Upload
others
View
0
Download
0
Embed Size (px)
Citation preview
11
Phylogeny-based systematization of Arabidopsis proteins with histone H1 globular domain 1 2 Maciej Kotlinski1, Lukasz Knizewski2, Anna Muszewska3, Kinga Rutowicz3,4, Maciej Lirski3, Anja 3
Schmidt5, Célia Baroux4*, Krzysztof Ginalski2 and Andrzej Jerzmanowski1,3 * 4
5 1Laboratory of Systems Biology, Faculty of Biology, University of Warsaw, Pawińskiego 5A, 02-6
106 Warsaw, Poland; 7 2Laboratory of Bioinformatics and Systems Biology, Centre of New Technologies, University of 8
Warsaw, Zwirki i Wigury 93, 02-089 Warsaw, Poland; 9 3Institute of Biochemistry and Biophysics, Polish Academy of Sciences, Pawińskiego 5A, 02-106 10
Warsaw, Poland; e-mail: [email protected] 11 4Institute of Plant Biology and Zürich-Basel Plant Science Center, University of Zürich, 12
Zollikerstrasse 107, 8008 Zürich, Switzerland; e-mail: [email protected] 13 5Heidelberg University - Centre for Organismal Studies, Im Neuenheimer Feld 345, 69120 14
Heidelberg, Germany 15
*Corresponding authors 16
17
A.J. and C.B. conceived the project; M.K., C.B. and A.J. designed the study; M.K. performed 18
proteomic analyses; K.R and M.L. performed transcriptomic analyses; L.K., A.M., M.K. and K.G. 19
performed structural and phylogenetic in silico analyses and database screens; A.S. contributed 20
transcriptomic atlas of different tissues; M.K., C.B. and A.J. wrote the paper. 21 22 One sentence summary: 23
We propose a unified nomenclature of an important group of plant chromatin proteins, based on 24
evolutionary relationships of their common nucleosome–recognition element – a linker histone-type 25
globular domain (GH1). 26
27
ABSTRACT 28 29 H1 (or linker) histones are basic nuclear proteins that possess an evolutionarily–conserved 30
nucleosome-binding globular domain – GH1. They perform critical functions in determining the 31
accessibility of chromatin DNA to trans–acting factors. In most metazoan species so far studied, 32
linker histones are highly heterogeneous, with numerous non–allelic variants co–occurring in the 33
same cells. The phylogenetic relationships among these variants as well as their structural and 34
functional properties have been relatively well established. This contrasts markedly with the rather 35
Plant Physiology Preview. Published on March 15, 2017, as DOI:10.1104/pp.16.00214
Copyright 2017 by the American Society of Plant Biologists
https://plantphysiol.orgDownloaded on April 2, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
https://plantphysiol.org
22
limited knowledge concerning the phylogeny and structural and functional roles of an unusually 36
diverse group of GH1-containing proteins in plants. The dearth of information and lack of a 37
coherent phylogeny-based nomenclature of these proteins can lead to misunderstandings as to their 38
identity and possible relationships, thereby hampering plant chromatin research. Based on published 39
data and our in silico and high-throughput analyses, we propose a systematization and coherent 40
nomenclature of GH1–containing proteins of Arabidopsis that will be useful for both identification 41
and structural and functional characterization of homologous proteins from other plant species. 42
43
H1s, also known as linker histones, are universal and ubiquitous component of chromatin fibers, in 44
which they occur at an average frequency of one molecule per nucleosome (Woodcock et al., 2006). 45
They are small basic proteins with a highly conserved central globular domain (GH1), and two less 46
conserved and mostly unstructured tail fragments: a short (~ 20 amino acids) N–terminal domain 47
(NTD) and a considerably longer (~ 100 amino acids) and highly positively charged C–terminal 48
domain (CTD). The GH1 consists of ~ 80 amino acids and belongs to the ‘winged helix’ family of 49
DNA–binding proteins. It contains a characteristic mixed α/β fold consisting of three α–helices (I–50
III) and two β–strands (S2-S3). The compact bundle comprised of the three helices forms the core 51
of this domain. The ‘wing’ structure (from which the name of this family of DNA–binding proteins 52
is derived) lies within the region located C–terminally to helix III and is an extended loop joining 53
β–strands S2 and S3. GH1 associates with the nucleosome outside the core particle and contacts 54
DNA via at least two different binding sites (Zhou et al., 1998; Brown et al., 2006; Syed et al., 55
2010; Zhou et al., 2013). In addition to GH1, the overall functional properties of H1 are strongly 56
influenced by the CTD, which binds to internucleosomal linker DNA. The CTD has an intrinsically 57
disordered structure capable of adopting different conformations depending on the geometry of the 58
target surfaces, which may be linker DNA or interacting proteins (Hansen et al., 2006). The prime 59
determinant of this property is the amino acid composition rather than the CTD sequence, with 60
charge neutralization upon DNA binding by its many lysine residues playing an important role 61
(Hendzel et al., 2004). According to current models, simultaneous and synergistic binding of both 62
GH1 and the CTD are prerequisites for correct H1 placement, and determine its role in chromatin 63
compaction (Stasevich et al., 2010). It is generally agreed that H1, by restricting nucleosome 64
mobility and impeding the access of trans–acting factors to their target sequences, exerts strong 65
effects on DNA–dependent activities, such as transcription and replication, and probably also 66
recombination and repair (Izzo et al., 2008). Recent evidence suggests an even more complex 67
pattern of H1 functions in the cell, in which its role as a universal architectural protein affecting 68
chromatin dynamics is complemented by a parallel function as a local and gene–specific regulator 69
(McBryant et al., 2010). Linker histones are a more divergent group of proteins than core histones. 70
https://plantphysiol.orgDownloaded on April 2, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
https://plantphysiol.org
33
In animals, numerous non–allelic variants, including cell type– and stage–specific isoforms, have 71
been described (Jerzmanowski, 2004; Sancho et al., 2008). In addition, and similarly to core 72
histones, major animal H1 variants undergo extensive posttranslational modifications of different 73
types (Wisniewski et al., 2007), the importance of most of which is unknown. 74
Plant H1s exhibit the universal features of the H1 family, including the occurrence of different 75
non–allelic variants and extensive posttranslational modifications see Tables 1 and S1 76
(Prymakowska-Bosak et al., 1996; Jerzmanowski et al., 2000; Jerzmanowski, 2004; Kotliński et al., 77
2016). Interest in their functional roles has grown considerably in recent years, since they are 78
frequently found in high–throughput screens aimed at identifying regulators involved in processes 79
related to development, physiology and adaptation to stresses (Wierzbicki and Jerzmanowski, 2005; 80
She et al., 2013; Zemach et al., 2013; Over and Michaels, 2014; Rutowicz et al., 2015), see also 81
Table S2. However, because of the exceptional diversity of plant GH1–containing proteins, a fact 82
not realized by most researchers, the relevant reference information about members of this group 83
available in databases is highly imprecise, lacks coherence and systematization, and is often 84
misleading, particularly for those unfamiliar with the classification of chromatin proteins. For 85
example, as illustrated in Table 1 and Table S1, plant linker histones, like HMGA (High Mobility 86
Group A) and certain other proteins, are described by the general term ‘winged-helix DNA–binding 87
transcription factor’ in several databases. Numerous plant GH1–containing proteins are listed as 88
‘putative’ or lack any description. Moreover, the annotation of the same proteins is inconsistent 89
between databases. 90
Here, we summarize currently available information, including both published data and the 91
findings of our in silico and high–throughput analyses, and propose a coherent system of phylogeny 92
and structure–based nomenclature and annotation of H1s and other GH1–containing proteins of 93
Arabidopsis. This system will be useful as a basic reference tool for the identification and 94
characterization of homologous proteins from different plant species. In addition, we highlight 95
some interesting trends in the evolution of chromatin–based regulation that may be specific for 96
plants. 97
98
RESULTS AND DISCUSSION 99 100 The Arabidopsis genome encodes 15 proteins containing a genuine GH1 domain. A scheme 101
linking GH1–based phylogenetic relationships with protein domain architectures within this group 102
is shown in Fig. 1. Phylogenetic analysis supports an early separation into three sub–groups, which 103
we rename here as 1) H1s, 2) GH1-HMGA-/GH1-HMGA-related, and 3) GH1-Myb-/GH1-Myb-104
related. The above pattern is generally conserved in angiosperm plants, as shown by a maximum–105
