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,2
* Department of Biochemistry and Microbiology, University of Victoria, Victoria, B.C., Canada, V8W 3P6, and
Department of Zoology, University of British Columbia, Vancouver, B.C., Canada, V6T 1Z4; and
Program in Evolutionary Biology, Canadian Institute for Advanced Research, Department of Biochemistry and Molecular Biology, Dalhousie University, Halifax, N.S., Canada, B3H 4H7
3Correspondence: Department of Biochemistry and Microbiology, University of Victoria, Petch Building, Room 220, Victoria, B.C., Canada, V8W 3P6. E-mail: jausio{at}uvic.ca
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONCORE HISTONES, LINKER HISTONES,...THE LYSINE-RICH CARBOXYL...H1 LINKER HISTONES IN...EVOLUTIONARY APPEARANCE OF THE...HISTONE H1-RELATED PROTEINS IN...OVERVIEWREFERENCES |
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Key Words: histone H1 • evolution • protists • bacteria
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONCORE HISTONES, LINKER HISTONES,...THE LYSINE-RICH CARBOXYL...H1 LINKER HISTONES IN...EVOLUTIONARY APPEARANCE OF THE...HISTONE H1-RELATED PROTEINS IN...OVERVIEWREFERENCES |
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and the globular winged helix domain
of the linker histones (2)
. Whereas the latter is
ubiquitous among animals, plants, and fungi, it is absent in some
protist taxa. Both the pattern of distribution of the H1 winged helix
and an examination of the remaining carboxyl-terminal region should
provide insights into the evolution of this protein family.
The characterization of the histone fold (1)
has shed an
important insight on the evolution of core histones, whose origin can
be traced to archaebacteria (3)
. However, the origin of
the linker histones has not been established. In what has already
become a classic work (ref 4
; see p. 178) for researchers
in the chromatin field, van Holde declared:
"The relationship of H1 to other histones is obscure. So far as we can tell the H1 sequences seem unrelated to either other histone sequences or those of prokaryotic proteins. This may, of course, simply be a consequence of the rapid evolution of this protein, which has obscured its origins: alternatively, H1 may have evolved from an entirely different protein."
In this review, we examine several important questions of H1 linker histone evolution: Can the origin of this family of linker histones be traced back to prokaryotes? If so, have H1 linker histones evolved from the same or entirely different genes than the core histones?
For this purpose, we survey the recent literature on histone H1 and H1-like protein and gene sequences in protists and bacteria and analyze their similarity to that of the sequence of their animal, plant, and fungal counterparts.
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CORE HISTONES, LINKER HISTONES, AND CHROMATIN |
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TOPABSTRACTINTRODUCTIONCORE HISTONES, LINKER HISTONES,...THE LYSINE-RICH CARBOXYL...H1 LINKER HISTONES IN...EVOLUTIONARY APPEARANCE OF THE...HISTONE H1-RELATED PROTEINS IN...OVERVIEWREFERENCES |
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. Histones are the major protein
component of chromatin and can be structurally grouped in two major
categories: ‘core’ and ‘linker’ histones. Core histones (histones
H2A, H2B, H3, and H4) are arranged as a globular octomeric core in
which an H3–H4 tetramer serves as scaffold to two adjacent H2A–H2B
dimers (5)
. Between 146–180 bp of DNA are wrapped around
this protein core in approximately two left-handed superhelical turns.
The nucleosome structures resulting from such association
(6)
are connected by a variable stretch of linker DNA.
Each of the core histones has a histone fold domain (1)
(see Fig. 1A
) that extends into less structured amino- and
carboxyl-terminal domains, commonly referred to as ‘tails’. The
amino-terminal tail of core histones has a highly basic amino acid
composition and together with the linker histones plays an important
role in chromatin folding. Core histones are among the most highly
evolutionarily conserved proteins (7)
and are present in
all eukaryotic cells. They are thought to have evolved from a DNA
binding protein such as Hmf found in the thermophilic archaeon
Methanofermus fervidus (8)
. Such DNA binding
proteins consist of the histone fold but lack the carboxyl- and
amino-terminal tails found in eukaryotic organisms. They are present in
the euryarchae, a major kingdom of archaebacteria, but are absent from
the one crenarchaeal genome sequenced thus far (9
, 10)
.
