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Validation of leaf undulation traits in the taxonomy of Epipactis muelleri Godfery, 1921 (Orchidaceae, Neottieae)

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Abstract

Leaf undulation is used as a diagnostic feature in the taxonomy of different taxa of the Epipactis (Orchidaceae) genus. It is considered a specifically important trait, apart from the column (gynostemium) structure, in the identification of E. muelleri. However, leaf undulation is a common developmental phenomenon in various plants, including orchids, thus the main goal of the research presented was to validate the usefulness of this feature in Epipactis taxonomy. In the course of this study, the leaf structure of six Epipactis species was analyzed, i.e., E. albensis, E. atrorubens, E. helleborine, E. muelleri, E. palustris and E. purpurata. The leaf margin outline and the cellular pattern of the leaf surface, as well as the presence of papillae, were examined in detail. The results obtained showed that in all taxa analyzed, representing different groups of the Epipactis genus, leaf undulation was present. The phenomenon was related to leaf blade development and the local differential growth of leaf sectors rather than to the taxonomic position of the species. Therefore, leaf undulation studied in Helleborines does not have a diagnostic value as a non-programmed intrinsic feature and should not be applied to taxa identification. The valid trait in Epipactis classification (including E. muelleri) is the column structure.

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References

  • Baumann H, Künkele S (1988) Die Orchideen Europas. Franckh-Kosmos Verlag, Stuttgart

    Google Scholar 

  • Baumann H, Künkele S, Lorenz R (2006) Orchideen Europas: mit angrenzenden gebieten. Eugen Ulmer KG, Stuttgart

    Google Scholar 

  • Bierhost DW (1977) On the stem apex, leaf initiation and early leaf ontogeny in filicalean ferns. Am J Bot 64:125–152

    Article  Google Scholar 

  • Cho K, Jun S, Jeong S, Lee Y, Kim G (2007) Developmental processes of leaf morphogenesis in Arabidopsis. J Plant Biol 50:282–290. doi:10.1007/BF03030656

    Article  CAS  Google Scholar 

  • Coen E, Rolland-Lagan AG, Matthews M, Bangham JA, Prusinkiewicz P (2004) The genetics of geometry. Proc Natl Acad Sci USA 101:4728–4735. doi:10.1073/pnas.0306308101

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Delforge P (2005) Orchids of Britain & Europe. Collins Photo Guide. Harper Collins Publishers, London

    Google Scholar 

  • Delforge P (2006) Orchids of Europe, North Africa and the Middle East. Timber Press Inc., Oregon

    Google Scholar 

  • Fleming A (2002) The mechanism of leaf morphogenesis. Planta 216:17–22. doi:10.1007/s00425-002-0864-8

    Article  CAS  PubMed  Google Scholar 

  • Fleming AJ (2003) The molecular regulation of leaf form. Plant Biol 5:341–349. doi:10.1055/s-2003-42718

    Article  CAS  Google Scholar 

  • Fleming AJ (2005) The control of leaf development. New Phytol 166:9–20. doi:10.1111/j.1469-8137.2004.01292.x

    Article  CAS  PubMed  Google Scholar 

  • Fleming AJ, McQueen-Mason S, Mandel T, Kuhlemeier C (1997) Induction of leaf primordia by the cell wall protein expansin. Science 276:1415–1418. doi:10.1126/science.276.5317.1415

    Article  CAS  Google Scholar 

  • Flora Catalana (2012) Epipactis helleborine (L.) Crantz subsp. muelleri (Godfery) O. Bolòs, Masalles et Vigo. http://www.floracatalana.net/epipactis-helleborine-l-crantz-subsp-muelleri-godfery-o-bolos-masalles-et-vigo. Accessed 3 Oct 2012

  • Gola EM, Jernstedt JA (2011) Impermanency of initial cells in Huperzia lucidula (Huperziaceae) shoot apices. Int J Plant Sci 172:847–855. doi:10.1086/660878

    Article  Google Scholar 

  • Green AA, Kennaway JR, Hanna AI, Bangham JA, Coen E (2010) Genetic control of organ shape and tissue polarity. PLoS Biol 8:e1000537. doi:10.1371/journal.pbio.1000537

