Publications by authors named "Yong E Zhang"

49 Publications

DNA transposons mediate duplications via transposition-independent and -dependent mechanisms in metazoans.

Nat Commun 2021 07 13;12(1):4280. Epub 2021 Jul 13.

Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, China.

Despite long being considered as "junk", transposable elements (TEs) are now accepted as catalysts of evolution. One example is Mutator-like elements (MULEs, one type of terminal inverted repeat DNA TEs, or TIR TEs) capturing sequences as Pack-MULEs in plants. However, their origination mechanism remains perplexing, and whether TIR TEs mediate duplication in animals is almost unexplored. Here we identify 370 Pack-TIRs in 100 animal reference genomes and one Pack-TIR (Ssk-FB4) family in fly populations. We find that single-copy Pack-TIRs are mostly generated via transposition-independent gap filling, and multicopy Pack-TIRs are likely generated by transposition after replication fork switching. We show that a proportion of Pack-TIRs are transcribed and often form chimeras with hosts. We also find that Ssk-FB4s represent a young protein family, as supported by proteomics and signatures of positive selection. Thus, TIR TEs catalyze new gene structures and new genes in animals via both transposition-independent and -dependent mechanisms.
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http://dx.doi.org/10.1038/s41467-021-24585-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8277862PMC
July 2021

Genomic analyses of new genes and their phenotypic effects reveal rapid evolution of essential functions in Drosophila development.

PLoS Genet 2021 Jul 9;17(7):e1009654. Epub 2021 Jul 9.

Department of Ecology and Evolution, The University of Chicago, Chicago, Illinois, United States of America.

It is a conventionally held dogma that the genetic basis underlying development is conserved in a long evolutionary time scale. Ample experiments based on mutational, biochemical, functional, and complementary knockdown/knockout approaches have revealed the unexpectedly important role of recently evolved new genes in the development of Drosophila. The recent progress in the genome-wide experimental testing of gene effects and improvements in the computational identification of new genes (< 40 million years ago, Mya) open the door to investigate the evolution of gene essentiality with a phylogenetically high resolution. These advancements also raised interesting issues in techniques and concepts related to phenotypic effect analyses of genes, particularly of those that recently originated. Here we reported our analyses of these issues, including reproducibility and efficiency of knockdown experiment and difference between RNAi libraries in the knockdown efficiency and testing of phenotypic effects. We further analyzed a large data from knockdowns of 11,354 genes (~75% of the Drosophila melanogaster total genes), including 702 new genes (~66% of the species total new genes that aged < 40 Mya), revealing a similarly high proportion (~32.2%) of essential genes that originated in various Sophophora subgenus lineages and distant ancestors beyond the Drosophila genus. The transcriptional compensation effect from CRISPR knockout were detected for highly similar duplicate copies. Knockout of a few young genes detected analogous essentiality in various functions in development. Taken together, our experimental and computational analyses provide valuable data for detection of phenotypic effects of genes in general and further strong evidence for the concept that new genes in Drosophila quickly evolved essential functions in viability during development.
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http://dx.doi.org/10.1371/journal.pgen.1009654DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8270118PMC
July 2021

[Quantitative separation of evapotranspiration components of ecosystem based on multiple isotope models].

Ying Yong Sheng Tai Xue Bao 2021 Jun;32(6):1971-1979

Ministry of Education Key Laboratory of Soil and Water Conservation and Desertification Combating, Beijing Forestry University, Beijing 100083, China.

To fully understand the changes in the evapotranspiration components in forest ecosystem and their contribution to evapotranspiration at daily scale, we used the hypothesis theory of isotopic steady state and non-steady state combined with the water isotope analyzer system to quantitatively split and compare the evapotranspiration components of ecosystem during the growing season. Results showed that the O of water from different sources during the four mea-surement days (August 5, 8, 10, 11, 2016) all showed surface soil water and oxygen isotope composition (δ) > branch water and oxygen isotope composition (δ) > atmospheric water vapor oxygen isotopes composition (δ), with obvious differences due to the isotope fractionation. Oxygen isotopes composition of soil evaporated water vapor (δ) was between -26.89‰~-59.68‰ at the daily scale, showing a pattern of first rising and then decreasing. The oxygen isotopic composition of evapotranspiration water vapor in forest ecosystem (δ) was between -15.99‰~-10.04‰. The oxygen isotopic composition of transpired water vapor under steady state(δ) was between -12.10‰~-9.51‰. The oxygen isotopic composition of transpired water vapor under non-steady state (δ) was between -13.02‰~-7.23‰. δ and δ had the same changing trend throughout the day at the daily scale, while the trend of δ, δ and δ was approximately the same during 11:00-17:00. In general, the contribution rate of plant transpiration to total evapotranspiration showed that was between 79.1%-98.7%, and was between 88.7%-93.7%. Our results suggested that water consumption through soil evaporation was far less than that of vegetation transpiration in the study area, and that vegetation transpiration dominated forest evapotranspiration.
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http://dx.doi.org/10.13287/j.1001-9332.202106.023DOI Listing
June 2021

The evolution of ancestral and species-specific adaptations in snowfinches at the Qinghai-Tibet Plateau.

