Chapter 27 : A Matter of Scale and Dimensions: Chromatin of Chromosome Landmarks in the Fungi

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Chromosomes of fungi are linear segments of DNA, covered by a diverse assembly of RNA and proteins. They contain three landmarks required for function, namely, origins for DNA replication, centromeric DNA as attachment points for kinetochores, and telomere repeats to circumvent the end replication problem for linear DNA. Because fungi have been excellent model organisms for trail-blazing basic research since the adoption of as one of the workhorses for genetics in the 1940s ( ), much of the foundation for general knowledge of eukaryotes was first uncovered with fungi, specifically the four species uniquely suited for genetics, biochemistry, and genomics: , , , and . This has also been true for studies on chromatin and chromosomes.

Citation: Erlendson A, Friedman S, Freitag M. 2017. A Matter of Scale and Dimensions: Chromatin of Chromosome Landmarks in the Fungi, p 571-597. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0054-2017
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Figure 1

Presence and absence of selected histone H3 and cytosine DNA methylation marks, structure of centromeres, and sequence of telomere repeats in selected fungi. Representative fungi from various clades were selected to show the phylogenetic distribution of chromatin characteristics. Species in which the presence (check) or absence (cross) were experimentally validated are largely found within the Ascomycota, while species for which only genome sequencing-based evidence for the presence (plus) or absence (minus) of genes is available are in the Basidiomycota and the large group of early-diverging lineages. No experimental data on chromatin modifications in chytrids and microsporidia are available; some chytrids have predicted DNA methyltransferases (DNMTs) that are similar to those in animals, while some zygomycetes (e.g., ) have DNMTs similar to those in ascomycetes ( ). has no cytosine methylation, but sister species have intact genes for DNMTs. No obvious DNMTs are found in the genome, yet there have been reports on cytosine DNA methylation. , unlike , appears to have genes to carry out all modifications listed here, suggesting large diversity in the Taphrinomycotina. More recently, an entirely new class of cytosine DNA methyltransferases has been identified in fungi, demonstrating DNA methylation in species that were long thought to be devoid of methylation such as ( ). The overall distribution pattern suggests that genes necessary to catalyze the two major gene silencing histone modifications, H3K9me and H3K27me, are ancient and have been lost in several branches over evolutionary time. The presence of conserved genes does not necessarily mean the presence of the expected chromatin modification. Centromeric DNA segments (Cen) are defined as regions with CENP-A or CENP-C enrichment, are highly variable in size, and even for some of the best-studied fungi such as , we still do not have experimental data. Pericentric regions, flanking the Cen regions, are larger and also of variable size. Most fungi use the mammalian and human () consensus telomeric repeat sequence, 5′-TTAGGG-3′, sometimes with a variable number of Gs like in . Data on telomere repeats were compiled from the literature ( ).

Citation: Erlendson A, Friedman S, Freitag M. 2017. A Matter of Scale and Dimensions: Chromatin of Chromosome Landmarks in the Fungi, p 571-597. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0054-2017
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Figure 2

Chromosome landmarks in four model organisms. Characteristics of DNA sequences for replication origins and centromere and telomere repeats are compared between budding yeast (), fission yeast (), , and the basidiomycete yeast . Few origins have been mapped in , so it seems premature to say whether they share specific characteristics ( ). ARS, autonomously replicating sequence.

Citation: Erlendson A, Friedman S, Freitag M. 2017. A Matter of Scale and Dimensions: Chromatin of Chromosome Landmarks in the Fungi, p 571-597. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0054-2017
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Figure 3

Telomere-repeat binding complexes homologous to mammalian shelterin. The buddding yeast has a CST (Cdc13, Stn1, Ten1) complex that binds to single-stranded 3′-G-rich-tail overhangs. The nucleosome-free double-stranded DNA is bound by Rap1, which in turn forms complexes with Rif1 and Rif2. Subtelomeric regions are transcriptionally silent because of hypoacetylation initiated by Sir2 and propagated by the Sir complex. The fission yeast has poorly conserved proteins serving similar functions as the CST complex, namely Pot1, Tpz1, and Ccq1. Poz1 creates a bridge to the Rap1/Taz1 complex, but Rap1 has different functions than in , even though there is slight sequence conservation. There is no Sir2-3-4 complex; instead, fission yeast uses H3K9me2-mediated silencing catalyzed by the Clr4 complex and recognized by HP1 (called Swi6 in ). The shelterin complex first identified in mammals by purification of the first telomere-repeat factors is very similar to the complex, though Ccq1 is apparently missing. In both and mammals, HP1 acts on the CST complex homologues, and in a histone deacetylase complex (SHREC) is involved.

