Publication Date

7-12-2016

Document Type

Article

Organizational Units

College of Natural Science and Mathematics, Biological Sciences

Keywords

Microvillus, Versatile organelle, Vertebrate, Freshwater sponge, Gene homologs, Choanocytes

Abstract

Background

The microvillus is a versatile organelle that serves important functions in disparate animal cell types. However, from a molecular perspective, the microvillus has been well studied in only a few, predominantly vertebrate, contexts. Little is known about how differences in microvillar structure contribute to differences in function, and how these differences evolved. We sequenced the transcriptome of the freshwater sponge, Ephydatia muelleri, and examined the expression of vertebrate microvillar gene homologs in choanocytes—the only microvilli-bearing cell type present in sponges. Sponges offer a distant phylogenetic comparison with vertebrates, and choanocytes are central to discussions about early animal evolution due to their similarity with choanoflagellates, the single-celled sister lineage of modern animals.

Results

We found that, from a genomic perspective, sponges have conserved homologs of most vertebrate microvillar genes, most of which are expressed in choanocytes, and many of which exhibit choanocyte-specific or choanocyte-enriched expression. Possible exceptions include the cadherins that form intermicrovillar links in the enterocyte brush border and hair cell stereocilia of vertebrates and cnidarians. No obvious orthologs of these proteins were detected in sponges, but at least four candidate cadherins were identified as choanocyte-enriched and might serve this function. In contrast to the evidence for conserved microvillar structure in sponges and vertebrates, we found that choanoflagellates and ctenophores lack homologs of many fundamental microvillar genes, suggesting that microvillar structure may diverge significantly in these lineages, warranting further study.

Conclusions

The available evidence suggests that microvilli evolved early in the prehistory of modern animals and have been repurposed to serve myriad functions in different cellular contexts. Detailed understanding of the sequence by which different microvilli-bearing cell/tissue types diversified will require further study of microvillar composition and development in disparate cell types and lineages. Of particular interest are the microvilli of choanoflagellates, ctenophores, and sponges, which collectively bracket the earliest events in animal evolution.

Copyright Date

7-12-2016

Copyright Statement / License for Reuse

Creative Commons Attribution 4.0 International License
This work is licensed under a Creative Commons Attribution 4.0 International License.

Rights Holder

The Authors

Provenance

Received from author

File Format

application/pdf

Language

English (eng)

Extent

15 pgs

File Size

6199 KB

Publication Statement

Copyright is held by the authors. User is responsible for all copyright compliance. This article was originally published as:

Peña, J. F., Alié, A., Richter, D. J., Wang, L., Funayama, N., & Nichols, S. A. (2016). Conserved expression of vertebrate microvillar gene homologs in choanocytes of freshwater sponges. EvoDevo, 7(1), 1-15. DOI: 10.1186/s13227-016-0050-x

Publication Title

EvoDevo

Volume

7

First Page

1

Last Page

15

ISSN

3091-3446

Included in

Biology Commons

Share

COinS