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Histones of the H1 family interact extensively with linker DNA and
hence are known as linker histones. Upon binding of histone H1 to the
linker DNA, the polynucleosomal fiber folds into a 30 nm chromatin
fiber (4)
. The linker histones of multicelled eukaryotes
exhibit a tripartite structural organization in which a globular domain
is flanked by two less structured basic amino- and carboxyl-terminal
domains. The crystallographic structure of the globular domain has been
determined and shown to consist of a winged helix motif
(2)
(see Fig. 1B
). This domain interacts with
the nucleosome at a region close to the pseudodyad axis of symmetry
(11)
. In contrast to core histones, linker histones are
less evolutionarily conserved (7
, 12)
. Whereas the
sequence of the winged helix motif is relatively well conserved through
evolution in animals, plants, and fungi (see Fig. 2
), the amino- and carboxyl-terminal domains are extremely heterogeneous,
both in length and amino acid composition. The histone H1 family in
metazoans and other multicelled eukaryotes is a heterogeneous family of
developmentally regulated histones (12)
that includes
highly tissue-specific proteins such as histone H5 from the nucleated
erythrocytes of birds (13)
and sperm PL-I proteins
(14)
. Henceforth, ‘H1’ will represent the entire histone
H1 family.
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THE LYSINE-RICH CARBOXYL-TERMINAL DOMAIN OF H1: A CRITICAL STRUCTURE FOR LINKER HISTONE FUNCTION |
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TOPABSTRACTINTRODUCTIONCORE HISTONES, LINKER HISTONES,...THE LYSINE-RICH CARBOXYL...H1 LINKER HISTONES IN...EVOLUTIONARY APPEARANCE OF THE...HISTONE H1-RELATED PROTEINS IN...OVERVIEWREFERENCES |
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, 15)
. Early sequence analysis showed that the lysine-rich nature
of the linker histone was mainly due to the frequent occurrence of this
amino acid in the carboxyl-terminal domain of these proteins
(12)
. The alternating occurrence of lysine (K) and alanine
(A) residues (two highly helicogenic amino acids) in this region and
the resulting charge distribution (16)
have been
postulated to result in a proline-kinked AK 
-helix organization
(17)
, which we will refer to as the AKP helix (see Fig. 1C
). In many instances, these putative -helical domains
exhibit a clear amphipathic nature (16)
, which may play a
role in linker histone-linker histone interactions in the chromatin
fiber or in the inter-chromatin fiber association mediated by these
histones. It is this particular distribution of AKP in the carboxyl
terminus that confers to histone H1 the unique ability to bind to the
linker DNA (16)
, and its presence is essential for the
processes of chromatin folding and condensation. As has already been
mentioned, the major function of histone H1 is to condense the linker
DNA to induce folding of the polynucleosome fiber into chromatin
structures of 
30 nm in diameter (4)
. These can
eventually condense into larger superstructures (chromosomes) during
mitosis. Although a polynucleosome fiber lacking linker histones is
able to fold to a certain extent (18)
, additional folding
into the 30 nm fiber, under physiological conditions, can only occur on
binding of histone H1 to the linker DNA. Chromatin reconstitution
experiments carried out with histone H1 fragments consisting of the
globular and carboxyl-terminal domain have shown that these fragments
are able to fold the chromatin fiber as effectively as the intact
native H1 molecule (19)
. In contrast, the globular histone
H1 domain alone is unable to condense the chromatin fiber to any
similar extent (20)
. Thus, of the three structural domains
of the linker histones, the carboxyl-terminal domain appears to be
critical for chromatin folding (19)
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H1 LINKER HISTONES IN SOME PROTISTS LACK THE WINGED HELIX MOTIF |
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TOPABSTRACTINTRODUCTIONCORE HISTONES, LINKER HISTONES,...THE LYSINE-RICH CARBOXYL...H1 LINKER HISTONES IN...EVOLUTIONARY APPEARANCE OF THE...HISTONE H1-RELATED PROTEINS IN...OVERVIEWREFERENCES |
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Euglenozoan protists, such as the kinetoplastids Trypanosoma
cruzi (21
) and Trypanosoma brucei
(22)
, possess linker histones that lack the winged helix
motif. These are small proteins that are compositionally and
structurally very similar to the carboxyl termini of histone H1 in
animals, plants, chlorophytes, and mycetozoans (see Table 1
and Fig. 3
) and bind to the linker DNA of the nucleosomally organized chromatin of
these organisms (22)
. In addition to trypanosomes, a gene
encoding a protein with a similar amino acid composition is present in
another kinetoplastid, Leishmania major (see Fig. 4
and Table 1
). A similar protein has been purified from Euglena
gracilis (23)
, also from the phylum Euglenozoa. (see
Table 1
and Fig. 4
). However, not all kinetoplastid H1 proteins match
the consensus carboxyl-terminal sequence so well. A protein has been
isolated by perchloric acid extraction [a method initially devised by
Johns (15)
to selectively fractionate histone H1 from core
histones] and the gene identified for a H1 homologue in the insect
trypanosomatid Crithidia fasciculata. Although related to
histone H1 (24)
, the protein has an amino acid composition
that departs significantly from the consensus amino acid composition of
the histone H1 carboxyl terminus and bears very low similarity to the
linker histone consensus sequence of the winged helix.
