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Glycogen Synthase Kinase 3 Promotes Multicellular Development Over Kawabe et al. EvoDevo (2018) 9:12 https://doi.org/10.1186/s13227-018-0101-6 EvoDevo RESEARCH Open Access Glycogen synthase kinase 3 promotes multicellular development over unicellular encystation in encysting Dictyostelia Yoshinori Kawabe1,2* , Takahiro Morio2, Yoshimasa Tanaka2 and Pauline Schaap1 Abstract Background: Glycogen synthase kinase 3 (GSK3) regulates many cell fate decisions in animal development. In mul- ticellular structures of the group 4 dictyostelid Dictyostelium discoideum, GSK3 promotes spore over stalk-like diferen- tiation. 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 afect spore or stalk diferentiation 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 efects. Conclusions: Our data show that GSK3 has a deeply conserved role in controlling cytokinesis, but not spore diferen- tiation 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: Encystment, Sporulation, Stress response, Polysphondylium, Life cycle choice, Glycogen synthase kinase 3, Cell-type specialization, Amoebozoa, Dictyostelia Background was lost in group 4, which contains the model organism Many unicellular protists, including Amoebozoa, sur- Dictyostelium discoideum [3, 4]. In D. discoideum, both vive adverse conditions by shutting down metabolism secreted and intracellular cyclic AMP (cAMP) play major and diferentiating into a walled cyst. Cysts are extremely roles in regulating the multicellular developmental pro- resilient, which, in case of amoeba pathogens, prevents gramme. Secreted cAMP, acting on G-protein-coupled their eradication by immune clearance or antibiotics [1, cAMP receptors (cARs), acts as a chemoattractant to 2]. Te multicellular Dictyostelia, members of Amoebo- coordinate aggregation and morphogenesis, and addi- zoa, evolved an additional strategy to survive starvation tionally induces prespore diferentiation, while inhibiting stress, in which amoebas aggregate to form a multicellu- stalk diferentiation. Intracellular cAMP, acting on PKA, lar fruiting structure and diferentiate into walled spores triggers the maturation of spore and stalk cells and keeps and stalk cells. Dictyostelia can be subdivided into four spore dormant in the fruiting body. cAMP is synthe- major groups, and while many species in groups 1–3 have sized by the adenylate cyclases ACA, ACR and ACG, but retained encystation as an alternative survival strategy, it intracellular levels are critically regulated by the cAMP phosphodiesterase RegA. RegA is activated/inhibited by *Correspondence: [email protected] sensor histidine kinases/phosphatases, which are the tar- 1 School of Life Sciences, University of Dundee, MSI/WTB Complex, Dow gets for signals that control timely spore and stalk matu- Street, Dundee DD15EH, UK ration and spore germination [5, 6]. Full list of author information is available at the end of the article © The Author(s) 2018. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat​iveco​mmons​.org/licen​ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creat​iveco​mmons​.org/ publi​cdoma​in/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Kawabe et al. EvoDevo (2018) 9:12 Page 2 of 11 Comparative functional analysis of PKA, ACR, ACG inverse PCR with primer pair GSKINV1 and GSKINV2 and RegA in the group 2 Dictyostelid Polysphondylium (Additional fle 1: Table 1), using religated HindIII or pallidum and the solitary amoebozoan pathogen Acan- BglII-digested Pp gDNA as template, respectively. All thamoeba castellani revealed that the intracellular role of PCR products were subcloned in pBluescript II KS cAMP in spore and stalk maturation and spore dormancy (-) (Stratagene) or pCR4-XL-TOPO (Invitrogen) and is evolutionary derived from a second messenger role in sequenced. stress-induced encystation [7–11]. PKA, ACR and RegA To determine the nucleotide sequence of the Pp GSK3 are deeply conserved in Amoebozoa, and their sequenced mRNAs, polyA+ RNA was isolated from Pp cells. Full- genomes contain many sensor histidine kinase/phos- length cDNAs were subsequently synthesized by RNA- phatases, which could act as food/stress sensors, respec- ligation-mediated rapid amplifcation of 5′ and 3′ cDNA tively, to regulate RegA [12, 13]. ends (RLM-RACE) and RT-PCR using the GeneRacer kit While PKA is required for both the spore and stalk (Invitrogen) according to the manufacturer’s instructions. cell diferentiation pathways, glycogen synthase kinase 3 (GSK3), a