Ancient eukaryotic origin and evolutionary plasticity of nuclear lamina

Abstract

The emergence of the nucleus was a major event of eukaryogenesis. How the nuclear envelope (NE) arose and acquired functions governing chromatin organization and epigenetic control has direct bearing on origins of developmental/stage-specific expression programs. The configuration of the NE and the associated lamina in the last eukaryotic common ancestor (LECA) is of major significance andcanprovide insight intoactivities within theLECAnucleus.Subsequent laminaevolution, alterations,andadaptations inform on the variation and selection of distinct mechanisms that subtend gene expression in distinct taxa. Understanding lamina evolutionhasbeendifficultdueto thediversityandlimited taxonomicdistributions of the three currently knownhighlydistinctnuclear lamina. We rigorously searched available sequence data for an expanded view of the distribution of known lamina and laminaassociated proteins.While the lamina proteins of plants and trypanosomes are indeed taxonomically restricted, homologs of metazoan lamins and key lamin-binding proteins have significantly broader distributions, and a lamin gene tree supports vertical evolution from the LECA. Two protist lamins from highly divergent taxa target the nucleus inmammalian cells and polymerize into filamentous structures, suggesting functional conservation of distant lamin homologs. Significantly, a high level of divergence of lamin homologs within certain eukaryotic groups and the apparent absence of lamins and/or the presence of seemingly different lamina proteins in many eukaryotes suggests great evolutionary plasticity in structures at the NE, and hence mechanisms of chromatin tethering and epigenetic gene control.