Earliest Holozoan Expansion of Phosphotyrosine Signaling

Phosphotyrosine (pTyr) signaling is involved in development and maintenance of metazoans’ multicellular body through cell-to-cell communication. Tyrosine kinases (TKs), tyrosine phosphatases, and other proteins relaying the signal compose the cascade. Domain architectures of the pTyr signaling prote...

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Main Authors: Suga, Hiroshi, Torruella, Guifré, Burger, Gertraud, Brown, Matthew W., Ruiz-Trillo, Iñaki
Format: Online
Language:English
Published: 2013
Online Access:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4342544/
id pubmed-4342544
recordtype oai_dc
spelling pubmed-43425442015-02-27 Earliest Holozoan Expansion of Phosphotyrosine Signaling Suga, Hiroshi Torruella, Guifré Burger, Gertraud Brown, Matthew W. Ruiz-Trillo, Iñaki Article Phosphotyrosine (pTyr) signaling is involved in development and maintenance of metazoans’ multicellular body through cell-to-cell communication. Tyrosine kinases (TKs), tyrosine phosphatases, and other proteins relaying the signal compose the cascade. Domain architectures of the pTyr signaling proteins are diverse in metazoans, reflecting their complex intercellular communication. Previous studies had shown that the metazoan-type TKs, as well as other pTyr signaling proteins, were already diversified in the common ancestor of metazoans, choanoflagellates, and filastereans (which are together included in the clade Holozoa) whereas they are absent in fungi and other nonholozoan lineages. However, the earliest-branching holozoans Ichthyosporea and Corallochytrea, as well as the two fungi-related amoebae Fonticula and Nuclearia, have not been studied. Here, we analyze the complete genome sequences of two ichthyosporeans and Fonticula, and RNAseq data of three additional ichthyosporeans, one corallochytrean, and Nuclearia. Both the ichthyosporean and corallochytrean genomes encode a large variety of receptor TKs (RTKs) and cytoplasmic TKs (CTKs), as well as other pTyr signaling components showing highly complex domain architectures. However, Nuclearia and Fonticula have no TK, and show much less diversity in other pTyr signaling components. The CTK repertoires of both Ichthyosporea and Corallochytrea are similar to those of Metazoa, Choanoflagellida, and Filasterea, but the RTK sets are totally different from each other. The complex pTyr signaling equipped with positive/negative feedback mechanism likely emerged already at an early stage of holozoan evolution, yet keeping a high evolutionary plasticity in extracellular signal reception until the co-option of the system for cell-to-cell communication in metazoans. 2013-12-03 2014-03 /pmc/articles/PMC4342544/ /pubmed/24307687 http://dx.doi.org/10.1093/molbev/mst241 Text en © The Author 2013. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com.
repository_type Open Access Journal
institution_category Foreign Institution
institution US National Center for Biotechnology Information
building NCBI PubMed
collection Online Access
language English
format Online
author Suga, Hiroshi
Torruella, Guifré
Burger, Gertraud
Brown, Matthew W.
Ruiz-Trillo, Iñaki
spellingShingle Suga, Hiroshi
Torruella, Guifré
Burger, Gertraud
Brown, Matthew W.
Ruiz-Trillo, Iñaki
Earliest Holozoan Expansion of Phosphotyrosine Signaling
author_facet Suga, Hiroshi
Torruella, Guifré
Burger, Gertraud
Brown, Matthew W.
Ruiz-Trillo, Iñaki
author_sort Suga, Hiroshi
title Earliest Holozoan Expansion of Phosphotyrosine Signaling
title_short Earliest Holozoan Expansion of Phosphotyrosine Signaling
title_full Earliest Holozoan Expansion of Phosphotyrosine Signaling
title_fullStr Earliest Holozoan Expansion of Phosphotyrosine Signaling
title_full_unstemmed Earliest Holozoan Expansion of Phosphotyrosine Signaling
title_sort earliest holozoan expansion of phosphotyrosine signaling
description Phosphotyrosine (pTyr) signaling is involved in development and maintenance of metazoans’ multicellular body through cell-to-cell communication. Tyrosine kinases (TKs), tyrosine phosphatases, and other proteins relaying the signal compose the cascade. Domain architectures of the pTyr signaling proteins are diverse in metazoans, reflecting their complex intercellular communication. Previous studies had shown that the metazoan-type TKs, as well as other pTyr signaling proteins, were already diversified in the common ancestor of metazoans, choanoflagellates, and filastereans (which are together included in the clade Holozoa) whereas they are absent in fungi and other nonholozoan lineages. However, the earliest-branching holozoans Ichthyosporea and Corallochytrea, as well as the two fungi-related amoebae Fonticula and Nuclearia, have not been studied. Here, we analyze the complete genome sequences of two ichthyosporeans and Fonticula, and RNAseq data of three additional ichthyosporeans, one corallochytrean, and Nuclearia. Both the ichthyosporean and corallochytrean genomes encode a large variety of receptor TKs (RTKs) and cytoplasmic TKs (CTKs), as well as other pTyr signaling components showing highly complex domain architectures. However, Nuclearia and Fonticula have no TK, and show much less diversity in other pTyr signaling components. The CTK repertoires of both Ichthyosporea and Corallochytrea are similar to those of Metazoa, Choanoflagellida, and Filasterea, but the RTK sets are totally different from each other. The complex pTyr signaling equipped with positive/negative feedback mechanism likely emerged already at an early stage of holozoan evolution, yet keeping a high evolutionary plasticity in extracellular signal reception until the co-option of the system for cell-to-cell communication in metazoans.
publishDate 2013
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4342544/
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