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Plant Systematics and Evolution

, Volume 304, Issue 4, pp 461–471 | Cite as

Floral development in Thermopsis turcica, an unusual multicarpellate papilionoid legume

  • Andrey A. Sinjushin
  • Dilek Tekdal
  • Cem Ciftci
  • Selim Cetiner
Original Article
  • 186 Downloads

Abstract

The vast majority of the species of family Leguminosae have an apocarpous monomerous gynoecium. However, only a few taxa regularly produce multicarpellate gynoecia. The only known species of papilionoid legumes which has both a typical “flag blossom” and more than one carpel is Thermopsis turcica (tribe Thermopsideae). We studied the floral ontogeny of T. turcica with special reference to its gynoecium initiation and development. Flowers arise in simple terminal racemes in a helical order and are subtended by bracts. Bracteoles are initiated but then suppressed. Sepals appear more or less simultaneously. Then, petals emerge and remain retarded in development until later stages. The gynoecium usually includes three carpels with an abaxial one initiating first and two adaxial carpels arising later and developing somewhat asynchronously. The abaxial carpel appears concomitant with the outer stamens and is always oriented with its cleft toward the adaxial side, while the adaxial carpels face each other with their clefts and have them slightly turned to the adaxial side. Rarely uni-, bi- or tetracarpellate flowers arise. Seed productivity of T. turcica is on approximately the same level as in unicarpellate species of Thermopsis hence supporting the fact that the multicarpellate habit is adaptive or at least not harmful in this species.

Keywords

Evolution Flag blossom Flower Monosymmetry Polymerous gynoecium 

Notes

Acknowledgements

The authors express their gratitude to Dr. Olga A. Volkova and Dr. Elena E. Severova for helpful comments on description of pollen morphology, to Margarita M. Markova for assistance with statistical procedures, to Dr. Louis Ronse de Craene and to two anonymous reviewers for helpful criticism on a manuscript. The assistance of Burçin Çıngay for Thermopsis collection (Garden Department of Nezahat Gökyiğit Botanic Garden) and Cleva Ow-Yang and Dilek Çakıroğlu at the SEM facility (Nanotechnology Research and Application Centre, Sabanci University) is greatly appreciated. Some details of SEM preparation protocol were discussed with Anatolii G. Bogdanov (Interdepartmental Laboratory of Electron Microscopy, Moscow State University) to whom authors are also thankful. The authors would like to thank Nezahat Gökyiğit Botanical Garden for providing research material and their support. The work was partially supported by the Russian Foundation for Basic Research (Project No. 15-04-6374) and by the Ali Nihat Gökyiğit Foundation of Turkey.

Compliance with ethical standards

Conflict of interest

The authors declare they have no potential conflict of interest.

