Changes in localization and expression levels of Shroom2 and spectrin contribute to variation in amphibian egg pigmentation patterns.
One contributing factor in the worldwide decline in amphibian populations is thought to be the exposure of eggs to UV light. Enrichment of pigment in the animal hemisphere of eggs laid in the sunlight defends against UV damage, but little is known about the cell biological mechanisms controlling such polarized pigment patterns. Even less is known about how such mechanisms were modified during evolution to achieve the array of amphibian egg pigment patterns. Here, we show that ectopic expression of the gamma-tubulin regulator, Shroom2, is sufficient to induce co-accumulation of pigment granules, spectrin, and dynactin in Xenopus blastomeres. Shroom2 and spectrin are enriched and co-localize specifically in the pigmented animal hemisphere of Xenopus eggs and blastulae. Moreover, Shroom2 messenger RNA (mRNA) is expressed maternally at high levels in Xenopus. In contrast to Xenopus, eggs and blastulae of Physalaemus pustulosus have very little surface pigmentation. Rather, we find that pigment is enriched in the perinuclear region of these embryos, where it co-localizes with spectrin. Moreover, maternal Shroom2 mRNA was barely detectable in Physaleamus, though zygotic levels were comparable to Xenopus. We therefore suggest that a Shroom2/spectrin/dynactin-based mechanism controls pigment localization in amphibian eggs and that variation in maternal Shroom2 mRNA levels accounts in part for variation in amphibian egg pigment patterns during evolution.
Lee
Chanjae
C
Department of Molecular Cell and Developmental Biology and Institute for Cellular and Molecular Biology, University of Texas, Austin, TX 78712, USA.
Le
Minh-Phuong
MP
Cannatella
David
D
Wallingford
John B
JB
D000818:Animals; D001001:Anura / Q000196:embryology / Q000378:metabolism; D001757:Blastomeres / Q000378:metabolism; D000072159:Dynactin Complex; D020460:Melanosomes / Q000378:metabolism; D008840:Microfilament Proteins / Q000032:analysis / Q000235:genetics / Q000378:metabolism*; D008869:Microtubule-Associated Proteins / Q000378:metabolism; D009866:Oogenesis; D010063:Ovum / Q000378:metabolism; D010858:Pigmentation; D023121:RNA, Messenger, Stored / Q000378:metabolism; D013049:Spectrin / Q000032:analysis / Q000378:metabolism*; D029867:Xenopus Proteins / Q000032:analysis / Q000378:metabolism*; D014982:Xenopus laevis / Q000196:embryology / Q000378:metabolism*
D000072159:Dynactin Complex; D008840:Microfilament Proteins; D008869:Microtubule-Associated Proteins; D023121:RNA, Messenger, Stored; D029867:Xenopus Proteins; D013049:Spectrin