Anatomical properties of Epilobium and Chamaenerion from a taxonomical perspective in Turkey

Abstract

In the present study, the anatomical features of stem, leaf, and fruit of 22 Epilobium L. and 4 Chamaenerion Séguier taxa were studied using light microscopy with the aim to find out taxonomically significant characters for the examined taxa. Principal component analysis indicated that the row number of collenchyma, presence of periderma and phloem fibers in the stem, the shape of midrib and idioblast, leaf type, and the shape of fruit in cross section are the most valuable anatomical traits delimiting the investigated taxa at generic and partly specific level. Additionally, the dendrograms resulted from unweighted pair-group method supported to describe members of Chamaenerion with circular or cordate midrib, equifacial leaf, cylindrical idioblast, and pericarp composed of T-form lobes and circular or rectangular central column and Epilobium with semicircular midrib, bifacial leaf, circular idioblast, and pericarp composed of m-form lobes and rectangular central column.

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References

  1. Akbari RS, Azizian D (2006) Seed morphology and seed coat sculpturing of Epilobium L. species (Onagraceae Juss.) from Iran. Turk J Bot 30:435–440

    Google Scholar 

  2. Battinelli L, Tita B, Evandri MG, Mazzanti G (2001) Antimicrobial activity of Epilobium spp. extracts. Il Farmaco 56:345–348. https://doi.org/10.1016/S0014-827X(01)01047-3

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  3. Baum DA, Sytsma KJ, Hoch PC (1994) A phylogenetic analysis of Epilobium (Onagraceae) based on nuclear ribosomal DNA sequences. Syst Bot 19(3):363–388. https://doi.org/10.2307/2419763

    Article  Google Scholar 

  4. Bobrov AVFC, Romanov MS (2019) Morphogenesis of fruits and types of fruit of angiosperms. Bot Lett 166(3):366–399. https://doi.org/10.1080/23818107.2019.1663448

    Article  Google Scholar 

  5. Canne-Hilliker JM, Kampny CM (1991) Taxonomic significance of leaf and stem anatomy of Agalinis (Scrophulariaceae) from the USA and Canada. Can J Bot 69(9):1935–1950. https://doi.org/10.1139/b91-243

    Article  Google Scholar 

  6. Casson S, Gray JE (2008) Influence of environmental factors on stomatal development. New Phytol 178:9–23. https://doi.org/10.1111/j.1469-8137.2007.02351.x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. Celik G, Semiz A, Karakurt S, Gencler-Ozkan AM, Arslan S, Adali O, Sen A (2016) Inhibitory action of Epilobium hirsutum extract and its constituent ellagic acid on drug-metabolizing enzymes. Eur J Drug Metab Pharmacokinet 41(2):109–116. https://doi.org/10.1007/s13318-014-0238-1

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  8. Chamberlain DF, Raven PH (1972) Epilobium L. In: Davis PH (ed) Flora of Turkey and the East Aegean Islands, vol 4. Edinburgh University Press, Edinburgh, pp 183–196

    Google Scholar 

  9. Chen CJ, Hoch PC, Raven PH (2007) Epilobium L. In: Wu S, Raven PH, Hong DY (eds) Flora of China, vol 13. Science Press and Missouri Botanical Garden Press, Beijing and St. Louis, pp 400–422

    Google Scholar 

  10. Chonan N (1978) Comparative anatomy of mesophyll among the leaves of gramineous crops. Jpn Agric Res Q 12:128–131

    Google Scholar 

  11. Coşkunçelebi K, Makbul S, Beyazoğlu O (2015) Bitki morfolojisi ve anatomisi, Gündüz Ofset Matbaacılık ve Yayıncılık, pp 223–271

  12. Coşkunçelebi K, Makbul S, Okur S (2017) Seed morphology of Epilobium and Chamaenerion (Onagraceae) in Turkey. Phytotaxa 331(2):169–184. https://doi.org/10.11646/phytotaxa.331.2.2

    Article  Google Scholar 

  13. Czerepanov SK (1995) Vascular plants of Russia and adjacent states (the former USSR). Cambridge University Press, Cambridge

    Google Scholar 

  14. Darók J, Borhidi A, Kaposvári F (2000) The taxonomic importance of leaf-surface characters in the genus Exostema (Rubiaceae). Acta Bot Hungar 42(1–4):85–96

