Protoplasma

, Volume 254, Issue 5, pp 1909–1922 | Cite as

Cytological analysis of ginseng carpel development

Original Article

Abstract

Panax ginseng Meyer, commonly known as ginseng, is considered one of the most important herbs with pharmaceutical values due to the presence of ginsenosides and is cultivated for its highly valued root for medicinal purposes. Recently, it has been recognized that ginseng fruit contains high contents of triterpene such as ginsenoside Re as pharmaceutical compounds. However, it is unclear how carpel, the female reproductive tissue of flowers, is formed during the three-year-old growth before fruit is formed in ginseng plants. Here, we report P. ginseng carpel development at the cytological level, starting from the initial stage of ovule development to seed development. The carpel of P. ginseng is composed of two free stigmas, two free styles, and one epigynous bilocular ovary containing one ovule in each locule. Based on our cytological study, we propose that the female reproductive development in P. ginseng can be classified into seven stages: early phase of ovule development, megasporogenesis, megagametogenesis, pre-fertilization, fertilization, post-fertilization, and seed development. We also describe the correlation of the female and male gametophyte development and compare morphological differences in carpel development between ginseng and other higher plants. One unique feature for ginseng seed development is that it takes 40 days for the embryo to develop to the early torpedo stage and that the embryo is small relative to the seed size, which could be a feature of taxonomic importance. This study will provide an integral tool for the study of the reproductive development and breeding of P. ginseng.

