Abstract
In pea, subtype H1-7 of histone H1 is specific for young actively growing tissues and disappears from chromatin of mature tissues. We sequenced the alleles coding for three main variants, numbered according to the increase of the electrophoretic mobility. Allele 1 differs from the most common allele 2 by eight nucleotide substitutions, two of them associated with amino acid replacements, His->Tyr in the globular domain and Ala->Val in the C-terminal domain. Allele 3 differs from alleles 1 and 2 by a 24-bp deletion in the part coding for the C-terminal domain. In three greenhouse experiments, we compared quantitative traits in nearly isogenic lines differing by these H1-7 variants. In experiment 1, three lines bearing either of the three allelic variants were compared, the other experiments involved pairs of lines bearing variants 1 and 3. In all experiments, statistically significant differences between the lines were registered, mostly related to the plant size. The most prominent effect was associated with plant growth dynamics. Plants of line 3, carrying the 8-amino acid deletion in histone H1-7, on average grew slower. In two experiments, the differences of the mean stem length persisted throughout plant growth while in experiment 2 differences disappeared upon maturity. The H1-7 subtype is supposed to be related to maintenance of chromatin state characteristic for cell growth and division.
Similar content being viewed by others
References
Alami R, Fan Y, Pack S, Sonbuchner TM, Besse A, Lin Q, Greally JM, Skoultchi AI, Bouhassira EE (2003) Mammalian linker-histone subtypes differentially affect gene expression in vivo. Proc Natl Acad Sci USA 100:5920–5925
Allan J, Hartman PG, Crane-Robinson C, Aviles FX (1980) The structure of histone H1 and its location in chromatin. Nature 288:675–679
Allan J, Mitchell N, Harborne L, Bohm C, Crane-Robinson C (1986) Roles of H1 domains in determining higher order chromatin structure and H1 location. J Mol Biol 187:591–601
The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815
Barra JL, Rhounim L, Rossignol J-L, Faugeron G (2000) Histone H1 is dispensable for methylation-associated gene silencing in Ascobolus immersus and essential for long life span. Mol Cell Biol 20:61–69
Bennetzen JL, Coleman C, Liu R, Ma J, Ramakrishna W (2004) Consistent over-estimation of gene number in complex plant genomes. Curr Opin Plant Biol 7:732–736
Berdnikov VA, Gorel FL (1975) A study of ratios between histone fractions. Molekulyarnaya Biologiya (USSR) 9:699–705
Berdnikov VA, Rozov SM, Temnykh SV, Gorel FL, Kosterin OE (1993a) Adaptive nature of interspecies variation of histone H1 in insects. J Mol Evol 36:497–507
Berdnikov VA, Bogdanova VS, Rozov SM, Kosterin OE (1993b) The geographic patterns of histone H1 allelic frequencies formed in the course of pea (Pisum sativum L.) cultivation. Heredity 71:199–209
Berdnikov VA, Gorel FL, Bogdanova VS, Kosterin OE, Trusov YA, Rozov SM (1999) Effect of a substitution of a short chromosome segment carrying a histone H1 locus on expression of the homeiotic gene Tl in heterozygote in the garden pea Pisum sativum L. Genet Res 73:93–109
Berdnikov VA, Bogdanova VS, Gorel FL, Kosterin OE, Trusov YA (2003) Large changes in the structure of the major histone H1 subtype result in small effects on quantitative traits in legumes. Genetica 119:168–182
Bogdanova VS, Rozov SM, Trusov YA, Berdnikov VA (1994). Phenotypic effect of substitutions of short chromosomal segments containing different alleles of histone H1 genes in garden pea (Pisum sativum L.). Genet Res 64:35–41
Bogdanova VS, Lester DR, Berdnikov VA, Andersson I (2005) Structure of allelic variants of subtype 5 of histone H1 in pea Pisum sativum L. Heredity 94:582–588
Brown DT (2001) Histone variants: are they functionally heterogeneous? Genome Biol 2:reviews0006.1-reviews0006.6
Bustin M, Catez F, Lim J-H (2005) The dynamics of histone H1 function in chromatin. Mol Cell 17:617–620
Dopico B, Labrador E (1999) cDNA sequence encoding a lysine-rich H1 histone of Cicer arietinum (Accession No AJ006767) (PGR99-020). Plant Physiol 119:806
