Spermidine is a morphogenetic determinant for cell fate specification in the male gametophyte of the water fern Marsilea vestita

Plant Cell

Volumn 22, Issue 11, 2010, Pages 3678-3691

  Deeb, Faten ^a,b   van der Weele, Corine M ^a   Wolniak, Stephen M ^a  

^a Bldg 142   (United States)

^b University of Missouri   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROPTERIDALES; MARSILEA VESTITA;

EID: 78650868797     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.109.073254     Document Type: Article

References (51)

1. Ackermann, J.M., Pegg, A.E., and McCloskey, D.E. (2003). Drugs affecting the cell cycle via actions on the polyamine metabolic pathway. Prog. Cell Cycle Res. 5: 461-468.
2. Banan, A., McCormack, A., and Johnson, L.R. (1998). Polyamines are required for microtubule formation during gastric mucosal healing. Am. J. Physiol. Gastrointest. Liver Physiol. 274: 879-885.
3. Baron, K., and Stasolla, C. (2008). The role of polyamines during in vivo and in vitro development. In Vitro Cell. Dev. Biol. Plant 44: 384-395.
4. Baskin, T., Busby, C.H., Fowke, L.C., Sammut, M., and Gubler, F. (1992). Improvements in immunostaining samples embedded in methacrylate: Localization of microtubules and other antigens throughout developing organs in plants of diverse taxa. Planta 187: 405-413.
5. Baskin, T.I., and Wilson, J.E. (1997). Inhibitors of protein kinases and phosphatases alter root morphology and disorganize cortical microtubules. Plant Physiol. 113: 493-502.
6. Carothers, Z.B. (1975).Comparative studies on spermatogenesis in bryophytes. In The Biology of the Male Gamete, J.G. Duckett and P.A. Racey, eds (New York: Academic Press), pp. 71-84.
7. Caruso, A., Pellati, A., Bosi, G., Arena, N., and Stabellini, G. (1994). Effects of spermidine synthase inhibition on cytoskeletal organization in cultured chick embryo fibroblasts. Eur. J. Histochem. 38: 245-252.
8. Clément, S., Delcros, J.G., Basu, H.S., Quash, G., Marton, L.J., and Feuerstein, B.G. (1995). The structure of polyamine analogues determines haemoglobin production and cytotoxicity in murine erythroleukaemia cells. Biochem. J. 309: 787-791.
9. Coueé, I., Hummel, I., Sulmon, C., Gouesbet, G., and El Amrani, A. (2004). Involvement of polyamines in root development. Plant Cell Tissue Organ Cult. 76: 1-10.
10. Covassin, L., Desjardins, M., Soulet, D., Charest-Gaudreault, R., Audette, M., and Poulin, R. (2003). Xylylated dimers of putrescine and polyamines: Influence of the polyamine backbone on spermidine transport inhibition. Bioorg. Med. Chem. Lett. 13: 3267-3271.
11. Dufe, V.T., Qiu, W., Müller, I.B., Hui, R., Walter, R.D., and Al-Karadaghi, S. (2007). Crystal structure of Plasmodium falciparum spermidine synthase in complex with the substrate decarboxylated S-adenosylmethionine and the potent inhibitors 4MCHA and AdoDATO. J. Mol. Biol. 373: 167-177.
12. Frydman, L., Rossomando, P.C., Frydman, V., Fernandez, C.O., Frydman, B., and Samejima, K.S. (1992). Interactions between natural polyamines and tRNA: an 15N NMR analysis. Proc. Natl. Acad. Sci. USA 89: 9186-9190.
13. Geall, A.J., Eaton, M.A.W., Baker, T., Catterall, C., and Blagbrough, I.S. (1999). The regiochemical distribution of positive charges along cholesterol polyamine carbamates plays significant roles in modulating DNA binding affinity and lipofection. FEBS Lett. 459: 337-342.
