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T cells are a type of white blood cell that play a critical role in the immune response against foreign pathogens through a process called T cell adaptive immunity (TCAI). However, the evolution of the genes and nucleotide sequences involved in TCAI is not well understood. To investigate this, we performed comparative studies of gene annotations and genome assemblies of 28 vertebrate species and identified sets of human genes that are involved in TCAI, carcinogenesis, and aging. We found that these gene sets share interaction pathways, which may have contributed to the evolution of longevity in the vertebrate lineage leading to humans. Our human gene age dating analyses revealed that there was rapid origination of genes with TCAI-related functions prior to the Cretaceous eutherian radiation and these new genes mainly encode negative regulators. We identified no new TCAI-related genes after the divergence of placental mammals, but we did detect an extensive number of amino acid substitutions under strong positive selection in recently evolved human immunity genes suggesting they are coevolving with adaptive immunity. More specifically, we observed that antigen processing and presentation and checkpoint genes are significantly enriched among new genes evolving under positive selection. These observations reveal evolutionary processes of TCAI that were associated with rapid gene duplication in the early stages of vertebrates and subsequent sequence changes in TCAI-related genes. The analysis of vertebrate genomes provides evidence that a "big bang" of adaptive immune genes occurred 300-500 million years ago. These processes together suggest an early genetic construction of the vertebrate immune system and subsequent molecular adaptation to diverse antigens.

Previous studies described gene age distributions in the focal species ofDrosophila melanogaster. Using third-generation PacBio technology to sequenceDrosophilaspecies we investigated gene age distribution in the two subgenera ofDrosophila. Our work resulted in several discoveries. First, our data detected abundant new genes in entireDrosophilagenus. Second, in analysis of subcellular expression, we found that new genes tend to secret into extracellular matrix and are involved in regulation, environmental adaption, and reproductive functions. We also found that extracellular localization for new genes provides a possible environment to promote their fast evolution. Third, old genes tend to be enriched in mitochondrion and the plasma membrane compared with young genes which may support the endosymbiotic theory that mitochondria originate from bacteria that once lived in primitive eukaryotic cells. Fourth, as gene age becomes older the subcellular compartments in which their products reside broadens suggesting that the evolution of new genes in subcellular location drives functional evolution and diversity inDrosophilaspecies. Additionally, based on the analysis of RNA-Seq of twoD. melanogasterpopulations, we determined a universal paradigm of “from specific to constitutive” expression pattern during the evolutionary process of new genes.

Young, or newly evolved, genes arise ubiquitously across the tree of life, and they can rapidly acquire novel functions that influence a diverse array of biological processes. Previous work identified a young regulatory duplicate gene in Drosophila, Zeus that unexpectedly diverged rapidly from its parent, Caf40, an extremely conserved component in the CCR4–NOT machinery in post-transcriptional and post-translational regulation of eukaryotic cells, and took on roles in the male reproductive system. This neofunctionalization was accompanied by differential binding of the Zeus protein to loci throughout the Drosophila melanogaster genome. However, the way in which new DNA-binding proteins acquire and coevolve with their targets in the genome is not understood. Here, by comparing Zeus ChIP-Seq data from D. melanogaster and D. simulans to the ancestral Caf40 binding events from D. yakuba, a species that diverged before the duplication event, we found a dynamic pattern in which Zeus binding rapidly coevolved with a previously unknown DNA motif, which we term Caf40 and Zeus-Associated Motif (CAZAM), under the influence of positive selection. Interestingly, while both copies of Zeus acquired targets at male-biased and testis-specific genes, D. melanogaster and D. simulans proteins have specialized binding on different chromosomes, a pattern echoed in the evolution of the associated motif. Using CRISPR-Cas9-mediated gene knockout of Zeus and RNA-Seq, we found that Zeus regulated the expression of 661 differentially expressed genes (DEGs). Our results suggest that the evolution of young regulatory genes can be coupled to substantial rewiring of the transcriptional networks into which they integrate, even over short evolutionary timescales. Our results thus uncover dynamic genome-wide evolutionary processes associated with new genes.

