Cellular, Molecular, and Genetic Changes During the Development of Ceratopteris richardii Gametophytes



Ceratopteris richardii is an aquatic fern that has proven to be a ­productive model system for studies in the genetics, biochemistry, and cell ­biology of early gametophytic development. Here we review and discuss the recent literature that documents the cellular, molecular, and gene expression changes that occur in gametophytes during polarity development and sexual differentiation, and in response to the environmental stimuli of light and gravity. Different approaches to achieve genetic transformation in this fern will also be discussed.


Spore Germination Nuclear Migration Feminine Trait Polarity Fixation Aquatic Fern 


  1. Alongi, D.A., Hill, J.P., and Germino, M.J. 2009. Opportunistic heterotrophy in gametophytes of the homosporous fern Ceratopteris richardii. Botany-Botanique 87:799–806.CrossRefGoogle Scholar
  2. Banks, J.A. 1994. Sex-determining genes in the homosporous fern Ceratopteris. Development 120:1949–1958.PubMedGoogle Scholar
  3. Banks, J.A. 1999. Gametophyte development in ferns. Annual Review of Plant Physiology and Plant Molecular Biology 50:163-+.CrossRefPubMedGoogle Scholar
  4. Banks, J.A., Hickok, L., and Webb, M.A. 1993. The programming of sexual phenotype in the homosporous fern Ceratopteris richardii. International Journal of Plant Sciences 154:522–534.CrossRefGoogle Scholar
  5. Bushart, T.J. and Roux, S.J. 2007. Conserved features of germination and polarized cell growth: a few insights from a pollen-fern spore comparison. Annals of Botany 99:9–17.CrossRefPubMedGoogle Scholar
  6. Bushart, T.J., Clark, G.B., Porterfield, D.M., and Roux, S.J. 2010. Testing the role of Ca2+-ATPases in the gravity-directed, trans-cell current of calcium in single-celled spores of Ceratopteris richardii. Gravitational and Space Biology 23.Google Scholar
  7. Chasan, R. 1992. Ceratopteris: a model-plant for the 90s. Plant Cell 4:113–115.CrossRefPubMedGoogle Scholar
  8. Chatterjee, A. and Roux, S.J. 2000. Ceratopteris richardii: a productive model for revealing secrets of signaling and development. Journal of Plant Growth Regulation 19:284–289.CrossRefPubMedGoogle Scholar
  9. Chatterjee, A., Porterfield, D.M., Smith, P.S., and Roux, S.J. 2000. Gravity-directed calcium ­current in germinating spores of Ceratopteris richardii. Planta 210:607–610.CrossRefPubMedGoogle Scholar
  10. Cooke, T.J., Racusen, R.H., Hickok, L.G., and Warne, T.R. 1987. The photocontrol of spore ­germination in the fern Ceratopteris richardii. Plant and Cell Physiology 28:753–759.Google Scholar
  11. Cooke, T.J., Hickok, L.G., and Sugai, M. 1995. The fern Ceratopteris richardii as a lower plant-model system for studying the genetic-regulation of plant photomorphogenesis. International Journal of Plant Sciences 156:367–373.CrossRefGoogle Scholar
  12. Edwards, E.S. and Roux, S.J. 1998. Influence of gravity and light on the developmental polarity of Ceratopteris richardii fern spores. Planta 205:553–560.CrossRefPubMedGoogle Scholar
  13. Gregorich, M. and Fisher, R. 2006. Auxin regulates lateral meristem activation in developing gametophytes of Ceratopteris richardii. Canadian Journal of Botany-Revue Canadienne De Botanique 84:1520–1530.CrossRefGoogle Scholar
  14. Hickok, L.G., Warne, T.R., and Fribourg, R.S. 1995. The biology of the fern Ceratopteris and its use as a model system. International Journal of Plant Sciences 156:332–345.CrossRefGoogle Scholar
  15. Hodgins-Davis, A. and Townsend, J.P. 2009. Evolving gene expression: from G to E to G × E. Trends in Ecology & Evolution 24:649–658.CrossRefGoogle Scholar
  16. Imaizumi, T., Kanegae, T., and Wada, M. 2000. Cryptochrome nucleocytoplasmic distribution and gene expression are regulated by light quality in the fern Adiantum capillus-veneris. Plant Cell 12:81–95.CrossRefPubMedGoogle Scholar
  17. Kagawa, T., Kasahara, M., Abe, T., Yoshida, S., and Wada, M. 2004. Function analysis of phototropin2 using fern mutants deficient in blue light-induced chloroplast avoidance movement. Plant and Cell Physiology 45:416–426.CrossRefPubMedGoogle Scholar
