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 Peace & 18 others Gérard 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

Fingerprint

Physarum polycephalum
metazoan
eukaryote
Eukaryota
Protein-Tyrosine Kinases
tyrosine
eukaryotic cells
Amoebozoa
phosphotransferases (kinases)
genome
Genome
Life Cycle Stages
Plant Photoreceptors
Phototropins
life cycle
Physarum
Cryptochromes
Phytochrome
Acanthamoeba
histidine kinase

Keywords

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

Cite this

Schaap, Pauline ; Barrantes, Israel ; Minx, Pat ; Sasaki, Narie ; Anderson, Roger W. ; Bénard, Marianne ; Biggar, Kyle K. ; Buchler, Nicolas E. ; Bundschuh, Ralf ; Chen, Xiao ; Fronick, Catrina ; Fulton, Lucinda ; Golderer, Georg ; Jahn, Niels ; Knoop, Volker ; Landweber, Laura F. ; Maric, Chrystelle ; Miller, Dennis ; Noegel, Angelika A. ; Peace, Rob ; Pierron, Gérard ; Sasaki, Taeko ; Schallenberg-Rüdinger, Mareike ; Schleicher, Michael ; Singh, Reema ; Spaller, Thomas ; Storey, Kenneth B. ; Suzuki, Takamasa ; Tomlinson, Chad ; Tyson, John J. ; Warren, Wesley C. ; Werner, Ernst R. ; Werner-Felmayer, Gabriele ; Wilson, Richard K. ; Winckler, Thomas ; Gott, Jonatha M. ; Glöckner, Gernot ; Marwan, Wolfgang. / The Physarum polycephalum Genome Reveals Extensive Use of Prokaryotic Two-Component and Metazoan-Type Tyrosine Kinase Signaling. In: Genome Biology and Evolution. 2016 ; Vol. 8, No. 1. pp. 109-125.
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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.",
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author = "Pauline Schaap and Israel Barrantes and Pat Minx and Narie Sasaki and Anderson, {Roger W.} and Marianne B{\'e}nard and Biggar, {Kyle K.} and Buchler, {Nicolas E.} and Ralf Bundschuh and Xiao Chen and Catrina Fronick and Lucinda Fulton and Georg Golderer and Niels Jahn and Volker Knoop and Landweber, {Laura F.} and Chrystelle Maric and Dennis Miller and Noegel, {Angelika A.} and Rob Peace and G{\'e}rard Pierron and Taeko Sasaki and Mareike Schallenberg-R{\"u}dinger and Michael Schleicher and Reema Singh and Thomas Spaller and Storey, {Kenneth B.} and Takamasa Suzuki and Chad Tomlinson and Tyson, {John J.} and Warren, {Wesley C.} and Werner, {Ernst R.} and Gabriele Werner-Felmayer and Wilson, {Richard K.} and Thomas Winckler and Gott, {Jonatha M.} and Gernot Gl{\"o}ckner and Wolfgang Marwan",
note = "Funding for the sequence characterization of the P. polycephalum genome was provided by National Institutes of Health (NIH) grant HG003079 to R.K.W. and The Genome Institute at Washington University School of Medicine. P.S. received funding from the Wellcome Trust (100293/Z/12/Z) and the BBSRC BB/K000799/1. I.B. was supported by the International Max Planck Research School, Magdeburg. W.M. received funding from the German Federal Ministry of Education and Research (BMBF) via the FORSYS program FKZ 0313922. Pteridine work was funded by the Austrian Science Fund (FWF), P22406 to E.R.W. J.M.G. was funded by National Institutes of Health (NIH) grant GM54663 and National Science Foundation (NSF) grant MCB-1243687.",
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Schaap, P, Barrantes, I, Minx, P, Sasaki, N, Anderson, RW, Bénard, M, Biggar, KK, Buchler, NE, Bundschuh, R, Chen, X, Fronick, C, Fulton, L, Golderer, G, Jahn, N, Knoop, V, Landweber, LF, Maric, C, Miller, D, Noegel, AA, Peace, R, Pierron, G, Sasaki, T, Schallenberg-Rüdinger, M, Schleicher, M, Singh, R, Spaller, T, Storey, KB, Suzuki, T, Tomlinson, C, Tyson, JJ, Warren, WC, Werner, ER, Werner-Felmayer, G, Wilson, RK, Winckler, T, Gott, JM, Glöckner, G & Marwan, W 2016, 'The Physarum polycephalum Genome Reveals Extensive Use of Prokaryotic Two-Component and Metazoan-Type Tyrosine Kinase Signaling', Genome Biology and Evolution, vol. 8, no. 1, pp. 109-125. https://doi.org/10.1093/gbe/evv237

