4.7 Article

Identification of Evolutionarily Conserved Nuclear Matrix Proteins and Their Prokaryotic Origins

Journal

JOURNAL OF PROTEOME RESEARCH
Volume 20, Issue 1, Pages 518-530

Publisher

AMER CHEMICAL SOC
DOI: 10.1021/acs.jproteome.0c00550

Keywords

nuclear matrix; nucleoskeleton; nuclear evolution; eukaryote evolution; LECA; core proteome

Funding

  1. Department of Biotechnology (DBT)
  2. Council for Scientific and Industrial Research (CSIR)
  3. CSIR

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By studying the developing embryos of Drosophila melanogaster and Danio rerio, 362 core NuMat proteins conserved between the two organisms were identified. Comparisons with publicly available Mus musculus NuMat dataset and Homo sapiens cellular localization dataset revealed 252 core homologous NuMat proteins, with 86 protein groups originating from preexisting proteins in prokaryotes. Thirty-six were conserved across all eukaryotic supergroups, 14 evolved before the last eukaryotic common ancestor, and these 50 proteins out of the 252 core conserved NuMat proteins have been conserved across all eukaryotes for over 1.5 billion years, indicating their crucial role in nuclear function.
Compared to prokaryotic cells, a typical eukaryotic cell is much more complex along with its endomembrane system and membrane-bound organelles. Although the endosymbiosis theories convincingly explain the evolution of membrane-bound organelles such as mitochondria and chloroplasts, very little is understood about the evolutionary origins of the nucleus, the defining feature of eukaryotes. Most studies on nuclear evolution have not been able to take into consideration the underlying structural framework of the nucleus, attributed to the nuclear matrix (NuMat), a ribonucleoproteinaceous structure. This can largely be attributed to the lack of annotation of its core components. Since NuMat has been shown to provide a structural platform for facilitating a variety of nuclear functions such as replication, transcription, and splicing, it is important to identify its protein components to better understand these processes. In this study, we address this issue using the developing embryos of Drosophila melanogaster and Danio rerio and identify 362 core NuMat proteins that are conserved between the two organisms. We further compare our results with publicly available Mus musculus NuMat dataset and Homo sapiens cellular localization dataset to define the core homologous NuMat proteins consisting of 252 proteins. We find that of them, 86 protein groups have originated from preexisting proteins in prokaryotes. While 36 were conserved across all eukaryotic supergroups, 14 new proteins evolved before the evolution of the last eukaryotic common ancestor and together, these 50 proteins out of the 252 core conserved NuMat proteins are conserved across all eukaryotes, indicating their indispensable nature for nuclear function for over 1.5 billion years of eukaryotic history. Our analysis paves the way to understand the evolution of the complex internal nuclear architecture and its functions.

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