The evolution of aggregative multicellularity and cell-cell communication in the Dictyostelia

Research output: Contribution to journalArticle

34 Citations (Scopus)
89 Downloads (Pure)

Abstract

Aggregative multicellularity, resulting in formation of a spore-bearing fruiting body, evolved at least six times independently amongst both eukaryotes and prokaryotes. Amongst eukaryotes, this form of multicellularity is mainly studied in the social amoeba Dictyostelium discoideum. In this review, we summarise trends in the evolution of cell-type specialisation and behavioural complexity in the four major groups of Dictyostelia. We describe the cell-cell communication systems that control the developmental programme of D. discoideum, highlighting the central role of cAMP in the regulation of cell movement and cell differentiation. Comparative genomic studies showed that the proteins involved in cAMP signalling are deeply conserved across Dictyostelia and their unicellular amoebozoan ancestors. Comparative functional analysis revealed that cAMP signalling in D. discoideum originated from a second messenger role in amoebozoan encystation. We highlight some molecular changes in cAMP signalling genes that were responsible for the novel roles of cAMP in multicellular development.

Original languageEnglish
Pages (from-to)3722-3733
Number of pages12
JournalJournal of Molecular Biology
Volume427
Issue number23
Early online date15 Aug 2015
DOIs
Publication statusPublished - 20 Nov 2015

Fingerprint

Dictyostelium
Cell Communication
Eukaryota
Amoeba
Second Messenger Systems
Spores
Cell Movement
Cell Differentiation
Genes
Proteins

Keywords

  • Cyclic nucleotide
  • Dual component signalling
  • Encystation
  • Evolution of multicellularity
  • Sporulation

Cite this

@article{0d67976fe4154ef1b0a7b9ca9c28221a,
title = "The evolution of aggregative multicellularity and cell-cell communication in the Dictyostelia",
abstract = "Aggregative multicellularity, resulting in formation of a spore-bearing fruiting body, evolved at least six times independently amongst both eukaryotes and prokaryotes. Amongst eukaryotes, this form of multicellularity is mainly studied in the social amoeba Dictyostelium discoideum. In this review, we summarise trends in the evolution of cell-type specialisation and behavioural complexity in the four major groups of Dictyostelia. We describe the cell-cell communication systems that control the developmental programme of D. discoideum, highlighting the central role of cAMP in the regulation of cell movement and cell differentiation. Comparative genomic studies showed that the proteins involved in cAMP signalling are deeply conserved across Dictyostelia and their unicellular amoebozoan ancestors. Comparative functional analysis revealed that cAMP signalling in D. discoideum originated from a second messenger role in amoebozoan encystation. We highlight some molecular changes in cAMP signalling genes that were responsible for the novel roles of cAMP in multicellular development.",
keywords = "Cyclic nucleotide, Dual component signalling, Encystation, Evolution of multicellularity, Sporulation",
author = "Qingyou Du and Yoshinori Kawabe and Christina Schilde and Zhi-hui Chen and Pauline Schaap",
year = "2015",
month = "11",
day = "20",
doi = "10.1016/j.jmb.2015.08.008",
language = "English",
volume = "427",
pages = "3722--3733",
journal = "Journal of Molecular Biology",
issn = "0022-2836",
publisher = "Elsevier",
number = "23",

}

TY - JOUR

T1 - The evolution of aggregative multicellularity and cell-cell communication in the Dictyostelia

AU - Du, Qingyou

AU - Kawabe, Yoshinori

AU - Schilde, Christina

AU - Chen, Zhi-hui

AU - Schaap, Pauline

PY - 2015/11/20

Y1 - 2015/11/20

N2 - Aggregative multicellularity, resulting in formation of a spore-bearing fruiting body, evolved at least six times independently amongst both eukaryotes and prokaryotes. Amongst eukaryotes, this form of multicellularity is mainly studied in the social amoeba Dictyostelium discoideum. In this review, we summarise trends in the evolution of cell-type specialisation and behavioural complexity in the four major groups of Dictyostelia. We describe the cell-cell communication systems that control the developmental programme of D. discoideum, highlighting the central role of cAMP in the regulation of cell movement and cell differentiation. Comparative genomic studies showed that the proteins involved in cAMP signalling are deeply conserved across Dictyostelia and their unicellular amoebozoan ancestors. Comparative functional analysis revealed that cAMP signalling in D. discoideum originated from a second messenger role in amoebozoan encystation. We highlight some molecular changes in cAMP signalling genes that were responsible for the novel roles of cAMP in multicellular development.

AB - Aggregative multicellularity, resulting in formation of a spore-bearing fruiting body, evolved at least six times independently amongst both eukaryotes and prokaryotes. Amongst eukaryotes, this form of multicellularity is mainly studied in the social amoeba Dictyostelium discoideum. In this review, we summarise trends in the evolution of cell-type specialisation and behavioural complexity in the four major groups of Dictyostelia. We describe the cell-cell communication systems that control the developmental programme of D. discoideum, highlighting the central role of cAMP in the regulation of cell movement and cell differentiation. Comparative genomic studies showed that the proteins involved in cAMP signalling are deeply conserved across Dictyostelia and their unicellular amoebozoan ancestors. Comparative functional analysis revealed that cAMP signalling in D. discoideum originated from a second messenger role in amoebozoan encystation. We highlight some molecular changes in cAMP signalling genes that were responsible for the novel roles of cAMP in multicellular development.

KW - Cyclic nucleotide

KW - Dual component signalling

KW - Encystation

KW - Evolution of multicellularity

KW - Sporulation

UR - http://www.scopus.com/record/display.uri?eid=2-s2.0-84947616340&origin=resultslist&sort=plf-f&src=s&st1=The+evolution+of+aggregative+multicellularity+and+cell-cell+communication+in+the+Dictyostelia&st2=&sid=9BE9E5CB762CDB49C6F894B3D30F1256.I0QkgbIjGqqLQ4Nw7dqZ4A%3a150&sot=b&sdt=b&sl=108&s=TITLE-ABS-KEY%28The+evolution+of+aggregative+multicellularity+and+cell-cell+communication+in+the+Dictyostelia%29&relpos=0&citeCnt=1&searchTerm=TITLE-ABS-KEY%28The+evolution+of+aggregative+multicellularity+and+cell-cell+communication+in+the+Dictyostelia%29

U2 - 10.1016/j.jmb.2015.08.008

DO - 10.1016/j.jmb.2015.08.008

M3 - Article

C2 - 26284972

VL - 427

SP - 3722

EP - 3733

JO - Journal of Molecular Biology

JF - Journal of Molecular Biology

SN - 0022-2836

IS - 23

ER -