Stress signaling: coregulation of hemoglobin and male sex determination through a terpenoid signaling pathway in a crustacean
Tóm tắt
Environmental signals can activate neuro-endocrine cascades that regulate various physiological processes. In the present study, we demonstrate that two responses to environmental stress signaling in the crustacean Daphnia magna - hemoglobin accumulation and male offspring production - are co-elevated by the crustacean terpenoid hormone methyl farnesoate and several synthetic analogs. Potency of the hormones with respect to the induction of both hemoglobin and male offspring was highly correlated, suggesting that both processes are regulated by the same terpenoid signaling pathway. Six clones of the D. pulex/pulicaria species complex that were previously characterized as unable to produce male offspring and five clones that were capable of producing males were evaluated for both hemoglobin induction and male offspring production in response to methyl farnesoate. Four of the five male-producing clones produced both hemoglobin and male offspring in response to the hormone. Five of the six non-male-producing clones produced neither hemoglobin nor males in response to the hormone. These results provide additional evidence that both physiological processes are regulated by the same signaling pathway. Furthermore, the results indicate that the non-male-producing clones are largely defective in some methyl farnesoate signaling component, downstream from methyl farnesoate synthesis but upstream from the genes regulated by the hormone. A likely candidate for the site of the defect is the methyl farnesoate receptor. As a consequence of this defect,non-male-producing clones have lost their responsiveness to environmental signals that are transduced by this endocrine pathway. This defect in signaling would be likely to enhance population growth in stable environments due to the elimination of males from the population, assuming that other processes critical to population growth are not also compromised by this defect.
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Benzie, J. A. H. (1997). A review of the effect of genetics and environment on the maturation and larval quality of the giant tiger prawn Penaeus monodon. Aquaculture155, 69-85.
Beye, M., Hasselmann, M., Fondrk, M. K., Page, R. E. and Omholt,S. W. (2003). The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-Type protein. Cell114,419-429.
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein using the principle of protein dye binding. Anal. Biochem.72,248-254.
Bronson, F. H. (1985). Mammalian reproduction:an ecological perspective. Biol. Reprod.32, 1-26.
Bunn, H. F. and Poyton, R. O. (1996). Oxygen sensing and molecular adapatation to hypoxia. Physiol. Rev.76,839-885.
Bustin, S. A. (2000). Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J. Mol. Endocrinol.25,169-193.
Carlberg, C., van Huijsduijnen, R. H., Staple, J. K.,DeLamarter, J. F. and Becker-Andre, M. (1994). RZRs, a new family of retinoid-related orphan receptors that function as both monomer and homodimers. Mol. Endocrinol.8, 757-770.
Carmi, I., Kopczynski, J. B. and Meyer, B. J.(1998). The nuclear hormone receptor SEX-1 is an X-chromosome signal that determines nematode sex. Nature396,168-173.
Carvalho, G. and Hughes, R. (1983). The effect of food availability, female culture-density, and photoperiod on ephippia production in Daphnia magna Straus (Crustacea: Cladocera). Freshwater Biol.13,37-46.
Dudycha, J. L. (2004). Mortality dynamics of Daphnia in contrasting habitats and their role in ecological divergence. Freshwater Biol.49,505-514.
Gorr, T. A., Cahn, J. D., Yamagata, H. and Bunn, H. F.(2004). Hypoxia-induced synthesis of hemoglobin in the crustacean Daphnia magna is hypoxia-inducible factor-dependent. J. Biol. Chem.279,36038-36047.
Hebert, P. D. N. (1978). The population biology of Daphnia (Crustacea, Daphnidae). Biol. Rev.53,387-426.
Horie, Y., Kanda, T. and Mochida, Y. (2000). Sorbitol as an arrester of embryonic development in diapausing eggs of the silkworm, Bombyx mori. J. Insect Physiol.46,1009-1016.
Hoshi, T., Yahagi, N. and Watanabe, T. (1977). Studies on physiology and ecology of plankton. Further studies on O2 response to haemoglobin of Daphnia magna in vivo. Sci. Rep. Niigata Univ. Ser. D11, 7-13.
Innes, D. J., Fox, C. J. and Winsor, G. L.(2000). Avoiding the cost of males in obligately asexual Daphnia pulex (Leydig). Proc. R. Soc. Lond. B267,991-997.
Kalavathy, T., Mamatha, P. and Sreenivasula Reddy, P.(1999). Methyl farnesoate stimulates testicular growth in the freshwater crab Oziotelphusa senex senes fabricius. Naturwissenschaften86,394-395.
Kimura, S., Tokishita, S. I., Ohta, T., Kobayashi, M.,Kobayashi, M. and Yamagata, H. (1999). Heterogeneity and differential expression under hypoxia of two-domain hemoglobin chains in the water flea, Daphnia magna. J. Biol. Chem.274,10649-10653.
Klevien, O., Larsson, P. and Hobaek, A. (1992). Sexual reproduction in Daphnia magna requires three stimuli. Oikos65,197-206.
Kobayashi, M. and Hoshi, T. (1982). Relationship between the haemoglobin concentration of Daphnia magnaand the ambient oxygen concentration. Comp. Biochem. Physiol.72A,247-249.