14. Gomurgen, A.N., Mutlu, F., and Bozcuk, S. (2004). Effects of polyamines (putrescine, spermidine and spermine) on root tip mitosis and chromosomes in Allium cepa L. Cytologia (Tokyo) 70: 217-224.
15. Haider, N., Eschbach, M.-L., Dias, Sde.S., Gilberger, T.-W., Walter, R.D., and Lüersen, K. (2005). The spermidine synthase of the malaria parasite Plasmodium falciparum: Molecular and biochemical characterisation of the polyamine synthesis enzyme. Mol. Biochem. Parasitol. 142: 224-236.
16. Hart, P.E., and Wolniak, S.M. (1998). Spermiogenesis in Marsilea vestita: A temporal correlation between centrin expression and blepharoplast differentiation. Cell Motil. Cytoskeleton 41: 39-48.
17. Hart, P.E., and Wolniak, S.M. (1999). Molecular cloning of a centrin homolog from Marsilea vestita and evidence for its translational control during spermiogenesis. Biochem. Cell Biol. 77: 101-108.
18. Hepler, P.K. (1976). The blepharoplast of Marsilea: Its de novo formation and spindle association. J. Cell Sci. 21: 361-390.
19. Hoffman, J.C., and Vaughn, K.C. (1995). Using developing spermatogenous cells of Ceratopteris to unlock the mysteries of the plant cytoskeleton. Int. J. Plant Sci. 156: 346-358.
20. Hoyt, M.A., Broun, M., and Davis, R.H. (2000). Polyamine regulation of ornithine decarboxylase synthesis in Neurospora crassa. Mol. Cell. Biol. 20: 2760-2773.
21. Igarashi, K., and Kashiwagi, K. (1999). Polyamine transport in bacteria and yeast. Biochem. J. 344: 633-642.
22. Igarashi, K., and Kashiwagi, K. (2000). Polyamines: Mysterious modulators of cellular functions. Biochem. Biophys. Res. Commun. 271: 559-564.
23. Imai, A., et al. (2004). Spermidine synthase genes are essential for survival of Arabidopsis. Plant Physiol. 135: 1565-1573.
24. Kaipia, A., Toppari, J., Mali, P., Kangasniemi, M., Alcivar, A.A., Hecht, N.B., and Parvinen, M. (1990). Stage-and cell-specific expression of the ornithine decarboxylase gene during rat and mouse spermatogenesis. Mol. Cell. Endocrinol. 73: 45-52.
25. Kaur-Sawhney, R., Tiburcio, A.F., Atlabells, T., and Galston, A.W. (2003). Polyamines in plants: An overview. J. Cell. Mol. Biol. 2: 1-12.
26. Klink, V.P., and Wolniak, S.M. (2001). Centrin is necessary for the formation of the motile apparatus in spermatids of Marsilea. Mol. Biol. Cell 12: 761-776.
27. Klink, V.P., and Wolniak, S.M. (2003). Changes in the abundance and distribution of conserved centrosomal, cytoskeletal and ciliary proteins during spermiogenesis in Marsilea vestita. Cell Motil. Cytoskeleton 56: 57-73.
28. Kwak, S.-H., and Lee, S.H. (2002). The transcript-level-independent activation of ornithine decarboxylase in suspension-cultured BY2 cells entering the cell cycle. Plant Cell Physiol. 43: 1165-1170.
29. Lomadze, N., Schneider, H.-J., Albelda, M.T., García-España, E., and Verdejo, B. (2006). Dramatic selectivity differences in the association of DNA and RNA models with new ethylene-and propylene diamine derivatives and their copper complexes. Org. Biomol. Chem. 4: 1755-1759.
30. Marc, J., and Gunning, B.E.S. (1986). Immunofluorescent localization of cytoskeletal tubulin and actin during spermatogenesis in Pteridium aquilinum (L.) Kuhn. Protoplasma 134: 163-177.
31. Mizukami, I., and Gall, J. (1966). Centriole replication. II. Sperm formation in the fern, Marsilea, and the cycad, Zamia. J. Cell Biol. 29: 97-111.
32. Myles, D.G., and Hepler, P.K. (1977). Spermiogenesis in the fern Marsilea microtubules, nuclear shaping, and cytomorphogenesis. J. Cell Sci. 23: 57-83.