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Similarly, proteins related to the histone H1 carboxyl terminus in both
amino acid composition (Table 1)
and sequence (Fig. 3)
can be found
(see Fig. 4
, Fig. 5
) in the protist phylum Alveolata (25)
. Examples of this
are the encoded histone H1 gene of the oligohymenophoran ciliate
Tetrahymena thermophila (26)
, the histones of
the hypotrich ciliate Oxytricha sp. (27)
, and
the encoded histone H1–1 gene from the hypotrich ciliate
Euplotes eurystomus (see Fig. 4
and Table 1
). The
Tetrahymena gene is expressed in macronuclei, where the H1
linker histone has been characterized by gel electrophoresis
(28)
. Within the alveolates, a lysine-rich basic protein,
HCc2, from the dinoflagellate Crypthecodinium cohnii has
also been identified (29
, 30)
. However, in this instance,
the extent of sequence similarity with the carboxyl terminus of histone
H1 is lower than in ciliates (see Fig. 3
). This is not surprising, as
dinoflagellates are known for their unusual nuclear organization
(4)
.
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In the subphylum Heterokonta (25)
, a histone H1-related
protein has also been purified from the unicellular golden alga
Olisthodiscus luteus (31)
. Although the
sequence of this protein is unknown, the similarity of its amino acid
composition to that of Crypthecodinium (see Table 1
)
suggests that their carboxyl-terminal domains may also be similar.
Finally, the encoded H1 histone for Entamoeba histolytica
(see Fig. 4
and Table 1
) lacks the winged helix motif entirely but
shows considerable similarity (Fig. 3)
to the carboxyl-terminal tail of
histone H1. Molecular sequence data indicate a deeply diverging
position for Entamoeba (Fig. 5)
, although this has been
brought into question (32)
. It may represent one of the
most primitive protists for which a histone H1-related protein has been
characterized.
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EVOLUTIONARY APPEARANCE OF THE WINGED HELIX MOTIF IN PROTISTS |
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TOPABSTRACTINTRODUCTIONCORE HISTONES, LINKER HISTONES,...THE LYSINE-RICH CARBOXYL...H1 LINKER HISTONES IN...EVOLUTIONARY APPEARANCE OF THE...HISTONE H1-RELATED PROTEINS IN...OVERVIEWREFERENCES |
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Figure 4
summarizes the results from the comparative analysis of the
sequences from histone H1 and histone H1-related proteins using the
alignment analysis shown in Figs. 2
and 3
, as well as the information
from Table 1
. As illustrated in Fig. 4
, genes coding for H1 linker
histones with an evolutionarily conserved winged helix motif can be
found in diverse protist groups: chlorophytes and mycetazoans (Fig. 5)
.
Figure 2
indicates that the putative protein products of encoded genes
H1-I and H1-II from the multicellular green alga Volvox
carteri and an H1 gene from the unicellular green alga
Chlamydomonas reinhardtii both display a sequence alignment
typical of the winged helix motif of linker histone H1 from plants and
animals (see also Table 1
). Of these, expression of the linker histone
genes has been demonstrated only in C. reinhardtii
(33)
. H1 histone has been purified by chromatography from
the unicellular green alga Chlorella ellipsoidea
(34)
. The composition in mol % of its three most abundant
aminoacyl residues Lys, Ala, and Pro (KAP) is similar to that of the
putative protein of the H1-I gene for V. carteri (see Table 1
). In the yeast Saccharomyces cerevisiae, there is an H1
gene of 258 aminoacyl residues encoded in the genome (35)
that is expressed as a poly(A)+ RNA and whose
gene product is localized to the nucleus (36)
. Although
there is biochemical in vitro evidence to suggest that this
protein indeed behaves as a canonical linker histone (37)
,
evidence for this role in vivo is still lacking. The
sequence data suggest that it may also contain a second winged helix
motif at its carboxyl-terminal end. On the contrary, the histone H1s
from the multicellular fungi Neurospora crassa (D. Folco, M.
