‘Institut Français de Recherche Scientifique pour le Développement en Coopération (ORSTOM), Paris; The Royal Botanic Gardens, Kew. pp. 168–226.
Hind DJN. 2011. Annotated systematic checklist of the Compositae of Bolivia, version 2, kew Gardens, Uk. Avaliable at: https://www.kew.org/science/our-science/projects/annotated-systematic-checklist-compositae-bolivia
Hocking PJ, Liddle MJ. 1986. The biology of Australian weeds: 15. Xanthium occidentale Bertol. complex and Xanthium spinosum L. Aust J Agric Res 50: 191-221.
Hoffmann O. 1890. Compositae. In: Engler A, Prantl K, eds. Die Natürlichen Pflanzenfamilien, Vol. 4, 87–391. Leipzig: Verlag von Wilhelm Engelmann.
Isaac NJ, Mallet J, Mace GM. 2004. Taxonomic inflation: its influence on macroecology and conservation. Trends Ecol Evol 19: 464–469.
Löve D, Dansureau P. 1959. Biosystematic studies on Xanthium: taxonomic appraisal and ecological status. Can J Bot 37: 173-208.
Löve D. 1976. Xanthium L. In: Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DM, Walters SM, Webb DA, eds. Flora Europaea, vol. 4, Plantaginaceae to Compositae (and Rubiaceae), 143. Cambridge, London, New York, Melbourne: Cambridge University Press.
Ma YT, Huang MC, Hsu FL, Chang HF. 1998. Thiazinedione from Xanthium strumarium. Phytochemistry. 48(6): 1083–1085.
Mace GM. 2004. The role of taxonomy in species conservation. Philos Trans R Soc Lond B 359: 711–719.
McMillan C. 1974. Experimental hybridization in Xanthium strumarium of American complexes with diverse photoperiodic adaptations. Can J Bot 52: 849-859.
Moore AJ, Moore WL, Baldwin BG. 2014. Genetic and ecotypic differentiation in a californian plant polyploid complex (Grindelia, Asteraceae). PLoS ONE 9(4): e956.
Moran GF, Marshall DR, Muller WJ. 1981. Phenotypic variation and plasticity in the colonizing species Xanthium strumarium (Noogoora Burr). Aust J Biol Sci 3634, 9-648.
Moran GF, Marshall DR. 1978. AlIozyme Uniformity Within and Variation Between Races of the Colonizing Species Xanthium Strumarium L. (Noogoora Burr). Aust J Biol Sci 31(3) 283-292.
Nadeau LH. 1961. Etude biosystematique sur le gene Xanthium [unpubl. PhD thesis]. Montreal: University of Montreal.
Nlander JAA. 2004. MrModeltest v2. Program distributed by the author, Evolutionary Biology Centre, Uppsala University. Avaliable at: http://www.abc.se/*nylander/
Page DM. 2001. TreeView (Win32) Version 1.6.6. http://taxonomy.zoology.gla.ac.uk/rod/rod.html
Pereira Coutinho A, Silveira P, Pita C, Santos MJ, Saraiva C, Perpétuo NC. 2020. Pollen morphology of Xanthium L. (sl) (Asteraceae, Asteroideae, Heliantheae, Ambrosiinae) in the Iberian Peninsula-a palynotaxonomic approach to a poisonous, allergenic and invasive genus. Grana 17: 1-22.
Pereira Coutinho A, Almeida R, Sá da Bandeira D, Ortiz S. 2012. Pollen morphology in tribe Dicomeae Panero & Funk (Asteraceae). Plant Syst Evol 298(10): 1851–1865.
Pereira Coutinho A, Dinis A. 2009. A light, scanning electron, and transmission electron microscopic study of pollen wall architecture in the subtribe Gnaphaliinae (Gnaphalieae, Asteraceae). Plant Syst Evol 283(1–2): 79–92.
Pereira Coutinho A, Paiva J. 2019. Xanthium L. In: Aedo C, Herrero A, eds. Flora Iberica – Plantas Vasculares de la Península Ibérica y Islas Baleares, Vol. 16, 2159–2165. Madrid: Editorial CSIC.
