Abstract
BackgroundThe evolutionary origins of cell polarity in metazoan embryos are unclear. In most bilaterian animals, embryonic and cell polarity are set up during embryogenesis with the same molecules being utilized to regulate tissue polarity at different life stages. Atypical protein kinase C (aPKC), lethal giant larvae (Lgl), and Partitioning-defective (Par) proteins are conserved components of cellular polarization, and their role in establishing embryonic asymmetry and tissue polarity have been widely studied in model bilaterian groups. However, the deployment and role of these proteins in animals outside Bilateria has not been studied. We address this by characterizing the localization of different components of the Par system during early development of the sea anemone Nematostella vectensis, a member of the clade Cnidaria, the sister group to bilaterian animals.ResultsImmunostaining using specific N. vectensis antibodies and the overexpression of mRNA-reporter constructs show that components of the N. vectensis Par system (NvPar-1, NvPar-3, NvPar-6, NvaPKC, and NvLgl) distribute throughout the microtubule cytoskeleton of eggs and early embryos without clear polarization along any embryonic axis. However, they become asymmetrically distributed at later stages, when the embryo forms an ectodermal epithelial layer. NvLgl and NvPar-1 localize in the basolateral cortex, and NvaPKC, NvPar-6, and NvPar-3 at the apical zone of the cell in a manner seen in bilaterian animals.ConclusionsThe cnidarian N. vectensis exhibits clear polarity at all stages of early embryonic development, which appears to be established independent of the Par system reported in many bilaterian embryos. However, in N. vectensis, using multiple immunohistochemical and fluorescently labeled markers in vivo, components of this system are deployed to organize epithelial cell polarity at later stages of development. This suggests that Par system proteins were co-opted to organize early embryonic cell polarity at the base of the Bilateria and that, therefore, different molecular mechanisms operate in early cnidarian embryogenesis.Electronic supplementary materialThe online version of this article (doi:10.1186/s13227-015-0014-6) contains supplementary material, which is available to authorized users.
Highlights
The evolutionary origins of cell polarity in metazoan embryos are unclear
Identification of maternal and zygotic mRNA distribution by whole-mount in situ hybridization We performed in situ hybridization experiments on five Par system genes (NvaPKC, N. vectensis Par-3 (NvPar-3), NvPar-6, NvPar-1, and N. vectensis Lgl (NvLgl)) in order to assess the distribution of the maternal and zygotic mRNA transcripts for different proteins at early stages of N. vectensis development (Figure 2)
Transcripts of all five genes are asymmetrically distributed in unfertilized eggs, fertilized eggs, and through the early cleavage stages due to the presence of the yolk gradient (Figure 2). This asymmetric distribution does not appear to be correlated with A/V polarity or the subsequent cleavage program per se because different patterns were observed across a number of embryos at the four-cell stage (Additional file 2), suggesting that mRNA distribution in N. vectensis is not linked to mitotic spindle orientation and the patterns of the initial cleavages
Summary
The evolutionary origins of cell polarity in metazoan embryos are unclear. In most bilaterian animals, embryonic and cell polarity are set up during embryogenesis with the same molecules being utilized to regulate tissue polarity at different life stages. Polarity in epithelial tissues is known to be influenced by cell-cell junctions, Salinas-Saavedra et al EvoDevo (2015) 6:20 bi/tripartite complex that localizes to different regions of the apical cortex of the cell, binding to the activated Rho protein CDC42 and CRUMBS (Figure 1B) [1,2,12,13,14]. Both Lgl and Par-1 localize at the basolateral cortex of the cell (Figure 1B) [1,2,15], but it is unclear whether these two components act individually or as an associated complex. This general mechanism is conserved in all bilaterian animals that have been studied (Figure 1C) [3,10,11,16,17,18,19]
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