    Google Scholar 

  15. Davis PH (1970) Flora of Turkey and the East Aegean Islands, vol. 3, Edinburgh University Press, pp 177–179.

  16. Esau K (1977) Anatomy of the seed plants, 2nd edn. John Wiley & Sons Ltd, New York

    Google Scholar 

  17. Gavrilova G, Sulcs V (1999) Latvijas Vaskularo Augu Flora, Taksonu saraksts. Latvijas Akademiska biblioteka, Riga

    Google Scholar 

  18. Gray SF (1821) A natural arrangement of British plants, vol 2. Baldwin, Cradock and Joy, London

    Google Scholar 

  19. Gudzinskas Z (1999) Lietuvos Induociai Augalai. Botanikos instituto leidykla, Vilnius

    Google Scholar 

  20. Güner A, Aslan S, Ekim T, Vural M, Babaç MT (2012) Türkiye bitkileri listesi, Damarlı bitkiler, Nezahat Gökyiğit Botanik Bahçesi Flora Araştırmaları Derneği Yayınları, İstanbul, 1290 p

  21. Güven S (2017) Türkiye Vincetoxicum Wolf (Apocynaceae-Asclepiadoideae) cinsinin taksonomik revizyonu. Doktora Tezi, Recep Tayyip Erdoğan Üniversitesi, Fen Bilimleri Enstitüsü, Rize, Türkiye. (in Turkish)

  22. Güven S, Beyazoğlu O, Makbul S, Türkmen Z, Kandemir A (2013) Anatomical features of six Onosma L. (Boraginaceae) species from Turkey. Iran J Bot 19(1):94–103

    Google Scholar 

  23. Haussknecht C (1884) Monographie der Gattung Epilobium. Jena, Germany, 318 pp

  24. Hoch PC, Raven PH (1992) Boisduvalia, a coma–less Epilobium (Onagraceae). Phytologia 73:456–459. https://doi.org/10.5962/bhl.part.16727

    Article  Google Scholar 

  25. Holub J (1972) Taxonomic and nomenclatural remarks on Chamaenerion auct. Folia Geobot Phytotaxon 7:81–90. https://doi.org/10.1007/BF02856384

    Article  Google Scholar 

  26. Johansen DA (1940) Plant microtechnique. McGraw- Hill, New York

    Google Scholar 

  27. Karakurt S, Semiz A, Celik G, Gencler-Ozkan AM, Sen A, Adali O (2013) Epilobium hirsutum alters xenobiotic metabolizing CYP1A1, CYP2E1, NQO1 and GPx activities, mRNA and protein levels in rats. Pharm Biol 51(5):650–658. https://doi.org/10.3109/13880209.2012.762404

    Article  PubMed  PubMed Central  Google Scholar 

  28. Karlsson T (1998) Förteckning över svenska karlvaxter, Svensk Bot. Tidskr. 91:241–560

    Google Scholar 

  29. Kartesz JT, Meacham CA (1999) Synthesis of the North Ameri- can flora, version 1.0 on CD-ROM. North Carolina Botanical Garden, University of North Carolina, Chapel Hill

    Google Scholar 

  30. Keating R (1982) The evolution and systematics of Onagraceae: leaf anatomy. Ann Mo Bot Gard 69:770–803

    Article  Google Scholar 

  31. Kotina EL, Oskolski AA, Stepanova AV, Tilney PM, Van Wyk B-E (2013) Notes on the taxonomic and ecological significance of bark structure in the genus Virgilia (Fabaceae, Podalyrieae). S Afr J Bot 89:240–243. https://doi.org/10.1016/j.sajb.2013.07.003

    Article  Google Scholar 

  32. Kovach WL (2007) MVSP - A MultiVariate Statistical Package for Windows, ver. 3.1. Kovach Computing Services, Pentraeth

    Google Scholar 

  33. Krajšek SS, Dermastia M, Jogan N (2006) Determination key for Central European Epilobium species based on trichome morphology. Bot Helv 2:169–178. https://doi.org/10.1007/s00035­006­0770­y

    Article  Google Scholar 

  34. Kukk T (1999) Eesti taimestik. Tartu & Tallinn: Teaduste Akadeemia Kirjastus

  35. Kumar P, Singh H, Kumar Singhal V (2018) A synopsis of cytology and cytogeography of tribe Epilobieae Endl. (Onagraceae). Cytologia 83(2):175–180

    Article  Google Scholar 

  36. Kundakçı S (2017) Türkiye Epilobium L. and Chamerion (Rafinesque) Rafinesque ex Holub (Onagraceae) taksonlarının nrDNA ITS dizilerine dayalı akrabalık ilişkileri. Yüksek Lisans Tezi, Recep Tayyip Erdoğan Üniversitesi, Fen Bilimleri Enstitüsü, Rize, Turkey

