The Physarum polycephalum Genome Reveals Extensive Use of Prokaryotic Two-Component and Metazoan-Type Tyrosine Kinase Signaling

Pauline Schaap, Israel Barrantes, Pat Minx, Narie Sasaki, Roger W. Anderson, Marianne Bénard, Kyle K. Biggar, Nicolas E. Buchler, Ralf Bundschuh, Xiao Chen, Catrina Fronick, Lucinda Fulton, Georg Golderer, Niels Jahn, Volker Knoop, Laura F. Landweber, Chrystelle Maric, Dennis Miller, Angelika A. Noegel, Rob PeaceGérard Pierron, Taeko Sasaki, Mareike Schallenberg-Rüdinger, Michael Schleicher, Reema Singh, Thomas Spaller, Kenneth B. Storey, Takamasa Suzuki, Chad Tomlinson, John J. Tyson, Wesley C. Warren, Ernst R. Werner, Gabriele Werner-Felmayer, Richard K. Wilson, Thomas Winckler, Jonatha M. Gott, Gernot Glöckner, Wolfgang Marwan

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Abstract

Physarum polycephalum is a well-studied microbial eukaryote with unique experimental attributes relative to other experimental model organisms. It has a sophisticated life cycle with several distinct stages including amoebal, flagellated, and plasmodial cells. It is unusual in switching between open and closed mitosis according to specific life-cycle stages. Here we present the analysis of the genome of this enigmatic and important model organism and compare it with closely related species. The genome is littered with simple and complex repeats and the coding regions are frequently interrupted by introns with a mean size of 100 bases. Complemented with extensive transcriptome data, we define approximately 31,000 gene loci, providing unexpected insights into early eukaryote evolution. We describe extensive use of histidine kinase-based two-component systems and tyrosine kinase signaling, the presence of bacterial and plant type photoreceptors (phytochromes, cryptochrome, and phototropin) and of plant-type pentatricopeptide repeat proteins, as well as metabolic pathways, and a cell cycle control system typically found in more complex eukaryotes. Our analysis characterizes P. polycephalum as a prototypical eukaryote with features attributed to the last common ancestor of Amorphea, that is, the Amoebozoa and Opisthokonts. Specifically, the presence of tyrosine kinases in Acanthamoeba and Physarum as representatives of two distantly related subdivisions of Amoebozoa argues against the later emergence of tyrosine kinase signaling in the opisthokont lineage and also against the acquisition by horizontal gene transfer.
Original languageEnglish
Pages (from-to)109-125
Number of pages17
JournalGenome Biology and Evolution
Volume8
Issue number1
Early online date27 Nov 2015
DOIs
Publication statusPublished - Jan 2016

Keywords

  • Amoebozoa
  • Tyrosine kinase receptor
  • two-component system
  • Signaling
  • phytochrome

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    Schaap, P., Barrantes, I., Minx, P., Sasaki, N., Anderson, R. W., Bénard, M., Biggar, K. K., Buchler, N. E., Bundschuh, R., Chen, X., Fronick, C., Fulton, L., Golderer, G., Jahn, N., Knoop, V., Landweber, L. F., Maric, C., Miller, D., Noegel, A. A., ... Marwan, W. (2016). The Physarum polycephalum Genome Reveals Extensive Use of Prokaryotic Two-Component and Metazoan-Type Tyrosine Kinase Signaling. Genome Biology and Evolution, 8(1), 109-125. https://doi.org/10.1093/gbe/evv237