Journal of Plant Research

, Volume 129, Issue 5, pp 883–897 | Cite as

Embryology of Cardiopteris (Cardiopteridaceae, Aquifoliales), with emphasis on unusual ovule and seed development

Regular Paper

Abstract

Cardiopteris (Cardiopteridaceae), a twining herb of two or three species distributed from Southeast Asia to Northern Australia, requires an embryological study for better understanding of its reproductive features. The present study of C. quinqueloba showed that the ovule and seed development involves a number of unusual structures, most of which are unknown elsewhere in angiosperms. The ovule pendant from the apical placenta is straight (not orthotropous), ategmic, and tenuinucellate, developing a monosporic seven-celled/eight-nucleate female gametophyte with an egg apparatus on the funicular side. Fertilization occurs by a pollen tube entering from the funicular side, resulting in a zygote on the funicular side. The endosperm is formed by the cell on the funicular side in the two endosperm cell stage. While retaining a (pro)embryo/endosperm as it is, the raphe (differentiating late in pre-fertilization stages) elongates toward the antiraphal side during post-fertilization stages, resulting in an anatropous seed. The two-cell-layered nucellar epidermis (belatedly forming by periclinal divisions), along with the raphe, envelops the embryo/endosperm entirely as the seed coat. The possibility was discussed that the arrested integument development triggers a series of the subsequent unusual structures of ovule and seed development. The fertilization mode in Cardiopteris underpins the hypothesis that the Polygonum‒type female gametophyte comprises two four-celled archegonia.

Keywords

Aquifoliales Cardiopteris Cardiopteridaceae Embryology Female gametophyte Seed development 

Supplementary material

10265_2016_845_MOESM1_ESM.xlsx (15 kb)
Supplementary material 1 (XLSX 15 kb)