  18. Kamachi, H., Matsunaga, E., Noguchi, M., and Inoue, H. 2004. Novel mutant phenotypes of a dark-germinating mutant dkg1 in the fern Ceratopteris richardii. Journal of Plant Research 117:163–170.CrossRefPubMedGoogle Scholar
  19. Kamachi, H., Iwasawa, O., Hickok, L.G., Nakayama, M., Noguchi, M., and Inoue, H. 2007. The effects of light on sex determination in gametophytes of the fern Ceratopteris richardii. Journal of Plant Research 120:629–634.CrossRefPubMedGoogle Scholar
  20. Kawai, H., Kanegae, T., Christensen, S., Kiyosue, T., Sato, Y., Imaizumi, T., Kadota, A., and Wada, M. 2003. Responses of ferns to red light are mediated by an unconventional photoreceptor. Nature 421:287–290.CrossRefPubMedGoogle Scholar
  21. Kawai-Toyooka, H., Kuramoto, C., Orui, K., Motoyama, K., Kikuchi, K., Kanegae, T., and Wada, M. 2004. DNA interference: a simple and efficient gene-silencing system for high-throughput functional analysis in the fern Adiantum. Plant and Cell Physiology 45:1648–1657.CrossRefPubMedGoogle Scholar
  22. Kiss, J.Z., Kumar, P., Millar, K.D.L., Edelmann, R.E., and Correll, M.J. 2009. Operations of a ­spaceflight experiment to investigate plant tropisms. Advances in Space Research 44:879–886.CrossRefGoogle Scholar
  23. Kodama, Y., Tsuboi, H., Kagawa, T., and Wada, M. 2008. Low temperature-induced chloroplast relocation mediated by a blue light receptor, phototropin 2, in fern gametophytes. Journal of Plant Research 121:441–448.CrossRefPubMedGoogle Scholar
  24. Long, L.K., Ou, X.F., Liu, J.C., Lin, X.Y., Sheng, L.X., and Liu, B. 2009. The spaceflight environment can induce transpositional activation of multiple endogenous transposable elements in a genotype-dependent manner in rice. Journal of Plant Physiology 166: 2035–2045.CrossRefPubMedGoogle Scholar
  25. Matia, I., Gonzalez-Camacho, F., Herranz, R., Kiss, J.Z., Gasset, G., van Loon, J., Marco, R., and Medina, F.J. 2010. Plant cell proliferation and growth are altered by microgravity conditions in spaceflight. Journal of Plant Physiology 167:184–193.CrossRefPubMedGoogle Scholar
  26. McGrath, J.M., Hickok, L.G., and Pichersky, E. 1994. Assessment of Gene Copy Number in the Homosporous Ferns Ceratopteris thalictroides and C. richardii (Parkeriaceae) by Restriction-Fragment-Length-Polymorphisms. Plant Systematics and Evolution 189:203–210.CrossRefGoogle Scholar
  27. Millar, K.D.L., Kumar, P., Correll, M.J., Mullen, J.L., Hangarter, R.P., Edelmann, R.E., and Kiss, J.Z. 2010. A novel phototropic response to red light is revealed in microgravity. New Phytologist 186:648–656.CrossRefPubMedGoogle Scholar
  28. Nakazato, T., Jung, M.K., Housworth, E.A., Rieseberg, L.H., and Gastony, G.J. 2006. Genetic map-based analysis of genome structure in the homosporous fern Ceratopteris richardii. Genetics 173:1585–1597.CrossRefPubMedGoogle Scholar
  29. Nozue, K., Kanegae, T., Imaizumi, T., Fukuda, S., Okamoto, H., Yeh, K.C., Lagarias, J.C., and Wada, M. 1998. A phytochrome from the fern Adiantum with features of the putative photoreceptor NPH1. Proceedings of the National Academy of Sciences of the United States of America 95:15826–15830.CrossRefPubMedGoogle Scholar
  30. Pruitt, K.D., Tatusova, T., and Maglott, D.R. 2007. NCBI reference sequences (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Research 35:D61-D65.CrossRefPubMedGoogle Scholar
  31. Renzaglia, K.S., Warne, T.R., and Hickok, L.G. 1995. Plant development and the fern life-cycle using Ceratopteris richardii. American Biology Teacher 57:38–442.Google Scholar
  32. Rutherford, G., Tanurdzic, M., Hasebe, M., and Banks, J. 2004. A systemic gene silencing method suitable for high throughput, reverse genetic analyses of gene function in fern gametophytes. BMC Plant Biology 4: 6.CrossRefPubMedGoogle Scholar
  33. Salmi, M.L. and Roux, S.J. 2008. Gene expression changes induced by space flight in single-cells of the fern Ceratopteris richardii. Planta 229:151–159.CrossRefPubMedGoogle Scholar
  34. Salmi, M.L., Bushart, T.J., Stout, S.C., and Roux, S.J. 2005. Profile and analysis of gene expression changes during early development in germinating spores of Ceratopteris richardii. Plant Physiology 138:1734–1745.CrossRefPubMedGoogle Scholar
