Origin and evolution of microvilli

Author:

Ansel Mylan123ORCID,Ramachandran Kaustubh2ORCID,Dey Gautam2,Brunet Thibaut1ORCID

Affiliation:

1. Institut Pasteur Université Paris‐Cité CNRS UMR3691 Evolutionary Cell Biology and Evolution of Morphogenesis Unit Paris France

2. Cell Biology and Biophysics European Molecular Biology Laboratory Heidelberg Germany

3. Master BioSciences, Département de Biologie Ecole Normale Supérieure de Lyon Lyon France

Abstract

AbstractBackground InformationMicrovilli are finger‐like, straight, and stable cellular protrusions that are filled with F‐actin and present a stereotypical length. They are present in a broad range of cell types across the animal tree of life and mediate several fundamental functions, including nutrient absorption, photosensation, and mechanosensation. Therefore, understanding the origin and evolution of microvilli is key to reconstructing the evolution of animal cellular form and function. Here, we review the current state of knowledge on microvilli evolution and perform a bioinformatic survey of the conservation of genes encoding microvillar proteins in animals and their unicellular relatives.ResultsWe first present a detailed description of mammalian microvilli based on two well‐studied examples, the brush border microvilli of enterocytes and the stereocilia of hair cells. We also survey the broader diversity of microvilli and discuss similarities and differences between microvilli and filopodia. Based on our bioinformatic survey coupled with carefully reconstructed molecular phylogenies, we reconstitute the order of evolutionary appearance of microvillar proteins. We document the stepwise evolutionary assembly of the “molecular microvillar toolkit” with notable bursts of innovation at two key nodes: the last common filozoan ancestor (correlated with the evolution of microvilli distinct from filopodia) and the last common choanozoan ancestor (correlated with the emergence of inter‐microvillar adhesions).Conclusion and SignificanceWe conclude with a scenario for the evolution of microvilli from filopodia‐like ancestral structures in unicellular precursors of animals.

Funder

European Research Council

Institut Pasteur

European Molecular Biology Laboratory

École Normale Supérieure de Lyon

Centre National de la Recherche Scientifique

Joachim Herz Stiftung

Publisher

Wiley

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4. Ansel M. Ramachandran K. Dey G.&Brunet T.(2024)Origin and evolution of microvilli. fishare. Online resource.https://doi.org/10.6084/M9.FIGSHARE.25828882.V2

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