Stepwise Evolution of Essential Centromere Function in a
            <i>Drosophila</i>
            Neogene

Ross, Benjamin D.; Rosin, Leah F.; Thomae, Andreas W.; Hiatt, Mary Alice; Vermaak, Danielle; Cruz, Aida Flor A. de la; Imhof, Axel; Mellone, Barbara G.; Malik, Harmit S.

doi:10.1126/science.1234393

Cited by 97 publications

(125 citation statements)

References 38 publications

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“…It has been previously hypothesized that genes that encode proteins interacting strongly with heterochromatin can be potential actors of genetic conflicts (10,15,19,23). We show here for the first time, to our knowledge, that such a gene, expressed in the male germ line, plays a key role in an extended intragenomic conflict in D. simulans.…”

Section: Resultsmentioning

confidence: 66%

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Rapid evolution of a Y-chromosome heterochromatin protein underlies sex chromosome meiotic drive

Helleu

Gérard

Dubruille

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Sex chromosome meiotic drive, the non-Mendelian transmission of sex chromosomes, is the expression of an intragenomic conflict that can have extreme evolutionary consequences. However, the molecular bases of such conflicts remain poorly understood. Here, we show that a young and rapidly evolving X-linked heterochromatin protein 1 (HP1) gene, HP1D2, plays a key role in the classical Paris sex-ratio (SR) meiotic drive occurring in Drosophila simulans. Driver HP1D2 alleles prevent the segregation of the Y chromatids during meiosis II, causing female-biased sex ratio in progeny. HP1D2 accumulates on the heterochromatic Y chromosome in male germ cells, strongly suggesting that it controls the segregation of sister chromatids through heterochromatin modification. We show that Paris SR drive is a consequence of dysfunctional HP1D2 alleles that fail to prepare the Y chromosome for meiosis, thus providing evidence that the rapid evolution of genes controlling the heterochromatin structure can be a significant source of intragenomic conflicts. meiotic drive | intragenomic conflict | heterochromatin | sex chromosomes

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Section: Resultsmentioning

confidence: 66%

“…However, because HP1D2 SR localizes to the Y chromosome as well, we cannot exclude that CSD-lacking HP1D2 proteins cause drive through aberrant interactions with other chromatin proteins. If it is the case, CSD-lacking HP1D2 may evolve a new function, which has been described for another HP1 (23).…”

Section: Hp1d2 Ismentioning

confidence: 99%

Rapid evolution of a Y-chromosome heterochromatin protein underlies sex chromosome meiotic drive

Helleu

Gérard

Dubruille

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Also notably, the CMS gene origination processes from the protogene orf367 to the functional genes WA352a/b/c and WA314 were completed within a relatively short timeframe in O. rufipogon (less than two million years [19]). This process appears to be much faster than the origination of most nuclear new genes, such as the new Drosophila gene Umbrea whose origination has spent 15 million years [45], thus reflecting the remarkably dynamic properties of plant mitochondrial genomes.…”

Section: Discussionmentioning

confidence: 99%

Multi-step formation, evolution, and functionalization of new cytoplasmic male sterility genes in the plant mitochondrial genomes

Tang

Zheng

et al. 2016

Cell Res

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New gene origination is a major source of genomic innovations that confer phenotypic changes and biological diversity. Generation of new mitochondrial genes in plants may cause cytoplasmic male sterility (CMS), which can promote outcrossing and increase fitness. However, how mitochondrial genes originate and evolve in structure and function remains unclear. The rice Wild Abortive type of CMS is conferred by the mitochondrial gene WA352c (previously named WA352) and has been widely exploited in hybrid rice breeding. Here, we reconstruct the evolutionary trajectory of WA352c by the identification and analyses of 11 mitochondrial genomic recombinant structures related to WA352c in wild and cultivated rice. We deduce that these structures arose through multiple rearrangements among conserved mitochondrial sequences in the mitochondrial genome of the wild rice Oryza rufipogon, coupled with substoichiometric shifting and sequence variation. We identify two expressed but nonfunctional protogenes among these structures, and show that they could evolve into functional CMS genes via sequence variations that could relieve the self-inhibitory potential of the proteins. These sequence changes would endow the proteins the ability to interact with the nucleus-encoded mitochondrial protein COX11, resulting in premature programmed cell death in the anther tapetum and male sterility. Furthermore, we show that the sequences that encode the COX11-interaction domains in these WA352c-related genes have experienced purifying selection during evolution. We propose a model for the formation and evolution of new CMS genes via a "multi-recombination/protogene formation/functionalization" mechanism involving gradual variations in the structure, sequence, copy number, and function.

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“…The availability of genome sequences from many organisms has revealed that gene duplication followed by retention of two functional copies is widespread (for reviews, see Prince and Pickett 2002;Long et al 2003; see also Chen et al 2010;Ross et al 2013). According to classical models, duplicated genes can have two main fates.…”

Section: Discussionmentioning

confidence: 99%

Gene duplication and neofunctionalization: POLR3G and POLR3GL

et al. 2013

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RNA polymerase III (Pol III) occurs in two versions, one containing the POLR3G subunit and the other the closely related POLR3GL subunit. It is not clear whether these two Pol III forms have the same function, in particular whether they recognize the same target genes. We show that the POLR3G and POLR3GL genes arose from a DNA-based gene duplication, probably in a common ancestor of vertebrates. POLR3G-as well as POLR3GL-containing Pol III are present in cultured cell lines and in normal mouse liver, although the relative amounts of the two forms vary, with the POLR3G-containing Pol III relatively more abundant in dividing cells. Genome-wide chromatin immunoprecipitations followed by high-throughput sequencing (ChIP-seq) reveal that both forms of Pol III occupy the same target genes, in very constant proportions within one cell line, suggesting that the two forms of Pol III have a similar function with regard to specificity for target genes. In contrast, the POLR3G promoter-not the POLR3GL promoter-binds the transcription factor MYC, as do all other promoters of genes encoding Pol III subunits. Thus, the POLR3G/POLR3GL duplication did not lead to neo-functionalization of the gene product (at least with regard to target gene specificity) but rather to neo-functionalization of the transcription units, which acquired different mechanisms of regulation, thus likely affording greater regulation potential to the cell.

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Stepwise Evolution of Essential Centromere Function in a Drosophila Neogene

Cited by 97 publications

References 38 publications

Rapid evolution of a Y-chromosome heterochromatin protein underlies sex chromosome meiotic drive

Rapid evolution of a Y-chromosome heterochromatin protein underlies sex chromosome meiotic drive

Multi-step formation, evolution, and functionalization of new cytoplasmic male sterility genes in the plant mitochondrial genomes

Gene duplication and neofunctionalization: POLR3G and POLR3GL

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