https://plantphysiol.orgDownloaded on April 2, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
https://plantphysiol.org
44
likelihood phylogenetic tree of GH1–containing proteins from a broad range of plant species (Fig. 106
S1). The split into typical H1s and GH1-HMGA-/GH1-HMGA-related preceded the separation of 107
the GH1-Myb-/GH1-Myb-related sub–group. Rapid diversification of the latter compared to the 108
H1s, suggests that it was not initially subjected to strong purifying selection, but might have been 109
important for ongoing adaptive evolution of plants. Perhaps this could be the reason that genes 110
encoding Arabidopsis GH1–containing proteins other than H1s show differential expression 111
patterns in different tissues and developmental stages (Fig. S3). Below, we discuss the properties of 112
the three sub–groups in more detail. 113
114 116
H1s 117 We have argued previously that the formal criteria that define a typical linker histone, i.e. a protein 118
with a GH1 domain flanked by two unstructured and highly basic tails, are fulfilled by the products 119
of only three Arabidopsis genes, designated H1.1, H1.2 and H1.3 (Wierzbicki and Jerzmanowski, 120
2005). As shown in Fig. 1, the sub–group of Arabidopsis H1s consists exclusively of this trio of 121
H1s, none of which has any recognizable domain except GH1. Consistent with earlier analyses of 122
phylogenetic relationships among known plant linker histones (Jerzmanowski et al., 2000; 123
Rutowicz et al., 2015), this sub–group contains a representative (H1.3) of a distinct branch of ‘stress 124
inducible’ H1 variants (Ascenzi and Gantt, 1997; Ascenzi and Gantt, 1999; Scippa et al., 2000; 125
Przewloka et al., 2002; Scippa et al., 2004; Jerzmanowski, 2007). Previously, we demonstrated that 126
this branch separated from the main H1 variants roughly 140 MYA, which coincided with the 127
appearance of angiosperm plants on Earth (Rutowicz et al., 2015). There are no orthologues of 128
stress inducible H1 variants in sequenced species representing green algae, bryophytes, lycophytes 129
and conifers (gymnosperms), analyzed in Fig. S1. Importantly, only members of the H1 sub–group 130 https://plantphysiol.orgDownloaded on April 2, 2021. - Published by
Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
https://plantphysiol.org
55
possess the characteristic regions of strong positive charge in all C–terminal and most N–terminal 131
domains (Fig. S2), beginning immediately adjacent to GH1. It should be noted that the regions of 132
the NTDs of H1.1 and H1.2 most distant from GH1 contain a negatively charged fragment that is 133
targeted by posttranslational modification by phosphorylation, which further increases its negative 134
charge (Kotliński et al., 2016). Thus, among Arabidopsis GH1–containing proteins, the pattern of 135
charge distribution in the N– and C–terminal domains of H1s appears to be as distinctive a feature 136
as the phylogenetic position of their GH1s. 137 138 GH1-HMGA-/GH1-HMGA-related versus putative true Arabidopsis HMGA proteins 139 In animals, High Mobility Group A (HMGA) proteins are distinguished by multiple AT–hook 140
DNA–binding motifs: conserved 9–amino acid peptides capable of strong binding to 6 bp or longer 141
AT–rich stretches of DNA, via the minor groove. Except for an acidic carboxy–terminal region, 142
these proteins do not have any other recognized domains. In contrast, proteins currently defined in 143
the literature as plant HMGA members contain a typical GH1 domain in addition to AT–hook 144
motifs. This arrangement is restricted to angiosperm plants (Fig. S1), suggesting a relatively late 145
occurrence of GH1-AT-hook fusion in the evolution of plants. Arabidopsis has three such proteins 146
(GH1-HMGA1-3) which possess 4 to 6 AT-hook motifs. All three were detected in our analysis of 147
the nuclear proteome of an Arabidopsis T87 cell suspension culture (Table S1, 148
http://proteome.arabidopsis.pl). Interestingly, the Arabidopsis GH1-HMGA cluster also includes a 149
protein with no AT–hook domains (AT5G08780.1, named GH1-HMGA-related4 in our proposed 150
nomenclature). We were unable to detect this protein in our T87 nuclear proteome (Table S1), but 151
its transcript was present in an Arabidopsis transcriptome derived by RNA–Seq analysis (Table S1). 152
Its GH1 sequence places GH1-HMGA-related4 distantly from the rest of the Arabidopsis H1-153
HMGA sub-group. Comparison of the charged amino acid profiles of non–GH1 fragments of 154
Arabidopsis GH1–containing proteins demonstrated that the CTDs of GH1-HMGA1-3 have an 155
island–like distribution of positively and negatively charged residues, with mostly the latter present 156
in fragments directly adjacent to GH1 (Fig. S2). The corresponding profile for GH1-HMGA-157
related4 is significantly different. Secondary structure predictions suggest a potentially novel 158
domain which lacks sequence similarity to any other protein domain of known or unknown 159
structure/function. Interestingly, similar sequences are present in proteins from other species of the 160
order Brassicales, in which they are also accompanied by GH1. The phylogenetic tree of GH1s 161
from model plant proteomes identifies a distinct cluster comprised of Arabidopsis GH1-HMGA-162
related4 and similar proteins from other species. Importantly, according to the InterPro database 163
(http://www.ebi.ac.uk/interpro/), some of the proteins from other species belonging to this cluster 164
retained AT-hook motifs. 165
https://plantphysiol.orgDownloaded on April 2, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
https://plantphysiol.org
66
The fusion of genuine GH1 and multiple AT–hook motifs which occurred in angiosperm plants, 166
can also be found in phylogenetic groups outside plant kingdom, e.g. in numerous fish species, in 167
Trichoplax adhaerens, the only extant representative of the phylum Placozoa (a primitive group of 168
multicellular animals), as well as in some yeast, nematode and insect species. The fish and T. 169
adhaerens genomes encode very large proteins (up to 2900 aa) in which GH1 and AT–hook motifs 170
co–occur with RING and PHD domains. The other mentioned organisms possess simpler proteins 171
in which GH1 co–exists exclusively with AT–hook motifs. The phylogenetic relationships among 172
these extremely diverse organisms suggest that multiple evolutionary events have resulted in the 173
co–occurrence of GH1 and AT–hook motifs within their proteins. 174
Surprisingly given the fundamental functions of HMGA proteins in animals, the functional 175
significance of the GH1/multiple AT–hook motif fusion has never been studied, despite its being 176
referred to in all the major literature concerning plant HMG proteins. Notably, in several 177
prokaryotes in which either HMGA–like or histone H1 CTD–like domains are present in important 178
hub proteins regulating critical cellular processes, these two domains were found functionally 179
equivalent and could be interchanged without any phenotypic consequences. Moreover, even 180
chimeras in which the AT–hook domain was substituted by the human histone H1 CTD or full–181
length human H1, functioned properly in prokaryotic hosts (García-Heras et al., 2009). Thus, 182
Arabidopsis GH1-HMGA proteins may be considered as a highly specialized derivatives of H1 in 183
which the typical CTD of H1 has been replaced by HMGA. To try and verify such a possibility, we 184
re–examined the long held view that Arabidopsis is devoid of canonical HMGA proteins. Using the 185
SMART tool (Schultz et al., 2000; http://smart.embl-heidelberg.de), we identified 48 Arabidopsis 186
proteins containing AT–hook motifs, 23 of which, unlike typical HMGA members, contain only a 187
single AT–hook. Most of the identified proteins, including those of the H1-HMGA sub–group, 188
contain additional domains. Only two proteins, the predicted products of the alternatively spliced 189
At1g48610 gene, contain 4 AT-hook motifs and no other domain. At1g48610.1 encodes a relatively 190
small protein (212 amino acids, about 21.6 kDa) with a high isoelectric point (pI = 11.6) – features 191
typical for HMGA. At1g48610.2 (transcript retains the last intron) encodes a shorter protein with a 192
pI of 11.4. The other putative proteins with the AT-hook motif are significantly larger and their 193
isoelectric point, unlike that of canonical HMGA, is below 10. Interestingly, a protein encoded by 194
At1g48610 was detected in our analyses of the nuclear proteome of Arabidopsis T87 cells, with a 195
score and peptide number similar to those of core– and linker histones, which indicated a 196
substantial concentration in nuclei (http://proteome.arabidopsis.pl). Moreover, and probably due to 197
its high isoelectric point, it was co–purified during the isolation of Arabidopsis linker histones by 198
extraction with 4.5% PCA and cation exchange chromatography (Kotliński, et al. 2016). In both 199
analyses, the larger version of AT1G48610 had a higher number of peptides and higher score than 200