Drabent B, Saftig P, Bode C, Doenecke D (2000) Spermatogenesis proceeds normally in mice without linker histone H1t. Histochem Cell Biol 113:433–442
Ellis THN, Poyser SJ (2002) Integration and comparison of pea genetic and cytogenetic maps. New Phytol 153:17–25
Fan Y, Sirotkin A, Russell RG, Ayala J, Skoultchi AI (2001) Individual somatic H1 subtypes are dispensable for mouse development even in mice lacking the H1(0) replacement subtype. Mol Cell Biol 21:7933–7943
Fan Y, Nikitina T, Morin-Kensicki EM, Zhao J, Magnuson TR, Woodcock CL, Skoultchi AI (2003) H1 linker histones are essential for mouse development and affect nucleosome spacing in vivo. Mol Cell Biol 23:4559–4572
Fan Y, Nikitina T, Zhao J, Fleury TJ, Bhattacharyya R, Bouhassira EE, Stein A, Woodcock CL, Skoultchi AI (2005) Histone H1 depletion in mammals alters global chromatin structure but causes specific changes in gene regulation. Cell 123:1199–1212
Felsenfeld G (1992) Chromatin as an essential part of the transcriptional mechanism. Nature 355:219–224
Folco HD, Freitag M, Ramon A, Temporini ED, Alvarez ME, Garcia I, Scazzocchio C, Selker EU, Rosa AL (2003) Histone H1 Is required for proper regulation of pyruvate decarboxylase gene expression in Neurospora crassa. Eukaryot Cell 2:341–350
Gantt JS, Key JL (1987) Molecular cloning of a pea H1 histone cDNA. Eur J Biochem 166:119–125
Georgel PT, Hansen JC (2001) Linker histone function in chromatin: dual mechanisms of action. Biochem Cell Biol 79:313–316
Gornicka-Michalska E, Palyga J, Kowalski A, Cywa-Benko K (2006) Sequence variants of chicken linker histone H1.a. FEBS J 273:1240–1250
Hanson WD, (1959) Early generation analysis of length of heterozygous chromosome segments around a locus held heterozygous with backcrossing or selfing. Genetics 44:833–838
Hendzel MJ, Lever MA, Crawford E, Th’ng JP (2004) The C-terminal domain is the primary determinant of histone H1 binding to chromatin in vivo. J Biol Chem 279:20,028–20,034
Jedrusik MA, Schulze E (2001) A single histone H1 isoform (H1.1) is essential for chromatin silencing and germline development in Caenorhabditis elegans. Development 128:1069–1080
Johns EW (1964) Studies of histones 7. Preparative methods for histone fractions from calf thymus. Biochem J 92:55–59
Konishi A, Shimizu S, Hirota J, Takao T, Fan Y, Matsuoka Y, Zhang L, Yoneda Y, Fujii Y, Skoultchi AI, Tsujimoto Y (2003) Involvement of histone H1.2 in apoptosis induced by DNA double-strand breaks. Cell 114:673–688
Kosterin OE (1992) Mapping of the third locus for histone H1 genes in pea. Pisum Genet 24:56–59
Kosterin OE, Bogdanova VS, Gorel FL, Rozov SM, Trusov YA, Berdnikov VA (1994) Histone H1 of the garden pea (Pisum sativum L.); composition, developmental changes, allelic polymorphism and inheritance. Plant Sci 101:189–202
Lee H, Habas R, Abate-Shen C (2004) MSX1 cooperates with histone H1b for inhibition of transcription and myogenesis. Science 304:1675–1678
Lin Q, Sirotkin A, Skoultchi AI (2000) Normal spermatogenesis in mice lacking the testis-specific linker histone H1t. Mol Cell Biol 20:2122–2128
Panyim S, Chalkley R (1969) High resolution in acrylamide gel electrophoresis of histones. Arch Biochem Biophys 130:337–346
Ponte I, Vidal-Taboada JM, Suau P (1998) Evolution of the vertebrate histone H1 class: evidence for the functional differentiation of the subtypes. Mol Biol Evol 15:702–708
Prymakowska-Bosak M, Przewloka MR, Iwkiewicz J, Egierszdorff S, Kuras M, Chaubet N, Gigot C, Spiker S, Jerzmanowski A (1996) Histone H1 overexpressed to high level in tobacco affects certain developmental programs but has limited effect on basal cellular functions. Proc Natl Acad Sci USA 93:10,250–10,255
Prymakowska-Bosak M, Przewloka MR, Slusarczyk J, Kuras M, Lichota J, Kilianczyk B, Jerzmanowski A (1999) Linker histones play a role in male meiosis and the development of pollen grains in tobacco. Plant Cell 11:2317–2329