In efforts to explain how duplicate gene copies may rise to fixation in a population, previous models of new gene origination have underappreciated the importance of the 3D genome in this process. We show that proximity-based regulatory recruitment in distally duplicated genes, i.e. enhancer capture, is an efficient mechanism for accommodation of new selective conditions. By performing a co-expression analysis onD. melanogastertissue data and comparing essential to non-essential genes that have newly evolved, we show that enhancer capture is a significant driver of new gene evolution in distally duplicated genes. The new essential gene, HP6/Umbrea, is used as a model for understanding enhancer capture, as it evolved via a full duplication of the parental gene, its subsequent protein evolution is known, and it duplicated into a gene-poor region of the genome. HP6/Umbrea’s expression pattern divergence from its parental gene, HP1b, as well as its high co-expression with neighboring genes suggest that it evolved via enhancer capture. ChIP-Seq data shows the presence of active enhancer marks appearing near HP6/Umbrea coinciding with onset of its expression which likely regulates HP6/Umbrea, its neighboring gene, as well as a distally located 6-gene cluster also found co-express with HP6/Umbrea. We find that these three loci, the putative enhancer, HP6/Umbrea, and the 6-gene cluster are in close physical proximity in the 3-D genome ofD. melanogaster. Finally, we compare Hi-C data from two species with HP6/Umbrea,D. melanogasterandD. yakuba, to two species pre-dating HP6/Umbrea’s insertion,D. pseudoobscuraandD. miranda, showing that co-regulation of these same elements is the ancestral state and thus that HP6/Umbrea evolved via enhancer capture.SIGNIFICANCE STATEMENTComprehensive analyses of new gene evolution across many clades have shown that the vast majority of new genes evolve via duplication-based methods, even in species with large population sizes. A few models have offered explanations for this seemingly paradoxical behavior, with the most commonly accepted ones being the duplication-divergence-complementation (DDC), escape-from-adaptive-conflict (EAC), and innovation-amplification-divergence (IAD) models. In this manuscript, we propose the enhancer-capture-divergence model of new duplicate gene evolution, where the rapid recombination of pre-existing protein-coding and regulatory elements offers the most efficient and evolvable path for modulating the protein production of an older gene. Subsequent to the fixation of this new variant, selection pressures are relaxed, e.g. through an environmental shift or the appearance of compensatory mutations elsewhere in the genome, allowing the new gene copy to begin to diverge in protein function. We provide genome-wide evidence for the enhancer-capture-divergence model using knock-down and expression data inD. melanogaster, while identifying the new essential gene HP6/Umbrea, a paralog of HP1b, as a model gene candidate for enhancer-capture-divergence.

Genes that originate during evolution are an important source of novel biological functions. Retrogenes are functional copies of genes produced by retroduplication and as such are located in different genomic positions. To investigate retroposition patterns and retrogene expression, we computationally identified interchromosomal retroduplication events in nine portions of the phylogenetic history of malaria mosquitoes, making use of species that do or do not have classical sex chromosomes to test the roles of sex-linkage. We found 40 interchromosomal events and a significant excess of retroduplications from the X chromosome to autosomes among a set of young retrogenes. These young retroposition events occurred within the last 100 million years in lineages where all species possessed differentiated sex chromosomes. An analysis of available microarray and RNA-seq expression data for Anopheles gambiae showed that many of the young retrogenes evolved male-biased expression in the reproductive organs. Young autosomal retrogenes with increased meiotic or postmeiotic expression in the testes tend to be male biased. In contrast, older retrogenes, i.e., in lineages with undifferentiated sex chromosomes, do not show this particular chromosomal bias and are enriched for female-biased expression in reproductive organs. Our reverse-transcription PCR data indicates that most of the youngest retrogenes, which originated within the last 47.6 million years in the subgenus Cellia, evolved non-uniform expression patterns across body parts in the males and females of An. coluzzii. Finally, gene annotation revealed that mitochondrial function is a prominent feature of the young autosomal retrogenes. We conclude that mRNA-mediated gene duplication has produced a set of genes that contribute to mosquito reproductive functions and that different biases are revealed after the sex chromosomes evolve. Overall, these results suggest potential roles for the evolution of meiotic sex chromosome inactivation in males and of sexually antagonistic conflict related to mitochondrial energy function as the main selective pressures for X-to-autosome gene reduplication and testis-biased expression in these mosquito lineages. Published version