    Article  PubMed Central  PubMed  Google Scholar 

  • Hejnowicz Z (1984) Trajectories of principal directions of growth, natural coordinate system in growing plant organs. Acta Soc Bot Pol 53:29–42

    Article  Google Scholar 

  • Hejnowicz Z (1992) Travelling pattern of acidity in the epidermis of tulip leaves. Bot Acta 105:266–272

    Article  CAS  Google Scholar 

  • Hollingsworth PM, Squirrell J, Hollingsworth ML, Richards AJ, Bateman RM (2006) Taxonomic complexity, conservation and recurrent origins of self-pollination in Epipactis (Orchidaceae). In: Bailey J, Ellis RG (eds) Current taxonomic research on the British and European flora. Botanical Society of the British Isles, London, pp 27–44

  • Jakubska-Busse A (2008) The range and significance of phenotypic plasticity of Broad-leaved Helleborine Epipactis helleborine (L.) Crantz for taxonomy (Orchidaceae: Neottieae). In: Borowiec L, Tarnawski D (eds) The importance of natural history museum of taxonomy. Polish Taxonomical Monographs 15. University of Wrocław, Wrocław, pp 85–92

    Google Scholar 

  • Jakubska-Busse A, Gola EM (2010) Morphological variability of Helleborines. I. Diagnostic significance of morphological features in Epipactis helleborine (L.) Crantz, Epipactis atrorubens (Hoffm.) Besser and their hybrid, Epipactis × schmalhausenii Richt. (Orchidaceae, Neottieae). Acta Soc Bot Pol 79:207–213

    Article  Google Scholar 

  • Liang H, Mahadevan L (2009) The shape of a long leaf. Proc Natl Acad Sci USA 106:22049–22054. doi:10.1073/pnas.0911954106

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nath U, Crawford BCW, Carpenter R, Coen E (2003) Genetic control of surface curvature. Science 299:1404–1407. doi:10.1126/science.1079354

    Article  CAS  PubMed  Google Scholar 

  • O’Brien TP, McCully ME (1981) The study of plant structure: principles and selected methods. Termarcarphi Pty Ltd, Melbourne

    Google Scholar 

  • Pien S, Wyrzykowska J, McQueen-Mason S, Smart C, Fleming A (2001) Local expression of expansin induces the entire process of leaf development and modifies leaf shape. Proc Natl Acad Sci USA 98:11812–11817. doi:10.1073/pnas.191380498

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Potůček O, Čačko L (1996) Všechno o orchidejích. Nakladatelstvi Slovart, Prague

    Google Scholar 

  • Procházka F, Velísek V (1983) Orchideje naši přirody. Academia, Prague

    Google Scholar 

  • Rankou H (2011) Epipactis muelleri. IUCN 2012. IUCN Red List of Threatened Species. Version 2012.1. http://www.iucnredlist.org. Accessed 13 Feb 2013

  • Reinhardt J, Schneider E (2002) Morphologische Veranderungen am Gynostemium bei Epipactis muelleri Godf. (Orchidaceae). Ber Arbeitskr Heim Orch 19:53–59

    Google Scholar 

  • Richards AJ, Porter AF (1982) On the identity of a Northumberland Epipactis. Watsonia 14:121–128

    Google Scholar 

  • Rothmaler W, Jäger E, Schubert R, Werner K (2007) Exkursionsflora für die Gebiete der DDR und der BRD, Bd. 3, Atlas der Gefäßpflanzen. Atlasband. 11 Aufl. Spektrum, Heidelberg

  • Sell P, Murrell G (1997) Flora of Great Britain and Ireland V: Butomaceae—Orchidaceae. Cambridge University Press, Cambridge

    Google Scholar 

  • Sharon E, Marder M, Swinney HL (2004) Leaves, flowers and garbage bags: making waves. Am Sci 92:254–261. doi:10.1511/2004.3.254

    Article  Google Scholar 

  • Sharon E, Roman B, Swinney HL (2007) Geometrically driven wrinkling observed in free plastic sheets and leaves. Phys Rev E 75:046211–1–046211–7. doi:10.1103/PhysRevE.75.046211

