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First published online December 15, 2004
Journal of Experimental Biology 208, 15-23 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01343

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Stress signaling: coregulation of hemoglobin and male sex determination through a terpenoid signaling pathway in a crustacean

Cynthia V. Rider¹, Thomas A. Gorr², Allen W. Olmstead¹, Beth A. Wasilak¹ and Gerald A. LeBlanc^1,*

¹ Department of Environmental and Molecular Toxicology, North Carolina State University, Raleigh, NC 27695-7633, USA
² Division of Hematology, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA

View larger version (15K): [in a new window]   Fig. 1. Colorimetric scoring of hemoglobin content of daphnids. Criteria used to assign a color score to individual daphnids are listed in Table 1. Animals that were scored 9 were placed on a color grid of progressively darker shades of copper and a score was assigned based upon the best color match with the grid. Example relationships between color score assigned to daphnids and hemoglobin content normalized to the soluble protein content of the daphnids (A) and as total hemoglobin per daphnid (B). Values are means ± S.E.M.(N=2-4).

View larger version (22K): [in a new window]   Fig. 2. Hemoglobin levels in juvenile daphnids (D. magna) following treatment with the crustacean terpenoid hormone methyl farnesoate (A) and three synthetic analogs (B-D). Hemoglobin levels were assessed colorimetrically after 48 h exposure to the terpenoids. Ten daphnids were exposed to each treatment. Values are means ± S.E.M. *Significant difference from the respective control (0 nmol l-1; P<0.05, ANOVA, Dunnetts t-test).

View larger version (12K): [in a new window]   Fig. 3. Relationship between the concentrations of methyl farnesoate and analogs that elevated hemoglobin to 70% of the maximum level (x axis) and concentrations that caused a 50% incidence of male broods of offspring (y axis) in D. magna. Male offspring assessments were reported previously (Olmstead and LeBlanc, 2003). The 70% of maximal induction was used as the descriptor of relative potency for hemoglobin levels because this value could be interpolated from all of the concentration-reponse relationships depicted in Fig. 2. Correlation coefficient r2=0.999.

View larger version (41K): [in a new window]   Fig. 4. Induction of hemoglobin in daphnids (Daphnia magna) exposed to 0 or 3 nmol l-1 pyriproxyfen. (A) Control (0) and exposed (3) daphnids. (B) Electrophoretically separated pigmented protein from individual control (0) and exposed (3) daphnids. (C) Hemoglobin protein levels (µg mg-1 protein) in daphnids by absorbance at 415 nm (dark bars) and relative hb2 mRNA levels, normalized to levels of actin transcripts, measured by real-time rtPCR (light bars). Hemoglobin protein levels are means ± S.E.M. (N=4 samples each prepared from 17-20 individuals). Hemoglobin mRNA levels are means ± S.E.M. (N=2 samples each prepared from 30 individuals). *Significant (P<0.05) difference between control and pyriproxyfen-treated daphnids (Student's t test).

View larger version (13K): [in a new window]   Fig. 5. Hemoglobin levels in juvenile daphnids (D. magna) during exposure to 0.93 nmol l-1 pyriproxyfen (circles) and concurrently maintained controls (squares). Values are means ± S.E.M., N=10 daphnids. Hemoglobin levels were measured colorimetrically.

View larger version (12K): [in a new window]   Fig. 6. Diagrammatic representation of the putative juvenoid signaling pathway.