Gene duplication is increasingly recognized as an important mechanism for the origination of new genes, as revealed by comparative genomic analysis. However, how new duplicate genes contribute to phenotypic evolution remains largely unknown, especially in plants. Here, we identified the new gene EXOV, derived from a partial gene duplication of its parental gene EXOVL in Arabidopsis thaliana. EXOV is a species-specific gene that originated within the last 3.5 million years and shows strong signals of positive selection. Unexpectedly, RNA-sequencing analyses revealed that, despite its young age, EXOV has acquired many novel direct and indirect interactions in which the parental gene does not engage. This observation is consistent with the high, selection-driven substitution rate of its encoded protein, in contrast to the slowly evolving EXOVL, suggesting an important role for EXOV in phenotypic evolution. We observed significant differentiation of morphological changes for all phenotypes assessed in genome-edited and T-DNA insertional single mutants and in double T-DNA insertion mutants in EXOV and EXOVL. We discovered a substantial divergence of phenotypic effects by principal component analyses, suggesting neofunctionalization of the new gene. These results reveal a young gene that plays critical roles in biological processes that underlie morphological evolution in A. thaliana.

It is conventionally assumed that conserved pathways evolve slowly with little participation of gene evolution. Nevertheless, it has been recently observed that young genes can take over fundamental functions in essential biological processes, for example, development and reproduction. It is unclear how newly duplicated genes are integrated into ancestral networks and reshape the conserved pathways of important functions. Here, we investigated origination and function of two autosomal genes that evolved recently in Drosophila: Poseidon and Zeus, which were created by RNA-based duplications from the X-linked CAF40, a subunit of the conserved CCR4–NOT deadenylase complex involved in posttranscriptional and translational regulation. Knockdown and knockout assays show that the two genes quickly evolved critically important functions in viability and male fertility. Moreover, our transcriptome analysis demonstrates that the three genes have a broad and distinct effect in the expression of hundreds of genes, with almost half of the differentially expressed genes being perturbed exclusively by one paralog, but not the others. Co-immunoprecipitation and tethering assays show that the CAF40 paralog Poseidon maintains the ability to interact with the CCR4–NOT deadenylase complex and might act in posttranscriptional mRNA regulation. The rapid gene evolution in the ancient posttranscriptional and translational regulatory system may be driven by evolution of sex chromosomes to compensate for the meiotic X chromosomal inactivation (MXCI) in Drosophila.

Background Events of gene fusion have been reported in several organisms. However, the general role of gene fusion as part of new gene origination remains unknown. Results We conduct genome-wide interrogations of four Oryza genomes by designing and implementing novel pipelines to detect fusion genes. Based on the phylogeny of ten plant species, we detect 310 fusion genes across four Oryza species. The estimated rate of origination of fusion genes in the Oryza genus is as high as 63 fusion genes per species per million years, which is fixed at 16 fusion genes per species per million years and much higher than that in flies. By RNA sequencing analysis, we find more than 44% of the fusion genes are expressed and 90% of gene pairs show strong signals of purifying selection. Further analysis of CRISPR/Cas9 knockout lines indicates that newly formed fusion genes regulate phenotype traits including seed germination, shoot length and root length, suggesting the functional significance of these genes. Conclusions We detect new fusion genes that may drive phenotype evolution in Oryza. This study provides novel insights into the genome evolution of Oryza.

