Glycogen synthase kinase 3 promotes multicellular development over unicellular encystation in encysting Dictyostelia

Yoshinori Kawabe, Takahiro Morio, Yoshimasa Tanaka, Pauline Schaap

Research output: Contribution to journalArticle

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Abstract

Background: Glycogen synthase kinase 3 (GSK3) regulates many cell fate decisions in animal development. In multicellular structures of the group 4 dictyostelid Dictyostelium discoideum, GSK3 promotes spore over stalk-like differentiation. We investigated whether, similar to other sporulation inducing genes such as cAMP dependent protein kinase (PKA), this role of GSK3 is derived from an ancestral role in encystation of unicellular amoebas.
Results: We deleted GSK3 in Polysphondylium pallidum, a group 2 dictyostelid which has retained encystation as an alternative survival strategy. Loss of GSK3 inhibited cytokinesis of cells in suspension, as also occurs in D. discoideum, but did not affect spore or stalk differentiation in P. pallidum. However, gsk3- amoebas entered into encystation under conditions that in wild-type favour aggregation and fruiting body formation. The gsk3- cells were hypersensitive to osmolytes, which are known to promote encystation, and to cyst inducing factors that are secreted during starvation. GSK3 was not itself regulated by these factors, but inhibited their effects.
Conclusions: Our data show that GSK3 has a deeply conserved role in controlling cytokinesis, but not spore differentiation in Dictyostelia. Instead, in P. pallidum, one of many Dictyostelia that like their solitary ancestors can still encyst to survive starvation, GSK3 promotes multicellular development into fruiting bodies over unicellular encystment.
Original languageEnglish
Article number12
Number of pages11
JournalEvoDevo
Volume9
Issue number1
DOIs
Publication statusPublished - 9 May 2018

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Glycogen Synthase Kinase 3
encystment
spore
fruiting
starvation
Globus Pallidus
sporulation
Spores
cyst
Dictyostelium discoideum
ancestry
Amoeba
Dictyostelium
Cytokinesis
spores
cytokinesis
fruiting bodies
Starvation
protein
gene

Keywords

  • Amoebozoa
  • Cell-type specialization
  • Dictyostelia
  • Encystment
  • Glycogen synthase kinase 3
  • Life cycle choice
  • Polysphondylium
  • Sporulation
  • Stress response

Cite this

@article{a1856f74406548ef885fd550d342346f,
title = "Glycogen synthase kinase 3 promotes multicellular development over unicellular encystation in encysting Dictyostelia",
abstract = "Background: Glycogen synthase kinase 3 (GSK3) regulates many cell fate decisions in animal development. In multicellular structures of the group 4 dictyostelid Dictyostelium discoideum, GSK3 promotes spore over stalk-like differentiation. We investigated whether, similar to other sporulation inducing genes such as cAMP dependent protein kinase (PKA), this role of GSK3 is derived from an ancestral role in encystation of unicellular amoebas. Results: We deleted GSK3 in Polysphondylium pallidum, a group 2 dictyostelid which has retained encystation as an alternative survival strategy. Loss of GSK3 inhibited cytokinesis of cells in suspension, as also occurs in D. discoideum, but did not affect spore or stalk differentiation in P. pallidum. However, gsk3- amoebas entered into encystation under conditions that in wild-type favour aggregation and fruiting body formation. The gsk3- cells were hypersensitive to osmolytes, which are known to promote encystation, and to cyst inducing factors that are secreted during starvation. GSK3 was not itself regulated by these factors, but inhibited their effects. Conclusions: Our data show that GSK3 has a deeply conserved role in controlling cytokinesis, but not spore differentiation in Dictyostelia. Instead, in P. pallidum, one of many Dictyostelia that like their solitary ancestors can still encyst to survive starvation, GSK3 promotes multicellular development into fruiting bodies over unicellular encystment.",
keywords = "Amoebozoa, Cell-type specialization, Dictyostelia, Encystment, Glycogen synthase kinase 3, Life cycle choice, Polysphondylium, Sporulation, Stress response",
author = "Yoshinori Kawabe and Takahiro Morio and Yoshimasa Tanaka and Pauline Schaap",
note = "The work was funded by BBSRC project grant BB/K000799/1 and ERC grant 742288.",
year = "2018",
month = "5",
day = "9",
doi = "10.1186/s13227-018-0101-6",
language = "English",
volume = "9",
journal = "EvoDevo",
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Glycogen synthase kinase 3 promotes multicellular development over unicellular encystation in encysting Dictyostelia. / Kawabe, Yoshinori; Morio, Takahiro; Tanaka, Yoshimasa; Schaap, Pauline.