Korpelainen, H. (1992). Lowered female reproductive effort as an indicator for increased male production and sexuality in Daphnia (Crustacea: Cladocera). Invert. Reprod. Dev.22,281-290.
Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature227,680-685.
Lamkemeyer, T., Zeis, B. and Paul, R. J.(2003). Temperature acclimation influences temperature-related behavious as well as oxygen-transport physiology and biochemistry in the water flea Daphnia magna. Can. J. Zool.81,237-249.
Laufer, H., Borst, D., Baker, F. C., Carrasco, C., Sinkus, M.,Reuter, C. C., Tsai, L. W. and Schooley, D. A. (1987). Identification of a juvenile hormone-like compound in a crustacean. Science235,202-205.
Laufer, H., Ahl, J. S. B. and Sagi, A. (1993). The role of juvenile hormones in crustacean reprodution. Amer. Zool.33,365-374.
Liu, L. and Laufer, H. (1996). Isolation and characterization of sinus gland neuropeptides with both mandibular organ inhibiting and hyperglycemic effects from the spider crab, lbinia emarginata. Arch. Insect Biochem. Physiol.32,375-385.
Nambu, J. R., Chen, W., Hu, S. and Crews, S. T.(1996). The Drosophila melanogaster similar bHLH-PAS gene encodes a protein related to human hypoxia-inducible factor 1 alpha and Drosophila single-minded. Gene172,249-254.
Olmstead, A. W. and LeBlanc, G. A. (2000). Effects of endocrine-active chemicals on the development of sex characteristics of Daphnia magna. Environ. Toxicol. Chem.19,2107-2113.
Olmstead, A. W. and LeBlanc, G. A. (2001). Temporal and quantitative changes in sexual reprodutive cycling of the cladoceran Daphnia magna by a juvenile hormone analog. J. Exp. Zool.290,148-155.
Olmstead, A. W. and LeBlanc, G. A. (2002). The juvenoid hormone methyl farnesoate is a sex determinant in the crustacean Daphnia magna. J. Exp. Zool.293,736-739.
Olmstead, A. W. and LeBlanc, G. A. (2003). Insecticidal juvenile hormone analogs stimulate the production of male offspring in the crustacean Daphnia magna. Environ. Health Perspect.111,919-924.
Pirow, R., Baumer, C. and Paul, R. J. (2001). Benefits of haemoglobin in the cladoceran Daphnia magna. J. Exp. Biol.204,3425-3441.
Reddy, P. S. and Ramamurthi, R. (1998). Methyl farnesoate stimulates ovarian maturation in freshwater crab Oziotelphusa senex senex Fabricius. Curr. Sci.74, 68-70.
Rispe, C. and Pierre, J. S. (1998). Coexistence between cyclical parthenogens, obligate parthenogens, and intermediates in a fluctuating environment. J. Theor. Biol.195,97-110.
Sambrook, J., Fritsch, E. F. and Maniatis, T.(1989). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor: Cold Spring Harbor Laboratory Press.
Steger, R. W. and Bartke, A. (1996). Environmental modulation of neuroendocrine function. In Handbook of Endocrinology, vol. I (ed. G. H. Gass and H. M. Kaplan), pp. 121-156. New York: CRC Press.
Stross, R. G. and Hill, J. C. (1968a). Photoperiod control of winter diapause in freshwater crustacean Daphnia. Biol. Bull.134,176-198.
Stross, R. G. and Hill, J. C. (1968b). Diapause induction in Daphnia requires two stimuli. Science150,1462-1464.
Tatarazako, N., Oda, S., Watanabe, H., Morita, M. and Iguchi,T. (2003). Juvenile hormone agonists affect the occurrence of male Daphnia. Chemosphere53,827-833.
van Dam, R. A., Barry, M. J., Ahokas, J. T. and Holdway, D. A. (1995). Toxicity of DTPA to Daphnia carinata as modified by oxygen stress and food limitation. Ecotoxicol. Environ. Safety31,117-126.
Vogel, J. M. and Borst, D. W. (1989). Spider crab yolk protein: Molecular characterization and the effects of methyl farnesoate (MF) on its hemolymph levels. Amer. Zool.29, 49A.
Wilson, T. E., Fahrner, T. J., Johnston, M. and Milbrandt,J. (1991). Identification of the DNA binding site of NGF1-B by genetic selection in yeast. Science252,1296-1300.
Wilson, T. E., Farhner, T. J. and Milbrandt, J.(1993). The orphan receptors NGF1-B and steroidogenic factor 1 establish monomer binding as a third paradigm of nuclear receptor-DNA interaction. Mol. Cell. Biol.13,5794-5804.
Yamashita, O. (1996). Diapause hormone of the silkworm, Bombyx mori: structure, gene expression and function. J. Insect Physiol.42,669-679.
Yi, W. and Zarkower, D. (1999). Similarity of DNA binding and transcriptional regulation by Caenorhabditis elegansMAB-3 and Drosophila melanogaster DSX suggests conservation of sex determining mechanisms. Development126,873-881.