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Diversification of histone H2A variants during plant evolution

https://doi.org/10.1016/j.tplants.2015.04.005Get rights and content

Highlights

  • Flowering plants have evolved a large array of unusual histone variants.

  • Three major features categorize H2A histones into distinct variant classes.

  • Canonical H2A and H2A.X diverged already in green algae.

  • Additional diversification of H2A.X took place gradually during land plant evolution.

  • In addition to H2A.Z and H2A.X, the land plant ancestors evolved two variant classes H2A.M and H2A.W.

Among eukaryotes, the four core histones show an extremely high conservation of their structure and form nucleosomes that compact, protect, and regulate access to genetic information. Nevertheless, in multicellular eukaryotes the two families, histone H2A and histone H3, have diversified significantly in key residues. We present a phylogenetic analysis across the green plant lineage that reveals an early diversification of the H2A family in unicellular green algae and remarkable expansions of H2A variants in flowering plants. We define motifs and domains that differentiate plant H2A proteins into distinct variant classes. In non-flowering land plants, we identify a new class of H2A variants and propose their possible role in the emergence of the H2A.W variant class in flowering plants.

Section snippets

Histone variants

Eukaryotic genomes are compacted into chromatin, consisting of histone proteins and DNA. A basic unit of chromatin is the nucleosome, which is organized as ∼150 bp DNA wrapped around a histone octamer made from two of each core histone family, H2A, H2B, H3, and H4 1, 2. Between nucleosomes, the linker DNA may be bound by a member of the histone family H1 3, 4. In multicellular eukaryotes, histones are commonly encoded by multigene families, and individual paralogous genes of a histone family

Features defining H2A variants in flowering plants

To classify histone variants from non-flowering plants, we first analyzed H2A variants from a large set of flowering plants with the aim of defining variant-specific signatures (Figure S1 in the supplementary material online). In general, the lengths and specific amino acid sequences of C-terminal tails differentiate H2A proteins into distinct variant classes (Figure 1A). C-terminal tails of canonical H2A variants invariably end with a cluster of acidic amino acids, while C-terminal tails of

The diversity of histone variants in non-flowering land plants and green algae

Evolution of land plants is marked by at least three major transitions: (i) the conquest of the land by bryophytes, (ii) vasculature development and the dominance of diploid sporophytic generation in lycophytes, and (iii) the acquisition of elaborate reproductive structures including seeds and flowers in gymnosperms and angiosperms 49, 50, 51, 52. We used recently released genome sequences of key species that mark each of these transitions to identify histone-coding genes. H2A variants show a

Variants related to H2A.W

In the genome of the gymnosperm Picea abies we identified 13 variants, and these contained most of the signatures characteristic of H2A.W. Of those, five clearly cluster with flowering plant H2A.Ws (Figure 2). The other eight variants cluster as a separate group and differ from gymnosperm bona fide H2A.Ws in their C-terminal tails by the presence of the conserved sequence KSPKSK instead of KSPKKA (Figure 3). The L1 loop and the docking domain signatures of these variants resemble those of bona

Concluding remarks

Our survey across key species as representatives of plant evolution confirms that a large diversity of histone variants arose with the exception of H4. The lack of H4 variants is also notable in metazoans, and this strong evolutionary conservation of H4 sequence, together with the minimal sequence differences among major H3 variants (i.e., H3.1 and H3.3), likely reflects the high structural constraints required for the stabilization of the H3/H4 tetramer and its incorporation into nucleosome [1]

Acknowledgments

We are grateful to Paul Talbert for critical comments on the manuscript and members of the Berger lab for discussion of the data. We thank the Joint Genome Institute for providing the genomic assemblies and transcriptomes of the ongoing M. polymorpha genome project. This work was supported by Österreichische Akademie der Wissenschaften (ÖAW) and by a grant from the Österreichischer Fonds zur Forderung der wissenschaftlichen Forschung (FWF) (grant number P26887) to F.B.

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