component of the wnt/wingless pathway that DNA constructs and transformation regulates many cell fate decisions in metazoa [14, 15], is Vectors for GSK3 gene disruption in D. discoideum considered to selectively promote pre- Partial GSK3 sequence with 2.2-kb 5′ UTR and 2.9-kb 3′ spore over prestalk diferentiation as target for secreted UTR was amplifed by inverse PCR from EcoRI-digested cAMP, which activates GSK3 [16, 17]. We are interested and religated Pp gDNA, using primers GSKINV3 and in expanding the range of encystation-inducing proteins GSKINV4 (Additional fle 1: Table 1) which contain that could act as therapeutic targets to prevent encysta- KpnI sites. Te KpnI-digested PCR product was cloned tion of pathogens. We therefore investigated whether, into KpnI-digested pLoxNeoII∆EcoRI, which was gener- similar to ACR, RegA and PKA, GSK3′s role in sporu- ated from pLoxNeoII [10] by destroying its EcoRI site by lation was also evolutionary derived from a role in digestion with EcoRI, fll-in with Klenow and self-ligation encystation. with T4 ligase. Tis yielded vector pPp-GSK3-KO, which To address this issue we deleted the GSK3 gene of P. was linearized by EcoRI digestion and transformed into pallidum, which, in addition to fruiting body formation, Pp cells as described previously [18]. Te gene disrup- has retained encystation as an alternative survival strat- tion was confrmed by Southern blot analysis (Additional egy. Surprisingly, loss of GSK3 had no negative efect on fle 1: Fig. 1). To remove the Neo cassette, the knockout P. pallidum sporulation and promoted instead of inhib- cells were transformed with pA15NLS.Cre for transient ited encystation. expression of Cre-recombinase [10] and G418-sensitive clones were selected. Methods Growth and development Complementation of Pp gsk3− with GSK3 Polysphondylium pallidum (Pp), strain PN500, was Te GSK3 coding sequence was amplifed from cDNA by routinely grown in association with Escherichia coli or RT-PCR using primers Pp-GSK3-S51 and Pp-GSK3-E31E Klebsiella aerogenes on lactose-peptone (LP) agar. For (Additional fle 1: Table 1) containing BglII and EcoRI multicellular development, Pp cells were harvested in sites, respectively. After cloning into pCR4-TOPO (Inv- 20 mM K/K-phosphate, pH 6.5 (KK2), washed free from itrogen) the PCR product was validated by sequencing, bacteria and incubated at 106 cells/cm2 and 21 °C on non- digested with BglII and EcoRI and cloned into BglII- and nutrient agar. To determine growth rate, Pp cells were EcoRI-digested vector pDdNYFP [19], yielding vector inoculated at 105 cells/ml in KK2 with autoclaved Kleb- pPp-A15GSK3-OE. To express GSK3 from its own pro- siella aerogenes at OD600 = 15. moter, the promoter region was amplifed by PCR using primers Pp-GSK3-51 and Pp-GSK3-31 (Additional fle 1: Amplifcation of a Pp GSK3 ortholog Table 1), cloned into pCR4-TOPO (Invitrogen) and Te Pp GSK3 gene was amplifed by PCR from genomic sequenced. After digestion with SpeI and BglII, the 1.5-kb DNA, using redundant primers GSKredF and GSKredR fragment, which contains the GSK3 promoter region, was (Additional fle 1: Table 1), which are complementary to cloned into NheI- and BglII-digested pPp-A15GSK3-OE. amino-acid sequences CHRDIKP and GTPTE/R/KQ, Tis yielded vector pPp-GSK3-OE, which was introduced respectively, that are conserved in eukaryote GSK3 pro- into gsk3− cells. teins. Te PCR products were subcloned, and their DNA sequence was determined from 3 independent clones. Encystation assay Te complete 1350-bp coding sequence of the Pp GSK3 For quantifcation of encystation, Pp cells were grown in with 3003-bp 5′ and 1579-bp 3′ UTR was obtained by a suspension of autoclaved K. aerogenes in KK2, until cell Kawabe et al. EvoDevo (2018) 9:12 Page 3 of 11 proliferation reached stationary phase. Cells were washed cassette of the mutant was removed by transformation free of bacteria, resuspended in KK2 at 10 7 cells/ml and with Cre-recombinase and a complementation vector, shaken at 180 rpm and 21 °C for 48 h. Aliquots of 0.1 ml which contains Pp GSK3 inclusive of its promoter, was were sampled at regular intervals and supplemented with introduced into the disruptant. 1 µl 0.1% Calcofuor (which reacts to cellulose in the cyst wall). Total amoeba and cyst numbers were determined Growth phenotype of the Pp gsk3 null mutant by counting cells in a haemocytometer under phase con- Te D. discoideum (Dd) gsk3− mutant becomes multinu- trast and UV illumination, respectively.
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