Structural diversity and distribution of NMCP-class nuclear lamina proteins in streptophytic algae

Abstract

Nuclear Matrix Constituent Proteins (NMCPs) in plants function like animal lamins, providing the structural foundation of the nuclear lamina and regulating nuclear organization and morphology. Although they are well-characterized in angiosperms, the presence and structure of NMCPs in more distantly related species, such as streptophytic algae, are relatively unknown. The rapid evolution of NMCPs throughout the plant lineage has caused a divergence in protein sequence that makes similarity-based searches less effective. Structural features are more likely to be conserved compared to primary amino acid sequence; therefore, we developed a filtration protocol to search for diverged NMCPs based on four physical characteristics: intrinsically disordered content, isoelectric point, number of amino acids, and the presence of a central coiled-coil domain. By setting parameters to recognize the properties of bona fide NMCP proteins in angiosperms, we filtered eight complete proteomes from streptophytic algae species and identified strong NMCP candidates in six taxa in the Classes Zygnematophyceae, Charophyceae, and Klebsormidophyceae. Through analysis of these proteins, we observed structural variance in domain size between NMCPs in algae and land plants, as well as a single block of amino acid conservation. Our analysis indicates that NMCPs are absent in the Mesostigmatophyceae. The presence versus absence of NMCP proteins does not correlate with the distribution of different forms of mitosis (e.g., closed/semi-closed/open) but does correspond to the transition from unicellularity to multicellularity in the streptophytic algae, suggesting that an NMCP-based nucleoskeleton plays important roles in supporting cell-to-cell interactions. SIGNIFICANCE STATEMENTAll eukaryotic organisms contain a membrane-bound nucleus, which holds a cells DNA, but plants and animals have distinct sets of proteins that make up the mesh-like scaffold inside the nucleus (i.e., nuclear lamina) that is essential for structural integrity and organization. Nonetheless, the major nuclear lamina proteins in plants and animals share structural features, and we exploited these characteristics to identify a key class of nuclear lamina proteins in streptophytic algae, allowing us to chart the distribution of these proteins across photosynthetic organisms and to gain insight into the evolution of nuclear organization. Our results indicate that the major class of nuclear lamina protein in plants evolved independently from structurally similar nuclear lamina proteins in animals.