Freitag, E. Selker and A. Rosa, unpublished results), Ascolobus
immersus (38)
and Aspergillus nidulans
(39)
contain the tripartite structural organization that
is found in all multicelled eukaryotes (see Fig. 2
, Fig. 4
, and Table 1
).
Genes encoding linker histones H1 and H1–2 are also present in a
mycetozoan, the cellular slime mold Dictyostelium discoideum
(Fig. 2)
, where the proteins have also been purified by chromatography
(40)
but not sequenced. In addition, a histone H1 was
chromatographically purified from plasmodia of the acellular slime mold
Physarum polycephalum (41)
, another mycetozoan.
These proteins have the lowest carboxy-terminal (KAP) amino acid
composition of all the winged helix containing H1s (see Table 1
). Yet
they contain a sequence with extensive similarity to the consensus
sequence of the winged helix motif of H1 histones in multicelled
eukaryotes (see Fig. 2
). These findings therefore indicate that H1
linker histones with a winged helix motif appeared separately in at
least two disparate lines of eukaryotes (Fig. 5)
, possibly as the
result of two separate fusion events between the carboxyl-terminal
domain of H1 and the proto-winged helix domain protein.
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HISTONE H1-RELATED PROTEINS IN EUBACTERIA AND THE CARBOXYL TERMINI OF METAZOAN H1 HISTONES |
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TOPABSTRACTINTRODUCTIONCORE HISTONES, LINKER HISTONES,...THE LYSINE-RICH CARBOXYL...H1 LINKER HISTONES IN...EVOLUTIONARY APPEARANCE OF THE...HISTONE H1-RELATED PROTEINS IN...OVERVIEWREFERENCES |
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, 42
43
44
45; R. Heilig, unpublished results)
.
The encoded genes for basic proteins in several eubacteria show more
similarity to the carboxyl terminus of a typical metazoan histone H1
than do the encoded H1 histone genes of some of the alveolates and
Entamoeba described in the preceding section (Fig. 3
, Fig. 4
, and Table 1
). The amino acid compositional similarity of the histone
H1-related proteins in Chlamydia pneumonia and C.
trachomatis (46)
to that of the carboxyl terminus of
histone H1 is striking (see Table 1
). Furthermore, their sequence
similarity is in some instances even higher than in their protist
counterparts (see Fig. 3
). Other examples of this kind include
Coxiella burnetii, Streptomyces coelicolor, and
Bordetella pertussis (see Fig. 4
and Table 1
).
In the proteobacteria (a subgroup of eubacteria), similar results can
be seen (Fig. 4)
for Salmonella typhimurium, Pseudomonas
aeruginosa, Escherichia coli, and Haemophilus
influenzae. However, the lysine content of these proteins is lower
than expected and, in general, they have a higher alanine content (see
Table 1
).
It is therefore quite likely that the lysine-rich DNA binding proteins
found in eubacteria are evolutionarily related to the histone H1
truncated versions also found in protists (see above) and to the
carboxyl terminus of histone H1 in metazoans and other multicelled
eukaryotes. The occurrence of histone H1-related proteins in eubacteria
stands in contrast to archaebacteria, which have core histones but not
H1-like histones in any of the five genomes that have been sequenced
from the euryarchaeal kingdom (42
43
44
45
; R. Helig,
unpublished results).
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OVERVIEW |
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TOPABSTRACTINTRODUCTIONCORE HISTONES, LINKER HISTONES,...THE LYSINE-RICH CARBOXYL...H1 LINKER HISTONES IN...EVOLUTIONARY APPEARANCE OF THE...HISTONE H1-RELATED PROTEINS IN...OVERVIEWREFERENCES |
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In the linker histones of multicelled eukaryotes, the lysine-rich
nature of these proteins is the result of the high lysine content of
their carboxyl-terminal domains. As mentioned earlier, the carboxyl
termini of these molecules play a critical role in their function of
chromatin condensation. Because of these very particular yet rather
simple compositional constraints of such domains, it should in
principle be possible to identify structurally and functionally related
proteins of this family by simply examining their amino acid
composition (see Table 1
). In our comparative analysis, we have used
histone H1 from the sea urchin Strongylocentrotus purpuratus
as a reference because it exhibits a high degree of sequence similarity
to the consensus sequence of the globular domain while containing a
good representation of the KAP repeats that are characteristic of the
carboxyl termini of H1s in multicelled eukaryotes (16
, 17)
.