https://plantphysiol.orgDownloaded on April 2, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
https://plantphysiol.org
77
the smaller form (100% and 92% of sequence coverage, respectively). Using 4 different proteases 201
(Trypsin, ArgC, Termolysin and Pepsin), we identified 516 peptides unique for AT1G48610.1., i.e. 202
matching the last 29 amino acids of this protein, including peptides spanning the exon–exon 203
junction. However, we detected no peptides unique for the smaller AT1G48610.2 form, i.e. 204
matching the last 14 amino acids that are different in this variant. Similarly, RNA–Seq analysis 205
revealed multiple reads spanning the junction of the last two exons of the gene, but only one low 206
quality read within the intron retained in At1g48610.2. These data indicate that the larger version of 207
the protein (AT1G48610.1) is the main product of this gene. According to the BAR Toronto 208
database (Toufighi et al., 2005), expression of At1g48610 is strongest in the central, rib and 209
peripheral zones of the shoot apical meristem, in pistil tissue primarily consisting of ovaries, and in 210
phloem companion cells at the border of the meristematic and elongation zones of the root. This 211
suggests that AT1G48610, which we believe to be a true Arabidopsis HMGA protein, is important 212
in the differentiation of stem cells, a role highly reminiscent of that played by animal HMGA–type 213
proteins (Ozturk et al., 2014). Interestingly, the At1g48610 locus in chromosome 1 is located next to 214
that encoding the H1-HMGA2 protein. 215
216
GH1-Myb-/GH1-Myb-related 217 This sub–group comprises five proteins with an additional N–terminal Myb domain accompanied 218
by a 17–18–amino acid–long Myb extension–like domain. They seem to be as evolutionary old as 219
H1s, as in addition to angiosperms, they occur in representatives of green algae, bryophytes, 220
lycophytes and gymnosperms (Fig. S1). They are known as ‘single myb histone’ (SMH) or 221
‘telomere repeat binding’ (TRB) proteins and two of them GH1-Myb-TRB1 and GH1-Myb-TRB2 222
were shown to bind Arabidopsis telomeric repeats in vitro through a Myb domain of the telo-box 223
(telomere motif AAACCCTAA) – type (Marian et al., 2003; Schrumpfová et al., 2004). The 224
demonstration of in vivo interactions of these proteins with Arabidopsis telomerase support a 225
suggestion that they are part of the greater plant telomeric interactome (Procházková Schrumpfová 226
et al., 2014). However, a recent mapping by chromatin immunoprecipitation sequencing (ChIP–seq) 227
of genome–wide distribution of TRB1:GFP revealed its presence in over 7800 genomic loci. The 228
majority of these loci contained telo–box–related motifs located at the transcription start sites 229
(TSS), with additional loci spreading across gene bodies as well as distal promoter regions. 230
Moreover, it was shown by genome–wide expression (RNAseq) analysis that TRB1, by binding at 231
these loci, plays a role of transcriptional regulator which is independent of its role in telomere 232
maintenance (Zhou et al., 2016). Given such wide–spread occurrence, it seems highly probable that 233
at least in some of the detected loci TRB1 through its GH1 domain, competes for nucleosome 234
binding with H1s. 235
https://plantphysiol.orgDownloaded on April 2, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
https://plantphysiol.org
88
Since GH1-Myb-TRB3 is very similar to GH1-Myb-TRB1 and GH1-Myb-TRB2 – all three 236
locate in the same branch on phylogenetic tree (Fig. S1), it may perform the same function. GH1-237
Myb-TRB1 was identified in our proteomic analysis of Arabidopsis nuclei, while GH1-Myb-TRB2 238
and GH1-Myb-TRB3 were detected below the established threshold (Table S1). Transcripts 239
encoding GH1-Myb-TRB1-3 were all present in our RNA–seq data. Two other GH1-Myb proteins 240
GH1-Myb4 and GH1-Myb5 (AT1G17520.1 and AT1G72740.1, respectively) are more distantly 241
related to GH1-Myb-TRB1-3 (Fig. S1). The three other proteins of this sub–group (GH1-Myb-242
related 6-8) lack the Myb domain, although the transcript of one them (AT1G54260.1) contains a 243
Myb–coding sequence in front of the start codon, suggesting the loss of this domain during 244
evolution. AT1G54260.1 also contains a strongly diverged and truncated GH1 domain at the C–245
terminal side of its regular GH1 domain. According to secondary structure predictions, the two 246
other proteins lacking the Myb domain (AT1G54230 and AT1G54240) have α–helical regions 247
within their CTDs. Interestingly, all three proteins lacking Myb are encoded by neighboring genes 248
on chromosome 1. The N– and C–terminal domains of all proteins from the GH1-Myb-/GH1-Myb-249
related sub-group are mostly negatively charged. 250
251
A rationale for the proposed new nomenclature of Arabidopsis GH1–containing proteins 252 253 At first glance, the evolutionary diversification of H1s into well distinguished and conserved 254
sub–types seems to be less pronounced in angiosperm plants than in animals, particularly 255
vertebrates. The most distinct structural and functional diversification of plant H1s coincided with 256
the appearance of angiosperms (ca. 140 MYA) and resulted in two major sub–types that have been 257
maintained ever since: the main– and stress–inducible H1s. Regarding H1s, the case of Arabidopsis 258
shows that two main variants and a single stress–inducible variant are sufficient to support the basic 259
processes of growth and development in a typical flowering plant. While this does not rule out the 260
functional significance of more subtle variation within these two major sub–types observed in 261
systematically distant families and species, proof of such significance has yet to be provided. The 262
above notwithstanding, the impression of a seemingly limited diversification of H1s during the 263
evolution of plants may be misleading and result from biased classification rules. These rules were 264
adopted from studies on typical animal H1s, and do not take into account the fundamentally 265
different life strategies and vastly different selection pressures shaping major chromatin structural 266
proteins in plants and animals during their long histories of separate evolution. The GH1-HMGA-267
/GH1-HMGA-related and GH1-Myb-/GH1-Myb-related sub–groups could be the end result of such 268
specific selection pressures in the plant kingdom. The concept that proteins of these two sub–groups 269
represent highly diverged and specialized derivatives of plant H1 that use GH1 as a common motif 270
https://plantphysiol.orgDownloaded on April 2, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
https://plantphysiol.org
99
for targeting nucleosomes, is supported by the conserved phylogenetic relationships among plant 271
GH1–containing proteins, a recently demonstrated wide–spread occurrence of GH1-Myb-TRB1 in 272
chromatin and its likely involvement in transcriptional regulation, as well as by the identification of 273
a candidate for a true Arabidopsis HMGA protein that does not contain GH1 domain. This concept 274
is by no means equivalent to suggesting that all plant GH1-containing proteins are bona fide ‘H1 275
variants’, in a sense ascribed to this subcategory in animal studies. Its main purpose is to draw 276
attention to the fact, that in plants the competition-based removal of H1 from chromatin may be 277
dependent on more diversified and specialized group of competitors than in animals, suggesting a 278
novel plant-specific mechanisms of chromatin regulation. We therefore propose a unified 279
nomenclature for plant GH1–containing proteins built simply on their GH1–based phylogenetic 280
relationships, as shown in Fig. 1. We further propose to distinguish proteins possessing two 281
characteristic domains (GH1-HMGA and GH1-Myb) and proteins belonging to the same sub–282
groups due to the phylogenetic position of their GH1, but lacking the second characteristic domain 283
– HMGA or Myb. We name these latter proteins GH1-HMGA-related and GH1-Myb-related, 284
respectively (they are marked by lighter color in Fig. S1). It is important to remember that proteins 285
of these two types from other species still retain their AT–hook motifs and Myb domains. Since the 286
GH1-Myb-TRB1-2 proteins have been experimentally confirmed to bind telomere repeats and were 287
therefore named Telomere Repeat Binding 1 and 2 (TRB1 and TRB2), we propose to retain this 288
functional reference in their names (as GH1-Myb-TRB) for the sake of clarity and tradition. The 289
same applies to GH1-Myb-TRB3, a very similar protein that has previously been described as 290
TRB3. With regard to GH1-Myb4 and GH1-Myb5, which are also described as TRB-proteins in 291
many databases, we suggest removing the designation TRB from their names. In Arabidopsis GH1 292
evolutionary tree, both of these proteins group in a clade separate from that of TRB1-3, suggesting 293
a greater evolutionary distance. Moreover, and unlike GH1-Myb-TRB1-3, they both contain a Myb 294