  37. Kytövuori I (1998) Epilobium L. In: Hamet-Ahti L, Suominen J, Ulvinen T, Uotila P (eds) Retkeilykasvio, 4th edn. Luonnontieteellinen keskusmuseo, Kasvimuseo, Helsinki, pp 295–301

    Google Scholar 

  38. Leroux O (2012) Collenchyma: a versatile mechanical tissue with dynamic cell walls. Ann Bot 110:1083–1098. https://doi.org/10.1093/aob/mcs186

    Article  PubMed  PubMed Central  Google Scholar 

  39. Lersten NR, Curtis JD (2001) Idioblasts and other unusual internal foliar secretary structures Scrophulariaceae. Plant Syst Evol 227:63–73

    Article  Google Scholar 

  40. Levin RA, Wagner WL, Hoch PC, Hahn WJ, Rodriguez A, Baum DA, Katinas L, Zimmer EA, Sytsma KJ (2004) Paraphyly in tribe Onagreae: insights into phylogenetic relationships of Onagraceae based on nuclear and chloroplast sequence data. Syst Bot 29:147–164

    Article  Google Scholar 

  41. Makbul S, Coskunçelebi K, Türkmen Z, Beyazoglu O (2006) Morphology and anatomy of Scrophularia L. (Scrophulariaceae) taxa from NE Anatolia. Acta Biol Cracov Ser Bot 48(1):33–43

    Google Scholar 

  42. Makbul S, Türkmen Z, Coşkunçelebi K, Beyazoğlu O (2008) Anatomical and polen characters in the genus EpilobiumL. (Onagraceae) from Northeast Anatolia. Acta Biol Cracov Ser Bot 50(1):51–62

    Google Scholar 

  43. Makbul S, Coskunçelebi K, Turkmen Z, Beyazoglu O (2011) Comparison of foliar anatomy of Scorzonera L. (Asteraceae) taxa from North East Anatolia. Pak J Bot 43:135–155

    Google Scholar 

  44. Makbul S, Coşkunçelebi K, Okur S (2015) Taxonomical contributions to Turkish Epilobium L. (Onagraceae) Taxa based on trichome features, 6th edn. Balkan Botanical Congres, Rijeka, p 88

    Google Scholar 

  45. Makbul S, Coşkunçelebi K, Okur S, Gültepe M (2016) Contribution to the taxonomy of Turkish Scorzonera (Asteraceae) taxa based on vegetetive anatomy. Nord J Bot 34(6):670–684. https://doi.org/10.1111/njb.01159

    Article  Google Scholar 

  46. Metcalfe CR, Chalk L (1950) Anatomy of Dicotyledons. Clarendon Press, Oxford

    Google Scholar 

  47. Mosquin T (1966) A new taxonomy for Epilobium angustifolium L.(Onagraceae). Brittonia 18(2):167–188

    Article  Google Scholar 

  48. Munz PA (1965) Onagraceae. North Am Flora II 5:1–278

    CAS  Google Scholar 

  49. Nieto Feliner G (1996) Notes on Epilobium (Onagraceae) from the Western Mediterranean. Anales Jardín Botanico De Madrid 54:255–264

    Google Scholar 

  50. Odintsova А, Klimovych N (2017) Anatomical and morphological fruit structure in Epilobium hirsutum and E. angustifolium (Onagraceae). Ukr Bot J 74(6):582–593

    Article  Google Scholar 

  51. Okur S (2019) Türkiye Epilobium L. (Onagraceae) taksonlarının biyosistematik yönden incelenmesi, Doktora Tezi, Recep Tayyip Erdoğan Üniversitesi, Fen Bilimleri Enstitüsü, Rize, Türkiye

  52. Okur S, Çoşkunçelebi K, Makbul S (2018) Floral variation within the genus Epilobium L. (Onagraceae) at infraspecific and interspecific level in Turkey. The 2nd International UNIDOKAP Black Sea Symposium on Biodiversity (pp.99-105). Samsun, Turkey

  53. Raimann R (1893) Onagraceae. In: Die Natürlichen Pflanzenfamilien. Engler A, Prantl K (eds), 3(7): 199–223. Leipzig: Wilhelm Engelmann

  54. Raven PH (1962) The genus Epilobium in Turkey. Notes R Bot Garden Edinburgh 24:183–203

    Google Scholar 

  55. Raven PH (1964) Onagraceae. In: Rechinger K (ed) Flora Iranica, No.7. Akademische Druck-U. Verlasanstalt, Graz

    Google Scholar 

  56. Raven PH (1976) Generic and sectional delimitation in Onagraceae, tribe Epilobieae. Ann Mo Bot Gard 63:326–340. https://doi.org/10.2307/2395311