From the analysis obtained with these tools (Table 1
, Figs. 2
3
4
), it
is possible to trace the evolutionary origin of histone H1 to the
DNA-condensing, lysine-rich proteins of eubacteria (see Fig. 5
). In
fact, the extent of sequence similarity of Chlamydia
H1-related proteins to the carboxyl-terminal domain of metazoan H1
histones is striking, considering the enormous overall variability of
this histone family.
One interesting question to address is the following: If core histones
arose in archaea and lysine-rich basic proteins arose in eubacteria,
then how did they come together in eukaryotes? This might have occurred
as a result of a lateral gene transfer (LGT) event in the early
proto-eukaryote (thought to resemble an archaeal ancestor), as LGT has
recently come to light as a major evolutionary force in both eubacteria
and archaea (47)
. The conjunction of the ancestral histone
proteins in eukaryotes could also have arisen from the large-scale
transfer of genes that accompanied the first endosymbiosis of the alpha
proteobacteria that gave rise to the mitochondria.
The ancestor of eukaryotes might already have had archaeal histone
precursors that incorporated the carboxyl- and amino-terminal domains
present in the core histones of all eukaryotic organisms. These
proteins led to the appearance of the nucleosome organization. Hence,
they represent the origin of eukaryotic chromatin. In a broad sense,
they provide the structural substrate on which eukaryotic gene
regulation takes place. The incorporation of the archaeal histone
precursors might either have been a by-product of, or the step allowing
for, the large-scale expansion that generally characterizes eukaryotic
genomes. DNA already bound by these proteins may have gained further
protection from the incorporation of the lysine-rich bacterial H1
precursors, providing an additional condensation of the ‘naked’
linker DNA regions connecting the nucleosome structures that resulted
from the core histone-DNA interactions. It has been shown that the
small lysine-rich H1-related protein from T. brucei
contributes both to the spacing of nucleosomes on the DNA and the
extensive condensation of the chromatin fiber (22)
,
demonstrating that this function for histone H1 is not restricted to
animal and plant taxa.
The acquisition of the globular winged helix occurred later in
eukaryotic evolution (see Figs. 4
and 5
), possibly to provide
specificity for the targeting of the H1 molecules to the linker DNA
regions by providing structural recognition of the four-way junction
DNA-like structures that are present at the sites of DNA entry and exit
in the nucleosome (48)
. Furthermore, such an incorporation
most likely contributed to enhance chromatin folding into the 30 nm
fiber (49)
, which is present in all multicelled eukaryotes
but absent in Trypanosoma (22)
. It is also
important to note that we have not found any H1 molecules in
multicelled eukaryotes that did not have an amino-terminal domain.
Thus, it appears that the amino-terminal and globular domains have
evolved together, although the rate of variation has been higher in the
amino-terminal region. Even though the amino-terminal domain of linker
histones does not seem to be critical for chromatin folding
(19)
and the functional and structural roles of this part
of the molecule are still obscure, this region may play an important
role in modulating the binding affinity of the whole histone H1
molecule to chromatin and/or in the head-to-tail interactions of the
linker histones that occur in the chromatin fiber (50)
.
If the histone fold of the core histones (see Fig. 1A
)
provides a structural signature for these proteins such as that
provided by the winged helix and carboxyl-terminal domains of the
linker histones (see Fig. 1B
, C
), then no genes or proteins
have been identified to date in eubacteria that resemble or have any
similarity to the core histones. It thus appears that ‘core’ and
‘linker’ histones, despite their common histone
nomenclature, have evolved quite independently from entirely unrelated
genes in archaebacteria and eubacteria, respectively. In contrast with
the evolutionarily conserved core histones (7)
, the
variability of linker histones and their increasing evolutionary
complexity mirrors the developmental variability and complexity of
living organisms, starting from eubacteria. Thus, the increase in
complexity of the linker histones most likely occurred in response to
(and reflects) the increasing functional complexity of the different
chromatin domains within the eukaryotic cell and has been
developmentally driven. Despite this variability and the limited
sequence information available so far, the information compiled in this
review indicates that linker histone evolution had its origin in
eubacteria.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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2 These authors have contributed equally to this work.
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REFERENCES |
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M. J. Hendzel, M. A. Lever, E |
