Abstract
Free full text
Identification and characterization of the genes encoding the core histones and histone variants of Neurospora crassa.
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.
Full Text
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Smith SR. Miscellaneous: In praise of the Basuto pony. Br Med J (Clin Res Ed) 1983 Dec 24;287(6409):1985–1987. [Europe PMC free article] [Abstract] [Google Scholar]
- Aronson BD, Lindgren KM, Dunlap JC, Loros JJ. An efficient method for gene disruption in Neurospora crassa. Mol Gen Genet. 1994 Feb;242(4):490–494. [Abstract] [Google Scholar]
- Berbee ML, Carmean DA, Winka K. Ribosomal DNA and resolution of branching order among the ascomycota: how many nucleotides are enough? Mol Phylogenet Evol. 2000 Dec;17(3):337–344. [Abstract] [Google Scholar]
- Brown NP, Leroy C, Sander C. MView: a web-compatible database search or multiple alignment viewer. Bioinformatics. 1998;14(4):380–381. [Abstract] [Google Scholar]
- Carr AM, Dorrington SM, Hindley J, Phear GA, Aves SJ, Nurse P. Analysis of a histone H2A variant from fission yeast: evidence for a role in chromosome stability. Mol Gen Genet. 1994 Dec 1;245(5):628–635. [Abstract] [Google Scholar]
- Catcheside DE, Storer PJ, Klein B. Cloning of the ARO cluster gene of Neurospora crassa and its expression in Escherichia coli. Mol Gen Genet. 1985;199(3):446–451. [Abstract] [Google Scholar]
- Centola M, Carbon J. Cloning and characterization of centromeric DNA from Neurospora crassa. Mol Cell Biol. 1994 Feb;14(2):1510–1519. [Europe PMC free article] [Abstract] [Google Scholar]
- Cervoni N, Szyf M. Demethylase activity is directed by histone acetylation. J Biol Chem. 2001 Nov 2;276(44):40778–40787. [Abstract] [Google Scholar]
- Chabouté ME, Chaubet N, Gigot C, Philipps G. Histones and histone genes in higher plants: structure and genomic organization. Biochimie. 1993;75(7):523–531. [Abstract] [Google Scholar]
- Choe J, Kolodrubetz D, Grunstein M. The two yeast histone H2A genes encode similar protein subtypes. Proc Natl Acad Sci U S A. 1982 Mar;79(5):1484–1487. [Europe PMC free article] [Abstract] [Google Scholar]
- Choe J, Schuster T, Grunstein M. Organization, primary structure, and evolution of histone H2A and H2B genes of the fission yeast Schizosaccharomyces pombe. Mol Cell Biol. 1985 Nov;5(11):3261–3269. [Europe PMC free article] [Abstract] [Google Scholar]
- Dobosy JR, Selker EU. Emerging connections between DNA methylation and histone acetylation. Cell Mol Life Sci. 2001 May;58(5-6):721–727. [Europe PMC free article] [Abstract] [Google Scholar]
- Ehinger A, Denison SH, May GS. Sequence, organization and expression of the core histone genes of Aspergillus nidulans. Mol Gen Genet. 1990 Jul;222(2-3):416–424. [Abstract] [Google Scholar]
- Fincham JR. Transformation in fungi. Microbiol Rev. 1989 Mar;53(1):148–170. [Europe PMC free article] [Abstract] [Google Scholar]
- Goff CG. Histones of Neurospora crassa. J Biol Chem. 1976 Jul 10;251(13):4131–4138. [Abstract] [Google Scholar]
- Goffeau A, Barrell BG, Bussey H, Davis RW, Dujon B, Feldmann H, Galibert F, Hoheisel JD, Jacq C, Johnston M, et al. Life with 6000 genes. Science. 1996 Oct 25;274(5287):546–567. [Abstract] [Google Scholar]
- Goyon C, Faugeron G. Targeted transformation of Ascobolus immersus and de novo methylation of the resulting duplicated DNA sequences. Mol Cell Biol. 1989 Jul;9(7):2818–2827. [Europe PMC free article] [Abstract] [Google Scholar]
