AJPS  Vol.3 No.7 , July 2012
The Effects of Sugars and Ethylene on Apospory and Regeneration in Ceratopteris richardii
Abstract: In land plants, two distinct generations, gametophyte and sporophyte, alternate to complete the life cycle. Sporophytes undergo meiosis to produce spores, from which gametophytes develop. Gametophytes produce gametes, which participate in fertilization to produce the zygote, the first cell of the sporophyte generation. In addition to this sexual reproduction pathway, some fern species can undergo apospory or apogamy, processes that bypass meiosis or fertilization, respectively, to alternate between the two generations without changing the chromosome number. Apospory is inducible in the laboratory in various fern species simply by altering the sugar level in the media. In sporophytes induced to undergo apospory, sporophyte regeneration is also observed. The ratio of aposporous gametophytes to regenerated sporophytes varies, in a manner consistent with being dependent on sugar level. Whereas the sugar signaling pathway is yet to be elucidated in lower plants, in angiosperms it has been shown to play a regulatory role in controlling essential processes including flowering and embryo development, which give rise to the gametophyte and the next sporophyte generation, respectively. Here, we present evidence for the role of different sugar levels on the balance of apospory and regeneration in the fern Ceratopteris richardii. The demonstration of crosstalk between sugar signaling and the hormone ethylene signaling in angiosperms prompted us to test the effects of this hormone in combination with sugar on apospory vs. regeneration. These results provide insight into how a group of redifferentiating cells determines which generation to become and lay the groundwork for further analysis of this asexual pathway.
Cite this paper: L. Bui, A. Hurst, E. Irish and C. Cheng, "The Effects of Sugars and Ethylene on Apospory and Regeneration in Ceratopteris richardii," American Journal of Plant Sciences, Vol. 3 No. 7, 2012, pp. 953-961. doi: 10.4236/ajps.2012.37113.

[1]   W. N. Steil, “Apogamy, apospory, and parthenogenesis in the pteridophytes,” Botanical Review, Vol. 5, No. 8, 1939, pp. 433-453.

[2]   P. R. Bell, “Apospory and apogamy: Implications for understanding the plant life cycle,” International Journal of Plant Science, Vol. 153, No. 3 (Part 2: The Katherine Esau International Symposium), 1992, pp. S123-S136.

[3]   T. G. Walker, “The cytogenetics of ferns,” In: A. F. Dyer (Ed.), The Experimental Biology of Ferns, Academic Press, London, New York, 1979, pp. 87-132.

[4]   V. Raghavan, “Developmental Biology of Fern Gametophytes,” Cambridge University Press, Cambridge, 1989.

[5]   A. R. Cordle, E. E. Irish, and C-L. Cheng, “Apogamy induction in Ceratopteris richardii,” International Journal of. Plant Science, Vol. 168, 2007, pp.361-369.

[6]   M. H. Munroe and I. M. Sussex, “Gametophyte formation in bracken fern root cultures,” Canadian Journal of Botany. Vol. 47, 1969, pp. 617-621.

[7]   B. DeYoung, T. Weber, T. Hass and J. A. Banks, “Generating autotetraploid sporophytes and their use in analyzing mutations affecting gametophyte development in the fern Ceratopteris,” Genetics. Vol. 147, No. 2, 1997, pp.809-814.

[8]   A. R. Cordle, L. T. Bui, E. E. Irish, and C-L. Cheng, “Laboratory-induced apogamy and apospory in Ceratopteris rihardii”, In: H. Fernandes, A Kumar, and M.A. Revilla (Eds.), Working with Ferns, Springer, 2011, pp. 25-36.

[9]   V. Menéndez, R. Arbesú, M. Somer, A. Revilla, and H. Fernández, “From spore to sporophyte: How to proceed in vitro,” In: H. Fernandes, A Kumar, and M.A. Revilla (Eds.), Working with Ferns, Springer, 2011, pp. 97-110.

[10]   B. J. Dekkers, J. A. Schuurmans, and S. C. Smeekens, “Interaction between sugar and abscisic acid signalling during early seedling development in Arabidopsis,” Plant Molecular Biology, Vol. 67, 2008, pp. 151-167.

[11]   M. Ramon, F. Rolland and J. Sheen, “Sugar Sensing and Signaling,” In: The Arabidopsis Book (TAB), 2008, ISSN: 1543-8120, pp. 1-22, doi: 10.1199/tab.0117

[12]   J. Hanson and S. Smeekens, “Sugar perception and signaling – an update,” Current Opinions in Plant Biology, Vol.12, 2009, pp. 562-567.

[13]   A. Nilsson, T. Olsson, M. Ulfstedt, M. Thelander and H. Ronne, “Two novel types of hexokinases in the moss Physcomitrella patens,” BMC Plant Biology, Vol. 11, No. 1, 2011, doi: 10.1186/1471-2229-11-32.

[14]   T. Olsson, M. Thelander and H. Ronne, “A novel type of chloroplast stromal hex-okinase is the major glucose phosphorylating enzyme in the moss Physcomitrella patens,” Journal of Biological Chemistry, Vol. 278, 2003, pp. 44439-44447.

[15]   H. Weber, L. Borisjuk and U. Wobus, “Sugar import and metabolism during seed development,” Trends in Plant Science, Vol. 2, 1997, pp. 169-174.

[16]   L. Zhou, J. C. Jang, T. L. Jones and J. Sheen, “Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucose insensitive mutant,” PNAS, Vol. 95: 1998, pp. 10294-10299.