The factors that drive the rapid changes in abundance of tandem arrays of highly repetitive sequences, known as satellite DNA, are not well understood. Drosophila virilis has one of the highest relative amounts of simple satellites of any organism that has been studied, with an estimated >40% of its genome composed of a few related 7-bp satellites. Here, we use D. virilis as a model to understand technical biases affecting satellite sequencing and the evolutionary processes that drive satellite composition. By analyzing sequencing data from Illumina, PacBio, and Nanopore platforms, we identify platform-specific biases and suggest best practices for accurate characterization of satellites by sequencing. We use comparative genomics and cytogenetics to demonstrate that the highly abundant AAACTAC satellite family arose from a related satellite in the branch leading to the virilis phylad 4.5–11 Ma before exploding in abundance in some species of the clade. The most abundant satellite is conserved in sequence and location in the pericentromeric region but has diverged widely in abundance among species, whereas the satellites nearest the centromere are rapidly turning over in sequence composition. By analyzing multiple strains of D. virilis, we saw that the abundances of two centromere-proximal satellites are anticorrelated along a geographical gradient, which we suggest could be caused by ongoing conflicts at the centromere. In conclusion, we illuminate several key attributes of satellite evolutionary dynamics that we hypothesize to be driven by processes including selection, meiotic drive, and constraints on satellite sequence and abundance.

Gene duplication is increasingly recognized as an important mechanism for the origination of new genes, as revealed by comparative genomic analysis. However, the ways in which new duplicate genes contribute to phenotypic evolution remain largely unknown, especially in plants, owing to a lack of experimental and phenotypic data. In this study, we identified the new geneExov,derived from a partial gene region duplication of its parental geneExov-L, which is a member of an exonuclease family, into a different chromosome inArabidopsis thaliana. We experimentally investigated the phenotypic effects ofExovandExov-Lin an attempt to understand how the new gene diverged from the parental copy and contributes to phenotypic evolution. Evolutionary analysis demonstrated thatExovis a species-specific gene that originated within the last 3.5 million years and shows strong signals of positive selection. Unexpectedly, RNAseq analyses reveal that the new gene, despite its young age, has acquired a large number of novel direct and indirect interactions in which the parental gene does not engage. This is consistent with a high, selection-driven substitution rate in the protein sequence encoded byExovin contrast to the slowly evolvingExov-L, suggesting an important role forExovin phenotypic evolution. We analyzed phenotypic effects ofexovandexov-lsingle T-DNA-insertion mutants;doubleexov, exov-lT-DNA insertion mutants; and CRISPR/Cas9-mediatedexovcrpandexov-lcrpknockouts on seven morphological traits in both the new and parental genes. We detected significant segregation of morphological changes for all seven traits when assessed in terms of single mutants, as well as morphological changes for seven traits associated with segregation of doubleexov, exov-lmutants. Substantial divergence of phenotypic effects between new and parental genes was revealed by principal component analyses, suggesting neofunctionalization in the new gene. These results reveal a young gene that plays critical roles in biological processes that underlie morphological and developmental evolution inArabidopsis thaliana.

Foraging behavior is critical for the fitness of individuals. However, the genetic basis of variation in foraging behavior and the evolutionary forces underlying such natural variation have rarely been investigated. We developed a systematic approach to assay the variation in survival rate in a foraging environment for adult flies derived from a wild Drosophila melanogaster population. Despite being such an essential trait, there is substantial variation of foraging behavior among D. melanogaster strains. Importantly, we provided the first evaluation of the potential caveats of using inbred Drosophila strains to perform genome-wide association studies on life-history traits, and concluded that inbreeding depression is unlikely a major contributor for the observed large variation in adult foraging behavior. We found that adult foraging behavior has a strong genetic component and, unlike larval foraging behavior, depends on multiple loci. Identified candidate genes are enriched in those with high expression in adult heads and, demonstrated by expression knock down assay, are involved in maintaining normal functions of the nervous system. Our study not only identified candidate genes for foraging behavior that is relevant to individual fitness, but also shed light on the initial stage underlying the evolution of the behavior.

