Diversification of the Histone Fold Motif in Plants: Evolution of New Functional Roles

<p>The Histone fold motif (HFM) is one of the most conserved structural motifs in biology, mainly found in the core histone sub-units of all eukaryotes. The HFM represents a helix-strand-helix motif having three alpha helices connected by two loops/beta strands. This helix-strand-helix motif has the unique property of binding strongly with proteins as well as with DNA. Apart from core histones, the HFM has been reported in a variety of other proteins in all forms of life. In this work, we review the various classes of proteins that contain the HFM, as well as the diverse roles played by these proteins in the plant kingdom. As will be clear from this review, formation of the core histones through multi-merisation is not the only role played by this conserved fold, although the characteristic ability of the HFM to dimerize with suitable partner proteins has been used by nature to perform several non-core-histone functions. Most of the information about plant HFM containing proteins, such as identification and classification, has been done based on homology with yeast and animal counterparts. However, the ability of plants genomes to duplicate extensively has led to the existence of large gene families of the HFM containing proteins, unlike other eukaryotes. Plant HFM containing proteins can broadly be classified under the following major categories; TBP-associated factors (TAF), Nuclear Factor Y (NF-Y), Dr1/DrAp1 proteins and the chromatin accessibility complex (CHRAC). These proteins families are known to be involved in transcriptional regulation, co-activation and chromosome maintenance. Partner recognition through dimer formation remains a major conserved feature of these groups when compared with core histone sub-units.</p>

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Eukaryotic core histone diversification in light of the histone doublet and DNA topo II genes of Marseilleviridae

10.1101/022236 ◽

2015 ◽

Cited By ~ 3

Author(s):

Albert J Erives

Keyword(s):

Topoisomerase Ii ◽

Domain Architecture ◽

Histone Variants ◽

Core Histone ◽

Histone Fold ◽

The Core ◽

Core Histones ◽

Topo Ii ◽

Phylogenomic Analyses ◽

Linear Chromosomes

While eukaryotic and archaean genomes encode the histone fold domain, only eukaryotes encode the core histones H2A, H2B, H3, and H4. Core histones assemble into a hetero-octamer rather than the homo-tetramer of Archaea. Thus it was unexpected that core histone “doublets” were identified in the cytoplasmic replication factories of the Marseilleviridae (MV), one family of Nucleo-Cytoplasmic Large DNA Viruses (NCLDV). Here we analyze the core histone doublet genes from all known Marseilleviridae genomes and show that they encode obligate H2B-H2A and H4-H3 dimers of likely proto-eukaryotic origin. Each MV core histone moiety forms a sister clade to a eukaryotic core histone clade inclusive of canonical core histone paralogs, suggesting that MV core histone moieties diverged prior to eukaryotic neofunctionalizations associated with paired linear chromosomes and variant histone octamer assembly. We also show that all MV genomes encode a eukaryote-like DNA topoisomerase II enzyme that forms a clade that is sister to the eukaryotic clade. As DNA topo II influences histone deposition and chromatin compaction and is the second most abundant nuclear protein after histones, we suggest MV genes underlie a proto-chromatinized replisome that diverged prior to diversification of eukaryotic core histone variants. Thus, combined domain architecture and phylogenomic analyses suggest that a primitive origin for MV chromatin genes is a more parsimonious explanation than horizontal gene transfers + gene fusions + long-branch attraction constrained to each core histone clade. These results imply that core histones were utilized ancestrally in viral DNA compaction, protection from host endonucleases, and/or other unknown processes associated with NCLDV-like progenitors.

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The Plant NF-Y DNA Matrix In Vitro and In Vivo

Plants ◽

10.3390/plants8100406 ◽

2019 ◽

Vol 8 (10) ◽

pp. 406 ◽

Cited By ~ 2

Author(s):

Nerina Gnesutta ◽

Matteo Chiara ◽

Andrea Bernardini ◽

Matteo Balestra ◽

David S. Horner ◽

...