    Article  Google Scholar 

  • Squirrell J, Hollingsworth PM, Bateman RM, Dickson JH, Light MHS, MacConaill Tebbitt MC (2001) Partitioning and diversity of nuclear and organelle markers in native and introduced populations of Epipactis helleborine (Orchidaceae). Am J Bot 88:1409–1418

    Article  CAS  PubMed  Google Scholar 

  • Squirrell J, Hollingsworth PM, Bateman RM, Tebbitt MC, Hollingsworth ML (2002) Taxonomic complexity and breeding system transitions: conservation genetics of the Epipactis leptochila complex (Orchidaceae). Mol Ecol 11:1957–1964. doi:10.1046/j.1365-294X.2002.01610.x

    Article  CAS  PubMed  Google Scholar 

  • Stace C (2010) New flora of the British Isles, 3rd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Sundermann H (1975) Europäische und mediterrane Orchideen—Eine Bestimmungsflora mit Berücksichtigung der Ökologie, 2nd edn. Brücke-Verlag Kurt Schmersow, Hildesheim

    Google Scholar 

  • Szlachetko DL (2001) Flora Polski—storczyki. Multico, Warsaw

    Google Scholar 

  • Szlachetko DL, Rutkowski P (2000) Gynostemia Orchidalium I: apostasiaceae, Cypripediaceae, Orchidaceae (Thelymitroideae to Vanilloideae). Acta Bot Fennica 169:1–380

    Google Scholar 

  • Szlachetko DL, Skakuj M (1997) Storczyki Polski. Sorus, Poznań

    Google Scholar 

  • Tałałaj I, Brzosko E (2008) Selfing potential in Epipactis palustris, E. helleborine and E. atrorubens (Orchidaceae). Plant Syst Evol 276(1/2):21–29. doi:10.1007/s00606-008-0082-3

    Google Scholar 

  • Tranchida-Lombardo V, Cafasso D, Cristaudo A, Cozzolino S (2010) Phylogeographic patterns, genetic affinities and morphological differentiation between Epipactis helleborine and related lineages in a Mediterranean glacial refugium. Ann Bot 107:427–436. doi:10.1093/aob/mcq256

    Article  PubMed Central  PubMed  Google Scholar 

  • Wyrzykowska J, Pien S, Shen WH, Fleming AJ (2002) Manipulation of leaf shape by modulation of cell division. Development 129:957–964

    CAS  PubMed  Google Scholar 

  • Zagórska-Marek B, Turzańska M (2000) Clonal analysis provides evidence for transient initial cells in shoot apical meristems of seed plants. J Plant Growth Regul 19:55–64. doi:10.1007/s003440000007

    Article  PubMed  Google Scholar 

  • Zagórska-Marek B, Wiss D (2003) Dislocations in the repetitive unit patterns of biological systems. In: Nation J, Trofimova I, Rand JD, Sulis W (eds) Formal descriptions of developing systems (Nato Science Series II). Kluwer Academic Publishers, Dordrecht

    Google Scholar 

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Acknowledgments

We wish to thank Prof. Dariusz L. Szlachetko (University of Gdańsk, Poland) for material confirmation and advice in the description of Fig. 3; Dr. Mindaugas Lapelė (Dzūkija National Park, Lithuania) and RNDr. Vítězslav Plášek, Ph.D. (University of Ostrava, the Czech Republik) for help in material collection; our colleagues from the Department of Developmental Plant Biology (Institute of Experimental Biology, University of Wrocław, Poland) for their discussions and Mr. Ian Anderson for language correction. We would like to thank the anonymous reviewers for valuable comments on the manuscript.

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Correspondence to Anna Jakubska-Busse.

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Jakubska-Busse, A., Gola, E.M. Validation of leaf undulation traits in the taxonomy of Epipactis muelleri Godfery, 1921 (Orchidaceae, Neottieae). Plant Syst Evol 300, 1707–1717 (2014). https://doi.org/10.1007/s00606-014-0996-x

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