Inverted duplicates are a type of repetitive DNA motifs consist of two copies of reverse complementary sequences separated by a spacer sequence. They can lead to genome instability and many may have no function, but some functional small RNAs are processed from hairpins transcribed from these elements. It is not clear whether the pervasive numbers of such elements in genomes, especially those of mammals, is the result of high generation rates of neutral or slightly deleterious duplication events or positive selection for functionality. To test the functionality of intergenic inverted duplicates without known functions, we used mirror duplicates, a type of repetitive DNA motifs with few reported functions and little potential to form hairpins when transcribed, as a nonfunctional control. We identified large numbers of inverted duplicates within intergenic regions of human and mouse genomes, as well as 19 other vertebrate genomes. Structure characterization of these inverted duplicates revealed higher proportion to form stable hairpins compared with converted mirror duplicates, suggesting that inverted duplicates may produce hairpin RNAs. Expression profiling across tissues demonstrated that 7.8% of human and 5.7% of mouse inverted duplicates were expressed even under strict criteria. We found that expressed inverted duplicates were more likely to be structurally stable than both unexpressed inverted duplicates and expressed converted mirror duplicates. By dating inverted duplicates in the vertebrate phylogenetic tree, we observed higher conservation of inverted duplicates than mirror duplicates. These observations support the notion that expressed inverted duplicates may be functional through forming hairpin RNAs.

Additional file 1. Additional figures and tables.

The factors that drive the rapid changes in satellite DNA genomic composition we see in eukaryotes are not well understood. Drosophila virilis has one of the highest relative amounts of simple satellites of any organism that has been studied, with an estimated 40+% of its genome composed of a few related 7 bp satellites. Here we use D. virilis as a model to understand technical biases affecting satellite sequencing and the evolutionary processes that drive satellite composition. By analyzing sequencing data from Illumina, PacBio, and Nanopore platforms, we identify platform-specific biases and suggest best practices for accurate characterization of satellites by sequencing. We use comparative genomics and cytogenetics to demonstrate that the satellite family arose in the branch leading to the virilis phylad 4.5 - 11 million years ago. The most abundant satellite is conserved in sequence and location in the pericentromeric region but has diverged widely in abundance among species, whereas the satellites nearest the centromere are rapidly turning over in sequence composition. The amount of satellite DNA is lowest in the species with the smallest effective population size in the D. virilis phylad, contrary to what would be expected if satellites were only evolving under weak negative selection. We found evidence for transposable elements flanking the satellite arrays as well as recent insertions into the arrays. By analyzing multiple strains of D. virilis, we saw that one centromere-proximal satellite is undergoing an expansion, while the other is contracting in a correlated manner, suggesting possible trade-offs or competition between satellites. In conclusion, we illuminate several key attributes of satellite evolutionary dynamics that we hypothesize to be driven by processes like positive selection, meiotic drive, and constraints on satellite sequence and abundance. Author summary Tandem arrays of sequence repeats, or satellite DNA, makes up large and variable proportions of eukaryote genomes. Satellites may be an important component of genomes, but their evolution is not well understood because they are subject to a variety of different evolutionary forces due to their repetitive nature and proximity to centromeres, and they are difficult to sequence. Here we use a fruit fly Drosophila virilis – whose genome experienced a recent explosion in satellite DNA to make up 40+% of its genome – to understand the evolutionary processes that drive satellite composition. We found that the satellite emerged and expanded rapidly, and is variable among related species. The satellites have different patterns of evolution depending on their proximity to the centromere. We show evidence that the satellites may act selfishly and result in trade-offs on other satellites due to the push-back of selection.