  35. Salmi, M.L., Morris, K.E., Roux, S.J., and Porterfield, D.M. 2007. Nitric oxide and cGMP signaling in calcium-dependent development of cell polarity in Ceratopteris richardii. Plant Physiology 144:94–104.CrossRefPubMedGoogle Scholar
  36. Scott, R.J. and Hickok, L.G. 1991. Inheritance and characterization of a dark-germinating, light-inhibited mutant in the fern Ceratopteris richardii. Canadian Journal of Botany-Revue Canadienne De Botanique 69:2616–2619.CrossRefGoogle Scholar
  37. Scott, R.J., Gastony, G.J., Weatherford, J.W., and Nakazato, T. 2007. Characterization of four members of the alpha-tubulin gene family in Ceratopteris richardii. American Fern Journal 97:47–65.CrossRefGoogle Scholar
  38. Spiro, M.D. and Knisely, K.I. 2008. Alternation of generations and experimental design: a guided-inquiry lab exploring the nature of the her1 developmental mutant of Ceratopteris richardii (C-Fern). Cbe-Life Sciences Education 7:82–88.PubMedGoogle Scholar
  39. Spiro, M.D., Torabi, B., and Cornell, C.N. 2004. Cytokinins induce photomorphogenic development in dark-grown gametophytes of Ceratopteris richardii. Plant and Cell Physiology 45:1252–1260.CrossRefPubMedGoogle Scholar
  40. Stilts, C.E. and Fisher, R. 2007. Synthesis of plant auxin derivatives and their effects on Ceratopteris richardii – A collaborative experiment between undergraduate organic and ­biochemistry laboratories. Journal of Chemical Education 84:999–1003.CrossRefGoogle Scholar
  41. Stout, S.C., Clark, G.B., Archer-Evans, S., and Roux, S.J. 2003. Rapid and efficient suppression of gene expression in a single-cell model system, Ceratopteris richardii. Plant Physiology 131:1165–1168.CrossRefPubMedGoogle Scholar
  42. Strain, E., Hass, B., and Banks, J.A. 2001. Characterization of mutations that feminize ­gametophytes of the fern Ceratopteris. Genetics 159:1271–1281.PubMedGoogle Scholar
  43. Tanurdzic, M. and Banks, J.A. 2004. Sex-determining mechanisms in land plants. Plant Cell 16: S61–S71.CrossRefPubMedGoogle Scholar
  44. ul Haque, A., Rokkam, M., De Carlo, A.R., Wereley, S.T., Wells, H.W., McLamb, W.T., Roux, S.J., Irazoqui, P.P., and Porterfield, D.M. 2006a. Design, fabrication and characterization of an in silico cell physiology lab for bio sensing applications. Journal of Physics: Conference Series 34:740–746.CrossRefGoogle Scholar
  45. ul Haque, A., Rokkam, M., DeCarlo, A.R., Wereley, S.T., Wells, H.W., McLamb, W.T., Roux, S.J., Irazoqui, P.P., and Porterfield, D.M. 2006b. In silico cell electrophysiology for measuring transcellular calcium currents. In Smart Medical and Biomedical Sensor Technology IV, eds. http://spie.org/x648.html?productid=673351&originid=x4323&startyear=2006&startat=21 B.M. Cullum and J.C. Carter, Vol. 6380, pp. U51–U59.
  46. ul Haque, A., Rokkam, M., De Carlo, A.R., Wereley, S.T., Roux, S.J., Irazoqui, P.P., and Porterfield, D.M. 2007. A MEMS fabricated cell electrophysiology biochip for in silico calcium measurements. Sensors and Actuators B-Chemical 123:391–399.CrossRefGoogle Scholar
  47. Wada, M. 2007. The fern as a model system to study photomorphogenesis. Journal of Plant Research 120:3–16.CrossRefPubMedGoogle Scholar
  48. Wada, M., Kadota, A., and Furuya, M. 1983. Intracellular-localization and dichroic orientation of phytochrome in plasma-membrane and or ectoplasm of a centrifuged protonema of fern Adiantum capillus-veneris L. Plant and Cell Physiology 24:1441–1447.Google Scholar
  49. Warne, T.R., Hickok, L.G., Sams, C.E., and Vogelien, D.L. 1999. Sodium/potassium selectivity and pleiotropy in stl2, a highly salt-tolerant mutation of Ceratopteris richardii. Plant Cell and Environment 22:1027–1034.CrossRefGoogle Scholar
  50. Wen, C.K., Smith, R., and Banks, J.A. 1999. ANI1: a sex pheromone-induced gene in ceratopteris gametophytes and its possible role in sex determination. Plant Cell 11:1307–1317.CrossRefPubMedGoogle Scholar
  51. Yao, J., Chang, C., Salmi, M.L., Hung, Y.S., Loraine, A., and Roux, S.J. 2008. Genome-scale cluster analysis of replicated microarrays using shrinkage correlation coefficient. BMC Bioinformatics 9:288.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Mari L. Salmi
    • 1
  • Thomas Bushart
  • Stanley J. Roux
  1. 1.MCDBThe University of Texas at AustinAustinUSA

Personalised recommendations