- Goyon C, Barry C, Grégoire A, Faugeron G, Rossignol JL. Methylation of DNA repeats of decreasing sizes in Ascobolus immersus. Mol Cell Biol. 1996 Jun;16(6):3054–3065. [Europe PMC free article] [Abstract] [Google Scholar]
- Horowitz S, Bowen JK, Bannon GA, Gorovsky MA. Unusual features of transcribed and translated regions of the histone H4 gene family of Tetrahymena thermophila. Nucleic Acids Res. 1987 Jan 12;15(1):141–160. [Europe PMC free article] [Abstract] [Google Scholar]
- Imhof A, Becker PB. Modifications of the histone N-terminal domains. Evidence for an "epigenetic code"? Mol Biotechnol. 2001 Jan;17(1):1–13. [Abstract] [Google Scholar]
- Irelan JT, Selker EU. Cytosine methylation associated with repeat-induced point mutation causes epigenetic gene silencing in Neurospora crassa. Genetics. 1997 Jun;146(2):509–523. [Europe PMC free article] [Abstract] [Google Scholar]
- Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997 Sep 1;25(17):3389–3402. [Europe PMC free article] [Abstract] [Google Scholar]
- Arents G, Burlingame RW, Wang BC, Love WE, Moudrianakis EN. The nucleosomal core histone octamer at 3.1 A resolution: a tripartite protein assembly and a left-handed superhelix. Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10148–10152. [Europe PMC free article] [Abstract] [Google Scholar]
- Kayne PS, Kim UJ, Han M, Mullen JR, Yoshizaki F, Grunstein M. Extremely conserved histone H4 N terminus is dispensable for growth but essential for repressing the silent mating loci in yeast. Cell. 1988 Oct 7;55(1):27–39. [Abstract] [Google Scholar]
- Kouzminova E, Selker EU. dim-2 encodes a DNA methyltransferase responsible for all known cytosine methylation in Neurospora. EMBO J. 2001 Aug 1;20(15):4309–4323. [Europe PMC free article] [Abstract] [Google Scholar]
- Rykowski MC, Wallis JW, Choe J, Grunstein M. Histone H2B subtypes are dispensable during the yeast cell cycle. Cell. 1981 Aug;25(2):477–487. [Abstract] [Google Scholar]
- Liu YJ, Whelen S, Hall BD. Phylogenetic relationships among ascomycetes: evidence from an RNA polymerse II subunit. Mol Biol Evol. 1999 Dec;16(12):1799–1808. [Abstract] [Google Scholar]
- Luger K, Mäder AW, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature. 1997 Sep 18;389(6648):251–260. [Abstract] [Google Scholar]
- Mackenzie DA, Wongwathanarat P, Carter AT, Archer DB. Isolation and use of a homologous histone H4 promoter and a ribosomal DNA region in a transformation vector for the oil-producing fungus Mortierella alpina. Appl Environ Microbiol. 2000 Nov;66(11):4655–4661. [Europe PMC free article] [Abstract] [Google Scholar]
- Schuster T, Han M, Grunstein M. Yeast histone H2A and H2B amino termini have interchangeable functions. Cell. 1986 May 9;45(3):445–451. [Abstract] [Google Scholar]
- Selker EU. Premeiotic instability of repeated sequences in Neurospora crassa. Annu Rev Genet. 1990;24:579–613. [Abstract] [Google Scholar]
- Selker EU. Trichostatin A causes selective loss of DNA methylation in Neurospora. Proc Natl Acad Sci U S A. 1998 Aug 4;95(16):9430–9435. [Europe PMC free article] [Abstract] [Google Scholar]
- Selker EU, Fritz DY, Singer MJ. Dense nonsymmetrical DNA methylation resulting from repeat-induced point mutation in Neurospora. Science. 1993 Dec 10;262(5140):1724–1728. [Abstract] [Google Scholar]
- Matsumoto S, Yanagida M. Histone gene organization of fission yeast: a common upstream sequence. EMBO J. 1985 Dec 16;4(13A):3531–3538. [Europe PMC free article] [Abstract] [Google Scholar]