In: EvoDevo, Vol. 9, No. 1, 12, 09.05.2018.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Glycogen synthase kinase 3 promotes multicellular development over unicellular encystation in encysting Dictyostelia

AU - Kawabe, Yoshinori

AU - Morio, Takahiro

AU - Tanaka, Yoshimasa

AU - Schaap, Pauline

N1 - The work was funded by BBSRC project grant BB/K000799/1 and ERC grant 742288.

PY - 2018/5/9

Y1 - 2018/5/9

N2 - Background: Glycogen synthase kinase 3 (GSK3) regulates many cell fate decisions in animal development. In multicellular structures of the group 4 dictyostelid Dictyostelium discoideum, GSK3 promotes spore over stalk-like differentiation. We investigated whether, similar to other sporulation inducing genes such as cAMP dependent protein kinase (PKA), this role of GSK3 is derived from an ancestral role in encystation of unicellular amoebas. Results: We deleted GSK3 in Polysphondylium pallidum, a group 2 dictyostelid which has retained encystation as an alternative survival strategy. Loss of GSK3 inhibited cytokinesis of cells in suspension, as also occurs in D. discoideum, but did not affect spore or stalk differentiation in P. pallidum. However, gsk3- amoebas entered into encystation under conditions that in wild-type favour aggregation and fruiting body formation. The gsk3- cells were hypersensitive to osmolytes, which are known to promote encystation, and to cyst inducing factors that are secreted during starvation. GSK3 was not itself regulated by these factors, but inhibited their effects. Conclusions: Our data show that GSK3 has a deeply conserved role in controlling cytokinesis, but not spore differentiation in Dictyostelia. Instead, in P. pallidum, one of many Dictyostelia that like their solitary ancestors can still encyst to survive starvation, GSK3 promotes multicellular development into fruiting bodies over unicellular encystment.

AB - Background: Glycogen synthase kinase 3 (GSK3) regulates many cell fate decisions in animal development. In multicellular structures of the group 4 dictyostelid Dictyostelium discoideum, GSK3 promotes spore over stalk-like differentiation. We investigated whether, similar to other sporulation inducing genes such as cAMP dependent protein kinase (PKA), this role of GSK3 is derived from an ancestral role in encystation of unicellular amoebas. Results: We deleted GSK3 in Polysphondylium pallidum, a group 2 dictyostelid which has retained encystation as an alternative survival strategy. Loss of GSK3 inhibited cytokinesis of cells in suspension, as also occurs in D. discoideum, but did not affect spore or stalk differentiation in P. pallidum. However, gsk3- amoebas entered into encystation under conditions that in wild-type favour aggregation and fruiting body formation. The gsk3- cells were hypersensitive to osmolytes, which are known to promote encystation, and to cyst inducing factors that are secreted during starvation. GSK3 was not itself regulated by these factors, but inhibited their effects. Conclusions: Our data show that GSK3 has a deeply conserved role in controlling cytokinesis, but not spore differentiation in Dictyostelia. Instead, in P. pallidum, one of many Dictyostelia that like their solitary ancestors can still encyst to survive starvation, GSK3 promotes multicellular development into fruiting bodies over unicellular encystment.

KW - Amoebozoa

KW - Cell-type specialization

KW - Dictyostelia

KW - Encystment

KW - Glycogen synthase kinase 3

KW - Life cycle choice

KW - Polysphondylium

KW - Sporulation

KW - Stress response

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U2 - 10.1186/s13227-018-0101-6

DO - 10.1186/s13227-018-0101-6

M3 - Article

C2 - 29760875

VL - 9

JO - EvoDevo

JF - EvoDevo

SN - 2041-9139

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