The Physarum polycephalum Genome Reveals Extensive Use of Prokaryotic Two-Component and Metazoan-Type Tyrosine Kinase Signaling. / Schaap, Pauline; Barrantes, Israel; Minx, Pat; Sasaki, Narie; Anderson, Roger W.; Bénard, Marianne; Biggar, Kyle K.; Buchler, Nicolas E.; Bundschuh, Ralf; Chen, Xiao; Fronick, Catrina; Fulton, Lucinda; Golderer, Georg; Jahn, Niels; Knoop, Volker; Landweber, Laura F.; Maric, Chrystelle; Miller, Dennis; Noegel, Angelika A.; Peace, Rob; Pierron, Gérard; Sasaki, Taeko; Schallenberg-Rüdinger, Mareike; Schleicher, Michael; Singh, Reema; Spaller, Thomas; Storey, Kenneth B.; Suzuki, Takamasa; Tomlinson, Chad; Tyson, John J.; Warren, Wesley C.; Werner, Ernst R.; Werner-Felmayer, Gabriele; Wilson, Richard K.; Winckler, Thomas; Gott, Jonatha M.; Glöckner, Gernot; Marwan, Wolfgang (Lead / Corresponding author).

In: Genome Biology and Evolution, Vol. 8, No. 1, 01.2016, p. 109-125.

Research output: Contribution to journalArticle

TY - JOUR

T1 - The Physarum polycephalum Genome Reveals Extensive Use of Prokaryotic Two-Component and Metazoan-Type Tyrosine Kinase Signaling

AU - Schaap, Pauline

AU - Barrantes, Israel

AU - Minx, Pat

AU - Sasaki, Narie

AU - Anderson, Roger W.

AU - Bénard, Marianne

AU - Biggar, Kyle K.

AU - Buchler, Nicolas E.

AU - Bundschuh, Ralf

AU - Chen, Xiao

AU - Fronick, Catrina

AU - Fulton, Lucinda

AU - Golderer, Georg

AU - Jahn, Niels

AU - Knoop, Volker

AU - Landweber, Laura F.

AU - Maric, Chrystelle

AU - Miller, Dennis

AU - Noegel, Angelika A.

AU - Peace, Rob

AU - Pierron, Gérard

AU - Sasaki, Taeko

AU - Schallenberg-Rüdinger, Mareike

AU - Schleicher, Michael

AU - Singh, Reema

AU - Spaller, Thomas

AU - Storey, Kenneth B.

AU - Suzuki, Takamasa

AU - Tomlinson, Chad

AU - Tyson, John J.

AU - Warren, Wesley C.

AU - Werner, Ernst R.

AU - Werner-Felmayer, Gabriele

AU - Wilson, Richard K.

AU - Winckler, Thomas

AU - Gott, Jonatha M.

AU - Glöckner, Gernot

AU - Marwan, Wolfgang

N1 - Funding for the sequence characterization of the P. polycephalum genome was provided by National Institutes of Health (NIH) grant HG003079 to R.K.W. and The Genome Institute at Washington University School of Medicine. P.S. received funding from the Wellcome Trust (100293/Z/12/Z) and the BBSRC BB/K000799/1. I.B. was supported by the International Max Planck Research School, Magdeburg. W.M. received funding from the German Federal Ministry of Education and Research (BMBF) via the FORSYS program FKZ 0313922. Pteridine work was funded by the Austrian Science Fund (FWF), P22406 to E.R.W. J.M.G. was funded by National Institutes of Health (NIH) grant GM54663 and National Science Foundation (NSF) grant MCB-1243687.

PY - 2016/1

Y1 - 2016/1

N2 - 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.

AB - 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.

KW - Amoebozoa

KW - Tyrosine kinase receptor

KW - two-component system

KW - Signaling

KW - phytochrome

U2 - 10.1093/gbe/evv237

DO - 10.1093/gbe/evv237

M3 - Article

VL - 8

SP - 109

EP - 125

JO - Genome Biology and Evolution

JF - Genome Biology and Evolution

SN - 1759-6653

IS - 1

ER -