Keywords

Panax ginseng Ontogeny Ovule Ultrastructure Stages of carpel development 

References

  1. Angenent GC, Colombo L (1996) Molecular control of ovule development. Trends Plant Sci 1(7):228–232CrossRefGoogle Scholar
  2. Bai F, Settles AM (2015) Imprinting in plants as a mechanism to generate seed phenotypic diversity. Front Plant Sci 5(780). doi:10.3389/fpls.2014.00780
  3. Baranov A (1966) Recent advances in our knowledge of the morphology, cultivation and uses of ginseng (Panax ginseng C. A. Meyer). Econ Bot 20(4):403–406CrossRefGoogle Scholar
  4. Baskin CC, Baskin JM (1998) Seeds: ecology, biogeography, and evolution of dormancy and germination. Academic Press, San DiegoGoogle Scholar
  5. Beeckman T, Viane R (2000) Embedding thin plant specimens for oriented sectioning. Biotech Histochem 75(1):23–26CrossRefPubMedGoogle Scholar
  6. Berg RY (2003) Development of ovule, embryo sac, and endosperm in Triteleia (Themidaceae) relative to taxonomy. Am J Bot 90(6):937–948CrossRefPubMedGoogle Scholar
  7. Castaño F, Stauffer F, Marquinez X, Crèvevoeur M, Collin M, Pintaud JC, Tregear J (2014) Floral structure and development in the monoecious palm Gaussia attenuata (Arecaeae; Arecoideae). Ann Bot 114(7):1483–1495CrossRefPubMedPubMedCentralGoogle Scholar
  8. Coombe BG (1976) The development of fleshy fruits. Ann Rev Plant Physiol 27(1976):507–528Google Scholar
  9. Costello A, Motley TJ (2004) The development of the superior ovary in Tetraplasandra (Araliaceae). Am J Bot 91(5):644–655CrossRefPubMedGoogle Scholar
  10. de Oliveira RR, Cesarino I, Mazzafera P, Dornelas MC (2014) Flower development in Coffea arabica L.: new insights into MADS-box genes. Plant Reprod 27(2):79–94CrossRefPubMedGoogle Scholar
  11. Douglas GE (1957) The inferior ovary, II. Bot Rev 23:1–41CrossRefGoogle Scholar
  12. Dresselhaus T, Sprunck S, Wessel M (2016) Fertilization mechanisms in flowering plants. Curr Biol 26(3):125–139CrossRefGoogle Scholar
  13. Endress PK (2011) Angiosperm ovules: diversity, development, evolution. Ann Bot 107(9):1465–1489CrossRefPubMedPubMedCentralGoogle Scholar
  14. Figueiredo RC, Masullo FA, Cardoso Vieira R, De Toni KLG (2013) Development of carpels and ovules in Psychotria carthagenensis (Psychotrieae) and Rudgea macrophylla (Palicoureeae) (Rubioideae, Rubiaceae). South African J Bot 84:110–114CrossRefGoogle Scholar
  15. Forbis TA, Floyd SK, De Queiroz A (2002) The evolution of embryo size in angiosperms and other seed plants: implications for the evolution of seed dormancy. Evolution 56(11):2112–2125CrossRefPubMedGoogle Scholar
  16. Igersheim A, Cichocki O (1996) A simple method for microtome sectioning of prehistoric charcoal specimens, embedded in 2- hydroxyethyl methacrylate (HEMA). Rev Palaeobot Palynol 92:389–393CrossRefGoogle Scholar
  17. Johri BM, Ambegaokar KB, Srivastava PS (1992) Comparative embryology of angiosperms, vol 1/2. Springer-Verlag, Berlin Heidelberg, BerlinCrossRefGoogle Scholar
  18. Kaplan DR (1967) Floral morphology, organogenesis and interpretation of the inferior ovary in Downingia bacigalupii. Am J Bot 54(10):1274–1290CrossRefGoogle Scholar
  19. Kawashima T, Golberg RB (2010) The suspensor: not just suspending the embryo. Trends Plant Sci 15(1):23–30CrossRefPubMedGoogle Scholar
  20. Kelley DR, Gasser CS (2009) Ovule development: genetic trends and evolutionary considerations. Sex Plant Reprod 2(4):229–234CrossRefGoogle Scholar
  21. Kiesselbach TA (1949) The structure and reproduction of corn. Research bulletin 161 Lincoln: Agricultural Experiment Station, University of Nebraska College of Agriculture, NebraskaGoogle Scholar
  22. Kim YJ, Zhang D, Yang DC (2015a) Biosynthesis and biotechnological production of ginsenosides. Biotechnol Adv 33(6):717–735CrossRefPubMedGoogle Scholar
  23. Kim YJ, Jang MG, Zhu L, Silva J, Zhu X, Sukweenadhi J, Kwon WS, Yang DC, Zhang D (2015b) Cytological characterization of anther development in Panax ginseng Meyer. Protoplasma. doi:10.1007/s00709-015-0869-3 Google Scholar
  24. Kim YJ, Silva J, Zhang D, Shi J, Joo SC, Jang MG, Kwon WS, Yang DC (2016) Development of interspecies hybrids to increase ginseng biomass and ginsenoside yield. Plant Cell Rep 35(4):779–790CrossRefPubMedGoogle Scholar
  25. Koizumi A, Yamanaka K, Kawano S (2009) Carpel development in a floral mutant of dioecious Silene latifolia producing asexual and female-like flowers. J Plant Physiol 166(16):1832–1838CrossRefPubMedGoogle Scholar
  26. Kubo T, Fujita M, Takahashi H, Nakazono M, Tsutsumi N, Kurata N (2013) Transcriptome analysis of developing ovules in rice isolated by laser microdissection. Plant Cell Physiol 54(5):750–765CrossRefPubMedGoogle Scholar
  27. Le BH, Cheng C, Bui AQ, Wagmaister JA, Henry KF, Pelletier J, Kwong L, Belmonte M, Kirkbride R, Horvath S, Drews GN, Fischer RL, Okamuro JK, Harada JJ, Goldberg RB (2010) Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proc Natl Acad Sci U S A 107(18):8063–8070CrossRefPubMedPubMedCentralGoogle Scholar
  28. Li TSC (1995) Asian and American ginseng–a review. Hortechnol 5(1):27–34Google Scholar
  29. Litt A, Stevenson DW (2003) Floral development and morphology of Vochysiaceae. I. The structure of the gynoecium. Am J Bot 90(11):1533–1547CrossRefPubMedGoogle Scholar
