Causes and consequences of the evolution of reproductive proteins

Turner, Leslie M.; Hoekstra, Hopi E.

doi:10.1387/ijdb.082577lt

Cited by 109 publications

(158 citation statements)

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“…Brain-expressed genes originating in the primate lineage may underlie neural reorganization and complex behaviors (13). Because reproductive genes tend to evolve rapidly and may contribute to speciation (14), reproductive genes unique to primates may have had a role in species-specific phenotypes.…”

Section: Resultsmentioning

confidence: 99%

Global discovery of primate-specific genes in the human genome

Tay

Blythe

Lipovich

2009

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

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The genomic basis of primate phenotypic uniqueness remains obscure, despite increasing genome and transcriptome sequence data availability. Although factors such as segmental duplications and positive selection have received much attention as potential drivers of primate phenotypes, single-copy primate-specific genes are poorly characterized. To discover such genes genomewide, we screened a catalog of 38,037 human transcriptional units (TUs), compiled from EST and cDNA sequences in conjunction with the FANTOM3 transcriptome project. We identified 131 TUs from transcribed sequences residing within primate-specific insertions in 9-species sequence alignments and outside of segmental duplications. Exons of 120 (92%) of the TUs contained interspersed repeats, indicating that repeat insertions may have contributed to primate-specific gene genesis. Fifty-nine (46%) primate-specific TUs may encode proteins. Although primate-specific TU transcript lengths were comparable to known human gene mRNA lengths overall, 92 (70%) primate-specific TUs were single-exon. Thirty-two (24%) primate-specific TUs were localized to subtelomeric and pericentromeric regions. Forty (31%) of the TUs were nested in introns of known genes, indicating that primate-specific TUs may arise within older, protein-coding regions. Primate-specific TUs were preferentially expressed in reproductive organs and tissues ( P < 0.011), consistent with the expectation that emergence of new, lineage-specific genes may accompany speciation or reproduction. Of the 33 primate-specific TUs with human Affymetrix microarray probe support, 21 were differentially expressed in human teratozoospermia. In addition to elucidating the likely functional relevance of primate-specific TUs to reproduction, we present a set of primate-specific genes for future functional studies, and we implicate nonduplicated pericentromeric and subtelomeric regions in gene genesis.

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Section: Resultsmentioning

confidence: 99%

Global discovery of primate-specific genes in the human genome

Tay

Blythe

Lipovich

2009

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

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“…S5 and S6). The younger genes in later development of D. rerio may have been influenced by the presence of the reproductive tract in the samples, as numerous TF innovations have been described in the reproductive tract (48).…”

Section: Phylostratigraphic Analysis Of Tfome Expression In Multicellmentioning

confidence: 99%

Transcription factor evolution in eukaryotes and the assembly of the regulatory toolkit in multicellular lineages

Mendoza

Sebé-Pedrós

Šestak

et al. 2013

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

200

224

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Transcription factors (TFs) are the main players in transcriptional regulation in eukaryotes. However, it remains unclear what role TFs played in the origin of all of the different eukaryotic multicellular lineages. In this paper, we explore how the origin of TF repertoires shaped eukaryotic evolution and, in particular, their role into the emergence of multicellular lineages. We traced the origin and expansion of all known TFs through the eukaryotic tree of life, using the broadest possible taxon sampling and an updated phylogenetic background. Our results show that the most complex multicellular lineages (i.e., those with embryonic development, Metazoa and Embryophyta) have the most complex TF repertoires, and that these repertoires were assembled in a stepwise manner. We also show that a significant part of the metazoan and embryophyte TF toolkits evolved earlier, in their respective unicellular ancestors. To gain insights into the role of TFs in the development of both embryophytes and metazoans, we analyzed TF expression patterns throughout their ontogeny. The expression patterns observed in both groups recapitulate those of the whole transcriptome, but reveal some important differences. Our comparative genomics and expression data reshape our view on how TFs contributed to eukaryotic evolution and reveal the importance of TFs to the origins of multicellularity and embryonic development.phylotypic stage | Holozoa | LECA T ranscription factors (TFs) are proteins that bind to DNA in a sequence-specific manner (1) and enhance or repress gene expression (2-4). In response to a broad range of stimuli, TFs coordinate many important biological processes, from cell cycle progression and physiological responses, to cell differentiation and development (5, 6). Thus, TFs have a central role in the transcriptional regulation of all cellular organisms, being present in all branches of the tree of life (bacteria, archaea, and eukaryotes). There appears to be a correlation between elaborate regulation of gene expression and the complexity of organisms (7), such that the amount (as a proportion of an organism's total gene content) and diversity of TF proteins is expected to be directly correlated with this complexity (8). Indeed, TFs play a crucial role in multicellular eukaryotes. For example, TFs are the master regulators of embryonic development in embryophytes and metazoans (9), and analyses of their embryonic transcriptional profiles support the presence of a phylotypic stage in both lineages (10-14). These studies have also shown that evolutionarily younger genes tend to be expressed at earlier and later stages of development, whereas the transcriptomes of the middle stages (the phylotypic stage) are dominated by ancient genes (10, 13). It remains to be investigated how the evolutionary age and the expression patterns of the different TFs shift throughout the ontogeny of these lineages and whether TF expression profiles correlate with the general transcriptome profiles.Previous studies have analyzed the evolutionary ...