New genes originated relatively recently and are only present in a subset of species in a phylogeny. Accumulated evidence suggests that new genes, like old genes that are conserved across species, can also take on important functions and be essential for the survival and reproductive success of organisms. While there are detailed analyses of the mechanisms underlying gained fertility functions by new genes, how new genes rapidly became essential for viability remains unclear. We focused on a young retro-duplicated gene (CG7804, which we namedCocoon) inDrosophilathat originated three million years ago. We found that, unlike its evolutionarily conserved and broadly expressed parental gene,Cocoonhas evolved rapidly under positive selection since its birth and accumulates many amino acid divergences at functional sites from the parental gene. Despite its young age,Cocoonis essential for the survival ofD. melanogasterat multiple developmental stages, including the critical embryonic stage, and its expression is essential in different tissues from its parental gene. Functional genomic analyses found thatCocoongained multiple DNA binding targets, which regulates the expression of genes that have other essential functions and/or have multiple gene-gene interactions. Our observations suggest thatCocoonacquired essential function to survival through forming interactions that have large impacts on the gene interaction network. Our study is an important step towards deciphering the evolutionary trajectory by which new genes functionally diverge from the parental gene and become essential.

Chimerical retroposition delineate a process by which RNA reverse transcribed integration into genome accompanied with recruiting flanking sequence, which is asserted to play essential roles and drive genome evolution. Although chimerical retrogenes hold high origination rate in plant genome, the evolutionary pattern of retrogenes and their parental genes are not well understood in rice genome. In this study, using maximum likelihood method, we evaluated the substitution ratio along lineages of 24 retrogenes and parental gene pairs to retrospect the evolutionary patterns. The results indicate that some specific lineages in 7 pairs underwent positive selection. Besides the rapid evolution in the initial stage of new chimerical retrogene evolution, an unexpected pattern was revealed: soon or some uncertain period after the origination of new chimerical retrogenes, their parental genes evolved rapidly under positive selection, rather than the rapid evolution of the new chimerical retrogenes themselves. This result lend support to the hypothesis that the new copy assistant the function evolution among parental gene and retrogene. Transcriptionally, we also found that one retrogene (RCG3) have a high expression at the period of calli infection which supported by chip data while its parental gene doesn’t have. Finally, by calibration to Ka/Ks analysis results in other species including Apis mellifera, we concluded that chimerical retrogenes are higher proportionally positive selected than the regular genes in the rice genome.

It has been widely observed that sex-related genes are copied from sex chromosomes and inserted into autosomes, a process termed 'gene traffic'. However, the adaptive significance of this phenomenon is unclear. Now, direct evidence has been provided that gene traffic may allow functional compensation during meiotic sex chromosome activation.

Orphan genes that lack detectable homologues in other lineages could contribute to a variety of biological functions. However, their origination and function mechanisms remain largely unknown. Herein, through a comprehensive and systematic computational pipeline, we identified 893 orphan genes in the lineage of C. elegans, of which only a low fraction (0.9%) were derived from transposon elements. Six new protein-coding genes that de novo originated from non-coding DNA sequences in the genome of C. elegans were also identified. The authenticity and functionality of these orphan genes and de novo genes are supported by three lines of evidences, consisting of transcriptional data, and in silico proteomic data, and the fixation status data in wild populations. Orphan genes and de novo genes exhibited simple gene structures, such as, short in protein length, of fewer exons, and are frequently X-linked. RNA-seq data analysis showed these orphan genes are enriched with expression in embryo development and gonad, and their potential function in early development was further supported by gene ontology enrichment analysis results. Meanwhile, de novo genes were found to be with significant expression in gonad, and functional enrichment analysis of the co-expression genes of these de novo genes suggested they may be functionally involved in signaling transduction pathway and metabolism process. Our results presented the first systematic evidence on the evolution of orphan genes and de novo origin of genes in nematodes and their impacts on the functional and phenotypic evolution, and thus could shed new light on our appreciation of the importance of these new genes.