Podani J. 2000. Introduction to the Exploration of multivariate Data. Backhuyes, Leiden, pp 407.
Punt W, Hoen PP, Blackmore S, Nilsson S, Le Thomas A. 2007. Glossary of pollen and spore terminology. Rev Palaeobot Palynol 143: 1-81.
Punt W, Hoen PP. 2009. The Northwest European Pollen Flora, vol. 70: Asteraceae-Asteroideae. Rev Palaeobot Palynol 157(1-2): 22-183.
Rambaut A, Drummond AJ. 2007. Tracer v 1.3. Avaliable at: http://evolve.zoo.ox.ac.uk
Rechinger KH. 1989. Helianthae in K. H. Rechinger Flora Iranica, no 164: 33-40. Graz-Austria.
Sheidai M, Ziaee S, Farahani F, Talebi SY, Noormohammadi Z, Hasheminejad-Ahangarani-Farahani Y. 2014. Infra-specific genetic and morphological diversity in Linum album (Linaceae). Biologia 69 (1): 32–39.
Simmons MP, Ochoterena H. 2000. Gaps as characters in sequencebased phylogenetic analyses. Syst Biol 49:369–381.
Skvarla JJ, Turner BL. 1966. Systematic implications from electron microscopic studies of compositae pollen – A review. Ann Mo Bot Gard 53(2): 109–164.
Skvarla, J.J., 1977. Pollen morphology in the Compositae and in morphologically related families. The biology and chemistry of the Compositae, pp.141-248. New York: Academic Press.
Strother JL. 2006. Xanthium in: Flora of north America. Editorial committee (eds) Flora of North America, vol 21. New York, Oxford university press, pp 19-20.
TelleríaMC, SanchoG, FunkVA, Ventosa I, Roque N. 2013. Pollen morphology and its taxonomic significance in the tribe Gochnatieae (Compositae, Gochnatioideae). Plant Syst Evol 299(5): 935–948.
Thompson JD, Higgins DG, Gibson TJ. 1994. Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680.
Tomasello S, Heubl G. 2017. Phylogenetic analysis and molecular characterization of Xanthium sibiricum using DNA barcoding, PCR-RFLP and specific primers. Planta Med 83: 946-953.
Tomasello S. 2018. How many names for a beloved genus? –Coalescent-based species delimitation in Xanthium L. (Ambrosiinae, Asteraceae). Mol Phyl and evol 127, 135-145.
Tong C, Chen RH, Liu DC, Zeng DS, Liu H. 2020. Chemical Constituents from the Fruits of Xanthium strumarium and Their Antitumor Effects. Nat Prod Commun 15(8) 1-5.
Wagenitz G. 1976. Systematics and phylogeny of the Compositae (Asteraceae). Plant Syst Evol 125(1) 29-46.
Wallace LJ, Boilard SM, Eagle SH, Spall JL, Shokralla S, Hajibabaei M. 2012. DNA barcodes for everyday life: routine authentication of natural health products. Food Res Int 49(1): 446-452.
Weaver SE, Lechowich MJ. 1982. The biology of Canadian weeds. 56. Xanthium strumarium L. J Plant Sci 63:211-225.
White TJ, Bruns T, Lee S, Taylor JW. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR protocols: a guide to methods and applications. Academic Press. New York, USA.
Widder FJ. 1923. Die arten der Gattung Xanthium. Beitrage Zu einer monographie. Rep spec Nov Regni veg 20:1-222.
Wortley AH, Blackmore S, Chissoe WF, Skvarla JJ. 2012. Recent advances in Compositae (Asteraceae) palynology, with emphasis on previously unstudied and unplaced taxa. Grana 51(2): 158–179.
Wortley AH, Funk VA, Skvarla JJ. 2008. Pollen and the evolution of Arctotideae (Compositae). Bot Rev 74(3): 438–466.
Zhao X, Hu W. 2014. Application of ITS2 sequence as DNA barcode in Xanthium. Agric Biotechnol 3(1), 19. Franco JA. 1984. Nova Flora de Portugal, vol. II, Clethraceae–Compositae. Lisboa: Escolar Editora.
