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Mating-type Gene Switching in

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  • Authors: Cheng-Sheng Lee1, James E. Haber2
  • Editors: Martin Gellert3, Nancy Craig4
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    Affiliations: 1: Department of Biology and Rosenstiel Basic Medical Sciences Research Center Brandeis University, Waltham, MA 02454-9110; 2: Department of Biology and Rosenstiel Basic Medical Sciences Research Center Brandeis University, Waltham, MA 02454-9110; 3: National Institutes of Health, Bethesda, MD; 4: Johns Hopkins University, Baltimore, MD
  • Source: microbiolspec April 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0013-2014
  • Received 11 April 2014 Accepted 24 April 2014 Published 27 April 2015
  • Jim Haber, haber@brandeis.edu
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  • Abstract:

    The budding yeast has two alternative mating types designated and α. These are distinguished by about 700 bp of unique sequences, Y or Yα, including divergent promoter sequences and part of the open reading frames of genes that regulate mating phenotype. Homothallic budding yeast, carrying an active HO endonuclease gene, , can switch mating type through a recombination process known as gene conversion, in which a site-specific double-strand break (DSB) created immediately adjacent to the Y region results in replacement of the Y sequences with a copy of the opposite mating type information, which is harbored in one of two heterochromatic donor loci, α or . HO gene expression is tightly regulated to ensure that only half of the cells in a lineage switch to the opposite allele, thus promoting conjugation and diploid formation. Study of the silencing of these loci has provided a great deal of information about the role of the Sir2 histone deacetylase and its associated Sir3 and Sir4 proteins in creating heterochromatic regions. switching has been examined in great detail to learn about the steps in homologous recombination. switching is remarkably directional, with recombining preferentially with α and α using . Donor preference is controlled by a -acting recombination enhancer located near . RE is turned off in α cells but in binds multiple copies of the Fkh1 transcription factor whose forkhead-associated phosphothreonine binding domain localizes at the DSB, bringing into conjunction with .

  • Citation: Lee C, Haber J. 2015. Mating-type Gene Switching in . Microbiol Spectrum 3(2):MDNA3-0013-2014. doi:10.1128/microbiolspec.MDNA3-0013-2014.

Key Concept Ranking

DNA Synthesis
0.6881968
DNA Polymerase Zeta
0.5234611
DNA Polymerase delta
0.46285906
DNA Polymerase epsilon
0.45940492
0.6881968

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/content/journal/microbiolspec/10.1128/microbiolspec.MDNA3-0013-2014
2015-04-27
2017-06-22

Abstract:

The budding yeast has two alternative mating types designated and α. These are distinguished by about 700 bp of unique sequences, Y or Yα, including divergent promoter sequences and part of the open reading frames of genes that regulate mating phenotype. Homothallic budding yeast, carrying an active HO endonuclease gene, , can switch mating type through a recombination process known as gene conversion, in which a site-specific double-strand break (DSB) created immediately adjacent to the Y region results in replacement of the Y sequences with a copy of the opposite mating type information, which is harbored in one of two heterochromatic donor loci, α or . HO gene expression is tightly regulated to ensure that only half of the cells in a lineage switch to the opposite allele, thus promoting conjugation and diploid formation. Study of the silencing of these loci has provided a great deal of information about the role of the Sir2 histone deacetylase and its associated Sir3 and Sir4 proteins in creating heterochromatic regions. switching has been examined in great detail to learn about the steps in homologous recombination. switching is remarkably directional, with recombining preferentially with α and α using . Donor preference is controlled by a -acting recombination enhancer located near . RE is turned off in α cells but in binds multiple copies of the Fkh1 transcription factor whose forkhead-associated phosphothreonine binding domain localizes at the DSB, bringing into conjunction with .

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FIGURE 1

Homothallic life cycle of . A homothallic (pink) mother cell and its new daughter can switch to α (light blue). This lineage is established by the asymmetric partitioning of the mRNA encoding the Ash1 repressor of gene expression in daughter cells (light green). These cells can conjugate to form a zygote that gives rise to /α diploids (lilac), in which gene expression is repressed. Under nitrogen starvation, diploids undergo meiosis and sporulation to produce four haploid spores (two and two α) in an ascus. The spores germinate and grow vegetatively and can repeat the homothallic cycle. Heterothallic cells have stable mating types and grow vegetatively until they exhaust their nutrients and enter stationary phase. Used with permission from the Genetics Society of America. doi:10.1128/microbiolspec.MDNA3-0013-2014.f1

Source: microbiolspec April 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0013-2014
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(A) Arrangement of , , and on chromosome 3. The gene conversion between and α is illustrated. Both and could be transcribed but are silenced by the creation of short regions of heterochromatin (ordered nucleosomes are presented as blue circles) by the interaction of silencing proteins with flanking -acting silencer E and I sequences. The recombination enhancer (RE), located 17 kb centromere-proximal to , acts to promote the usage of as the donor in cells. (B) Control of mating type-specific genes. Transcription of - and α-regulatory genes at occurs from a bidirectional promoter. The Mcm1 protein, in combination with Matα1 and Matα2, activates the transcription of α-specific genes or represses -specific genes, respectively, while a Mat1–Matα2 repressor turns off haploid-specific genes. Mat2 has no known function. doi:10.1128/microbiolspec.MDNA3-0013-2014.f2

