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Punctuated evolution and transitional hybrid network in an ancestral cell cycle of fungi.

Medina EM, Turner JJ, Gordân R, Skotheim JM, Buchler NE - Elife (2016)

Bottom Line: Cell cycle evolution in the fungal ancestor then proceeded through a hybrid network containing both SBF and its ancestral animal counterpart E2F, which is still maintained in many basal fungi.We hypothesize that a virally-derived SBF may have initially hijacked cell cycle control by activating transcription via the cis-regulatory elements targeted by the ancestral cell cycle regulator E2F, much like extant viral oncogenes.Consistent with this hypothesis, we show that SBF can regulate promoters with E2F binding sites in budding yeast.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Duke University, Durham, United States.

ABSTRACT
Although cell cycle control is an ancient, conserved, and essential process, some core animal and fungal cell cycle regulators share no more sequence identity than non-homologous proteins. Here, we show that evolution along the fungal lineage was punctuated by the early acquisition and entrainment of the SBF transcription factor through horizontal gene transfer. Cell cycle evolution in the fungal ancestor then proceeded through a hybrid network containing both SBF and its ancestral animal counterpart E2F, which is still maintained in many basal fungi. We hypothesize that a virally-derived SBF may have initially hijacked cell cycle control by activating transcription via the cis-regulatory elements targeted by the ancestral cell cycle regulator E2F, much like extant viral oncogenes. Consistent with this hypothesis, we show that SBF can regulate promoters with E2F binding sites in budding yeast.

No MeSH data available.


Related in: MedlinePlus

Phylogeny of fungal SBF/MBF and APSES transcription factors.SBF/MBF and APSES transcription factors (Asm1, Phd1, Sok2, Efg1, StuA) share a common DNA-binding domain (KilA-N), which is derived from DNA viruses. During our search for SBF and APSES homologs, we consistently detected two additional fungal sub-families with homology to KilA-N: XBP1 (family name taken from S. cerevisiae) and BQT4 (family name taken from S. pombe). To detect APSES, XBP1, and BQT4 homologs, we built profile-HMMs (APSES.hmm, XBP1.hmm, and BQT4.hmm) by combining APSES, XBP1, and BQT4 homologs from S. cerevisiae, C. albicans, N. crassa, A. nidulans, and S. pombe. A domain threshold of E-10 was used to identify APSES, XBP1, and BQT4 homologs. Our final dataset (Figure 3—source data 2) contains all fungal KILA sub-families (SBF/MBF, APSES, XBP1, BQT4) and has a total of 301 sequences. Columns with the top 10% Zorro score (447 positions) were used in our alignment. Confidence at nodes was assessed with multiple support metrics using different phylogenetic programs under LG model of evolution (aBayes and SH-aLRT metrics with PhyML, RBS with RAxML, Bayesian Posterior Probability with Phylobayes (15,251 sampled trees, meandiff=0.012, maxdiff=0.25)). Colored dots in branches indicate corresponding branch supports. Thick branches indicate significant support by at least two metrics, one parametric and one non-parametric; branch support thresholds are shown in the center of the figure; see Materials and methods.DOI:http://dx.doi.org/10.7554/eLife.09492.022
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fig3s3: Phylogeny of fungal SBF/MBF and APSES transcription factors.SBF/MBF and APSES transcription factors (Asm1, Phd1, Sok2, Efg1, StuA) share a common DNA-binding domain (KilA-N), which is derived from DNA viruses. During our search for SBF and APSES homologs, we consistently detected two additional fungal sub-families with homology to KilA-N: XBP1 (family name taken from S. cerevisiae) and BQT4 (family name taken from S. pombe). To detect APSES, XBP1, and BQT4 homologs, we built profile-HMMs (APSES.hmm, XBP1.hmm, and BQT4.hmm) by combining APSES, XBP1, and BQT4 homologs from S. cerevisiae, C. albicans, N. crassa, A. nidulans, and S. pombe. A domain threshold of E-10 was used to identify APSES, XBP1, and BQT4 homologs. Our final dataset (Figure 3—source data 2) contains all fungal KILA sub-families (SBF/MBF, APSES, XBP1, BQT4) and has a total of 301 sequences. Columns with the top 10% Zorro score (447 positions) were used in our alignment. Confidence at nodes was assessed with multiple support metrics using different phylogenetic programs under LG model of evolution (aBayes and SH-aLRT metrics with PhyML, RBS with RAxML, Bayesian Posterior Probability with Phylobayes (15,251 sampled trees, meandiff=0.012, maxdiff=0.25)). Colored dots in branches indicate corresponding branch supports. Thick branches indicate significant support by at least two metrics, one parametric and one non-parametric; branch support thresholds are shown in the center of the figure; see Materials and methods.DOI:http://dx.doi.org/10.7554/eLife.09492.022

Mentions: Basal fungi and 'Zygomycota' contain hybrid networks comprised of both ancestral and fungal specific cell cycle regulators. Check marks indicate the presence of at least one member of a protein family in at least one sequenced species from the group; see Figure 3—figure supplement 1 for a complete list of homologs in all fungal species. Cells are omitted (rather than left unchecked) when a family is completely absent from a clade. For each fungal regulatory family (e.g., SBF/MBF), we used molecular phylogeny to classify eukaryotic sequences into sub-families (e.g., SBF/MBF, APSES, Xbp1, Bqt4). See Materials and methods for details and Figure 3—figure supplement 2 (SBF/MBF only), Figure 3—figure supplement 3 (SBF/MBF+APSES), and Figure 3—figure supplement 4 (Whi5/Nrm1) for final phylogenies.