The patulin biosynthesis is one of model pathways in an understanding of secondary metabolite biology and network novelties in fungi. However, molecular regulation mechanism of patulin biosynthesis and contribution of each gene related to the different catalytic enzymes in the biochemical steps of the pathway remain largely unknown in fungi. In this study, the genetic components of patulin biosynthetic pathway were systematically dissected in Penicillium expansum, which is an important fungal pathogen and patulin producer in harvested fruits and vegetables. Our results revealed that all the 15 genes in the cluster are involved in patulin biosynthesis. Proteins encoded by those genes are compartmentalized in various subcellular locations, including cytosol, nucleus, vacuole, endoplasmic reticulum, plasma membrane and cell wall. The subcellular localizations of some proteins, such as PatE and PatH, are required for the patulin production. Further, the functions of eight enzymes in the 10-step patulin biosynthetic pathway were verified in P. expansum. Moreover, velvet family proteins, VeA, VelB and VelC, were proved to be involved in the regulation of patulin biosynthesis, but not VosA. These findings provide a thorough understanding of the biosynthesis pathway, spatial control and regulation mechanism of patulin in fungi.

We analyze the global structure and evolution of human gene coexpression networks driven by new gene integration. When the Pearson correlation coefficient is greater than or equal to 0.5, we find that the coexpression network consists of 334 small components and one “giant” connected subnet comprising of 6317 interacting genes. This network shows the properties of power-law degree distribution and small-world. The average clustering coefficient of younger genes is larger than that of the elderly genes (0.6685 vs. 0.5762). Particularly, we find that the younger genes with a larger degree also show a property of hierarchical architecture. The younger genes play an important role in the overall pivotability of the network and this network contains few redundant duplicate genes. Moreover, we find that gene duplication and orphan genes are two dominant evolutionary forces in shaping this network. Both the duplicate genes and orphan genes develop new links through a “rich-gets-richer” mechanism. With the gradual integration of new genes into the ancestral network, most of the topological structure features of the network would gradually increase. However, the exponent of degree distribution and modularity coefficient of the whole network do not change significantly, which implies that the evolution of coexpression networks maintains the hierarchical and modular structures in human ancestors.

This article was not made open access when initially published online, which was corrected before print publication. In addition, ORCID links were missing for 12 authors and have been added to the HTML and PDF versions of the article.

New protein-coding genes that arise de novo from non-coding DNA sequences contribute to protein diversity. However, de novo gene origination is challenging to study as it requires high-quality reference genomes for closely related species, evidence for ancestral non-coding sequences, and transcription and translation of the new genes. High-quality genomes of 13 closely related Oryza species provide unprecedented opportunities to understand de novo origination events. Here, we identify a large number of young de novo genes with discernible recent ancestral non-coding sequences and evidence of translation. Using pipelines examining the synteny relationship between genomes and reciprocal-best whole-genome alignments, we detected at least 175 de novo open reading frames in the focal species O. sativa subspecies japonica, which were all detected in RNA sequencing-based transcriptomes. Mass spectrometry-based targeted proteomics and ribosomal profiling show translational evidence for 57% of the de novo genes. In recent divergence of Oryza, an average of 51.5 de novo genes per million years were generated and retained. We observed evolutionary patterns in which excess indels and early transcription were favoured in origination with a stepwise formation of gene structure. These data reveal that de novo genes contribute to the rapid evolution of protein diversity under positive selection.