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“…Therefore, it was a surprise when the first molecular evolutionary analyses on reproduction-related genes (or proteins) revealed their faster than normal evolutionary rates (see, e.g., Swanson et al 2001;Swanson and Vacquier 2002a,b). Since then, analyses of additional reproductive genes in additional species continue to support the initial observation that reproductive genes evolve more rapidly than the genomic average (e.g., Cutter and Ward 2005;Clark et al 2006Clark et al , 2009Ramm et al 2008;Turner and Hoekstra 2008;Findlay and Swanson 2010;Wong 2011). A common and particularly typical pattern for reproductive genes is a higher ratio, often denoted as d N /d S (= v), of the number of nonsynonymous nucleotide substitutions per nonsynonymous site (d N ) to the number of synonymous nucleotide substitutions per synonymous site (d S ).…”

mentioning

confidence: 93%

“…This pattern seems to be particularly remarkable among "sperm genes", namely, genes whose protein products are found in sperm (e.g., Wyckoff et al 2000;Torgerson et al 2002;Swanson et al 2003;Nielsen et al 2005;Artieri et al 2008;Dorus et al 2010 et al 1997), but this applies only to genes that are involved in battles against pathogens; and (iii) reinforcement of reproductive incompatibility in a speciation event can also accelerate the evolution of sperm genes (Dobzhansky 1940;Howard 1993), but this works only on special occasions where two closely related sympatric species coexist. Most other models and hypotheses invoke either postcopulatory sexual selection, namely selection on reproductive genes after mating (reviewed, e.g., in Birkhead and Pizzari 2002;Swanson and Vacquier 2002b;Clark et al 2006;Turner and Hoekstra 2008), or sexual conflict (e.g., Rice and Holland 1997;Frank 2000;Gavrilets 2000;Chapman et al 2003;Hayashi et al 2007). So far, these models have mainly focused on selection and/or competition at the individual level; when they consider a competition among sperm, it is almost always among sperm produced by different males.…”

mentioning

confidence: 99%

Competition Between the Sperm of a Single Male Can Increase the Evolutionary Rate of Haploid Expressed Genes

Ezawa

Innan

2013

Genetics

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The population genetic behavior of mutations in sperm genes is theoretically investigated. We modeled the processes at two levels. One is the standard population genetic process, in which the population allele frequencies change generation by generation, depending on the difference in selective advantages. The other is the sperm competition during each genetic transmission from one generation to the next generation. For the sperm competition process, we formulate the situation where a huge number of sperm with alleles A and B, produced by a single heterozygous male, compete to fertilize a single egg. This "minimal model" demonstrates that a very slight difference in sperm performance amounts to quite a large difference between the alleles' winning probabilities. By incorporating this effect of paternity-sharing sperm competition into the standard population genetic process, we show that fierce sperm competition can enhance the fixation probability of a mutation with a very small phenotypic effect at the singlesperm level, suggesting a contribution of sperm competition to rapid amino acid substitutions in haploid-expressed sperm genes. Considering recent genome-wide demonstrations that a substantial fraction of the mammalian sperm genes are haploid expressed, our model could provide a potential explanation of rapid evolution of sperm genes with a wide variety of functions (as long as they are expressed in the haploid phase). Another advantage of our model is that it is applicable to a wide range of species, irrespective of whether the species is externally fertilizing, polygamous, or monogamous. The theoretical result was applied to mammalian data to estimate the selection intensity on nonsynonymous mutations in sperm genes. FOR sexual organisms, reproduction is an essential process that allows an individual's genomic information to survive beyond its lifetime. Years ago, it was thought that the functional constraints on genes involved in reproduction should be as strong as those on functionally important genes such as histones, etc. (e.g., Miyata and Yasunaga 1980;Li 1997); hence it was predicted that such genes should evolve much more slowly than average. Therefore, it was a surprise when the first molecular evolutionary analyses on reproduction-related genes (or proteins) revealed their faster than normal evolutionary rates (see, e.g., Swanson et al. 2001; Swanson and Vacquier 2002a,b). Since then, analyses of additional reproductive genes in additional species continue to support the initial observation that reproductive genes evolve more rapidly than the genomic average (e.g., Cutter and Ward 2005;Clark et al. 2006Clark et al. , 2009Ramm et al. 2008;Turner and Hoekstra 2008;Findlay and Swanson 2010; Wong 2011). A common and particularly typical pattern for reproductive genes is a higher ratio, often denoted as d N /d S (= v), of the number of nonsynonymous nucleotide substitutions per nonsynonymous site (d N ) to the number of synonymous nucleotide substitutions per synonymous site (d S ). This pa...

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Causes and consequences of the evolution of reproductive proteins

Cited by 109 publications

References 118 publications

Global discovery of primate-specific genes in the human genome

Global discovery of primate-specific genes in the human genome

Transcription factor evolution in eukaryotes and the assembly of the regulatory toolkit in multicellular lineages

Competition Between the Sperm of a Single Male Can Increase the Evolutionary Rate of Haploid Expressed Genes

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