    Article  Google Scholar 

  57. Raven PH (1980) Epilobium L. In: Tutin TG (ed) Flora Europaea 5. Cambridge University Press, Cambridge, pp 308–311

    Google Scholar 

  58. Raven PH (1988) Onagraceae as a model of plant evolution. In: Gottlieb LD, Jain SK (eds) Plant Evolutionary Biology. Chapman and Hall, New York, pp 85–107. https://doi.org/10.1007/978-94-009-1207-6_4

    Google Scholar 

  59. Raven PH, Raven TE (1976) The genus Epilobium (Onagraceae) in Australasia: a systematic and evolutionary study. N Z Dept Sci Ind Res Bull 216:1–321

  60. Samuelsson G (1923) Revision der Siidamerikanischen Epilobium–arten. Svensk Botanisk Tidskirift 17:241–295

    Google Scholar 

  61. Samuelsson G (1930) Zur Epilobium–Flora sudamerikas. Svensk Botanisk Tidskirift 24:1–11

    Google Scholar 

  62. Sayık A, Yusufoğlu A, Açık L, Türker G, Aydın B, Arslan L (2017) DNA- binding, biological activities and chemical composition of wild growing Epilobium angustifolium L. Extracts from Canakkale, Turkey. J Turk Chem Soc Sect A Chem 4(3):811–840. https://doi.org/10.18596/jotcsa.319789

  63. Sennikov AN (2011) Chamerion or Chamaenerion (Onagraceae)? The old story in new words. Taxon 60:1485–1488

    Article  Google Scholar 

  64. Shteinberg EI (1949) Onagraceae. In: Shishkin BK (ed) Flora of the USSR, vol 15. Nauko, Moscow, pp 425–472

    Google Scholar 

  65. Sneath PHA, Sokal RR (1973) Numerical taxonomy: The principles and practice of numerical classification. WH Freeman and Company, San Francisco

    Google Scholar 

  66. Snogerup S (2010) Chamerion Raf. ex Holub. pp 89-90. In: Jonsell B, Karlsson T (eds) Flora Nordica, vol 6. The Swedish Museum of Natural History, Stockholm

    Google Scholar 

  67. Solomon JC (1982) The systematics and evolution of Epilobium (Onagraceae) in South America. Ann Missouri Bot Garden 69:239–335. https://doi.org/10.2307/2398938

    Article  Google Scholar 

  68. Spach E (1835a) Synopsis Monographia Onagrearum. Annales des sciences naturelles, Botanique 4:161–178

    Google Scholar 

  69. Spach E (1835b) Histoire natürelle des végétaux phanéro games. Librairie Encyclopédique De Roret, Paris 446 pp

    Google Scholar 

  70. Stace C (1999) Field flora of the British Isles. Cambridge University Press, Cambridge

    Google Scholar 

  71. Tobler F (1957) Die mechanischen Elemente und das mecanische System. In: Linsbauer K (editor). Handbuch der Pflanzenanatomie. 2nd edn. Band 4, Teil 6

  72. Tzvelev NN (2000) Manual of the vascular plants of North-West Russia (Leningrad, Pskov and Novgorod Provinces). St. Petersburg Chemical-Pharmateutical Academy Publishing House, St. Petersburg (in Russian)

    Google Scholar 

  73. Vardar Y (1962) Botanikte Preparasyon Tekniği. Ege Üniversitesi Matbaası, Ege Üniversitesi Fen Fakültesi Kitaplar Serisi No:1, 66 p

  74. Wagner WL, Hoch PC, Raven PH (2007) Revised classification of the Onagraceae. Syst Bot Monogr 83:1–193

    Google Scholar 

  75. Yentür S (2003) Bitki Anatomisi. İstanbul Üniversitesi, Fen Fakültesi, Biyoloji Bölümü, No: 227, İstanbul (in Turkish)

  76. Zeybek N, Zeybek U (1994) Farmasotik Botanik. Ege Üniversitesi Basım Evi, İzmir (in Turkish)

    Google Scholar 

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Funding

The authors extend their thanks to the Scientific and Technological Research Council of Turkey (TUBITAK, 113Z782) and Recep Tayyip Erdogan University Scientific Research Projects Coordination Unit (FBA-2016-529) for the financial support.

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Appendix

Appendix

Table 4 Anatomical scores used in the numerical analyses

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Güven, S., Makbul, S., Mertayak, F. et al. Anatomical properties of Epilobium and Chamaenerion from a taxonomical perspective in Turkey. Protoplasma (2021). https://doi.org/10.1007/s00709-020-01602-0

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Keywords

  • Carpology
  • Fruit
  • Internal morphology
  • Leaf
  • Numerical analysis
  • Stem