The origination of new genes contributes to phenotypic evolution in humans. Two major challenges in the study of new genes are the inference of gene ages and annotation of their protein-coding potential. To tackle these challenges, we created GenTree, an integrated online database that compiles age inferences from three major methods together with functional genomic data for new genes. Genome-wide comparison of the age inference methods revealed that the synteny-based pipeline (SBP) is most suited for recently duplicated genes, whereas the protein-family–based methods are useful for ancient genes. For SBP-dated primate-specific protein-coding genes (PSGs), we performed manual evaluation based on published PSG lists and showed that SBP generated a conservative data set of PSGs by masking less reliable syntenic regions. After assessing the coding potential based on evolutionary constraint and peptide evidence from proteomic data, we curated a list of 254 PSGs with different levels of protein evidence. This list also includes 41 candidate misannotated pseudogenes that encode primate-specific short proteins. Coexpression analysis showed that PSGs are preferentially recruited into organs with rapidly evolving pathways such as spermatogenesis, immune response, mother–fetus interaction, and brain development. For brain development, primate-specific KRAB zinc-finger proteins (KZNFs) are specifically up-regulated in the mid-fetal stage, which may have contributed to the evolution of this critical stage. Altogether, hundreds of PSGs are either recruited to processes under strong selection pressure or to processes supporting an evolving novel organ.

The genus Oryza is a model system for the study of molecular evolution over time scales ranging from a few thousand to 15 million years. Using 13 reference genomes spanning the Oryza species tree, we show that despite few large-scale chromosomal rearrangements rapid species diversification is mirrored by lineage-specific emergence and turnover of many novel elements, including transposons, and potential new coding and noncoding genes. Our study resolves controversial areas of the Oryza phylogeny, showing a complex history of introgression among different chromosomes in the young 'AA' subclade containing the two domesticated species. This study highlights the prevalence of functionally coupled disease resistance genes and identifies many new haplotypes of potential use for future crop protection. Finally, this study marks a milestone in modern rice research with the release of a complete long-read assembly of IR 8 'Miracle Rice', which relieved famine and drove the Green Revolution in Asia 50 years ago.

Males and females have different fitness optima but share the vast majority of their genomes, causing an inherent genetic conflict between the two sexes that must be resolved to achieve maximal population fitness. We show that two tandem duplicate genes found specifically in Drosophila melanogaster are sexually antagonistic, but rapidly evolved sex-specific functions and expression patterns that mitigate their antagonistic effects. We use copy-specific knockouts and rescue experiments to show that Apollo (Apl) is essential for male fertility but detrimental to female fertility, in addition to its important role in development, while Artemis (Arts) is essential for female fertility but detrimental to male fertility. Further analyses show that Apl and Arts have essential roles in spermatogenesis and oogenesis. These duplicates formed ~200,000 years ago, underwent a strong selective sweep and lost most expression in the antagonized sex. These data provide direct evidence that gene duplication allowed rapid mitigation of sexual conflict by allowing Apl and Arts to evolve essential sex-specific reproductive functions and complementary expression in male and female gonads.

Patulin, a potent mycotoxin, contaminates fruits and derived products worldwide, and is a serious health concern. Several yeast strains have shown the ability to effectively degrade patulin. However, the mechanisms of its biodegradation still remain unclear at this time. In the present study, biodegradation and involved mechanisms of patulin by an antagonistic yeast Candida guilliermondii were investigated. The results indicated that C. guilliermondii was capable of not only multiplying to a high population in medium containing patulin, but also effectively reducing patulin content in culture medium. Degradation of patulin by C. guilliermondii was dependent on the yeast cell viability, and mainly occurred inside cells. E-ascladiol was the main degradation product of patulin. An iTRAQ-based proteomic analysis revealed that the responses of C. guilliermondii to patulin were complex. A total of 30 differential proteins involved in 10 biological processes were identified, and more than two-thirds of the differential proteins were down-accumulated. Notably, a short-chain dehydrogenase (gi|190348612) was markedly induced by patulin at both the protein and mRNA levels. Our findings will provide a foundation to help enable the commercial development of an enzyme formulation for the detoxification of patulin in fruit-derived products.