Punctuated evolution and transitional hybrid network in an ancestral cell cycle of fungi.

Medina EM, Turner JJ, Gordân R, Skotheim JM, Buchler NE - Elife (2016)

Phylogeny of fungal SBF/MBF and APSES transcription factors.SBF/MBF and APSES transcription factors (Asm1, Phd1, Sok2, Efg1, StuA) share a common DNA-binding domain (KilA-N), which is derived from DNA viruses. During our search for SBF and APSES homologs, we consistently detected two additional fungal sub-families with homology to KilA-N: XBP1 (family name taken from S. cerevisiae) and BQT4 (family name taken from S. pombe). To detect APSES, XBP1, and BQT4 homologs, we built profile-HMMs (APSES.hmm, XBP1.hmm, and BQT4.hmm) by combining APSES, XBP1, and BQT4 homologs from S. cerevisiae, C. albicans, N. crassa, A. nidulans, and S. pombe. A domain threshold of E-10 was used to identify APSES, XBP1, and BQT4 homologs. Our final dataset (Figure 3—source data 2) contains all fungal KILA sub-families (SBF/MBF, APSES, XBP1, BQT4) and has a total of 301 sequences. Columns with the top 10% Zorro score (447 positions) were used in our alignment. Confidence at nodes was assessed with multiple support metrics using different phylogenetic programs under LG model of evolution (aBayes and SH-aLRT metrics with PhyML, RBS with RAxML, Bayesian Posterior Probability with Phylobayes (15,251 sampled trees, meandiff=0.012, maxdiff=0.25)). Colored dots in branches indicate corresponding branch supports. Thick branches indicate significant support by at least two metrics, one parametric and one non-parametric; branch support thresholds are shown in the center of the figure; see Materials and methods.DOI:http://dx.doi.org/10.7554/eLife.09492.022
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4862756&req=5

fig3s3: Phylogeny of fungal SBF/MBF and APSES transcription factors.SBF/MBF and APSES transcription factors (Asm1, Phd1, Sok2, Efg1, StuA) share a common DNA-binding domain (KilA-N), which is derived from DNA viruses. During our search for SBF and APSES homologs, we consistently detected two additional fungal sub-families with homology to KilA-N: XBP1 (family name taken from S. cerevisiae) and BQT4 (family name taken from S. pombe). To detect APSES, XBP1, and BQT4 homologs, we built profile-HMMs (APSES.hmm, XBP1.hmm, and BQT4.hmm) by combining APSES, XBP1, and BQT4 homologs from S. cerevisiae, C. albicans, N. crassa, A. nidulans, and S. pombe. A domain threshold of E-10 was used to identify APSES, XBP1, and BQT4 homologs. Our final dataset (Figure 3—source data 2) contains all fungal KILA sub-families (SBF/MBF, APSES, XBP1, BQT4) and has a total of 301 sequences. Columns with the top 10% Zorro score (447 positions) were used in our alignment. Confidence at nodes was assessed with multiple support metrics using different phylogenetic programs under LG model of evolution (aBayes and SH-aLRT metrics with PhyML, RBS with RAxML, Bayesian Posterior Probability with Phylobayes (15,251 sampled trees, meandiff=0.012, maxdiff=0.25)). Colored dots in branches indicate corresponding branch supports. Thick branches indicate significant support by at least two metrics, one parametric and one non-parametric; branch support thresholds are shown in the center of the figure; see Materials and methods.DOI:http://dx.doi.org/10.7554/eLife.09492.022
Mentions: Basal fungi and 'Zygomycota' contain hybrid networks comprised of both ancestral and fungal specific cell cycle regulators. Check marks indicate the presence of at least one member of a protein family in at least one sequenced species from the group; see Figure 3—figure supplement 1 for a complete list of homologs in all fungal species. Cells are omitted (rather than left unchecked) when a family is completely absent from a clade. For each fungal regulatory family (e.g., SBF/MBF), we used molecular phylogeny to classify eukaryotic sequences into sub-families (e.g., SBF/MBF, APSES, Xbp1, Bqt4). See Materials and methods for details and Figure 3—figure supplement 2 (SBF/MBF only), Figure 3—figure supplement 3 (SBF/MBF+APSES), and Figure 3—figure supplement 4 (Whi5/Nrm1) for final phylogenies.

Bottom Line: Cell cycle evolution in the fungal ancestor then proceeded through a hybrid network containing both SBF and its ancestral animal counterpart E2F, which is still maintained in many basal fungi.We hypothesize that a virally-derived SBF may have initially hijacked cell cycle control by activating transcription via the cis-regulatory elements targeted by the ancestral cell cycle regulator E2F, much like extant viral oncogenes.Consistent with this hypothesis, we show that SBF can regulate promoters with E2F binding sites in budding yeast.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Duke University, Durham, United States.

ABSTRACT
Although cell cycle control is an ancient, conserved, and essential process, some core animal and fungal cell cycle regulators share no more sequence identity than non-homologous proteins. Here, we show that evolution along the fungal lineage was punctuated by the early acquisition and entrainment of the SBF transcription factor through horizontal gene transfer. Cell cycle evolution in the fungal ancestor then proceeded through a hybrid network containing both SBF and its ancestral animal counterpart E2F, which is still maintained in many basal fungi. We hypothesize that a virally-derived SBF may have initially hijacked cell cycle control by activating transcription via the cis-regulatory elements targeted by the ancestral cell cycle regulator E2F, much like extant viral oncogenes. Consistent with this hypothesis, we show that SBF can regulate promoters with E2F binding sites in budding yeast.

No MeSH data available.


Related in: MedlinePlus