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Recurrent Evolution of DNA-Binding Motifs in the Drosophila Centromeric Histone

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Recurrent Evolution of DNA-Binding Motifs in the Drosophila Centromeric Histone Recurrent evolution of DNA-binding motifs in the Drosophila centromeric histone Harmit S. Malik*, Danielle Vermaak*, and Steven Henikoff*†‡ †Howard Hughes Medical Institute, *Basic Sciences Division, Fred Hutchinson Cancer Research Center, Seattle, WA 98109 Communicated by Stanley M. Gartler, University of Washington, Seattle, WA, December 12, 2001 (received for review October 29, 2001) All eukaryotes contain centromere-specific histone H3 variants being one of the most evolutionarily constrained classes of (CenH3s), which replace H3 in centromeric chromatin. We have eukaryotic proteins. Second, CenH3s are evolving adaptively, previously documented the adaptive evolution of the Drosophila presumably in concert with centromeres, which consist of the CenH3 (Cid) in comparisons of Drosophila melanogaster and Dro- most rapidly evolving DNA in the genome. sophila simulans, a divergence of Ϸ2.5 million years. We have Chromosomes (and their centromeres) may compete at mei- proposed that rapidly changing centromeric DNA may be driving osis I for inclusion into the oocyte (11). A centromeric satellite CenH3’s altered DNA-binding specificity. Here, we compare Cid expansion could bias centromeric strength, leading to preferred sequences from a phylogenetically broader group of Drosophila inclusion in the oocyte, but also to increased nondisjunction. A species to suggest that Cid has been evolving adaptively for at least subsequent alteration of CenH3’s DNA-binding preferences 25 million years. Our analysis also reveals conserved blocks not could restore parity among different chromosomes (2), thereby only in the histone-fold domain but also in the N-terminal tail. In alleviating the deleterious consequences of satellite drive. Suc- several lineages, the N-terminal tail of Cid is characterized by cessive rounds of satellite and CenH3 drive are detected as an subgroup-specific oligopeptide expansions. These expansions re- excess of replacement changes in CenH3. Adaptive evolution of semble minor groove DNA binding motifs found in various histone CenH3 has been documented in the histone fold domain of tails. Remarkably, similar oligopeptides are also found in N-termi- Drosophila (10). The N-terminal tails of CenH3 in both Dro- nal tails of human and mouse CenH3 (Cenp-A). The recurrent sophila and Arabidopsis are also subject to adaptive evolution, evolution of these motifs in CenH3 suggests a packaging function consistent with their proposed role in contacting centromeric for the N-terminal tail, which results in a unique chromatin orga- DNA (10, 12). In addition, deletion studies in Saccharomyces nization at the primary constriction, the cytological marker of cerevisiae have revealed essential protein–protein interaction centromeres. sites encoded within the N-terminal tail of CenH3 (13). Al- though sequence divergence precludes aligning the N-terminal entromeres are the chromosomal loci responsible for pole- tails of CenH3s from different lineages, a comprehensive study Cward movement at meiosis and mitosis, and are essential for of the molecular evolution within a particular lineage of CenH3s could help elucidate function for this important feature of the faithful segregation of genetic information. Despite their GENETICS crucial role in the cell cycle, relatively little is known about how centromeric chromatin by revealing the architecture of evolu- most centromeres are organized at the molecular level. In tionary constraint. complex eukaryotes, centromeres contain large arrays of tan- To this end, we present a detailed analysis of the evolution of demly repeated satellite sequences, yet their inheritance appears the Drosophila centromeric histone (Cid) in the melanogaster to be largely sequence-independent (reviewed in refs. 1–3). group of species. Comparison of Cid genes across this 25-million- Instead, the presence of specialized centromeric histones is year divergence reveal highly conserved blocks in the histone thought to be a key determinant of centromere identity and fold domain, as expected, with the DNA-binding Loop 1 region maintenance. Centromeric histones (CenH3s) belong to the (14) evolving most rapidly. This analysis also revealed the histone H3 family of proteins, based on homology in the histone unexpected presence of oligopeptide repeats in the N-terminal fold domain, and can replace H3 in nucleosomes (4, 5). However, tail of at least three different lineages of Drosophila Cids. The centromeric chromatin is distinct from the rest of the genome, occurrence of these expansions in some vertebrate CenH3s and as demonstrated by nuclease accessibility studies in both budding their similarity to previously documented