Source: microbiolspec April 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0013-2014
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FIGURE 3

Silencing of and . The processive process of silencing establishment from -E is illustrated. Proteins (ORC proteins, Rap1, and Abf1, all in gray) bound to the three elements [autonomously replicating sequence consensus sequence (ACS), Rap1-binding site, and Abf1-binding site] of the -E silencer recruit Sir1 that in turn recruits the Sir2–Sir3–Sir4 complex. The NAD- dependent HDAC Sir2 deacetylates lysines on the N-terminal tails of histones H3 and H4, which allows the Sir3–Sir4complex to bind and stabilize the position of the nucleosome. Sir2 can then deactylate the next nucleosome and silencing spreads further. The progressing spread of silencing in the simplified figure is shown only in one direction and from one of the two silencers. doi:10.1128/microbiolspec.MDNA3-0013-2014.f3

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FIGURE 4

Physical monitoring of switching. Southern blot analysis of I-digested DNA after galactose induction of the HO endonuclease. The probe detects sequences just distal to - Z1/Z2 and shows a difference in the size of the I restriction fragments of and α. In this experiment, an ade3::GAL::HO strain carrying α Δ was used. The cleavage of into a smaller HO-cut segment was followed by the appearance of the α product. (Figure modified from 149 ). doi:10.1128/microbiolspec.MDNA3-0013-2014.f4

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FIGURE 5

Mechanism of switching. Key steps in the switching of to α by a synthesis-dependent strand-annealing (SDSA) mechanism. An HO-induced DSB is resected by 5′-to-3′ exonucleases or helicase endonucleases to produce a 3′-end single-stranded DNA (ssDNA) tail, on which assembles a Rad51 filament (shown only on one side of the DSB). The Rad51::ssDNA complex engages in a search for homology. Strand invasion of -Z into the homologous -Z can be detected by anti-Rad51 chromatin immunoprecipitation followed by quantitative PCR using the primer pair P and P. Strand invasion can form an interwound (plectonemic) joint molecule (D-loop) that can assemble DNA replication factors to copy the Yα sequences, which can be monitored by a primer extension assay using the primer pair P and P. The D-loop is thought to migrate as DNA synthesis proceeds. Unlike normal replication, the newly copied strand is postulated to dissociate from the template and, when sufficiently extended, anneal with the second end, still blocked from forming a plectonemic structure by the long nonhomologous Y tail. The single-stranded tail is clipped off once strand annealing occurs by the Rad1– Rad10 flap endonuclease, so that the new 3′ end can also be used as a primer to fill in the gap. Consequently, all newly synthesized DNA is found at the locus, while the donor is unaltered. However, a small fraction of DSB repair events apparently proceed by a different repair mechanism involving the formation of a double Holliday junction. doi:10.1128/microbiolspec.MDNA3-0013-2014.f5

Source: microbiolspec April 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0013-2014
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FIGURE 6

Protein binding to consensus elements in the RE. In cells, Mcm1 binding facilitates the binding of Swi4–Swi6 and multiple copies of Fkh1. These proteins are important for the ability of RE in promoting usage in cells. In α cells, binding of the Matα2–Mcm1 repressor to a 31-bp conserved operator, shared by -specific genes, leads to the formation of highly positioned nucleosomes between the two flanking genes and excludes binding of Fkh1 or Swi4–Swi6. doi:10.1128/microbiolspec.MDNA3-0013-2014.f6

Source: microbiolspec April 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0013-2014
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FIGURE 7

Role of the recombination enhancer in donor preference. (A) Arrangement of α, , and α–HI (α-). When RE is replaced by four LexA-binding sites (LexA), usage is strongly impaired. Expression of LexA–FHA (the phosphothreonine-binding domain of Fkh1) fusion protein completely rescues usage, while expression of the mutant LexA–FHA, which has lost phosphothreonine-binding activity, fails to rescue it. (B) Southern blot data after induction of switching showing the proportion of HI-digested α or α- DNA in the strains depicted above. (Figure modified from 85 .) doi:10.1128/microbiolspec.MDNA3-0013-2014.f7

Source: microbiolspec April 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0013-2014
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FIGURE 8

Model for Fkh1-regulated donor preference. A cluster of Fkh1 bound to RE in cells can associate with phosphothreonine residues that are located near the DSB and created by casein kinase II, and possibly other kinases, in response to the DSB. The association of Fkh1 and the DSB, which has been demonstrated by ChIP, tethers within ∼20 kb of the DSB ends and facilitates its use over , located 100 kb away. doi:10.1128/microbiolspec.MDNA3-0013-2014.f8

Source: microbiolspec April 2015 vol. 3 no. 2 doi:10.1128/microbiolspec.MDNA3-0013-2014
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