References

  1. Angiosperm Phylogeny Group (2003) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Bot J Linn Soc 141:399–436CrossRefGoogle Scholar
  2. Angiosperm Phylogeny Group (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APGIII. Bot J Linn Soc 161:105–121CrossRefGoogle Scholar
  3. Ao C, Tobe H (2015) Floral morphology and embryology of Helwingia (Helwingiaceae, Aquifoliales): systematic and evolutionary implications. J Plant Res 128:161–175CrossRefPubMedGoogle Scholar
  4. Bentham G, Hooker JD (1862‒1867) Genera plantarum, vol 9. Reeve Co., LondonGoogle Scholar
  5. Blume CL (1847) De genere Cardiopteri. Rumphia 3:205–207Google Scholar
  6. Bouman F (1984) The ovule. In: Johri BM (ed) Embryology of angiosperms. Springer, Berlin, pp 123–157CrossRefGoogle Scholar
  7. Brewbaker JL (1967) The distribution and phylogenetic significance of binucleate and trinucleate pollen grains in angiosperms. Am J Bot 54:1069–1083CrossRefGoogle Scholar
  8. Chamberlain CJ (1935) Gymnosperms: structure and evolution. The University of Chicago Press, ChicagoGoogle Scholar
  9. Copeland HF (1963) Structural notes on hollies (Ilex aquifolium and I. cornuta, family Aquifoliaceae). Phytomorphology 13:455–464Google Scholar
  10. Corner EJH (1976) The seeds of dicotyledons, vols 1, 2. Cambridge University Press, CambridgeGoogle Scholar
  11. Cronquist S (1981) An integrated system of classification of flowering plants. Columbia University Press, New YorkGoogle Scholar
  12. Davis GL (1966) Systematic embryology of flowering plants. Wiley, New YorkGoogle Scholar
  13. Doweld AB (2000) Cardiopteridaceae. In: Takhtajan A (ed) Comparative seed anatomy, vol 6. Nauka, St. Petersburg, pp 120–121 (in Russian) Google Scholar
  14. Engler A (1897) Icacinaceae. In: Engler A, Prantl K (eds) Die natürlichen Pflanzenfamilien, Teil 3(5). Wilhelm Engelmann, Leipzig, pp 233–257Google Scholar
  15. Fagerlind F (1945) Bau des Gynöceums, der Samenanlage und des Embryosackes bei einigen Repräsentanten der Familie Icacinaceae. Svensk Bot Tidskr 39:346–364Google Scholar
  16. Friedman WE, Williams JH (2003) Modularity of the angiosperm female gametophyte and its bearing on the early revolution of endosperm in flowering plants. Evolution 57:216–230CrossRefPubMedGoogle Scholar
  17. Herr JM Jr (1959) The development of the ovule and the megagametophyte in the genus Ilex. J Elisha Mitchell Sci Soc 75:107–128Google Scholar
  18. Herr JM Jr (1961) Endosperm development and associated ovule modifications in the genus Ilex. J Elisha Mitchell Sci Soc 77:26–32Google Scholar
  19. Hutchinson J (1973) The Families of flowering plants, 3rd edn. Oxford University Press, OxfordGoogle Scholar
  20. Jackson BD (1928) A glossary of botanic terms, 4th edn. Duckworth, LondonGoogle Scholar
  21. Kårehed J (2001) Multiple origin of the tropical forest tree family Icacinaceae. Am J Bot 88:2259–2274CrossRefPubMedGoogle Scholar
  22. Kong D-R, Peng H, Liang H-X (2002) A new type of embryo sac in Cardiopteris and its systematic implications. Acta Bot Sin 44:496–498Google Scholar
  23. Kong DR, Schori M, Lu SG, Li L, Peng H (2014) Floral development of Cardiopteris, with emphasis on gynoecial structure and ovular morphology. J Syst Evol 52:629–642CrossRefGoogle Scholar
  24. Mabberley DJ (2008) Mabberley’s plant book. A portable dictionary of plants, their classification and uses. Cambridge University Press, New YorkGoogle Scholar
  25. Mauritzon J (1936) Embryologische Angaben über Stackhousiaceae, Hippocrateaceae und Icacinaceae. Svensk Bot Tidskr 30:541–550Google Scholar
  26. Ohnishi T, Takanashi H, Mogi M, Takahashi H, Kikuchi S, Yano K, Okamoto T, Fujita M, Kurata N, Tsutsumi N (2011) Distinct gene expression profiles in egg and synergid cells of rice as revealed by cell type-specific microarrays. Plant Physiol 155:881–891CrossRefPubMedGoogle Scholar
  27. Padmanabhan D (1961) A contribution to the embryology of Gomphandra polymorpha. Proc Natl Inst Sci India B 27:389–398Google Scholar
  28. Porsch O (1907) Versuch einer phylogenetischen Erkärung des Embryosackes und der doppelten Befruchtung der Angiospermen. Gustav Fischer, JenaGoogle Scholar
  29. Reveal JL (2012) An outline of a classification scheme for extant flowering plants. Phytoneuron 37:1–221Google Scholar
  30. Scholz H (1964) Celastrales. In: Melchior H (ed) A Engler’s Syllabus der Pflanzenfamilien. II. Gebrüder Borntraeger, Berlin, pp 289–300Google Scholar
  31. Schori M, Furness CA (2014) Pollen diversity in Aquifoliales. Bot J Linn Soc 175:169–190CrossRefGoogle Scholar
  32. Schürhoff PN (1921) Die Entwicklungsgeschichte von Ilex aquifolium. Ber Dtsch Bot Ges 39:377–379Google Scholar
  33. Sleumer H (1942) Peripterygiaceae. In: Engler A, Prantl K (eds) Die Natürlichen Pflanzenfamilien, 20b. Duncker & Humblot, Berlin, pp 397–400Google Scholar
  34. Sleumer H (1971) Cardiopteridaceae. In: van Steenis CGGJ (ed) Flora Malesiana, vol 7. Noordhoff International Publishing, Leyden, pp 93–96Google Scholar
  35. Sogo A, Tobe H (2005) Intermittent pollen-tube growth in pistils of alders (Alnus). Proc Natl Acad Sci USA 102:8770–8775CrossRefPubMedPubMedCentralGoogle Scholar
  36. Sogo A, Noguchi J, Jaffré T, Tobe H (2004) Pollen-tube growth pattern and chalazogamy in Casuarina equisetifolia (Casuarinaceae). J Plant Res 117:37–46CrossRefPubMedGoogle Scholar
  37. Soltis DE, Smith SA, Cellinese N, Wurdack KJ, Tank DC, Brockington SF, Refulio-Rodriguez NF, Walker JB, Moore MJ, Carlsward BS, Bell CD, Matvis M, Crawley S, Black C, Diouf D, Xi Z, Rushworth CA, Gitzendanner MA, Sytsma KJ, Qiu Y-L, Hilu KW, Davis CC, Sanderson MJ, Beaman RS, Olmstead RG, Judd WS, Donoghue MJ, Soltis PS (2011) Angiosperm phylogeny: 17 genes, 640 taxa. Am J Bot 98:704–730CrossRefPubMedGoogle Scholar
  38. Stevens PF (2001 onwards) Angiosperm phylogeny Website. Version 12, July 2012. http://www.mobot.org/MOBOT/research/APweb/. Accessed 27 Feb 2015
  39. Takhtajan A (1997) Diversity and classification of flowering plants. Columbia University Press, New YorkGoogle Scholar
  40. Takhtajan A (2009) Flowering plants, 2nd edn. Springer, New YorkCrossRefGoogle Scholar
  41. Tank DC, Donoghue MJ (2010) Phylogeny and phylogenetic nomenclature of the Campanulidae based on an expanded sample of genes and taxa. Syst Bot 35:425–441CrossRefGoogle Scholar
  42. The Plant List (2013) Version 1.1. Published on the Internet; http://www.theplantlist.org/. Accessed 1st Jan
  43. Thorne RF (1992) Classification and geography of the flowering plants. Bot Rev (Lancaster) 58:225–348CrossRefGoogle Scholar
  44. Tobe H (2012) Floral morphology and structure of Cardiopteris (Cardiopteridaceae) with special reference emphasis on the gynoecium: systematic and evolutionary implications. J Plant Res 125:361–369CrossRefPubMedGoogle Scholar
  45. Tobe H (2015) Embryology of Phyllonoma (Phyllonomaceae, Aquifoliales): characteristics and character evolution. J Plant Res 128:633–642CrossRefPubMedGoogle Scholar
  46. Tobe H, Kimoto Y, Prakash N (2007) Development of the female gametophyte in Austrobaileya scandens (Austrobaileyaceae). J Plant Res 120:431–436CrossRefPubMedGoogle Scholar
  47. van Tieghem P (1898) Structure de quelques ovules et patti qu’on en pent tirer am liorer la classification. J Bot (Morot) 12:197–220Google Scholar
  48. Williams JH, Friedman WE (2004) The four-celled female gametophyte of Illicium (Illiciaceae; Austrobaileyales): implications for understanding the origin and early evolution of monocots, eumagnoliids, and eudicots. Am J Bot 91:332–351CrossRefPubMedGoogle Scholar

Copyright information

© The Botanical Society of Japan and Springer Japan 2016

Authors and Affiliations

  1. 1.Graduate School of ScienceKyoto UniversityKyotoJapan

Personalised recommendations