peptides that interact and fission yeast (6–8), as well as by topoisomerase II cleavage with the minor groove of DNA suggest an attractive model for patterns of human centromeres (9). Instead of the regular the unique chromatin structure present at centromeres. nucleosomal arrays observed in surrounding heterochromatin, Methods centromeric DNA appears uniformly accessible to nucleases. These findings have led to suggestions that centromeric nucleo- Drosophila species (Table 1) were obtained from the Drosophila somes are randomly arranged (6, 7). A better understanding of Species Center (presently at Tucson, AZ) except for Drosophila this atypical chromatin might be gained by a closer examination trilutea (kind gift of Dr. M.T. Kimura, Hokkaido University, of CenH3 evolution. Japan). Genomic DNA was extracted from all flies and PCR was The structural organization of the C-terminal histone fold carried out to amplify the Cid gene and flanking regions as domain of CenH3 is believed to be very similar to that of H3 described in ref. 10. For more divergent species, additional itself, based on greater than 40% amino acid identity and analysis primers were designed to internal regions of Cid that are Ј Ј of reconstituted nucleosomes (2, 4). However, this domain relatively conserved, 5 -CGGCAGCTTGGGTATCAGTGT-3 evolves more rapidly in CenH3s than in canonical H3s. In addition, whereas H3 has a conserved 45-aa N-terminal tail, those of CenH3s vary in size from 20 to 200 aa, and cannot be Abbreviation: CenH3, centromeric histone H3. Data deposition: The sequences reported in this paper have been deposited in the GenBank aligned across different eukaryotic lineages (2). database (accession nos. AF435454–AF435467). This dichotomy in evolutionary rates between CenH3s and ‡To whom reprint requests should be addressed at: 1100 Fairview Avenue North A1-162, H3s is believed to have two causes. First, whereas the CenH3s are Seattle, WA 98109-1024. E-mail: [email protected]. only required to interact with centromeric DNA, conventional The publication costs of this article were defrayed in part by page charge payment. This H3 needs to interact with, and mediate the expression of, the rest article must therefore be hereby marked “advertisement” in accordance with 18 U.S.C. of the genome (10). This requirement results in the latter class §1734 solely to indicate this fact. www.pnas.org͞cgi͞doi͞10.1073͞pnas.032664299 PNAS ͉ February 5, 2002 ͉ vol. 99 ͉ no. 3 ͉ 1449–1454 Downloaded by guest on October 2, 2021 Table 1. Species used in the present study bio.psu.edu͞adaptivevol.html). Briefly, the alignment and phy- Drosophila GenBank logenetic tree are used to infer ancestral codons at all interior species Species group Stock center ID accession nos. nodes of the tree. Next, the total number of synonymous and nonsynonymous substitutions are calculated for each codon and melanogaster melanogaster ref. 3 AF259371 a global average is computed. Adaptive evolution is inferred simulans melanogaster ref. 3 AF321923 when the rate of nonsynonymous substitutions per nonsynony- sechellia melanogaster 14021-0248.0 AF321925 mous site (rN) exceeds that of synonymous substitutions per Ͻ mauritiana melanogaster 14021-0241.0 AF321924 synonymous site (rS) at a significant level. Conversely, if rS rN, yakuba melanogaster 14021-0261.0 AF435454 purifying selection is inferred. The 9-aa expansions in both the teissieri melanogaster 14021-0257.0 AF321926 takahashii and ananassae groups were examined for evidence of orena melanogaster 14021-0245.0 AF435456 natural selection. We used adaptsite-d (Poisson) to calculate rN erecta melanogaster 14021-0224.0 AF435455 and rS followed by adaptsite-t to evaluate statistical significance. takahashii takahashii 14022-0311.0 AF435460 PDB structures of the nucleosome core particle (1AOI, ref. trilutea takahashii Dr. M.T. Kimura AF435457 14) were displayed using the SWISSPDB VIEWER (Version 3.7b2, prostipennis takahashii 14022-0291.0 AF435354 http:͞͞www.expasy.ch͞spdbv). paralutea takahashii 14022-0281.0 AF435458 lutescens takahashii 14022-0271.0 AF435459 Results lucipennis suzukii 14023-0331.0 AF435356 To amplify a phylogenetic range of Cid sequences (Table 1), we mimetica suzukii 14023-0341.0 AF435461 used a PCR strategy using internal primers in conjunction with rajasekhari suzukii 14023-0361.0 AF435355 primers to upstream and downstream genes (10). In all 22 species ananassae ananassae 14024-0371.0 AF435466 studied, the Cid gene lacks introns and varies from 639 to 879 bipectinata ananassae 14024-0381.0* AF435462 nucleotides in length. Most of the length variation in Cid can be malerkotliana ananassae 14024-0391.0 AF435463 attributed to the N-terminal tail, whereas the histone fold pseudoananassae ananassae 14024-0411.0 AF435465 domain is nearly constant in length (schematized in Fig. 1A). parabipectinata ananassae 14024-0401.0
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