extension-like sequence different than GH1-Myb-TRB1-3, so their binding preferences may be 295
different. We have also indicated (Table S1 and, in parentheses, in Fig. S1) the former names of 296
GH1-Myb proteins as Single Myb Histone (SMH) that were used in the discontinued ChromDB and 297
in Maize genomic databases. Importantly, our inspection in SMART/UniProt of the domain 298
structure of all proteins included in the tree in Fig. S1, revealed some singularities. In Medicago 299
truncatula a GH1-Myb protein has an additional RNA-recognition motif. Another GH1-Myb of this 300
species has strongly changed GH1 domain. Both Brassica rapa and Oryza sativa, have a GH1-Myb 301
protein carrying additional domain, and Zea mays contains a GH1-HMGA protein with S/T kinase 302
domain. Moreover, in Z. mays H1 group there is a protein with two AT-hook motifs (indicative that 303
such fusions are not unusual in plants). While exception proves the rule, it cannot be excluded that 304
at least some of the above singularities resulted from errors in genomes assemblies or gene models. 305
https://plantphysiol.orgDownloaded on April 2, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
https://plantphysiol.org
101
We believe that the proposed phylogeny– and structure–supported system of classification, 306
apart from practical convenience, will foster novel approaches in studies on the functional roles of 307
GH1–containing proteins in plants. 308
309
ACKNOWLEDGEMENTS 310 311 We thank Fred Berger, Franziska Turck, Fredy Barneche, J. Mark Cock, Lars Hennig, Motoaki 312
Seki, Anna Amtmann and Doris Wagner for comments and fruitful discussions. This work was 313
supported by grants from the European Cooperation in Science and Technology (MNiSW 212/N–314 COST/2008/0) and the Ministry of Science and Higher Education (MNiSW 212/N–COST/2008/0) 315
to A. Jerzmanowski and M. Kotlinski, the Foundation for Polish Science (TEAM) and the National 316
Science Centre (2011/02/A/NZ2/00014, 2014/15/B/NZ1/03357) to K. Ginalski, and the National 317
Science Centre grant (2012/07/D/NZ2/04286), the scholarship for outstanding young researchers 318
from Ministry of Science and Higher Educations to A. Muszewska and Swiss National Science 319
Fundation (SNSF grant 31003A_149974/1) to C. Baroux. 320 321
FIGURE LEGENDS 322 323
Table 1. Accession numbers and descriptions of Arabidopsis canonical linker histones in different 324
databases: TAIR10, UniProt, NCBI and ChromDB (a copy of this discontinued database in the web 325
archive was used). 326
327
Fig. 1 Maximum–likelihood phylogenetic tree and domain architecture of Arabidopsis thaliana 328
GH1-containing proteins. Protein sequences were aligned with the local pair iterative algorithm 329
implemented in Mafft (Yamada et al., 2016). Conserved columns from each multiple sequence 330
alignment were selected manually. The phylogenetic analysis was performed with PhyML 331
(Guindon et al., 2005), with the JTT model of amino acid substitutions and three random starting 332
trees. Approximate likelihood ratio test SH-like branch supports above 50% are shown. The tree 333
was rooted using GH1-Myb as an internal sister outgroup for both GH1-HMGA and Histone H1 334
clades. The tree image was prepared with iTol (Letunic and Bork, 2011). Domain architecture 335
analysis was carried out using the SMART (Letunic et al., 2015) and GeneSilico (Kurowski and 336
Bujnicki, 2003) webservers and Meta-BASIC (Ginalski et al., 2004). 337
338
SUPPLEMENTAL DATA 339
340 https://plantphysiol.orgDownloaded on April 2, 2021. - Published by
Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
https://plantphysiol.org
111
Supplementary Table S1. Accession numbers and descriptions of Arabidopsis thaliana proteins 341
containing a GH1 domain from different databases (TAIR10, UniProt, NCBI and ChromDB*). 342
Supplementary Table S2. List of articles referring to the role of plant linker histones. 343
Supplementary Table S3. List of GH1 containing protein identifiers in selected model plants. 344
Supplementary Fig. S1 Maximum-likelihood phylogenetic tree of GH1-containing proteins from 345
selected plants. 346
Supplementary Fig. S2. Moving sum plot of net charge for N- and C- terminal domains of all 347
Arabidopsis GH1–containing proteins. 348
Supplementary Fig. S3. Relative expression levels of GH1-containing protein coding genes in 349
Arabidopsis, across 74 tissue– or cell–specific microarrays. 350
Supplemental Methods 351
Supplementary Table S1. Accession numbers and descriptions of Arabidopsis thaliana proteins 352
containing a GH1 domain from different databases (TAIR10, UniProt, NCBI and ChromDB*). This 353
table is supplemented with data concerning the occurrence, rank and scores of proteins identified in 354
the nuclear proteome of Arabidopsis T-87 suspension culture cells (6753 proteins identified in total, 355
www.proteome.arabidopsis.pl) and localization of gene expression according to the BAR Toronto 356
database (Fucile et al., 2011)(http://bar.utoronto.ca/). 357
*a copy of this discontinued database in the web archive was used. 358
359
Supplementary Table S2. List of articles referring to the role of plant linker histones. 360
361
Supplementary Table S3. List of GH1 containing protein identifiers in selected model plants. GH1 362
protein identifiers and names listed for 18 complete plant proteomes in a tabular format. 363
364
365
Supplementary Fig. S1 Maximum-likelihood phylogenetic tree of GH1-containing proteins from 366
selected plants. 367
368
Supplementary Fig. S2. Moving sum plot of net charge for N- and C- terminal domains of all 369
Arabidopsis GH1–containing proteins. The net charge (y-axis) is summed in a 20–aa sliding 370
window, with the position along the N– and C–terminal domains, with respect to GH1, denoted on 371
the x-axis. For each N- and C-terminus, the percentages of both positively (K, R) and negatively (D, 372
E) charged residues, total charge and theoretical isoelectric point (pI, calculated with 373
http://web.expasy.org/compute_pi) are also shown. 374
375
https://plantphysiol.orgDownloaded on April 2, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
https://plantphysiol.org
121
Supplementary Fig. S3. Relative expression levels of GH1-containing protein coding genes in 376
Arabidopsis, across 74 tissue– or cell–specific microarrays (as used in Schmidt et al., 2011). The 377
arrangement of genes and samples is based on Euclidean distance and hierarchical agglomerative 378
clustering. Colors are scaled per row. Red and green ranges correspond to high and low expression 379
levels, respectively. The pictograms indicate the cell and tissue types. 380
381 Supplementary methods 382 383
Database screen 384 All proteins from TAIR (http://arabidopsis.org) database and protein records from Arabidopsis 385
thaliana deposited in NCBInr (https://www.ncbi.nlm.nih.gov/) and UniProt 386
(http://www.uniprot.org/) databases were searched with use of BLAST (Altschul et al., 1990) for 387
proteins containing GH1 domain. Sequences of GH1 from all 15 Arabidopsis GH1-containing 388
proteins were used as query. All records found are included in Tables 1 and S1. Additionally, full 389
genomic sequence from TAIR repository was translated in six reading frames and searched by 390
position specific BLAST (Altschul et al., 1997). All 15 GH1 sequences from known proteins were 391
used as query. We have not found any new GH1-containing proteins in Arabidopsis. 392
393
Domain architecture 394 Domain architecture analysis was carried out for all A. thaliana proteins containing GH1 395
domain using Meta-BASIC (Ginalski et al., 2004) as well as SMART (Letunic et al., 2015) and 396
GeneSilico (Kurowski and Bujnicki, 2003) webservers. The regions with no detectable homology to 397
known protein domains, yet with conserved sequence and predicted secondary structures (with 398
PSIPRED (Jones, 1999)), have been additionally denoted as potential new domains. 399
For proteins previously assigned to GH1-Myb subfamily, yet lacking Myb domain, 400
nucleotide upstream/downstream sequence of coded genes were verified using both manual 401
translations and data from TAIR gene model and exon confidence ranking system 402
(https://www.arabidopsis.org/download_files/Genes/TAIR10_genome_release/TAIR10_gene_confi403
dence_ranking/DOCUMENTATION_TAIR_Gene_Confidence.pdf). Truncated GH1 domain 404
detected in AT1G54260 was verified in similar manner. 405
406
Moving sum plot 407 Moving sum plot of net charge was generated for both N- and C-terminal regions (with 408
respect to GH1 domain) of all Arabidopsis GH1-containing proteins. The net charge was summed 409
in a 20-aa sliding window along N- and C-terminal regions, starting from GH1 domain. For each 410
https://plantphysiol.orgDownloaded on April 2, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
https://plantphysiol.org
131
region, the percentages of both positively (K, R) and negatively (D, E) charged residues, total 411
charge and theoretical isoelectric point (pI, calculated with http://web.expasy.org/compute_pi) were 412
also calculated. 413
