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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.


Punctuated evolution of a conserved regulatory network.Evolution can replace components in an essential pathway by proceeding through a hybrid intermediate. Once established, the hybrid network can evolve dramatically and lose previously essential regulators, while sometimes retaining the original network topology. We hypothesize that SBF may have hijacked the cell cycle of a fungal ancestor by binding cis-regulatory DNA sites of E2F and activating expression of G1/S genes, thus promoting cell cycle entry. Cell cycle hijacking in a fungal ancestor was followed by evolution of Whi5 to inhibit SBF and Whi5 was subsequently entrained to upstream cell cycle control through phospho-regulation by old or new cyclin-CDKs to create a hybrid network with parallel pathways. The hybrid network likely provided redundant control of the G1/S regulatory network, which could explain the eventual loss of E2F and its replacement by the SBF pathway in more derived fungi (Dikarya). Interestingly, zoosporic fungi such as Chytrids have hybrid networks and are transitional species because they exhibit animal-like features of the opisthokont ancestor (centrioles, flagella) and fungal-like features (cell wall, hyphal growth). We hypothesize that E2F and SBF also bind and regulate a subset of animal-specific and fungal-specific G1/S genes, which could help explain the preservation of the hybrid network in Chytrids. Ancestral SBF expanded to create an entire family of transcription factors (APSES) that regulate fungal-specific traits such as sporulation, differentiation, morphogenesis, and virulence.DOI:http://dx.doi.org/10.7554/eLife.09492.032
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fig9: Punctuated evolution of a conserved regulatory network.Evolution can replace components in an essential pathway by proceeding through a hybrid intermediate. Once established, the hybrid network can evolve dramatically and lose previously essential regulators, while sometimes retaining the original network topology. We hypothesize that SBF may have hijacked the cell cycle of a fungal ancestor by binding cis-regulatory DNA sites of E2F and activating expression of G1/S genes, thus promoting cell cycle entry. Cell cycle hijacking in a fungal ancestor was followed by evolution of Whi5 to inhibit SBF and Whi5 was subsequently entrained to upstream cell cycle control through phospho-regulation by old or new cyclin-CDKs to create a hybrid network with parallel pathways. The hybrid network likely provided redundant control of the G1/S regulatory network, which could explain the eventual loss of E2F and its replacement by the SBF pathway in more derived fungi (Dikarya). Interestingly, zoosporic fungi such as Chytrids have hybrid networks and are transitional species because they exhibit animal-like features of the opisthokont ancestor (centrioles, flagella) and fungal-like features (cell wall, hyphal growth). We hypothesize that E2F and SBF also bind and regulate a subset of animal-specific and fungal-specific G1/S genes, which could help explain the preservation of the hybrid network in Chytrids. Ancestral SBF expanded to create an entire family of transcription factors (APSES) that regulate fungal-specific traits such as sporulation, differentiation, morphogenesis, and virulence.DOI:http://dx.doi.org/10.7554/eLife.09492.032

Mentions: In contrast, SBF was not present in the last common eukaryotic ancestor, and abruptly emerged, with its regulator Whi5, in fungi likely due to the co-option of a viral KilA-N protein at the base of the fungal lineage. The origin of Whi5 is unclear because we found no homologs outside of fungi. Whi5 is a mostly unstructured protein, which, like pRb, recruits transcriptional inhibitor proteins to specific sites on DNA via transcription factor binding (Huang et al., 2009; Travesa et al., 2013; Wang et al., 2009). The relatively simple structure of Whi5 suggests that it may have been subsequently co-opted as a phosphopeptide to entrain SBF activity to cell cycle regulated changes in Cdk activity (Figure 9).10.7554/eLife.09492.032Figure 9.Punctuated evolution of a conserved regulatory network.


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)

Punctuated evolution of a conserved regulatory network.Evolution can replace components in an essential pathway by proceeding through a hybrid intermediate. Once established, the hybrid network can evolve dramatically and lose previously essential regulators, while sometimes retaining the original network topology. We hypothesize that SBF may have hijacked the cell cycle of a fungal ancestor by binding cis-regulatory DNA sites of E2F and activating expression of G1/S genes, thus promoting cell cycle entry. Cell cycle hijacking in a fungal ancestor was followed by evolution of Whi5 to inhibit SBF and Whi5 was subsequently entrained to upstream cell cycle control through phospho-regulation by old or new cyclin-CDKs to create a hybrid network with parallel pathways. The hybrid network likely provided redundant control of the G1/S regulatory network, which could explain the eventual loss of E2F and its replacement by the SBF pathway in more derived fungi (Dikarya). Interestingly, zoosporic fungi such as Chytrids have hybrid networks and are transitional species because they exhibit animal-like features of the opisthokont ancestor (centrioles, flagella) and fungal-like features (cell wall, hyphal growth). We hypothesize that E2F and SBF also bind and regulate a subset of animal-specific and fungal-specific G1/S genes, which could help explain the preservation of the hybrid network in Chytrids. Ancestral SBF expanded to create an entire family of transcription factors (APSES) that regulate fungal-specific traits such as sporulation, differentiation, morphogenesis, and virulence.DOI:http://dx.doi.org/10.7554/eLife.09492.032
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fig9: Punctuated evolution of a conserved regulatory network.Evolution can replace components in an essential pathway by proceeding through a hybrid intermediate. Once established, the hybrid network can evolve dramatically and lose previously essential regulators, while sometimes retaining the original network topology. We hypothesize that SBF may have hijacked the cell cycle of a fungal ancestor by binding cis-regulatory DNA sites of E2F and activating expression of G1/S genes, thus promoting cell cycle entry. Cell cycle hijacking in a fungal ancestor was followed by evolution of Whi5 to inhibit SBF and Whi5 was subsequently entrained to upstream cell cycle control through phospho-regulation by old or new cyclin-CDKs to create a hybrid network with parallel pathways. The hybrid network likely provided redundant control of the G1/S regulatory network, which could explain the eventual loss of E2F and its replacement by the SBF pathway in more derived fungi (Dikarya). Interestingly, zoosporic fungi such as Chytrids have hybrid networks and are transitional species because they exhibit animal-like features of the opisthokont ancestor (centrioles, flagella) and fungal-like features (cell wall, hyphal growth). We hypothesize that E2F and SBF also bind and regulate a subset of animal-specific and fungal-specific G1/S genes, which could help explain the preservation of the hybrid network in Chytrids. Ancestral SBF expanded to create an entire family of transcription factors (APSES) that regulate fungal-specific traits such as sporulation, differentiation, morphogenesis, and virulence.DOI:http://dx.doi.org/10.7554/eLife.09492.032
Mentions: In contrast, SBF was not present in the last common eukaryotic ancestor, and abruptly emerged, with its regulator Whi5, in fungi likely due to the co-option of a viral KilA-N protein at the base of the fungal lineage. The origin of Whi5 is unclear because we found no homologs outside of fungi. Whi5 is a mostly unstructured protein, which, like pRb, recruits transcriptional inhibitor proteins to specific sites on DNA via transcription factor binding (Huang et al., 2009; Travesa et al., 2013; Wang et al., 2009). The relatively simple structure of Whi5 suggests that it may have been subsequently co-opted as a phosphopeptide to entrain SBF activity to cell cycle regulated changes in Cdk activity (Figure 9).10.7554/eLife.09492.032Figure 9.Punctuated evolution of a conserved regulatory network.

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.