Keyword(s):

Saturation Mutagenesis ◽

Sequence Specificity ◽

Histone Fold ◽

Nuclear Factor Y ◽

Histone Fold Domain ◽

Genes Encoding ◽

Core Histones ◽

Ccaat Box

Nuclear Factor Y (NF-Y) is an evolutionarily conserved trimer formed by a Histone-Fold Domain (HFD) heterodimeric module shared by core histones, and the sequence-specific NF-YA subunit. In plants, the genes encoding each of the three subunits have expanded in number, giving rise to hundreds of potential trimers. While in mammals NF-Y binds a well-characterized motif, with a defined matrix centered on the CCAAT box, the specificity of the plant trimers has yet to be determined. Here we report that Arabidopsis thaliana NF-Y trimeric complexes, containing two different NF-YA subunits, bind DNA in vitro with similar affinities. We assayed precisely sequence-specificity by saturation mutagenesis, and analyzed genomic DNA sites bound in vivo by selected HFDs. The plant NF-Y CCAAT matrix is different in nucleotides flanking CCAAT with respect to the mammalian matrix, in vitro and in vivo. Our data point to flexible DNA-binding rules by plant NF-Ys, serving the scope of adapting to a diverse audience of genomic motifs.

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Periodic binding of individual core histones to DNA: inadvertent purification of the core histone H2B as a putative enhancer-binding factor

Nucleic Acids Research ◽

10.1093/nar/20.24.6673 ◽

1992 ◽

Vol 20 (24) ◽

pp. 6673-6680 ◽

Cited By ~ 9

Author(s):

Leslie A. Kerrigan ◽

James T. Kadonaga

Keyword(s):

Core Histone ◽

Histone H2b ◽

The Core ◽

Binding Factor ◽

Core Histones ◽

Putative Enhancer ◽

Individual Core

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Unraveling the evolutionary origins of Histone fold motif (HFM) in plants

10.21203/rs.2.14114/v1 ◽

2019 ◽

Author(s):

Amish Kumar ◽

Gitanjali Yadav

Keyword(s):

Markov Models ◽

Search Algorithm ◽

Phylogenetic Analyses ◽

Core Histone ◽

Histone Proteins ◽

Histone Fold ◽

Evolutionary Origins ◽

Sequence Search ◽

Core Histones ◽

Remote Homologs

Abstract Background The three helical Histone Fold Motif (HFM) of core histone proteins provides an evolutionarily favoured site for the protein-DNA interface. Despite significant variation in sequence, the HFM retains a distinctive structural fold that has diversified into several non-histone protein families in. In this work we explore the ancestry of non-histone HFM containing families in the plant kingdom.Results A sequence search algorithm was developed using iterative profile Hidden Markov Models to identify remote homologs of core-histone proteins. The resulting hits were functionally annotated, classified into families, and subjected to comprehensive phylogenetic analyses via Maximum likelihood and Bayesian methods. We have identified over 4000 HFM containing proteins in the plant kingdom that are not histones, mostly existing as diverse transcription factor families, distributed widely within and across taxonomic groups.Conclusion Patterns of homology suggest that core histone subunit H2A has evolved into newer families like NF-YC and DrAp1, whereas the H2B subunit of core histones shares a common ancestry with NF-YB and Dr1 class of TFs. Core histone subunits H3 and H4 were found to have evolved into DPE and TAF proteins, respectively. Taken together these results provide insights into diversification events during the evolution of the histone fold motif, including sub-functionalization and neo-functionalization of the HFM.

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The core histone fold: Limits to functional versatility

Journal of Molecular Evolution ◽

10.1007/bf02202101 ◽

1996 ◽

Vol 43 (6) ◽

pp. 541-542 ◽

Cited By ~ 2

Author(s):

Christos A. Ouzounis ◽

Nikos C. Kyrpides

Keyword(s):

Core Histone ◽

Histone Fold ◽

The Core ◽

Functional Versatility

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Participation of core histone "tails" in the stabilization of the chromatin solenoid.

The Journal of Cell Biology ◽

10.1083/jcb.93.2.285 ◽

1982 ◽

Vol 93 (2) ◽

pp. 285-297 ◽

Cited By ~ 166

Author(s):

J Allan ◽

N Harborne ◽

D C Rau ◽

H Gould

Keyword(s):

Core Histone ◽

Order Structure ◽

Histone Tails ◽

Linker Histones ◽

Nucleosome Core ◽

The Core ◽

Core Histones ◽

Minor Part ◽

Core Histone Tail ◽

A Minor

We show here that the solenoid is maintained by the combination of linker histones and the nonglobular, highly basic "tails" of the core histones, which play only a minor part in the formation of the nucleosome core (Whitlock and Simpson, 1977. J. Biol. Chem. 252:6,516--6,520; Lilley and Tatchell, 1977. Nucleic Acids Res. 4:2,039--2,055; and Whitlock and Stein, 1978. J. Biol. Chem. 253:3,857--3,861). Polynucleosomes that contain core histones devoid of tails remain substantially unfolded under conditions otherwise favorable for the formation of solenoids. The tails can be replaced by extraneous basic polypeptides and in the presence of the linker histones the solenoid structure is then spontaneously recovered, as judged by a wide variety of structural criteria. The inference is that the core histone tail segments function by providing electrostatic shielding of the DNA charge and at the same time bridging adjacent nucleosomes in the solenoid. Our results carry the further implication that posttranscriptional modifications, such as acetylation of epsilon-amino groups, that reduce the positive charge of the core histone tails will tend to destabilize the higher-order structure and could thus render the DNA with which they are associated more readily available for transcription.