414
Phylogenetic analyses 415 Protein sequences for model plants were collected via phmmer (Finn et al., 2011) available from 416
Ensembl Plants website (Kersey et al., 2014). Ensamble database was chosen to ensure data 417
quality, limiting the dataset to well studied organisms with possibly complete proteomes. Such 418
dataset enables observations of specific subfamily expansions (due to consecutive duplications) in 419
some angiosperms from Brassicaceae and Fabaceae. For better taxon sampling, the following 420
representatives of missing major taxon groups were added: Auxenochlorella protothecoides, 421
Coccomyxa subellipsoidea, Marchantia polymorpha, Picea sitchensis, Pinus taeda (from 422
UNIPROT) and Klebsormidium flaccidum (from NCBI genomes). 423
Sequence searches were performed using H1.2, GH1-HMGA2, GH1-Myb-TRB1 and TRB1 424
from Arabidopsis thaliana as queries. All hits were mapped on Uniprot identifiers 425
(http://www.uniprot.org), except for Physcomitrella patens (which lacks Uniprot ids for 2 out of 9 426
analyzed sequences). Subsequently, representative plants were chosen with emphasis on 427
Brassicaceae (3 taxa) and including all basal plant model organisms present in the aforementioned 428
database (for a list of identifiers and names see Supplementary Table S3). Incomplete truncated 429
sequences were discarded. Phylogenetic trees were inferred both for A. thaliana GH1 proteins (see 430
Fig 1) and for 282 representative plant sequences (Fig S1). 431
Sequences of all GH1-containing proteins used for phylogenetic comparison were screened 432
with SMART (Schultz et al., 2000; Letunic et al., 2015) for presence of any additional domains or 433
loss of domains (other than GH1). The results are included in Fig. S1. 434
435
436
437
438
439
440
441
442
443
444
445
https://plantphysiol.orgDownloaded on April 2, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
https://plantphysiol.org
141
446
447
448
449
450
451
452
453
454
455 Table 1. Accession numbers and descriptions of Arabidopsis canonical linker histones in different databases: TAIR10, 456 UniProt, NCBI and ChromDB (a copy of this discontinued database in the web archive was used). 457
Gene spl.
var. TAIR10 UniProt NCBInr Chrom
DB Length
[aa] id description id description id description
H1.1 1 AT1G06760.1
winged-helix
DNA-binding
transcription
factor family
protein
P26568
(H11_AR
ATH) Histone H1.1
NP_172161.1
P26568.1
AAF63139.1
AAL16244.1
CAA44314.1
AAK91467.1
AAM19868.1
AAM64441.1
AEE28032.1
CAA44312.1
(partial)
histone H1.1;
histone H1-1 HON1 274
H1.2
1 AT2G30620.1
winged-helix
DNA-binding
transcription
factor family
protein
P26569
(H12_AR
ATH) Histone H1.2
NP_180620.1
P26569.1
AAK25921.1
AAK64117.1
AEC08419.1
AAM63006.1
AAM15525.1
CAA44316.1
histone H1.2;
Histone H1-2;
putative
histone H1
protein;
histone H1 HON2
273
2 AT2G30620.2
winged-helix
DNA-binding
transcription
factor family
protein
F4INW2 Histone H1.2NP_0011896
43.1
AEC08420.1
histone H1.2 202
https://plantphysiol.orgDownloaded on April 2, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
https://plantphysiol.org
151
3 - - C0Z3A1 AT2G30620
protein BAH57180.1 AT2G30620 208
H1.3 1 AT2G18050.1
HIS1-3 | histone
H1-3 P94109
His1-3 |
Histone H1
NP_179396.1
AAC49789.1
AAC49790.1
AAD20121.1
AAK76471.1
AAL85145.1
AAM61167.1
AEC06720.1
histone H1-3;
histone H1 HON3
167
2 AT2G18050.2 HIS1-3 | histone
H1-3 Q3EBY3
Histone H1-3
HIS1-3 NP_849970.1
AEC06721.1histone H1-3 138
458
https://plantphysiol.orgDownloaded on April 2, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
https://plantphysiol.org
161
459
https://plantphysiol.orgDownloaded on April 2, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
https://plantphysiol.org
Parsed CitationsAltschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a newgeneration of protein database search programs. Nucleic Acids Res 25: 3389-3402
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Ascenzi R, Gantt JS (1997) A drought-stress-inducible histone gene in Arabidopsis thaliana is a member of a distinct class of plantlinker histone variants. Plant Mol Biol 34: 629-641
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Ascenzi R, Gantt JS (1999) Molecular genetic analysis of the drought-inducible linker histone variant in Arabidopsis thaliana. PlantMol Biol 41: 159-169
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Brown DT, Izard T, Misteli T (2006) Mapping the interaction surface of linker histone H1(0) with the nucleosome of nativechromatin in vivo. Nat Struct Mol Biol 13: 250-255
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39: W29-37Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Fucile G, Di Biase D, Nahal H, La G, Khodabandeh S, Chen Y, Easley K, Christendat D, Kelley L, Provart NJ (2011) ePlant and the3D data display initiative: integrative systems biology on the world wide web. PloS One 6: e15237
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
García-Heras F, Padmanabhan S, Murillo FJ, Elías-Arnanz M (2009) Functional equivalence of HMGA- and histone H1-like domainsin a bacterial transcriptional factor. Proc Natl Acad Sci U S A 106: 13546-13551
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Ginalski K, von Grotthuss M, Grishin NV, Rychlewski L (2004) Detecting distant homology with Meta-BASIC. Nucleic Acids Res 32:W576-581
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Guindon S, Lethiec F, Duroux P, Gascuel O (2005) PHYML Online--a web server for fast maximum likelihood-based phylogeneticinference. Nucleic Acids Res 33: W557-559
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Hansen JC, Lu X, Ross ED, Woody RW (2006) Intrinsic protein disorder, amino acid composition, and histone terminal domains. JBiol Chem 281: 1853-1856
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Hendzel MJ, Lever MA, Crawford E, Th'ng JPH (2004) The C-terminal domain is the primary determinant of histone H1 binding tochromatin in vivo. J Biol Chem 279: 20028-20034
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Izzo A, Kamieniarz K, Schneider R (2008) The histone H1 family: specific members, specific functions? Biol Chem 389: 333-343Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Jerzmanowski A (2004) The linker histones. New Compr. Biochem. Elsevier, pp 75-102Pubmed: Author and TitleCrossRef: Author and Title https://plantphysiol.orgDownloaded on April 2, 2021. - Published by
Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
http://www.ncbi.nlm.nih.gov/pubmed?term=Altschul SF%2C Gish W%2C Miller W%2C Myers EW%2C Lipman DJ %281990%29 Basic local alignment search tool%2E J Mol Biol 215%3A 403%2D410&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Altschul&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Basic local alignment search tool&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Basic local alignment search tool&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Altschul&as_ylo=1990&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Altschul SF%2C Madden TL%2C Schaffer AA%2C Zhang J%2C Zhang Z%2C Miller W%2C Lipman DJ %281997%29 Gapped BLAST and PSI%2DBLAST%3A a new generation of protein database search programs%2E Nucleic Acids Res 25%3A 3389%2D3402&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Altschul&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Gapped BLAST and PSI-BLAST: a new generation of protein database search programs&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Gapped BLAST and PSI-BLAST: a new generation of protein database search programs&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Altschul&as_ylo=1997&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Ascenzi R%2C Gantt JS %281997%29 A drought%2Dstress%2Dinducible histone gene in Arabidopsis thaliana is a member of a distinct class of plant linker histone variants%2E Plant Mol Biol 34%3A 629%2D641&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Ascenzi R, Gantt JS (1997) A drought-stress-inducible histone gene in Arabidopsis thaliana is a member of a distinct class of plant linker histone variants. Plant Mol Biol 34: 629-641http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ascenzi&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=A drought-stress-inducible histone gene in Arabidopsis thaliana is a member of a distinct class of plant linker histone variants&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=A drought-stress-inducible histone gene in Arabidopsis thaliana is a member of a distinct class of plant linker histone variants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ascenzi&as_ylo=1997&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Ascenzi R%2C Gantt JS %281999%29 Molecular genetic analysis of the drought%2Dinducible linker histone variant in Arabidopsis thaliana%2E Plant Mol Biol 41%3A 159%2D169&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Ascenzi R, Gantt JS (1999) Molecular genetic analysis of the drought-inducible linker histone variant in Arabidopsis thaliana. Plant Mol Biol 41: 