Evolving protein functional diversity in new genes of
            <i>Drosophila</i>

Zhang, Jianming; Dean, Anthony M.; Brunet, Frédéric; Long, Manyuan

doi:10.1073/pnas.0407066101

Cited by 109 publications

(87 citation statements)

References 34 publications

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“…In this study we show the first case of protogenes identified in eukaryotic cytoplasmic genomes, and suggest that the generation of protogenes, as well as SSS, had served as a buffer, thus could also be a critical step for the establishment of CMS genes in natural populations. Our results also suggest that the previously recognized general features of new nuclear gene origination, including (1) recombination of existing genes and/ or previously non-coding sequences, leading to a hybrid gene structure, (2) sequence evolution driven by natural selection, and (3) acquisition of new functions [32,38,39], may also hold true for new mitochondrial gene formation. However, the microevolutionary process of the new mitochondrial genes we demonstrate here are much complicated than that of new nuclear genes reported so far.…”

Section: Discussionmentioning

confidence: 53%

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: 53%

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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“…So far only a few Drosophila new genes have received evidence for possible functions, such as Jingwei and Sphinx [26,27]. One of the most striking findings in this study is that MDF1, most likely generated de novo from a non-coding sequence, plays very important roles in two fundamental biological processes, namely mating and growth.…”

Section: Mdf1 Is An Unprecedented Example For the De Novo Originationmentioning

confidence: 62%

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

et al. 2010

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Recent transcription profiling studies have revealed an unexpectedly large proportion of antisense transcripts in eukaryotic genomes. These antisense genes seem to regulate gene expression by interacting with sense genes. Previous studies have focused on the non-coding antisense genes, but the possible regulatory role of the antisense protein is poorly understood. In this study, we found that a protein encoded by the antisense gene ADF1 acts as a transcription suppressor, regulating the expression of sense gene MDF1 in Saccharomyces cerevisiae. Based on the evolutionary, genetic, cytological and biochemical evidence, we show that the protein-coding sense gene MDF1 most likely originated de novo from a previously non-coding sequence and can significantly suppress the mating efficiency of baker's yeast in rich medium by binding MATα2 and thus promote vegetative growth. These results shed new light on several important issues, including a new sense-antisense interaction mechanism, the de novo origination of a functional gene, and the regulation of yeast mating pathway.

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“…Thus, duplicated genes that have evolved under a model of neofunctionalization provide an interesting case for exploring this question. Although the rise of novel gene functions has been studied in great detail in some examples of duplicated genes (2)(3)(4), how selection and the rise of a new function in the duplicated copy affects the evolution of the sister copy remains unclear. This evolutionary interference has not yet been studied in paralogous genes.…”

mentioning

confidence: 99%

Origin of a function by tandem gene duplication limits the evolutionary capability of its sister copy

Hasselmann

Lechner

Schulte

et al. 2010

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

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The most remarkable outcome of a gene duplication event is the evolution of a novel function. Little information exists on how the rise of a novel function affects the evolution of its paralogous sister gene copy, however. We studied the evolution of the feminizer (fem) gene from which the gene complementary sex determiner (csd) recently derived by tandem duplication within the honey bee (Apis) lineage. Previous studies showed that fem retained its sex determination function, whereas the rise of csd established a new primary signal of sex determination. We observed a specific reduction of nonsynonymous to synonymous substitution ratios in Apis to non-Apis fem. We found a contrasting pattern at two other genetically linked genes, suggesting that hitchhiking effects to csd, the locus under balancing selection, is not the cause of this evolutionary pattern. We also excluded higher synonymous substitution rates by relative rate testing. These results imply that stronger purifying selection is operating at the fem gene in the presence of csd. We propose that csd's new function interferes with the function of Fem protein, resulting in molecular constraints and limited evolvability of fem in the Apis lineage. Elevated silent nucleotide polymorphism in fem relative to the genome-wide average suggests that genetic linkage to the csd gene maintained more nucleotide variation in today's population. Our findings provide evidence that csd functionally and genetically interferes with fem, suggesting that a newly evolved gene and its functions can limit the evolutionary capability of other genes in the genome. A n important question in genome evolution is how the rise of a gene with a novel function influences the genomic region around that gene and the evolution of other genes in the genome. Under neofunctionalization, the newly arisen gene gains a function not present in the progenitor gene, whereas the original copy retains its function (1). Thus, duplicated genes that have evolved under a model of neofunctionalization provide an interesting case for exploring this question. Although the rise of novel gene functions has been studied in great detail in some examples of duplicated genes (2-4), how selection and the rise of a new function in the duplicated copy affects the evolution of the sister copy remains unclear. This evolutionary interference has not yet been studied in paralogous genes. This process differs from coevolutionary effects that implicate bidirectional interference between the tandem duplicated genes. Coevolution has been intensively studied in interacting protein systems, such as the cellular signaling pathway of protein ligands and their receptors (5, 6).By examining the paralogous genes feminizer (fem) and complementary sex determiner (csd), which control sex determination in honey bees (7, 8), we can explore whether evolutionary interference plays a role in the evolution of tandemly arranged genes. We previously showed that after the duplication event in the honey bee lineage, fem preserved its ancestral ...

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Evolving protein functional diversity in new genes of Drosophila

Cited by 109 publications

References 34 publications

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

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

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

Origin of a function by tandem gene duplication limits the evolutionary capability of its sister copy

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