A de novo originated gene depresses budding yeast mating pathway and is repressed by the protein encoded by its antisense strand

Li, Dan; Dong, Yang; Jiang, Yu; Jiang, Huifeng; Cai, Jing; Wang, Wen

doi:10.1038/cr.2010.31

Cited by 114 publications

(119 citation statements)

References 34 publications

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“…This model has some features distinct from the current models for the origination of new nuclear genes [32,37,[40][41][42][43][44], including the "RNA-first" and "ORF-first" routes for generation of de novo genes [44]. 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]).…”

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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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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“…When presented with environmental challenges, organisms adapt by using a range of strategies, including new enzymatic functions and novel regulatory processes. In natural systems, there are numerous precedents showing that selecting for growth under specified conditions can yield mutations that rewire gene regulation (27)(28)(29)(30)(31). For example, Taylor et al (27) showed that immotile mutants of Pseudomonas fluorescens subjected to selections for motility evolve by repurposing a protein that normally functions in nitrogen uptake toward a new function involving flagellar regulation.…”

Section: Discussionmentioning

confidence: 99%

A protein constructed de novo enables cell growth by altering gene regulation

Digianantonio

Hecht

2016

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

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Recent advances in protein design rely on rational and computational approaches to create novel sequences that fold and function. In contrast, natural systems selected functional proteins without any design a priori. In an attempt to mimic nature, we used large libraries of novel sequences and selected for functional proteins that rescue Escherichia coli cells in which a conditionally essential gene has been deleted. In this way, the de novo protein SynSerB3 was selected as a rescuer of cells in which serB, which encodes phosphoserine phosphatase, an enzyme essential for serine biosynthesis, was deleted. However, SynSerB3 does not rescue the deleted activity by catalyzing hydrolysis of phosphoserine. Instead, SynSerB3 upregulates hisB, a gene encoding histidinol phosphate phosphatase. This endogenous E. coli phosphatase has promiscuous activity that, when overexpressed, compensates for the deletion of phosphoserine phosphatase. Thus, the de novo protein SynSerB3 rescues the deletion of serB by altering the natural regulation of the His operon.O ne of the key goals of synthetic biology is to design novel proteins that fold and function in vivo. A particularly challenging objective would be to produce nonnatural proteins that do not merely generate interesting phenotypes but actually provide essential functions necessary for the growth of living cells. The successful design of such life-sustaining proteins would represent an initial step toward constructing artificial "proteomes" of nonnatural sequences.We initiated work toward artificial proteomes by constructing large combinatorial libraries of novel sequences designed to fold into stable four-helix structures (1, 2). Our libraries were based on a strategy for protein design, which assumes that the overall fold of a simple structure can be specified by the pattern of polar and nonpolar residues in the linear sequence. Because only the type of residue-polar versus nonpolar-is specified, this strategy has been called a "binary code" for protein design (1-3). At the same time, because the exact identities of the side chains at each polar and nonpolar position are not specified explicitly, this strategy is well suited for constructing large combinatorial libraries of novel sequences (3). To express these libraries of binary-patterned sequences in vivo, we construct collections of synthetic genes using degenerate DNA codons. For example, the degenerate codon NTN (N = A,T,C,G) is used to encode five nonpolar residues, and the degenerate codon VAN (V = A,C,G) is used to encode six polar residues.We have shown previously that several proteins from these binary patterned libraries fold into stable four-helix bundles, and both crystallographic and NMR structures have been determined (4-6). Moreover, in initial steps probing the potential for functional activity, proteins from these libraries were shown to bind small molecules, including cofactors, and to catalyze rudimentary reactions (7,8). Although those experiments screened a subset of library proteins for activity in ...

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“…A de novo originated gene has been described in yeast that acts to depress the mating pathway. Curiously, this gene in turn represses the protein encoded on its antisense strand (Li et al 2010b). A second example comes from Hydra in which the expression of a small, secreted orphan protein recapitulates phenotypic differences seen between species (Khalturin et al 2008).…”

Section: Evolution Of New Genesmentioning

confidence: 99%

“…Evolutionary divergence characteristics are commonly used as a filter to distinguish de novo gene candidates from neutrally evolving genomic regions. De novo gene emergence have been reported from many organisms such as insects (Begun et al 2007;Reinhardt et al 2013), yeast (Cai et al 2008;Li et al 2010b), Hydra (Khalturin et al 2008), primates (Johnson et al 2001;Knowles and McLysaght 2009;Toll-Riera et al 2009;Li et al 2010a;Wu et al 2011;Xie et al 2012), mouse (Murphy and McLysaght 2012;Neme and Tautz 2013), Plasmodium (Yang and Huang 2011), and plants (Donoghue et al 2011).…”

Section: Evidence For De Novo Emergence Of Genesmentioning

confidence: 99%