159-169http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ascenzi&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Molecular genetic analysis of the drought-inducible linker histone variant in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Molecular genetic analysis of the drought-inducible linker histone variant in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ascenzi&as_ylo=1999&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Brown DT%2C Izard T%2C Misteli T %282006%29 Mapping the interaction surface of linker histone H1%280%29 with the nucleosome of native chromatin in vivo%2E Nat Struct Mol Biol 13%3A 250%2D255&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Brown DT, Izard T, Misteli T (2006) Mapping the interaction surface of linker histone H1(0) with the nucleosome of native chromatin in vivo. Nat Struct Mol Biol 13: 250-255http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Brown&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Mapping the interaction surface of linker histone H1(0) with the nucleosome of native chromatin in vivo&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Mapping the interaction surface of linker histone H1(0) with the nucleosome of native chromatin in vivo&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Brown&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Finn RD%2C Clements J%2C Eddy SR %282011%29 HMMER web server%3A interactive sequence similarity searching%2E Nucleic Acids Res 39%3A W29%2D37&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Finn RD, Clements J, Eddy SR (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 39: W29-37http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Finn&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=HMMER web server: interactive sequence similarity searching&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=HMMER web server: interactive sequence similarity searching&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Finn&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Fucile G%2C Di Biase D%2C Nahal H%2C La G%2C Khodabandeh S%2C Chen Y%2C Easley K%2C Christendat D%2C Kelley L%2C Provart NJ %282011%29 ePlant and the 3D data display initiative%3A integrative systems biology on the world wide web%2E PloS One 6%3A e15237&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Fucile G, Di Biase D, Nahal H, La G, Khodabandeh S, Chen Y, Easley K, Christendat D, Kelley L, Provart NJ (2011) ePlant and the 3D data display initiative: integrative systems biology on the world wide web. PloS One 6: e15237http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Fucile&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=ePlant and the 3D data display initiative: integrative systems biology on the world wide web.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=ePlant and the 3D data display initiative: integrative systems biology on the world wide web.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Fucile&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Garc�a%2DHeras F%2C Padmanabhan S%2C Murillo FJ%2C El�as%2DArnanz M %282009%29 Functional equivalence of HMGA%2D and histone H1%2Dlike domains in a bacterial transcriptional factor%2E Proc Natl Acad Sci U S A 106%3A 13546%2D13551&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Garc�a-Heras F, Padmanabhan S, Murillo FJ, El�as-Arnanz M (2009) Functional equivalence of HMGA- and histone H1-like domains in a bacterial transcriptional factor. Proc Natl Acad Sci U S A 106: 13546-13551http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Garc�a-Heras&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Functional equivalence of HMGA- and histone H1-like domains in a bacterial transcriptional factor&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Functional equivalence of HMGA- and histone H1-like domains in a bacterial transcriptional factor&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Garc�a-Heras&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Ginalski K%2C von Grotthuss M%2C Grishin NV%2C Rychlewski L %282004%29 Detecting distant homology with Meta%2DBASIC%2E Nucleic Acids Res 32%3A W576%2D581&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Ginalski K, von Grotthuss M, Grishin NV, Rychlewski L (2004) Detecting distant homology with Meta-BASIC. Nucleic Acids Res 32: W576-581http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ginalski&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Detecting distant homology with Meta-BASIC&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Detecting distant homology with Meta-BASIC&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ginalski&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Guindon S%2C Lethiec F%2C Duroux P%2C Gascuel O %282005%29 PHYML Online%2D%2Da web server for fast maximum likelihood%2Dbased phylogenetic inference%2E Nucleic Acids Res 33%3A W557%2D559&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Guindon S, Lethiec F, Duroux P, Gascuel O (2005) PHYML Online--a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Res 33: W557-559http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Guindon&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=PHYML Online--a web server for fast maximum likelihood-based phylogenetic inference&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=PHYML Online--a web server for fast maximum likelihood-based phylogenetic inference&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Guindon&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Hansen JC%2C Lu X%2C Ross ED%2C Woody RW %282006%29 Intrinsic protein disorder%2C amino acid composition%2C and histone terminal domains%2E J Biol Chem 281%3A 1853%2D1856&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Hansen JC, Lu X, Ross ED, Woody RW (2006) Intrinsic protein disorder, amino acid composition, and histone terminal domains. J Biol Chem 281: 1853-1856http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Hansen&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Intrinsic protein disorder, amino acid composition, and histone terminal domains&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Intrinsic protein disorder, amino acid composition, and histone terminal domains&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hansen&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Hendzel MJ%2C Lever MA%2C Crawford E%2C Th%27ng JPH %282004%29 The C%2Dterminal domain is the primary determinant of histone H1 binding to chromatin in vivo%2E J Biol Chem 279%3A 20028%2D20034&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Hendzel MJ, Lever MA, Crawford E, Th'ng JPH (2004) The C-terminal domain is the primary determinant of histone H1 binding to chromatin in vivo. J Biol Chem 279: 20028-20034http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Hendzel&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=The C-terminal domain is the primary determinant of histone H1 binding to chromatin in vivo&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=The C-terminal domain is the primary determinant of histone H1 binding to chromatin in vivo&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Hendzel&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Izzo A%2C Kamieniarz K%2C Schneider R %282008%29 The histone H1 family%3A specific members%2C specific functions%3F Biol Chem 389%3A 333%2D343&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Izzo A, Kamieniarz K, Schneider R (2008) The histone H1 family: specific members, specific functions? Biol Chem 389: 333-343http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Izzo&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=The histone H1 family: specific members, specific functions&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=The histone H1 family: specific members, specific functions&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Izzo&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Jerzmanowski A %282004%29 The linker histones%2E New Compr%2E Biochem%2E Elsevier%2C pp 75%2D102&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Jerzmanowski A (2004) The linker histones. New Compr. Biochem. Elsevier, pp 75-102https://plantphysiol.org
Google Scholar: Author Only Title Only Author and Title
Jerzmanowski A (2007) SWI/SNF chromatin remodeling and linker histones in plants. Biochim Biophys Acta 1769: 330-345Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Jerzmanowski A, Przewloka M, Grasser KD (2000) Linker Histones and HMG1 Proteins of Higher Plants. Plant Biol 2: 586-597Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Jones DT (1999) Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol. doi:10.1006/jmbi.1999.3091
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Kersey PJ, Allen JE, Christensen M, Davis P, Falin LJ, Grabmueller C, Hughes DST, Humphrey J, Kerhornou A, Khobova J, et al(2014) Ensembl Genomes 2013: scaling up access to genome-wide data. Nucleic Acids Res 42: D546-552