References

  1. Bachelier JB, Endress PK (2007) Development of inflorescences, cupules, and flowers in Amphipterygium and comparison with Pistacia (Anacardiaceae). Int J Pl Sci 168:1237–1253.  https://doi.org/10.1086/521795 CrossRefGoogle Scholar
  2. Bali EB, Açık L, Akca G, Sarper M, Elçi MP, Avcu F, Vural M (2014) Antimicrobial activity against periodontopathogenic bacteria, antioxidant and cytotoxic effects of various extracts from endemic Thermopsis turcica. Asian Pacific J Trop Biomed 4:505–514.  https://doi.org/10.12980/APJTB.4.2014APJTB-2013-0010 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Brewbaker JL (2013) ‘KX4-Hawaii’, seedless interspecific hybrid Leucaena. HortScience 48:390–391Google Scholar
  4. Buzgo M, Endress PK (2000) Floral structure and development of Acoraceae and its systematic relationships with basal angiosperms. Int J Pl Sci 161:23–41.  https://doi.org/10.1086/314241 CrossRefPubMedGoogle Scholar
  5. Cenkci S, Kargioglu M, Dayan S, Konuk M (2007) Endangered status and propagation of an endemic plant species, Thermopsis turcica (Fabaceae). Asian J Pl Sci 6:288–293CrossRefGoogle Scholar
  6. Cenkci S, Kargıoğlu M, Dedeoğlu A, Kahraman B, Karakurt Y (2016) Isolation and expression analysis of three different flowering genes (TtLFY, TtAP1, and TtAP2) from an unusual legume species, Thermopsis turcica. Turk J Bot 40:447–460.  https://doi.org/10.3906/bot-1509-15 CrossRefGoogle Scholar
  7. Chen CJ, Mendenhall MG, Turner BL (1994) Taxonomy of Thermopsis (Fabaceae) in North America. Ann Missouri Bot Gard 81:714–742.  https://doi.org/10.2307/2399917 CrossRefGoogle Scholar
  8. Cowan RS (1981) Swartzieae. In: Polhill RM, Raven PH (eds) Advances in legume systematics: part 1. Royal Botanic Gardens, Kew, pp 209–212Google Scholar
  9. Davis PH, Mill RR, Kit T (1988) Flora of Turkey and the East Aegean Islands, vol. 10. Edinburgh University Press, EdinburgGoogle Scholar
  10. Douglas AW, Tucker SC (1996) The developmental basis of diverse carpel orientation in Greviolleoideae (Proteaceae). Int J Pl Sci 157:373–397.  https://doi.org/10.1086/297355 CrossRefGoogle Scholar
  11. Ekim T, Koyuncu M, Vural M, Duman H, Aytaç Z, Adıgüzel N (2000) Red data book of Turkish plants. Bariscan Ofset, AnkaraGoogle Scholar
  12. Gonzales AM (2016) Floral structure, development of the gynoecium, and embryology in Schinopsis balansae Engler (Anacardiaceae) with particular reference to aporogamy. Int J Pl Sci 177:326–338.  https://doi.org/10.1086/684847 CrossRefGoogle Scholar
  13. Kocyan A, Endress PK (2001) Floral structure and development of Apostasia and Neuwiedia (Apostasioideae) and their relation to other Orchidaceae. Int J Pl Sci 162:847–867.  https://doi.org/10.1086/320781 CrossRefGoogle Scholar
  14. Korcan SE, Cigerci IE, Dilek M, Kargioglu M, Cenkci S, Konuk M (2009) Antimicrobial activity of an endemic species “Thermopsis turcica” Turkey. Kuwait J Sci Engin 36:101–112Google Scholar
  15. Leebens-Mack J, Milligan BG (1998) Pollination biology in hybridizing Baptisia (Fabaceae) populations. Am J Bot 85:500–507CrossRefPubMedGoogle Scholar
  16. Legume Phylogeny Working Group (LPWG) (2017) A new subfamily classification of the Leguminosae based on a taxonomically comprehensive phylogeny. Taxon 66:44–77.  https://doi.org/10.12705/661.3 CrossRefGoogle Scholar
  17. Novikoff AV, Jabbour F (2014) Floral anatomy of Delphinieae (Ranunculaceae): comparing flower organization and vascular patterns. Modern Phytomorphol 5:35–44.  https://doi.org/10.5281/zenodo.161001 Google Scholar
  18. Özdemir C, Dural H, Ertuǧrul K, Küçüködük M, Baran P, Şanda MA (2008) Morphology and anatomy of endemic Thermopsis turcica Kit Tan, Vural & Küçüködük. Bangladesh J Bot 37:105–114.  https://doi.org/10.3329/bjb.v37i2.1714 Google Scholar
  19. Paulino JV, Prenner G, Mansano VF, Teixeira SP (2014) Comparative development of rare cases of a polycarpellate gynoecium in an otherwise monocarpellate family, Leguminosae. Amer J Bot 101:572–586.  https://doi.org/10.3732/ajb.1300355 CrossRefPubMedGoogle Scholar
  20. Penin AA, Logacheva MD (2011) Correlation between number and position of floral organs in Arabidopsis. Ann Bot (Oxford) 108:123–131.  https://doi.org/10.1093/aob/mcr115 CrossRefGoogle Scholar
  21. Prenner G (2004a) New aspects in floral development of Papilionoideae: initiated but suppressed bracteoles and variable initiation of sepals. Ann Bot (Oxford) 93:537–545.  https://doi.org/10.1093/aob/mch076 CrossRefGoogle Scholar