- Singer MJ, Marcotte BA, Selker EU. DNA methylation associated with repeat-induced point mutation in Neurospora crassa. Mol Cell Biol. 1995 Oct;15(10):5586–5597. [Europe PMC free article] [Abstract] [Google Scholar]
- Maxson R, Cohn R, Kedes L, Mohun T. Expression and organization of histone genes. Annu Rev Genet. 1983;17:239–277. [Abstract] [Google Scholar]
- Smith MM, Andrésson OS. DNA sequences of yeast H3 and H4 histone genes from two non-allelic gene sets encode identical H3 and H4 proteins. J Mol Biol. 1983 Sep 25;169(3):663–690. [Abstract] [Google Scholar]
- May GS, Morris NR. The unique histone H2A gene of Aspergillus nidulans contains three introns. Gene. 1987;58(1):59–66. [Abstract] [Google Scholar]
- McGhee JD, Felsenfeld G. Nucleosome structure. Annu Rev Biochem. 1980;49:1115–1156. [Abstract] [Google Scholar]
- Stark MJ, Milner JS. Cloning and analysis of the Kluyveromyces lactis TRP1 gene: a chromosomal locus flanked by genes encoding inorganic pyrophosphatase and histone H3. Yeast. 1989 Jan-Feb;5(1):35–50. [Abstract] [Google Scholar]
- Stoler S, Keith KC, Curnick KE, Fitzgerald-Hayes M. A mutation in CSE4, an essential gene encoding a novel chromatin-associated protein in yeast, causes chromosome nondisjunction and cell cycle arrest at mitosis. Genes Dev. 1995 Mar 1;9(5):573–586. [Abstract] [Google Scholar]
- Tamaru H, Selker EU. A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature. 2001 Nov 15;414(6861):277–283. [Abstract] [Google Scholar]
- Thatcher TH, Gorovsky MA. Phylogenetic analysis of the core histones H2A, H2B, H3, and H4. Nucleic Acids Res. 1994 Jan 25;22(2):174–179. [Europe PMC free article] [Abstract] [Google Scholar]
- Nelson MA, Kang S, Braun EL, Crawford ME, Dolan PL, Leonard PM, Mitchell J, Armijo AM, Bean L, Blueyes E, et al. Expressed sequences from conidial, mycelial, and sexual stages of Neurospora crassa. Fungal Genet Biol. 1997 Jun;21(3):348–363. [Abstract] [Google Scholar]
- Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. [Europe PMC free article] [Abstract] [Google Scholar]
- Noll M. Differences and similarities in chromatin structure of Neurospora crassa and higher eucaryotes. Cell. 1976 Jul;8(3):349–355. [Abstract] [Google Scholar]
- Vollmer SJ, Yanofsky C. Efficient cloning of genes of Neurospora crassa. Proc Natl Acad Sci U S A. 1986 Jul;83(13):4869–4873. [Europe PMC free article] [Abstract] [Google Scholar]
- Old RW, Woodland HR. Histone genes: not so simple after all. Cell. 1984 Oct;38(3):624–626. [Abstract] [Google Scholar]
- Wallis JW, Hereford L, Grunstein M. Histone H2B genes of yeast encode two different proteins. Cell. 1980 Dec;22(3):799–805. [Abstract] [Google Scholar]
- Wang H, Huang ZQ, Xia L, Feng Q, Erdjument-Bromage H, Strahl BD, Briggs SD, Allis CD, Wong J, Tempst P, et al. Methylation of histone H4 at arginine 3 facilitating transcriptional activation by nuclear hormone receptor. Science. 2001 Aug 3;293(5531):853–857. [Abstract] [Google Scholar]
- Watters MK, Randall TA, Margolin BS, Selker EU, Stadler DR. Action of repeat-induced point mutation on both strands of a duplex and on tandem duplications of various sizes in Neurospora. Genetics. 1999 Oct;153(2):705–714. [Europe PMC free article] [Abstract] [Google Scholar]
- Puerta C, Martin J, Alonso C, López MC. Isolation and characterization of the gene encoding histone H2A from Trypanosoma cruzi. Mol Biochem Parasitol. 1994 Mar;64(1):1–10. [Abstract] [Google Scholar]