Alorfi HS, Alshehry AA, Ghandourah MA, Bawakid NO, Elfaky MA, Ali AM, Alarif WM. 2020. Cytotoxic isoprenoids from Xanthium strumarium linn. Phcog Mag 16(70): 391-395.
Baldoni G, Viggiani P, Bonetti A, Dinelli G, Catizone P. 2000. Classification of Italian Xanthium strumarium complex based on biological traits, electrophoretic analysis and response to maize interference. Weed Res 40: 191-204.
Barth OM, Melhem TS. 1988. Glossário ilustrado de Palinologia. Editora Unicamp, Campinas.
Bentham G. 1873. Notes on the classification, history and geographical distribution of the Compositae. Botanical Journal of the Linnean Society 13: 335–557.
Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K, Ingram KK, Das I. 2007. Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22: 148–155.
Blackmore S, Wortley AH, Skvarla JJ, Gabarayeva NI, Rowley JJ. 2010. Developmental origins of structural diversity in pollen walls of Compositae. Plant Syst Evol 284(1–2): 17–32.
Blais PA, Lechowicz MJ. 1989. Variation among populations of Xanthium strumarium (Compositae) from natural and ruderal habitats. Amer J Bot 76: 901-908.
Bordbar F, Mirtadzadini M. 2015. Palynological study of Jurinea (Asteraceae) and related genera from flora of Iran. Plant Syst Evol 301(1): 151–162.
Caius JF. 1986. Medicinal and poisonous plants of India. Pbl Sci Publ Jodhpur India 1: 375-376.
Chandel S, Bagai U, Vashishat N. 2012. Antiplasmodial activity of Xanthium strumarium against Plasmodium berghei-infected BALB/c mice. Parasitol Res 110(3):1179-1183.
Cole RJ, Stuart BP, Lansden JA, Cox Rh. 1980. Isolation and redefinition of the toxic agent from cocklebur (Xanthium strumarium). J Agric Food Chem 28(6): 1330-1332.
Coutinho AP, Silveira P, Pita C, Santos MJ, Saraiva C, Perpétuo NC. 2020. Pollen morphology of Xanthium L. (sl) (Asteraceae, Asteroideae, Heliantheae, Ambrosiinae) in the Iberian Peninsula-a palynotaxonomic approach to a poisonous, allergenic and invasive genus. Grana 17: 1-22.
Davis PH. 1975. Flora of Turkey and the East Aegean Island, Vol. 5. Edinburgh University Press: Edinburgh.
Dinelli G, Bonetti A, Viggiani P. 2003. Genetic Structure and Mating System of Italian Xanthium strumarium Complex. Weed Sci 51(1): 69-77.
Dittrich M. 1989. Compositae VII. In: K. H. Rechinger (eds) Flora Iranica, no. 164, pp 125, 83tab, Graz-Austria.
Doyle JJ, Doyle JL. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19: 11–15.
Erdtman G. 1963. Palynology. In Advances in botanical research (Vol. 1). Academic Press.
Gautam R, Saklani A, Jachak SM. 2007. Indian medicinal plants as a source of antimycobacterial agents. J Ethnopharmacol 110(2): 200-34.
Hall TA. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98.
Hammer O, Harper DAT, Ryan PD. 2009. Past version 1.91: Paleontological Statical Software package for education and data analysis. Palaeontol Electron 4: 4.
Hare JD. 1980. Variation in fruit size and susceptibility to seed predation among and within populations of the cocklebur, Xanthium strumarium L. Oecol 46: 217-222.
Hicks JA. 1971. Systematic studies of Xanthium (compositae: Ambrosieae): The cockleburs of Tazewell country: Illionois [Dissertation]. Urbana-champaign: University Illinois.
Hind DJN. 1993. Heliantheae. In: D.J.N. Hind, C. Jeffrey, & A. J. Scott, Flore des Mascareignes: La Rénion, Maurice, Rodrigues. 109. Composées. The Sugar Industry Research Institute, Mauritius; L‘Institut Français de Recherche Scientifique pour le Développement en Coopération (ORSTOM), Paris; The Royal Botanic Gardens, Kew. pp. 168–226.