[17]   S. I. Gibson, R. J. Laby and D. G. Kim, “The sugar-insensitive1 (sis1) mutant of Arabidopsis is allelic to ctr1,” Biochemistry and Biophysics Reserach Communication,Vol. 280, 2001, pp. 196-203.

[18]   S. Gazzarrini and P. McCourt, “Genetic interactions between ABA, ethylene and sugar signaling pathways,” Current Opinion in Plant Biololgy, Vol. 4, 2001, pp. 387-391.

[19]   S. Gazzarrini and P. McCourt, “Cross-talk in plant hormone signaling: What Arabidopsis mutants are telling us,” Annuals of Botany, Vol. 91, 2003, pp. 605-612.

[20]   A. L. Eveland and D. P. Jackson, “Sugars, signaling, and plant development,” Journal of Experimental Botany, 2011, doi:10.1093/jxb/err379.

[21]   Y-H. Cho, J. Sheen and S-D. Yoo, “Low glucose uncouples Hexokinase1-dependent sugar signaling from stress and defense hormone Abscisic Acid and C2H4 responses in Arabidopsis,” Plant Physiology, Vol. 152, 2010, pp. 1180-1182.

[22]   P. M. Miller, H. C. Sweet, H. C. and J. H. Miller, “Growth regulation by ethylene in fern gametophytes. I. effects on protonemal and rhizoidal growth and interaction with auxin,”, American Journal of Botany, Vol. 57, No. 2, 1970, pp. 212-217.

[23]   S. H. Kwa, Y. C. Wee and P. P. Kumar, “Role of ethylene in the production of sporophytes from Platycerium coronarium (Koenig) Desv. frond and rhizome pieces cultured in vitro,” Journal of Plant Growth Regulation, Vol. 14, No. 4, 1995, pp.183-189.

[24]   D. J. Osborne, J. Walters, B. V. Milborrow, A. Norville and L. M. C. Stange, “Special publication evidence for a non-ACC ethylene biosynthesis pathway in lower plants,” Phytochemistry, Vol. 42, No. 1, 1996, pp. 51-60. doi:DOI: 10.1016/0031-9422(96)00032-5.

[25]   J. Chernys and H. Kende, “Ethylene biosynthesis in Regnellidium diphyllum and Marsilea quadrifolia,” Planta, Vol. 200, 1996, pp. 113-118.

[26]   A. Anterola and E. Shanle, “Genomic insights in moss gibberellins biosynthesis,” The Bryologist, Vol. 111, No. 2, 2008, pp. 218-230.

[27]   K. E. Brooks, “Reproductive Biology of Selaginella. I. Determination of megasporangia by 2-Chloroethylphosphonic acid, an ethylene releasing compound,” Plant Physiology, Vol. 51, 1973, pp. 718-722.

[28]   S. F. Yang, “Ethylene evolution from 2-Chloro ethylphosphonic acid,” Plant Physiology, Vol. 44, 1969, pp. 1203-1204.

[29]   F. B. Abeles, P. W. Morgan and M. E. Saltveit, Jr., “Ethylene in plant biology” 2nd edition, Academic Press, Inc., San Diego, 1992, pp. 1-13.

[30]   L. G. Hickok, T. R. Warne and R. S. Fribourg, “The biology of the fern Ceratopteris and its use as a model system,” Inernational Journal of Plant Science, Vol. 156, 1995, pp. 332-345.

[31]   W. C. Yang and V. Sundaresan, “Genetics of gametophyte biogenesis in Arabidopsis,” Current Opinion in Plant Biology, Vol. 3, 2000, pp. 53-57.

[32]   A. M. Hirsch, “The effect of sucrose on the differentiation of excised fern leaf tissue into either gametophytes or sporophytes,” Plant Physiology, Vol.56, 1975, pp. 390-393.

[33]   J. Ambrozic-Dolinsek, M. Camloh, B. Bohanec and J. Zel, “Apospory in leaf culture of staghorn fern Platycerium bifurcatum,” Plant Cell Reports, Vol. 20, No. 9, 2002, pp. 791-796.

[34]   M. R. Bolouri-Moghaddam, K. L. Roy, L. Xiang, F. Rolland and W. Van den Ende, “Sugar signaling and antioxidant network connections in plant cells,” FEBS Journal,Vol. 277, 2010, pp. 2022-2037.

[35]   S. D. Yoo, Y. Cho and J. Sheen, “Emerging connections in the ethylene signaling network,” Cell press, Elsevier Ltd, 2009, doi:10.10.1016/j.tplants.2009.02.007.

[36]   T. R. Warner and L. G. Hickok, “(2-Chloroethyl) phosphonic acid promotes germinationof immature spores of Ceratopteris richardii Brongn,” Plant Physiology, Vol. 83, 1987, pp. 723-725.

[37]   H. W. Elmore and D. P. Whittier, “The role of ethylene in the induction of apogamous buds in Pteridium gametophytes,” Planta, Vol. 111, 1973, pp. 85-90.

[38]   D. De Martinis and C. Mariani, “Silencing gene expression of the ethylene-forming enzyme results in a reversible inhibition of ovule development in transgenic tobacco plants,” The Plant Cell, Vol. 11, 1999, pp. 1061-1071.

[39]   G. N. Drews, D. Lee and C. A. Christensen, “Genetic analysis of female gametophyte development and function,” The Plant Cell, Vol. 10, 1998, pp. 5-17.

[40]   P. Carbonell-Bejerano, C. Urbez, A. Granell, J. Carbonell and M. Perez-Amador, “ Ethylene is involved in pistil fate by modulating the onset of ovule senescence and the GA-mediated fruit set in Arabidopsis,” BMC Plant Biology, Vol. 11, No. 84, 2011, pp. 11-84.