  30. Musiał K, Płachno BJ, Świątek P, Marciniuk J (2013) Anatomy of ovary and ovule in dandelions (Taraxacum, Asteraceae). Protoplasma 250(3):715–722CrossRefPubMedGoogle Scholar
  31. Oskolski AA, Sokoloff DD, Van Wyk BE (2010) False paracarpy in Seemannaralia (Araliaceae): from bilocular ovary to unilocular fruit. Ann Bot 106(1):29–36CrossRefPubMedPubMedCentralGoogle Scholar
  32. Qi J, Sun P, Liao D, Sun T, Zhu J, Li X (2015) Transcriptomic analysis of American ginseng seeds during the dormancy release process by RNA-Seq. PLoS One 10(3). doi:10.1371/journal.pone.0118558
  33. Reiser L, Fischer RL (1993) The ovule and the embryo sac. Plant Cell 5(10):1291–1301CrossRefPubMedPubMedCentralGoogle Scholar
  34. Robert HS, Crhak Khaitova L, Mroue S, Benková E (2015) The importance of localized auxin production for morphogenesis of reproductive organs and embryos in Arabidopsis. J Exp Bot 66(16):5029–5042Google Scholar
  35. Rodondi G, Beretta M, Andreis C (2009) Ovule and pollen development in the natural hybrid Drosera x obovata Mert. & Koch (Droseraceae) and its parents. Flora 204(9):685–691CrossRefGoogle Scholar
  36. Rodríguez-Riaño T, Valtueña FJ, Ortega-Olivencia A (2006) Megasporogenesis, megagametogenesis and ontogeny of the aril in Cytisus striatus and C. multiflorus (Leguminosae: Papilionoideae). Ann Bot 98(4):777–791CrossRefPubMedPubMedCentralGoogle Scholar
  37. Rudall PJ, Remizowa MV, Beer AS, Bradshaw E, Stevenson DW, Macfarlane TD, Tuckett RE, Yadav SR, Sokoloff DD (2008) Comparative ovule and megagametophyte development in Hydatellaceae and water lilies reveal a mosaic of features among the earliest angiosperms. Ann Bot 101(7):941–956CrossRefPubMedPubMedCentralGoogle Scholar
  38. Sachs J, Bennett AW (2011) A text-book of botany: morphological and physiological. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  39. Schluter C, Punja ZK (2000) Floral biology and seed production in cultivated North American ginseng (Panax quinquefolius). J Amer Hort Sci 125(5):567–575Google Scholar
  40. Schneitz K (1999) The molecular and genetic control of ovule development. Curr Opin Plant Biol 2(1):13–17CrossRefPubMedGoogle Scholar
  41. Schneitz K, Huiskamp M, Pruitt RE (1995) Wild-type ovule development in Arabidopsis thaliana: a light microscope study of cleared whole-mount tissue. Plant J 7(5):731–749CrossRefGoogle Scholar
  42. Singh G (2010) Plant systematics an integrated approach. CRC Press, DelhiCrossRefGoogle Scholar
  43. Sokoloff DD, Oskolski AA, Remizowa MV, Nuraliev MS (2007) Flower structure and development in Tupidanthus calyptratus (Araliaceae): an extreme case of polymery among asterids. Pl Syst Evol 268(1):209–234CrossRefGoogle Scholar
  44. Venugopal N, Ahuja P, Lalchhanhimi (2013) A unique type of endosperm in Panax wangianus S. C. Sun. J Plant Develop 20(2013):45–50Google Scholar
  45. Vivian-Smith A, Luo M, Chaudhury A, Koltunow A (2001) Fruit development is actively restricted in the absence of fertilization in Arabidopsis. Development 128(12):2321–2331Google Scholar
  46. Wang ZF, Ren Y (2008) Ovule morphogenesis in Ranunculaceae and its systematic significance. Ann Bot 101(3):447–462CrossRefPubMedGoogle Scholar
  47. Wilson CA (2001) Floral stages, ovule development, and ovule and fruit success in Iris tenax, focusin on var. Gormanii, a taxon with low seed set. Am J Bot 88(12):2221–2231CrossRefPubMedGoogle Scholar
  48. Woodenberg WR, Berjak P, Pammenter NW, Farrant JM (2014) Development of cycad ovules and seeds. 2. Histological and ultrastructural aspects of ontogeny of the embryo in Encephalartos natalensis. Protoplasma 251(4):797–816CrossRefPubMedGoogle Scholar
  49. Wu X, Liu J, Li D, Liu CM (2016a) Rice caryopsis development I: Dynamic changes in different cell layers. J Integr Plant Biol 58(9):772–785Google Scholar
  50. Wu X, Liu J, Li D, Liu CM (2016b) Rice caryopsis development II: Dynamic changes in the endosperm. J Integr Plant Biol 58(9):786–798Google Scholar
  51. Yu SC, Kim WK (1992) Structural changes and histochemical study of endosperm on Panax ginseng C. A. Meyer during embryo development. Korean J Ginseng Sci 16(1):37–43Google Scholar
  52. Zhang Y, Liang W, Shi J, Xu J, Zhang D (2013) MYB56 encoding a R2R3 MYB transcription factor regulates seed size in Arabidopsis thaliana. J Integr Plant Biol 55(11):1166–1178CrossRefPubMedGoogle Scholar
  53. Zhang J, Tang W, Huang Y, Niu X, Zhao Y, Han Y, Liu Y (2015) Down-regulation of a LBD-like gene, OsIG1, leads to occurrence of unusual double ovules and developmental abnormalities of various floral organs and megagametophyte in rice. J Exp Bot 66(1):99–112CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Wien 2017

Authors and Affiliations

  1. 1.Department of Oriental Medicine Biotechnology and Graduate School of Biotechnology, College of Life ScienceKyung Hee UniversityYonginSouth Korea
  2. 2.Joint International Research Laboratory of Metabolic and Developmental Sciences, Shanghai Jiao Tong University–University of Adelaide Joint Centre for Agriculture and Health, School of Life Sciences and BiotechnologyShanghai Jiao Tong UniversityShanghaiChina
  3. 3.Department of Energy Plant Research LaboratoryMichigan State UniversityEast LansingUSA

Personalised recommendations