Hind DJN. 2011. Annotated systematic checklist of the Compositae of Bolivia, version 2, kew Gardens, Uk. Avaliable at: https://www.kew.org/science/our-science/projects/annotated-systematic-checklist-compositae-bolivia
Hocking PJ, Liddle MJ. 1986. The biology of Australian weeds: 15. Xanthium occidentale Bertol. complex and Xanthium spinosum L. Aust J Agric Res 50: 191-221.
Hoffmann O. 1890. Compositae. In: Engler A, Prantl K, eds. Die Natürlichen Pflanzenfamilien, Vol. 4, 87–391. Leipzig: Verlag von Wilhelm Engelmann.
Isaac NJ, Mallet J, Mace GM. 2004. Taxonomic inflation: its influence on macroecology and conservation. Trends Ecol Evol 19: 464–469.
Löve D, Dansureau P. 1959. Biosystematic studies on Xanthium: taxonomic appraisal and ecological status. Can J Bot 37: 173-208.
Löve D. 1976. Xanthium L. In: Tutin TG, Heywood VH, Burges NA, Moore DM, Valentine DM, Walters SM, Webb DA, eds. Flora Europaea, vol. 4, Plantaginaceae to Compositae (and Rubiaceae), 143. Cambridge, London, New York, Melbourne: Cambridge University Press.
Ma YT, Huang MC, Hsu FL, Chang HF. 1998. Thiazinedione from Xanthium strumarium. Phytochemistry. 48(6): 1083–1085.
Mace GM. 2004. The role of taxonomy in species conservation. Philos Trans R Soc Lond B 359: 711–719.
McMillan C. 1974. Experimental hybridization in Xanthium strumarium of American complexes with diverse photoperiodic adaptations. Can J Bot 52: 849-859.
Moore AJ, Moore WL, Baldwin BG. 2014. Genetic and ecotypic differentiation in a californian plant polyploid complex (Grindelia, Asteraceae). PLoS ONE 9(4): e956.
Moran GF, Marshall DR, Muller WJ. 1981. Phenotypic variation and plasticity in the colonizing species Xanthium strumarium (Noogoora Burr). Aust J Biol Sci 3634, 9-648.
Moran GF, Marshall DR. 1978. AlIozyme Uniformity Within and Variation Between Races of the Colonizing Species Xanthium Strumarium L. (Noogoora Burr). Aust J Biol Sci 31(3) 283-292.
Nadeau LH. 1961. Etude biosystematique sur le gene Xanthium [unpubl. PhD thesis]. Montreal: University of Montreal.
Nlander JAA. 2004. MrModeltest v2. Program distributed by the author, Evolutionary Biology Centre, Uppsala University. Avaliable at: http://www.abc.se/*nylander/
Page DM. 2001. TreeView (Win32) Version 1.6.6. http://taxonomy.zoology.gla.ac.uk/rod/rod.html
Pereira Coutinho A, Silveira P, Pita C, Santos MJ, Saraiva C, Perpétuo NC. 2020. Pollen morphology of Xanthium L. (sl) (Asteraceae, Asteroideae, Heliantheae, Ambrosiinae) in the Iberian Peninsula-a palynotaxonomic approach to a poisonous, allergenic and invasive genus. Grana 17: 1-22.
Pereira Coutinho A, Almeida R, Sá da Bandeira D, Ortiz S. 2012. Pollen morphology in tribe Dicomeae Panero & Funk (Asteraceae). Plant Syst Evol 298(10): 1851–1865.
Pereira Coutinho A, Dinis A. 2009. A light, scanning electron, and transmission electron microscopic study of pollen wall architecture in the subtribe Gnaphaliinae (Gnaphalieae, Asteraceae). Plant Syst Evol 283(1–2): 79–92.
Pereira Coutinho A, Paiva J. 2019. Xanthium L. In: Aedo C, Herrero A, eds. Flora Iberica – Plantas Vasculares de la Península Ibérica y Islas Baleares, Vol. 16, 2159–2165. Madrid: Editorial CSIC.