Citation: Erlendson A, Friedman S, Freitag M. 2017. A Matter of Scale and Dimensions: Chromatin of Chromosome Landmarks in the Fungi, p 571-597. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0054-2017
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Figure 4

Polycomb repressive complex 2 (PRC2) from three fungi has different components. Facultative heterochromatin, enriched with H3K27me2/3, is generated by PRC2 complexes. Approximate arrangement of complex subunits is based on published structures of human ( ) and PRC2 ( ). has a core PRC2 complex that lacks a homologue of the Msi1 homologue (crossed out MSL1) that is found in PRC2 of (NPF) and (Msl1). While genes for KMT6, EED, and SUZ12 homologues are found in many taxa, the CnCcc1 and CnBnd1 proteins are restricted in distribution, suggesting diversification of PRC2 across the fungi. Ezh ( KMT6, E(z), human EZH2, SET-7, Ezh) contains 10 structurally distinct motifs (adapted from reference ): (i) SBD (SANT1L-binding domain), (ii) EBD (Eed-binding domain), (iii) BAM (b-addition motif), (iv) SAL (SET activation loop), (v) SRM (stimulation-responsive motif), (vi) SANT1L (SANT1-like), (vii) MCSS (motif connecting SANT1L and SANT2L), (viii) SANT2L (SANT2-like), (ix) CXC (cysteine-rich pre-SET domain), and (x) the catalytic SET domain. The SANT motifs are the least conserved surfaces in the crystal structure. Fungal EED proteins ( Esc) contain WD40 (WD) domains that generate a seven-bladed propeller structure, for which the C-terminus folds back toward the N-terminus to generate propeller 1. The function of the extended C-terminal insertion domain is unknown. The accessory Msl1/NPF subunit of and is conserved in humans (RBAp46/48); all Msi1-like proteins share the WD40 propeller structure with EED. SUZ12 [ Su(z)12] contains an Eed-binding domain ( ), a Zn-finger region (Z), and a conserved VEFS domain that in the crystal structure is wedged between KMT6 and EED.

Citation: Erlendson A, Friedman S, Freitag M. 2017. A Matter of Scale and Dimensions: Chromatin of Chromosome Landmarks in the Fungi, p 571-597. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0054-2017
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Figure 5

Histone modifications associated with transcriptionally active euchromatin and transcriptionally silent heterochromatin on four types of chromosomes found in many fungi. Core or “A” chromosomes have a mixture of transcriptionally active euchromatin (green), constitutively silent heterochromatin (gray) that remains densely packaged even in interphase, and facultative heterochromatin (orange) that becomes transcriptionally active upon external or internal cues. Modifications on core chromosomes most often correlated with euchromatin are H3K4 di- and trimethylation (H3K4me2/3), which are usually found in sharp peaks around the nucleosome-free transcriptional start sites or in the 5′ regions of genes. In constitutive heterochromatin, which is often found in repetitive DNA sequences such as centromeric regions that also contain CenH3 nucleosomes (purple), in pericentric (dark gray) regions, or in transposable elements (light gray), H3K9 is di- or trimethylated (H3K9me2/3) and DNA is often methylated at cytosines. In facultative heterochromatin, H3K27 is di- or trimethylated (H3K27me2/3) and controls the expression of genes in a time- and space-dependent manner. Telomeric repeats (blue) have specialized chromatin structures in many fungi; some are free of nucleosomes and bound by shelterin-like complexes. In addition to the histone modifications shown here, lysines in the H3 and H4 tails of euchromatic regions are hyperacetylated (H3ac, H4ac), H3K79 and H3K36 are trimethylated (H3K79me3, H3K36me3), and H2BK120 is mono-ubiquitylated (H2BK120ub1); canonical H2A is replaced by the variant H2AZ. In heterochromatin, H3 and H4 lysines are hypoacetylated and H2AK119 is mono-ubiquitylated (H2A119ub1). In several species and in , complete chromosomes or segments of chromosome arms from accessory chromosomes that are enriched for H3K27 methylation have translocated onto core chromosomes, generating bipartite chromosomes with different histone modification environments. Most accessory chromosomes from and species that have been studied show almost complete coverage with H3K27me3. A very minor fraction of genes is active and enriched with H3K4me2/3, while pericentric regions and centromeric regions in species are enriched with H3K9me3. In , H3K9me3 and H3K27me3 are partially overlapping in repeat-rich regions, but H3K27me3 is mostly found at silent genes. In this species no clear correlation with centromeric chromatin and any tested histone modification has been found. The shortest accessory chromosomes have no active genes and show equal fractions of H3K27me3 and H3K9me3. Predicted structure of true “B” chromosomes similar to those that have been found in plants and animals. These simplest chromosomes are completely gene-free and have only constitutive H3K9me3-enriched heterochromatin, centromeres, and telomeres. No such true B chromosomes have been documented in fungi.

Citation: Erlendson A, Friedman S, Freitag M. 2017. A Matter of Scale and Dimensions: Chromatin of Chromosome Landmarks in the Fungi, p 571-597. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0054-2017
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Figure 6

Three-dimensional models of linkage group (LG) VII based on Hi-C data. Chromosomes are represented as wire diagrams, where the wire path runs through the center of a series of 50-kb “spheres” determined by the contact frequencies calculated from Hi-C datasets for the wild type and three chromatin mutants (, , ). The chromosome path is calculated by attractive or repulsive forces between each sphere so that the system relaxes to a low energy state. Regions that are enriched with one heterochromatic mark, H3K9me3, in the wild type are shaded in red. Centromeres and subtelomeres are separated, but telomeres are closer to each other than to the centromere (adapted from reference ).

Citation: Erlendson A, Friedman S, Freitag M. 2017. A Matter of Scale and Dimensions: Chromatin of Chromosome Landmarks in the Fungi, p 571-597. In Heitman J, Howlett B, Crous P, Stukenbrock E, James T, Gow N (ed), The Fungal Kingdom. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.FUNK-0054-2017
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