Przewloka MR, Wierzbicki AT, Slusarczyk J, Kuras M, Grasser KD, Stemmer C, Jerzmanowski A (2002) The “drought-inducible” histone H1s of tobacco play no role in male sterility linked to alterations in H1 variants. Planta 215:371–379
Ramon A, Muro-Pastor MI, Scazzocchio C, Gonzalez R (2000) Deletion of the unique gene encoding a typical histone H1 has no apparent phenotype in Aspergillus nidulans. Mol Microbiol 35:223–233
Rozov SM, Bogdanova VS, Berdnikov VA (1986) Different chromosomal localizations of genes coding for Pisum histone H1 fractions. Genetika (USSR) 22:2159–2166
Sarg B, Green A, Soderkvist P, Helliger W, Rundquist I, Lindner HH (2005) Characterization of sequence variations in human histone H1.2 and H1.4 subtypes. FEBS J 272:3673–3683
Sato MH, Ura K, Hohmura KI, Tokumasu F, Yoshimura SH, Hanaoka F, Takeyasu K (1999) Atomic force microscopy sees nucleosome positioning and histone H1-induced compaction in reconstituted chromatin. FEBS Lett 452:267–271
Sera T, Wolffe AP (1998) Role of histone H1 as an architectural determinant of chromatin structure and as a specific repressor of transcription on Xenopus oocyte 5S rRNA genes. Mol Cell Biol 18:3668–3680
Shen X, Yu L, Weir JW, Gorovsky MA (1995) Linker histones are not essential and affect chromatin condensation in vivo. Cell 82:47–56
Shen X, Gorovsky MA 1996. Linker histone H1 regulates specific gene expression but not global transcription in vivo. Cell 86:475–483
Sirotkin AM, Edelmann W, Cheng H, Klein-Szanto A, Kucherlapati R, Skoultchi AI (1995) Mice develop normally without the H10 linker histone. Proc Natl Acad Sci USA 92:6434–6438
Stein GS, Stein JL, Marzluff WF (eds) (1984) Histone genes: structure, organization, and regulation. John Willey & Sons, NY
Steinbach OC, Wolffe AP, Rupp RA (1997) Somatic linker histones cause loss of mesodermal competence in Xenopus. Nature 389:395–399
Takami Y, Nishi R, Nakayama T (2000) Histone H1 variants play individual roles in transcription regulation in the DT40 chicken B cell line. Biochem Biophys Res Comm 268:501–508
Tanaka I, Akahori Y, Gomi K, Suzuki T, Ueda K (1999) A novel histone variant localized in nucleoli of higher plant cells. Chromosoma 108:190–199
Th’ng JP, Sung R, Ye M, Hendzel MJ (2005) H1 family histones in the nucleus: control of binding and localization by the C-terminal domain. J Biol Chem 280:27,809–27,814
Thoma F, Losa R, Koller T (1983) Involvement of the domains of histones H1 and H5 in the structural organization of soluble chromatin. J Mol Biol 167:619–640
Thomas JO (1999) Histone H1: location and role. Curr Opin Cell Biol 11:312–317
Trieschmann L, Schultze E, Schultze B, Grossbach U (1997) The histone H1 genes of the dipteran insect, Chironomus thummi, fall under two divergent classes and encode proteins with distinct intranuclear distribution and potentially different functions. Eur J Biochem 250:184–196
van Holde KE (1988) Chromatin. Springer Verlag, New York
Weeden NF, Ellis THN, Timmerman-Vaughan GM, Swiecicki WK, Rozov SM, Berdnikov VA (1998) A consensus linkage map for Pisum sativum. Pisum Genet 30:1–4
Wierzbicki AT, Jerzmanowski A (2005) Suppression of histone H1 genes in Arabidopsis results in heritable developmental defects and stochastic changes in DNA methylation. Genetics 169:997–1008
Wolffe AP, Khochbin S, Dimitrov S (1997) What do linker histone do in chromatin? BioEssays 19:249–255
Woo HH, Brigham LA, Hawes MC (1995) Molecular cloning and expression of mRNAs encoding H1 histone and an H1 histone-like sequences in root tips of pea (Pisum sativum L.). Plant Mol Biol 28:1143–1147
Acknowledgements
This work was supported by the Russian State Program ‘Russian Fund for Fundamental Research’, Grant No. 02-04-49426 and the “Biosphere origin and evolution” project of the Russian Academy of Sciences.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Bogdanova, V.S., Kosterin, O.E. & Berdnikov, V.A. Phenotypic effect of substitution of allelic variants for a histone H1 subtype specific for growing tissues in the garden pea (Pisum sativum L.). Genetica 130, 61–72 (2007). https://doi.org/10.1007/s10709-006-0021-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10709-006-0021-6