Podani J. 2000. Introduction to the Exploration of multivariate Data. Backhuyes, Leiden, pp 407.
Punt W, Hoen PP, Blackmore S, Nilsson S, Le Thomas A. 2007. Glossary of pollen and spore terminology. Rev Palaeobot Palynol 143: 1-81.
Punt W, Hoen PP. 2009. The Northwest European Pollen Flora, vol. 70: Asteraceae-Asteroideae. Rev Palaeobot Palynol 157(1-2): 22-183.
Rambaut A, Drummond AJ. 2007. Tracer v 1.3. Avaliable at: http://evolve.zoo.ox.ac.uk
Rechinger KH. 1989. Helianthae in K. H. Rechinger Flora Iranica, no 164: 33-40. Graz-Austria.
Sheidai M, Ziaee S, Farahani F, Talebi SY, Noormohammadi Z, Hasheminejad-Ahangarani-Farahani Y. 2014. Infra-specific genetic and morphological diversity in Linum album (Linaceae). Biologia 69 (1): 32–39.
Simmons MP, Ochoterena H. 2000. Gaps as characters in sequencebased phylogenetic analyses. Syst Biol 49:369–381.
Skvarla JJ, Turner BL. 1966. Systematic implications from electron microscopic studies of compositae pollen – A review. Ann Mo Bot Gard 53(2): 109–164.
Skvarla, J.J., 1977. Pollen morphology in the Compositae and in morphologically related families. The biology and chemistry of the Compositae, pp.141-248. New York: Academic Press.
Strother JL. 2006. Xanthium in: Flora of north America. Editorial committee (eds) Flora of North America, vol 21. New York, Oxford university press, pp 19-20.
TelleríaMC, SanchoG, FunkVA, Ventosa I, Roque N. 2013. Pollen morphology and its taxonomic significance in the tribe Gochnatieae (Compositae, Gochnatioideae). Plant Syst Evol 299(5): 935–948.
Thompson JD, Higgins DG, Gibson TJ. 1994. Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673–4680.
Tomasello S, Heubl G. 2017. Phylogenetic analysis and molecular characterization of Xanthium sibiricum using DNA barcoding, PCR-RFLP and specific primers. Planta Med 83: 946-953.
Tomasello S. 2018. How many names for a beloved genus? –Coalescent-based species delimitation in Xanthium L. (Ambrosiinae, Asteraceae). Mol Phyl and evol 127, 135-145.
Tong C, Chen RH, Liu DC, Zeng DS, Liu H. 2020. Chemical Constituents from the Fruits of Xanthium strumarium and Their Antitumor Effects. Nat Prod Commun 15(8) 1-5.
Wagenitz G. 1976. Systematics and phylogeny of the Compositae (Asteraceae). Plant Syst Evol 125(1) 29-46.
Wallace LJ, Boilard SM, Eagle SH, Spall JL, Shokralla S, Hajibabaei M. 2012. DNA barcodes for everyday life: routine authentication of natural health products. Food Res Int 49(1): 446-452.
Weaver SE, Lechowich MJ. 1982. The biology of Canadian weeds. 56. Xanthium strumarium L. J Plant Sci 63:211-225.
White TJ, Bruns T, Lee S, Taylor JW. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: PCR protocols: a guide to methods and applications. Academic Press. New York, USA.
Widder FJ. 1923. Die arten der Gattung Xanthium. Beitrage Zu einer monographie. Rep spec Nov Regni veg 20:1-222.
Wortley AH, Blackmore S, Chissoe WF, Skvarla JJ. 2012. Recent advances in Compositae (Asteraceae) palynology, with emphasis on previously unstudied and unplaced taxa. Grana 51(2): 158–179.
Wortley AH, Funk VA, Skvarla JJ. 2008. Pollen and the evolution of Arctotideae (Compositae). Bot Rev 74(3): 438–466.
Zhao X, Hu W. 2014. Application of ITS2 sequence as DNA barcode in Xanthium. Agric Biotechnol 3(1), 19. Franco JA. 1984. Nova Flora de Portugal, vol. II, Clethraceae–Compositae. Lisboa: Escolar Editora.