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Kotlinski M, Rutowicz K, Knizewski L, Palusinski A, Oledzki J, Fogtman A, Rubel T, Koblowska M, Dadlez M, Ginalski K, et al (2016)Histone H1 Variants in Arabidopsis Are Subject to Numerous Post-Translational Modifications, Both Conserved and PreviouslyUnknown in Histones, Suggesting Complex Functions of H1 in Plants. PloS One 11: e0147908
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Kurowski MA, Bujnicki JM (2003) GeneSilico protein structure prediction meta-server. Nucleic Acids Res 31: 3305-3307Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Letunic I, Bork P (2011) Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic AcidsRes 39: W475-478
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Letunic I, Doerks T, Bork P (2015) SMART: recent updates, new developments and status in 2015. Nucleic Acids Res 43: D257-260Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Marian CO, Bordoli SJ, Goltz M, Santarella RA, Jackson LP, Danilevskaya O, Beckstette M, Meeley R, Bass HW (2003) The maizeSingle myb histone 1 gene, Smh1, belongs to a novel gene family and encodes a protein that binds telomere DNA repeats in vitro.Plant Physiol 133: 1336-1350
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
McBryant SJ, Lu X, Hansen JC (2010) Multifunctionality of the linker histones: an emerging role for protein-protein interactions.Cell Res 20: 519-528
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Over RS, Michaels SD (2014) Open and closed: the roles of linker histones in plants and animals. Mol Plant 7: 481-491Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Ozturk N, Singh I, Mehta A, Braun T, Barreto G (2014) HMGA proteins as modulators of chromatin structure during transcriptionalactivation. Front Cell Dev Biol 2: 5
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Procházková Schrumpfová P, Vychodilová I, Dvorácková M, Majerská J, Dokládal L, Schorová Š, Fajkus J (2014) Telomere repeatbinding proteins are functional components of Arabidopsis telomeres and interact with telomerase. Plant J 77: 770-781
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
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 cellularfunctions. Proc Natl Acad Sci U S A 93: 10250-10255
Pubmed: Author and Title https://plantphysiol.orgDownloaded on April 2, 2021. - Published by Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Jerzmanowski&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=The linker histones.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=The linker histones.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Jerzmanowski&as_ylo=2004&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Jerzmanowski A %282007%29 SWI%2FSNF chromatin remodeling and linker histones in plants%2E Biochim Biophys Acta 1769%3A 330%2D345&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Jerzmanowski A (2007) SWI/SNF chromatin remodeling and linker histones in plants. Biochim Biophys Acta 1769: 330-345http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Jerzmanowski&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=SWI/SNF chromatin remodeling and linker histones in plants&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=SWI/SNF chromatin remodeling and linker histones in plants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Jerzmanowski&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Jerzmanowski A%2C Przewloka M%2C Grasser KD %282000%29 Linker Histones and HMG1 Proteins of Higher Plants%2E Plant Biol 2%3A 586%2D597&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Jerzmanowski A, Przewloka M, Grasser KD (2000) Linker Histones and HMG1 Proteins of Higher Plants. Plant Biol 2: 586-597http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Jerzmanowski&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Linker Histones and HMG1 Proteins of Higher Plants&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Linker Histones and HMG1 Proteins of Higher Plants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Jerzmanowski&as_ylo=2000&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Jones DT %281999%29 Protein secondary structure prediction based on position%2Dspecific scoring matrices%2E J Mol Biol%2E doi%3A 10%2E1006%2Fjmbi%2E1999%2E3091&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Jones DT (1999) Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol. doi: 10.1006/jmbi.1999.3091http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Jones&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Protein secondary structure prediction based on position-specific scoring matrices.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Protein secondary structure prediction based on position-specific scoring matrices.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Jones&as_ylo=1999&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Kersey PJ%2C Allen JE%2C Christensen M%2C Davis P%2C Falin LJ%2C Grabmueller C%2C Hughes DST%2C Humphrey J%2C Kerhornou A%2C Khobova J%2C et al %282014%29 Ensembl Genomes 2013%3A scaling up access to genome%2Dwide data%2E Nucleic Acids Res 42%3A D546%2D552&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Kersey PJ, Allen JE, Christensen M, Davis P, Falin LJ, Grabmueller C, Hughes DST, Humphrey J, Kerhornou A, Khobova J, et al (2014) Ensembl Genomes 2013: scaling up access to genome-wide data. Nucleic Acids Res 42: D546-552http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kersey&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kersey&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Kotlinski M%2C Rutowicz K%2C Knizewski L%2C Palusinski A%2C Oledzki J%2C Fogtman A%2C Rubel T%2C Koblowska M%2C Dadlez M%2C Ginalski K%2C et al %282016%29 Histone H1 Variants in Arabidopsis Are Subject to Numerous Post%2DTranslational Modifications%2C Both Conserved and Previously Unknown in Histones%2C Suggesting Complex Functions of H1 in Plants%2E PloS One 11%3A e0147908&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Kotlinski M, Rutowicz K, Knizewski L, Palusinski A, Oledzki J, Fogtman A, Rubel T, Koblowska M, Dadlez M, Ginalski K, et al (2016) Histone H1 Variants in Arabidopsis Are Subject to Numerous Post-Translational Modifications, Both Conserved and Previously Unknown in Histones, Suggesting Complex Functions of H1 in Plants. PloS One 11: e0147908http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kotlinski&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Histone H1 Variants in Arabidopsis Are Subject to Numerous Post-Translational Modifications, Both Conserved and Previously Unknown in Histones, Suggesting Complex Functions of H1 in Plants.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Histone H1 Variants in Arabidopsis Are Subject to Numerous Post-Translational Modifications, Both Conserved and Previously Unknown in Histones, Suggesting Complex Functions of H1 in Plants.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kotlinski&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Kurowski MA%2C Bujnicki JM %282003%29 GeneSilico protein structure prediction meta%2Dserver%2E Nucleic Acids Res 31%3A 3305%2D3307&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Kurowski MA, Bujnicki JM (2003) GeneSilico protein structure prediction meta-server. Nucleic Acids Res 31: 3305-3307http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kurowski&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=GeneSilico protein structure prediction meta-server&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=GeneSilico protein structure prediction meta-server&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kurowski&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Letunic I%2C Bork P %282011%29 Interactive Tree Of Life v2%3A online annotation and display of phylogenetic trees made easy%2E Nucleic Acids Res 39%3A W475%2D478&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Letunic I, Bork P (2011) Interactive Tree Of Life v2: online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 39: W475-478http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Letunic&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Letunic&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Letunic I%2C Doerks T%2C Bork P %282015%29 SMART%3A recent updates%2C new developments and status in 2015%2E Nucleic Acids Res 43%3A D257%2D260&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Letunic I, Doerks T, Bork P (2015) SMART: recent updates, new developments and status in 2015. Nucleic Acids Res 43: D257-260http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Letunic&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=SMART: recent updates, new developments and status in 2015&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=SMART: recent updates, new developments and status in 2015&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Letunic&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Marian CO%2C Bordoli SJ%2C Goltz M%2C Santarella RA%2C Jackson LP%2C Danilevskaya O%2C Beckstette M%2C Meeley R%2C Bass HW %282003%29 The maize Single myb histone 1 gene%2C Smh1%2C belongs to a novel gene