Development Genes and Evolution

, Volume 228, Issue 1, pp 31–48 | Cite as

Two Drosophilids exhibit distinct EGF pathway patterns in oogenesis

  • Kenley N. O’Hanlon
  • Rachel A. Dam
  • Sophie L. Archambeault
  • Celeste A. Berg
Original Article

Abstract

Deciphering the evolution of morphological structures is a remaining challenge in the field of developmental biology. The respiratory structures of insect eggshells, called the dorsal appendages, provide an outstanding system for exploring these processes since considerable information is known about their patterning and morphogenesis in Drosophila melanogaster and dorsal appendage number and morphology vary widely across Drosophilid species. We investigated the patterning differences that might facilitate morphogenetic differences between D. melanogaster, which produces two oar-like structures first by wrapping and then elongating the tubes via cell intercalation and cell crawling, and Scaptodrosophila lebanonensis, which produces a variable number of appendages simply by cell intercalation and crawling. Analyses of BMP pathway components thickveins and P-Mad demonstrate that anterior patterning is conserved between these species. In contrast, EGF signaling exhibits significant differences. Transcripts for the ligand encoded by gurken localize similarly in the two species, but this morphogen creates a single dorsolateral primordium in S. lebanonensis as defined by activated MAP kinase and the downstream marker broad. Expression patterns of pointed, argos, and Capicua, early steps in the EGF pathway, exhibit a heterochronic shift in S. lebanonensis relative to those seen in D. melanogaster. We demonstrate that the S. lebanonensis Gurken homolog is active in D. melanogaster but is insufficient to alter downstream patterning responses, indicating that Gurken-EGF receptor interactions do not distinguish the two species’ patterning. Altogether, these results differentiate EGF signaling patterns between species and shed light on how changes to the regulation of patterning genes may contribute to different tube-forming mechanisms.

Keywords

Dorsal appendages Scaptodrosophila Drosophila Follicle cells Eggshell Epithelial morphogenesis 

Notes

Acknowledgements

We thank Sydney Bowker, Vincent So, and Jill Kumasaka for their help with in situ hybridization experiments; Dr. Scott Roy at San Francisco State University for his advice on Scaptodrosophila gene annotation; Dr. Robert Waterston and Dr. Evan Eichler for the use of their compound microscopes; and Dr. Miriam Osterfield and members of the Berg lab for their helpful discussions. For technical support and advice on imaging, we thank Dr. Nathaniel Peters at the University of Washington W. M. Keck Imaging Center, which is supported by the National Institutes of Health (NIH) grant 1S10 OD016240. We are grateful to FlyBase for exceptional genetic, genomic, and bibliographic resources, the Bloomington Drosophila Stock Center for the MTD-GAL4 driver, the Drosophila Genomics Resource Center for the UASp-attB plasmid, the Drosophila Species Stock Center (formerly at Bowling Green and Tucson but now in San Diego) for providing Scaptodrosophila lebanonensis flies, and Drs. Norbert Perrimon and Christian Ghiglione for the UASp-grk.mb strain. We thank Dr. Tom Jessell and colleagues E. Laufer, S. Morton, and D. Vasiliauskas for the antibody against phosphorylated Smad1/5/8 (P-Mad). We obtained anti-Gurken, anti-Broad, and anti-DE-Cadherin monoclonal antibodies from the Developmental Studies Hybridoma Bank, created by the National Institute of Child Health and Human Development of the National Institutes of Health and maintained by the University of Iowa, Department of Biology

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Supplementary material

427_2017_601_Fig11_ESM.gif (74 kb)
Fig. A1

Oogenesis timing and development differ between D. melanogaster and S. lebanonensis. (a, b) DAPI staining reveals egg-chamber distribution within ovarioles of 2-day-old mated females fed a diet supplemented with wet yeast. (a) A D. melanogaster ovary contains most stages of oogenesis. One ovariole is labeled with several stages of egg chambers. (b) At two days post eclosion, a S. lebanonensis ovary contains only germaria, S5, and S9 stages of oogenesis. (c) Timeline schematic of oogenesis for both species in hours. D. melanogaster eggs are ready to be laid two days post eclosion, while S. lebanonensis eggs are not mature until three days. (GIF 74 kb)

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Fig. A2

S. lebanonensis grk transcripts are localized near the oocyte nucleus but br mRNA is present in a dorsolateral band. (a) At S9, br mRNA is present in all follicle cells. (b) br expression is upregulated in a dorsolateral band by S10B. (c) All remaining br mRNA is degraded by S12. (d, e) In S1, S5, and S6 egg chambers, grk mRNA fills the oocyte at the posterior of the egg chamber. (f) In this larger S7 egg chamber, grk transcripts associate with the oocyte nucleus during its migration to the anterior cortex. (g) By S8, the oocyte nucleus has arrived at the dorsal anterior corner of oocyte; grk mRNA is enriched near the nucleus but is also present in a wide band at the anterior of the oocyte. (h) In S9 egg chambers, grk transcripts form a modest-sized cloud at the dorsal-anterior cortex of the oocyte. (i) Some S10 egg chambers exhibit grk transcript localized slightly laterally around the oocyte nucleus. (j) Diffuse expression of grk is visible in a S12 egg chamber. (GIF 172 kb)

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427_2017_601_Fig13_ESM.gif (113 kb)
Fig. A3

S. lebanonensis pnt and aos expression patterns are unexpected. (a) At S9, pnt mRNA is expressed both at the posterior and in a thin dorsolateral band that is slightly posterior to the anterior cortex. (b) The anterior domain of pnt expression expands toward the posterior into a wider dorsolateral band, and the strictly posterior expression remains. (c) By S12, only the posterior pnt expression is present. (d) aos mRNA is not detectable in S9 egg chambers. (e) At S10B, aos expression is present in a thin dorsolateral band, shifted posteriorly from the anterior cortex. (f) The anterior domain of aos expression widens and a posterior patch of expression appears. (GIF 113 kb)

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Fig. A4

S. lebanonensis Grk is active in a D. melanogaster background and the degree of dorsalization depends on temperature. Females were reared for 3 days at the indicated temperatures prior to egg collection. The MTD-GAL4 driver, which is active in the germline at all stages of oogenesis, was crossed to w 1118 , UASp-grk Dm , or UASp-grk Sl . Phenotypic classes are as described in Fig. 8. Chart shows quantitation of phenotypic classes; N > 270 for each genotype at a given temperature. (GIF 68 kb)

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Fig. A5

grk transcript distribution and abundance in egg chambers expressing grk Dm or grk Sl transgenes. All images show a lateral orientation with anterior to the left and dorsal up. N > 80 for each genotype. (a, b) Controls: grk Sl and grk Dm antisense probes do not cross-react to transcripts present in the other species. (a) grk Sl antisense probe hybridized to D. melanogaster MTD > w 1118 egg chambers. (b) grk Dm antisense probe hybridized to S. lebanonensis wild-type egg chambers. (c, d) Over-expression of grk Dm in MTD > grk Dm egg chambers produces aberrant grk Dm localization (c) during S10-S11, as quantified in (d). (e, f) In MTD > grk Sl egg chambers, grk Sl is expressed highly in the nurse cells (e), as quantified in (f). (GIF 98 kb)

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ESM 1

(GIF 1873 kb)

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ESM 2

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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Department of Genome SciencesUniversity of WashingtonSeattleUSA
  2. 2.Molecular and Cellular Biology ProgramUniversity of WashingtonSeattleUSA
  3. 3.Institute of Ecology and EvolutionUniversity of BernBernSwitzerland

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