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Heparin increases chromatin accessibility by binding the trypsin-sensitive basic residues in histones

Biochemical Journal ◽

10.1042/bj2880953 ◽

1992 ◽

Vol 288 (3) ◽

pp. 953-958 ◽

Cited By ~ 23

Author(s):

B Villeponteau

Keyword(s):

Chromatin Structure ◽

Gradient Analysis ◽

Chromatin Accessibility ◽

Micrococcal Nuclease ◽

The Core ◽

Core Histones ◽

Arginine Residues ◽

Rna And Dna Synthesis ◽

Rna And Dna ◽

Regulatory Significance

Recent evidence indicates that chromatin accessibility to transcription factors is of regulatory significance. The polyanion heparin is known to increase chromatin accessibility to DNAase I and to stimulate both RNA and DNA synthesis. In the present study, chromatin structure and its modification by polyanions were examined by using trypsin and micrococcal nuclease as probes. Both heparin and poly(glutamic acid) were found to be equivalent to trypsin digestion of histones in their ability to increase nuclease accessibility in chromatin. However, no increase in nuclease accessibility was observed when trypsin-digested chromatin was further treated with heparin, indicating that polyanions and trypsin are not additive in their effects on chromatin accessibility. Moreover, sucrose-gradient analysis demonstrated that heparin binds tightly to intact nucleosomes but not to trypsin-digested nucleosomes. These data suggest that polyanions interact predominantly with the trypsin-sensitive lysine and arginine residues in histone H1 and the N-terminal segments of the core histones. The possible relevance of these results to the chromatin structure of actively transcribed regions is discussed.

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Identification and Characterization of the Genes Encoding the Core Histones and Histone Variants of Neurospora crassa

Genetics ◽

10.1093/genetics/160.3.961 ◽

2002 ◽

Vol 160 (3) ◽

pp. 961-973 ◽

Cited By ~ 1

Author(s):

Shan M Hays ◽

Johanna Swanson ◽

Eric U Selker

Keyword(s):

Neurospora Crassa ◽

Histone Variants ◽

Null Alleles ◽

Histone Genes ◽

Histone H4 ◽

Coding Regions ◽

The Core ◽

Genomic Arrangement ◽

Genes Encoding ◽

Core Histones

Abstract We have identified and characterized the complete complement of genes encoding the core histones of Neurospora crassa. In addition to the previously identified pair of genes that encode histones H3 and H4 (hH3 and hH4-1), we identified a second histone H4 gene (hH4-2), a divergently transcribed pair of genes that encode H2A and H2B (hH2A and hH2B), a homolog of the F/Z family of H2A variants (hH2Az), a homolog of the H3 variant CSE4 from Saccharomyces cerevisiae (hH3v), and a highly diverged H4 variant (hH4v) not described in other species. The hH4-1 and hH4-2 genes, which are 96% identical in their coding regions and encode identical proteins, were inactivated independently. Strains with inactivating mutations in either gene were phenotypically wild type, in terms of growth rates and fertility, but the double mutants were inviable. As expected, we were unable to isolate null alleles of hH2A, hH2B, or hH3. The genomic arrangement of the histone and histone variant genes was determined. hH2Az and the hH3-hH4-1 gene pair are on LG IIR, with hH2Az centromere-proximal to hH3-hH4-1 and hH3 centromere-proximal to hH4-1. hH3v and hH4-2 are on LG IIIR with hH3v centromere-proximal to hH4-2. hH4v is on LG IVR and the hH2A-hH2B pair is located immediately right of the LG VII centromere, with hH2A centromere-proximal to hH2B. Except for the centromere-distal gene in the pairs, all of the histone genes are transcribed toward the centromere. Phylogenetic analysis of the N. crassa histone genes places them in the Euascomycota lineage. In contrast to the general case in eukaryotes, histone genes in euascomycetes are few in number and contain introns. This may be a reflection of the evolution of the RIP (repeat-induced point mutation) and MIP (methylation induced premeiotically) processes that detect sizable duplications and silence associated genes.

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