family and encodes a protein that binds telomere DNA repeats in vitro%2E Plant Physiol 133%3A 1336%2D1350&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Marian CO, Bordoli SJ, Goltz M, Santarella RA, Jackson LP, Danilevskaya O, Beckstette M, Meeley R, Bass HW (2003) The maize Single myb histone 1 gene, Smh1, belongs to a novel gene family and encodes a protein that binds telomere DNA repeats in vitro. Plant Physiol 133: 1336-1350http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Marian&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Marian&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=McBryant SJ%2C Lu X%2C Hansen JC %282010%29 Multifunctionality of the linker histones%3A an emerging role for protein%2Dprotein interactions%2E Cell Res 20%3A 519%2D528&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=McBryant SJ, Lu X, Hansen JC (2010) Multifunctionality of the linker histones: an emerging role for protein-protein interactions. Cell Res 20: 519-528http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=McBryant&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Multifunctionality of the linker histones: an emerging role for protein-protein interactions&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Multifunctionality of the linker histones: an emerging role for protein-protein interactions&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=McBryant&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Over RS%2C Michaels SD %282014%29 Open and closed%3A the roles of linker histones in plants and animals%2E Mol Plant 7%3A 481%2D491&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Over RS, Michaels SD (2014) Open and closed: the roles of linker histones in plants and animals. Mol Plant 7: 481-491http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Over&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Open and closed: the roles of linker histones in plants and animals&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Open and closed: the roles of linker histones in plants and animals&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Over&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Ozturk N%2C Singh I%2C Mehta A%2C Braun T%2C Barreto G %282014%29 HMGA proteins as modulators of chromatin structure during transcriptional activation%2E Front Cell Dev Biol 2%3A 5&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Ozturk N, Singh I, Mehta A, Braun T, Barreto G (2014) HMGA proteins as modulators of chromatin structure during transcriptional activation. Front Cell Dev Biol 2: 5http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ozturk&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=HMGA proteins as modulators of chromatin structure during transcriptional activation.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=HMGA proteins as modulators of chromatin structure during transcriptional activation.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ozturk&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Proch�zkov� Schrumpfov� P%2C Vychodilov� I%2C Dvor�ckov� M%2C Majersk� J%2C Dokl�dal L%2C Schorov� ?%2C Fajkus J %282014%29 Telomere repeat binding proteins are functional components of Arabidopsis telomeres and interact with telomerase%2E Plant J 77%3A 770%2D781&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=Proch�zkov� Schrumpfov� P, Vychodilov� I, Dvor�ckov� M, Majersk� J, Dokl�dal L, Schorov� ?, Fajkus J (2014) Telomere repeat binding proteins are functional components of Arabidopsis telomeres and interact with telomerase. Plant J 77: 770-781http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Proch�zkov�&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Telomere repeat binding proteins are functional components of Arabidopsis telomeres and interact with telomerase&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Telomere repeat binding proteins are functional components of Arabidopsis telomeres and interact with telomerase&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Proch�zkov�&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Prymakowska%2DBosak M%2C Przewloka MR%2C Iwkiewicz J%2C Egierszdorff S%2C Kuras M%2C Chaubet N%2C Gigot C%2C Spiker S%2C Jerzmanowski A %281996%29 Histone H1 overexpressed to high level in tobacco affects certain developmental programs but has limited effect on basal cellular functions%2E Proc Natl Acad Sci U S A 93%3A 10250%2D10255&dopt=abstracthttps://plantphysiol.org
CrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
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
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Rutowicz K, Puzio M, Halibart-Puzio J, Lirski M, Kroten MA, Kotlinski M, Knizewski L, Lange B, Muszewska A, Sniegowska-SwierkK, et al (2015) A specialized histone H1 variant is required for adaptive responses to complex abiotic stress and related DNAmethylation in Arabidopsis. Plant Physiol. doi: 10.1104/pp.15.00493
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Sancho M, Diani E, Beato M, Jordan A (2008) Depletion of human histone H1 variants uncovers specific roles in gene expressionand cell growth. PLoS Genet 4: e1000227
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Schmidt A, Wuest SE, Vijverberg K, Baroux C, Kleen D, Grossniklaus U (2011) Transcriptome analysis of the Arabidopsismegaspore mother cell uncovers the importance of RNA helicases for plant germline development. PLoS Biol 9: e1001155
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Schrumpfová P, Kuchar M, Miková G, Skrísovská L, Kubicárová T, Fajkus J (2004) Characterization of two Arabidopsis thalianamyb-like proteins showing affinity to telomeric DNA sequence. Genome 47: 316-324
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Schultz J, Copley RR, Doerks T, Ponting CP, Bork P (2000) SMART: a web-based tool for the study of genetically mobile domains.Nucleic Acids Res 28: 231-234
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Scippa GS, Di Michele M, Onelli E, Patrignani G, Chiatante D, Bray EA (2004) The histone-like protein H1-S and the response oftomato leaves to water deficit. J Exp Bot 55: 99-109
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Scippa GS, Griffiths A, Chiatante D, Bray EA (2000) The H1 histone variant of tomato, H1-S, is targeted to the nucleus andaccumulates in chromatin in response to water-deficit stress. Planta 211: 173-181
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
She W, Grimanelli D, Rutowicz K, Whitehead MWJ, Puzio M, Kotlinski M, Jerzmanowski A, Baroux C (2013) Chromatinreprogramming during the somatic-to-reproductive cell fate transition in plants. Dev Camb Engl 140: 4008-4019
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Stasevich TJ, Mueller F, Brown DT, McNally JG (2010) Dissecting the binding mechanism of the linker histone in live cells: anintegrated FRAP analysis. EMBO J 29: 1225-1234
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Syed SH, Goutte-Gattat D, Becker N, Meyer S, Shukla MS, Hayes JJ, Everaers R, Angelov D, Bednar J, Dimitrov S (2010) Single-base resolution mapping of H1-nucleosome interactions and 3D organization of the nucleosome. Proc Natl Acad Sci U S A 107:9620-9625
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Toufighi K, Brady SM, Austin R, Ly E, Provart NJ (2005) The Botany Array Resource: e-Northerns, Expression Angling, andpromoter analyses. Plant J Cell Mol Biol 43: 153-163
Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title
Wierzbicki AT, Jerzmanowski A (2005) Suppression of histone H1 genes in Arabidopsis results in heritable developmental defectsand stochastic changes in DNA methylation. Genetics. doi: 10.1534/genetics.104.031997
Pubmed: Author and Titlehttps://plantphysiol.orgDownloaded on April 2, 2021. - Published by
Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.
http://search.crossref.org/?page=1&rows=2&q=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 U S A 93: 10250-10255http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Prymakowska-Bosak&hl=en&c2coff=1http://scholar.google.com/scholar?as_q=Histone H1 overexpressed to high level in tobacco affects certain developmental programs but has limited effect on basal cellular functions&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1http://scholar.google.com/scholar?as_q=Histone H1 overexpressed to high level in tobacco affects certain developmental programs but has limited effect on basal cellular functions&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Prymakowska-Bosak&as_ylo=1996&as_allsubj=all&hl=en&c2coff=1http://www.ncbi.nlm.nih.gov/pubmed?term=Przewloka MR%2C Wierzbicki AT%2C Slusarczyk J%2C Kuras M%2C Grasser KD%2C Stemmer C%2C Jerzmanowski A %282002%29 The %22drought%2Dinducible%22 histone H1s of tobacco play no role in male sterility linked to alterations in H1 variants%2E Planta 215%3A 371%2D379&dopt=abstracthttp://search.crossref.org/?page=1&rows=2&q=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: 371-379http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Przewloka