Nuclear actin: ancient clue to evolution in eukaryotes?

Abstract

Until recently it was widely accepted that the dynamic cytoskeletal matrix is exclusive to the cytoplasm of eukaryotes, evolving before the emergence of the cell nucleus to enable phagocytosis, cell motility and the sophisticated functioning of the endomembrane system within the cytosol. The discovery of the existence of a prokaryotic cytoskeleton has changed this picture significantly. As a result, the idea has taken shape that the appearance of actin occurred in the very first cell; therefore, the emergence of microfilaments precedes that of the eukaryotic cytoskeleton. The discovery of nuclear actin opened new perspective on the field, suggesting that the nuclear activities of actin reflect the functions of primordial actin-like proteins. In this paper, we review the recent literature to explore the evolutionary origin of nuclear actin. We conclude that both ancient and eukaryotic features of the actin world can be detected in the nucleus today, which supports the idea that the cytoskeleton attained significant eukaryotic innovations before the tandem evolution of the cytoskeleton and nucleus occurred.

The Cytoskeleton—A Complex Interacting Meshwork

“…This is in agreement with two studies demonstrating an association of actin and Arp2/3 with sites of DNA damage and decreased damage repair after reduced Arp2/3 dependent actin nucleation [198,199]. For more information on the role of actin in the nucleus the interested reader is referred to other reviews [188,200].…”

“…As in the cytoplasm, nuclear actin exists in a monomeric and polymeric form [187]. Nuclear G-actin was shown to associate with all three RNA polymerases, participating in transcription initiation and elongation [188]. The exact function of G-actin in the transcription complex remains unclear, but G-actin levels need to be precisely tuned for normal translation [189] and cofilin is required for its elongation [190].…”

Giant viruses encode novel types of actins possibly related to the origin of eukaryotic actin: the viractins

“…Different authors previously emphasized a possible evolutionary relationship between the eukaryotic nucleus and NCLDV viral factories 22,23 . In this context, it is interesting to note that actin is present in both the cytoplasm and nucleus of eukaryotic cells and that, in collaboration with nuclear ARPs, seems to be involved in several nuclear-related processes 24 . The viral eukaryogenesis hypotheses, which attribute various roles in the emergence of eukaryotes to viruses, have notably been recently boosted by the discovery of Caudovirales lineages producing a nucleus-like structure within infected bacterial cells 25 .…”

In focus in HCB

“…In their review on Nuclear actin, Bajusz et al (2018) analyze the aspects of the evolutionary history and ancient functions of actin as they relate to the development of the nucleus, and critically evaluate the diverse biological functions of nuclear actin and their underlying molecular mechanisms. The function of monomeric actin in transcription and its association with different chromatin-remodeling complexes is highlighted.…”