33. Needleman, D.J., Ojeda-Lopez, M.A., Raviv, U., Miller, H.P., Wilson, L., and Safinya, C.R. (2004). Higher-order assembly of microtubules by counterions: From hexagonal bundles to living necklaces. Proc. Natl. Acad. Sci. USA 101: 16099-16103.
34. O'Brien, T.P., and McCully, M.E. 1981. The Study of Plant Structure. Principles and Selected Methods. (Melbourne, Australia: Termarcarphi Pty. Ltd.).
35. Oliva, R., Vidal, S., and Mezquita, C. (1982). Cellular content and biosynthesis of polyamines during rooster spermatogenesis. Biochem. J. 208: 269-273.
36. Osborne, H.B., Cormier, P., Lorillon, O., Maniey, D., and Bellé, R. (1993). An appraisal of the developmental importance of polyamine changes in early Xenopus embryos. Int. J. Dev. Biol. 37: 615-618.
37. Pohjanpelto, P., Virtanen, I., and Hölttä, E. (1981). Polyamine starvation causes disappearance of actin filaments and microtubules in polyamine-auxotrophic CHO cells. Nature 293: 475-477.
38. Pollard, K.J., Samuels, M.L., Crowley, K.A., Hansen, J.C., and Peterson, C.L. (1999). Functional interaction between GCN5 and polyamines: A new role for core histone acetylation. EMBO J. 18: 5622-5633.
39. Quemener, V., Blanchard, Y., Lescoat, D., Havouis, R., and Moulinoux, J.P. (1992). Depletion in nuclear spermine during human spermatogenesis, a natural process of cell differentiation. Am. J. Physiol. Cell Physiol. 263: 343-347.
40. Reynolds, W.F., and Wolfe, S.L. (1978). Changes in basic proteins during sperm maturation in a plant, Marchantia polymorpha. Exp. Cell Res. 116: 269-273.
41. Reynolds, W.F., and Wolfe, S.L. (1984). Protamines in plant sperm. Exp. Cell Res. 152: 443-448.
42. Sharp, L.W. (1914). Spermatogenesis in Marsilia. Bot. Gaz. 58: 419-432.
43. Sible, J.C., Marsh, A.G., and Walker, C.W. (1990). Effect of extrinsic polyamines on post-spawning testes of the sea star, Asterias vulgaris (Echinodermata): Implications for the seasonal regulation of spermatogenesis. Invertebr. Reprod. Dev. 19: 257-264.
44. Steel, J.H., Gordon, L., and Polak, J.M. (1998). Principles and applications of complementary RNA probes. In In Situ Hybridization: Principles and Practice, J. Polak and J.O.D. McGee, eds (Oxford, UK: Oxford University Press), pp. 49-69.
45. Tabor, C.W., and Tabor, H. (1984). Polyamines. Annu. Rev. Biochem. 53: 749-790.
46. Tsai, C.W., Van Der Weele, C.M., and Wolniak, S.M. (2004). Differential segregation and modification of mRNA during spermiogenesis in Marsilea vestita. Dev. Biol. 269: 319-330.
47. Tsai, C.W., and Wolniak, S.M. (2001). Cell cycle arrest allows centrin translation but not basal body formation during spermiogenesis in Marsilea. J. Cell Sci. 114: 4265-4272.
48. Unal, M., Palavan-Unsal, N., and Tufekci, M.A. (2008). Effects of polyamines and polyamine biosynthetic inhibitors on mitotic activity of Allium cepa root tips. Acta Biol. Hung. 59: 93-102.
49. van der Weele, C.M., Tsai, C.W., and Wolniak, S.M. (2007). Mago nashi is essential for spermatogenesis in Marsilea. Mol. Biol. Cell 18: 3711-3722.
50. Watts, S.A., Lee, K.J., Hines, G.A., and Walker, C.W. (1987). Determination of polyamines in digestive and reproductive tissues of adult Asterias vulgaris (Echinodermata: Asteroidea). Comp. Biochem. Physiol. B 88: 309-312.
51. Yatin, M. (2002). Polyamines in living organisms. J. Cell Mol. Biol. 1: 57-67.