  22. Prenner G (2004b) The asymmetric androecium in Papilionoideae (Leguminosae): definition, occurrence, and possible systematic value. Int J Pl Sci 165:499–510.  https://doi.org/10.1086/386377 CrossRefGoogle Scholar
  23. Prenner G (2011) Floral ontogeny of Acacia celastrifolia: an enigmatic mimosoid legume with pronounced polyandry and multiple carpels. In: Wanntorp L, Craene LP (eds) Flowers on the tree of life. Cambridge University Press, Cambridge, pp 256–278CrossRefGoogle Scholar
  24. Punt W, Hoen PP, Blackmore S, Nilsson S, Le Thomas A (2007) Glossary of pollen and spores terminology. Rev Palaeobot Palynol 143:1–81.  https://doi.org/10.1016/j.revpalbo.2006.06.008 CrossRefGoogle Scholar
  25. Sinjushin AA (2014) Origin and variation of polymerous gynoecia in Fabaceae: evidence from floral mutants of pea (Pisum sativum L.). Pl Syst Evol 300:717–727.  https://doi.org/10.1007/s00606-013-0915-6 CrossRefGoogle Scholar
  26. Sinjushin AA (2015) Is the leguminous flower closed? Wulfenia 22:281–287Google Scholar
  27. Sinjushin AA (2016) Effects of stem fasciation on inflorescence and flower morphology in legumes. Wulfenia 23:127–134Google Scholar
  28. Stergios BD, Aymard GAC (2008) A striking new species of Aldina (Fabaceae-Swartzieae-Aldiniinae) from the Venezuelan Guayana highlands. Harv Pap Bot 13:29–33. https://doi.org/10.3100/1043-4534(2008)13[29:ASNSOA]2.0.CO;2CrossRefGoogle Scholar
  29. Stirton CH (1981) Petal sculpturing in papilionoid legumes. In: Polhill RM, Raven PH (eds) Advances in legume systematics. Royal Botanic Gardens, Kew, pp 209–212Google Scholar
  30. Strange A, Rudall PJ, Prychid CJ (2004) Comparative floral anatomy of Pontederiaceae. Bot J Linn Soc 144:395–408.  https://doi.org/10.1111/j.1095-8339.2003.00262.x CrossRefGoogle Scholar
  31. Tan K, Vural M, Küçüködük M (1983) An unusual new Thermopsis from Turkey. Notes Roy Bot Gard Edinburgh 40:515–518Google Scholar
  32. Tekdal D, Cetiner S (2014) In vitro plant regeneration derived from leaf and stem explants of endemic Thermopsis turcica. Biologia (Bratislava) 69:863–869.  https://doi.org/10.2478/s11756-014-0383-7 CrossRefGoogle Scholar
  33. Tekdal D, Cetiner S (2017) Investigation of intergeneric crossability of Vicia faba L. and Thermopsis turcica Kit Tan, Vural & Küçüködük. Genet Resources Crop Evol 64:1605–1611.  https://doi.org/10.1007/s10722-016-0459-z CrossRefGoogle Scholar
  34. Tekdal D, Çetiner S (2014) The determination of self-compatibility status of Thermopsis turcica through histological analysis. J Appl Biol Sci 8:64–67Google Scholar
  35. Uysal T, Ertuğrul K, Bozkurt M (2014) A new genus segregated from Thermopsis (Fabaceae: Papilionoideae): Vuralia. Pl Syst Evol 300:1627–1637.  https://doi.org/10.1007/s00606-014-0988-x CrossRefGoogle Scholar
  36. Vural M (2009) Piyan (Thermopsis turcica). Bağbahçe 25:14–16Google Scholar
  37. Wang HC, Sun H, Compton JA, Yang JB (2006) A phylogeny of Thermopsideae (Leguminosae: Papilionoideae) inferred from nuclear ribosomal internal transcribed spacer (ITS) sequences. Bot J Linn Soc 151:365–373.  https://doi.org/10.1111/j.1095-8339.2006.00512.x CrossRefGoogle Scholar
  38. Yakovlev GP (1972) Contributions to a system of order Fabales. Bot Zhurn (St Petersburg) 57:585–592 (in Russian)Google Scholar
  39. Yang JW, Xu HL, Sun JR, Hu HY (2010) Nectar-robbing behavior of Megachile (Xanthosaurus) japonica Alfken (Hymenoptera: Megachilidae) on its nectar plant Thermopsis lupinoides (Leguminosae). Acta Entomol Sin 53:1015–1021Google Scholar
  40. Yıldız M, Pehlivan E, Terzi H (2017) Proteomic analysis of flowers at two developmental stages in Thermopsis turcica (Fabaceae). Turk J Bot 41:234–243.  https://doi.org/10.3906/bot-1608-10 CrossRefGoogle Scholar
  41. Zhang ML, Huang JF, Sanderson SC, Yan P, Wu YH, Pan BR (2015) Molecular biogeography of tribe Thermopsideae (Leguminosae): a Madreyan-Tethyan disjunction pattern with an African origin of core genistoides. BioMed Res Int 2015:864804.  https://doi.org/10.1155/2015/864804 Google Scholar
  42. Zimmerman M (1982) Effect of nectar production on neighborhood size. Oecologia 52:104–108.  https://doi.org/10.1007/BF00349017 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  • Andrey A. Sinjushin
    • 1
  • Dilek Tekdal
    • 2
  • Cem Ciftci
    • 2
  • Selim Cetiner
    • 2
  1. 1.Department of Genetics, Biological FacultyM.V. Lomonosov Moscow State UniversityMoscowRussia
  2. 2.Faculty of Engineering and Natural SciencesSabancı UniversityOrhanlı, TuzlaTurkey

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