- Wefes I, Lipps HJ. The two macronuclear histone H4 genes of the hypotrichous ciliate Stylonychia lemnae. DNA Seq. 1990;1(1):25–32. [Abstract] [Google Scholar]
- Radford A, Parish JH. The genome and genes of Neurospora crassa. Fungal Genet Biol. 1997 Jun;21(3):258–266. [Abstract] [Google Scholar]
- Woudt LP, Pastink A, Kempers-Veenstra AE, Jansen AE, Mager WH, Planta RJ. The genes coding for histone H3 and H4 in Neurospora crassa are unique and contain intervening sequences. Nucleic Acids Res. 1983 Aug 25;11(16):5347–5360. [Europe PMC free article] [Abstract] [Google Scholar]
Articles from Genetics are provided here courtesy of Oxford University Press
Full text links
Read article at publisher's site: https://doi.org/10.1093/genetics/160.3.961
Read article for free, from open access legal sources, via Unpaywall: https://academic.oup.com/genetics/article-pdf/160/3/961/35170042/genetics0961.pdf
Free to read at intl.genetics.org
http://intl.genetics.org/cgi/content/abstract/160/3/961
Subscription required at intl.genetics.org
http://intl.genetics.org/cgi/reprint/160/3/961.pdf
Subscription required at intl.genetics.org
http://intl.genetics.org/cgi/content/full/160/3/961
Citations & impact
Impact metrics
Citations of article over time
Alternative metrics
Article citations
H3T11 phosphorylation by CKII is required for heterochromatin formation in Neurospora.
Nucleic Acids Res, 52(16):9536-9550, 01 Sep 2024
Cited by: 0 articles | PMID: 39106166 | PMCID: PMC11381320
An ascomycete H4 variant with an unknown function.
R Soc Open Sci, 11(2):231705, 21 Feb 2024
Cited by: 1 article | PMID: 38384781 | PMCID: PMC10878826
The histone replacement gene His4r is involved in heat stress induced chromatin rearrangement.
Sci Rep, 11(1):4878, 01 Mar 2021
Cited by: 3 articles | PMID: 33649489 | PMCID: PMC7921661
Effect of H2A.Z deletion is rescued by compensatory mutations in Fusarium graminearum.
PLoS Genet, 16(10):e1009125, 22 Oct 2020
Cited by: 7 articles | PMID: 33091009 | PMCID: PMC7608984
The Candida albicans biofilm gene circuit modulated at the chromatin level by a recent molecular histone innovation.
PLoS Biol, 17(8):e3000422, 09 Aug 2019
Cited by: 15 articles | PMID: 31398188 | PMCID: PMC6703697
Go to all (23) article citations
Data
Data behind the article
This data has been text mined from the article, or deposited into data resources.
BioStudies: supplemental material and supporting data
Similar Articles
To arrive at the top five similar articles we use a word-weighted algorithm to compare words from the Title and Abstract of each citation.
Structure of the chromosome VII centromere region in Neurospora crassa: degenerate transposons and simple repeats.
Mol Cell Biol, 18(9):5465-5477, 01 Sep 1998
Cited by: 60 articles | PMID: 9710630 | PMCID: PMC109131
The organization structure and regulatory elements of Chlamydomonas histone genes reveal features linking plant and animal genes.
Curr Genet, 28(4):333-345, 01 Sep 1995
Cited by: 15 articles | PMID: 8590479
The genes coding for histone H3 and H4 in Neurospora crassa are unique and contain intervening sequences.
Nucleic Acids Res, 11(16):5347-5360, 01 Aug 1983
Cited by: 99 articles | PMID: 6310494 | PMCID: PMC326282
Methylation of histone H3 lysine 36 is required for normal development in Neurospora crassa.
Eukaryot Cell, 4(8):1455-1464, 01 Aug 2005
Cited by: 57 articles | PMID: 16087750 | PMCID: PMC1214527
Funding
Funders who supported this work.
NIGMS NIH HHS (2)
Grant ID: GM-35690
Grant ID: GM-07759