Proc Natl Acad Sci U S A 2021 Mar;118(13)

Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, 100101 Beijing, China;

Species in a shared environment tend to evolve similar adaptations under the influence of their phylogenetic context. Using snowfinches, a monophyletic group of passerine birds (Passeridae), we study the relative roles of ancestral and species-specific adaptations to an extreme high-elevation environment, the Qinghai-Tibet Plateau. Our ancestral trait reconstruction shows that the ancestral snowfinch occupied high elevations and had a larger body mass than most nonsnowfinches in Passeridae. Subsequently, this phenotypic adaptation diversified in the descendant species. By comparing high-quality genomes from representatives of the three phylogenetic lineages, we find that about 95% of genes under positive selection in the descendant species are different from those in the ancestor. Consistently, the biological functions enriched for these species differ from those of their ancestor to various degrees (semantic similarity values ranging from 0.27 to 0.5), suggesting that the three descendant species have evolved divergently from the initial adaptation in their common ancestor. Using a functional assay to a highly selective gene, , we demonstrate that the nonsynonymous substitutions in the ancestor and descendant species have improved the repair capacity of ultraviolet-induced DNA damage. The repair kinetics of the gene shows a twofold to fourfold variation across the ancestor and the descendants. Collectively, this study reveals an exceptional case of adaptive evolution to high-elevation environments, an evolutionary process with an initial adaptation in the common ancestor followed by adaptive diversification of the descendant species.
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http://dx.doi.org/10.1073/pnas.2012398118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8020664PMC
March 2021

Tracing the genetic footprints of vertebrate landing in non-teleost ray-finned fishes.

Cell 2021 03 4;184(5):1377-1391.e14. Epub 2021 Feb 4.

BGI-Shenzhen, Shenzhen 518083, China; Center for Excellence in Animal Evolution and Genetics, Chinese Academy of Sciences, 32 Jiaochang Donglu, Kunming 650223, China; State Key Laboratory of Genetic Resources and Evolution, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China; Villum Center for Biodiversity Genomics, Section for Ecology and Evolution, Department of Biology, University of Copenhagen, Copenhagen, Denmark. Electronic address:

Rich fossil evidence suggests that many traits and functions related to terrestrial evolution were present long before the ancestor of lobe- and ray-finned fishes. Here, we present genome sequences of the bichir, paddlefish, bowfin, and alligator gar, covering all major early divergent lineages of ray-finned fishes. Our analyses show that these species exhibit many mosaic genomic features of lobe- and ray-finned fishes. In particular, many regulatory elements for limb development are present in these fishes, supporting the hypothesis that the relevant ancestral regulation networks emerged before the origin of tetrapods. Transcriptome analyses confirm the homology between the lung and swim bladder and reveal the presence of functional lung-related genes in early ray-finned fishes. Furthermore, we functionally validate the essential role of a jawed vertebrate highly conserved element for cardiovascular development. Our results imply the ancestors of jawed vertebrates already had the potential gene networks for cardio-respiratory systems supporting air breathing.
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http://dx.doi.org/10.1016/j.cell.2021.01.046DOI Listing
March 2021

The mutational load in natural populations is significantly affected by high primary rates of retroposition.

Proc Natl Acad Sci U S A 2021 02;118(6)

Department of Evolutionary Genetics, Max Planck Institute for Evolutionary Biology, D-24306 Plön, Germany;

Gene retroposition is known to contribute to patterns of gene evolution and adaptations. However, possible negative effects of gene retroposition remain largely unexplored since most previous studies have focused on between-species comparisons where negatively selected copies are mostly not observed, as they are quickly lost from populations. Here, we show for natural house mouse populations that the primary rate of retroposition is orders of magnitude higher than the long-term rate. Comparisons with single-nucleotide polymorphism distribution patterns in the same populations show that most retroposition events are deleterious. Transcriptomic profiling analysis shows that new retroposed copies become easily subject to transcription and have an influence on the expression levels of their parental genes, especially when transcribed in the antisense direction. Our results imply that the impact of retroposition on the mutational load has been highly underestimated in natural populations. This has additional implications for strategies of disease allele detection in humans.
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http://dx.doi.org/10.1073/pnas.2013043118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8017666PMC
February 2021

Genome-wide analysis of pseudogenes reveals HBBP1's human-specific essentiality in erythropoiesis and implication in β-thalassemia.

Dev Cell 2021 02 20;56(4):478-493.e11. Epub 2021 Jan 20.

State Key Laboratory of Medical Molecular Biology, Institute of Basic Medical Science, Chinese Academy of Medical Sciences (CAMS) & School of Basic Medicine, Peking Union Medical College (PUMC), Beijing 100005, China; Key Laboratory of RNA and Hematopoietic Regulation, Chinese Academy of Medical Sciences, Beijing 100005, China.

The human genome harbors 14,000 duplicated or retroposed pseudogenes. Given their functionality as regulatory RNAs and low conservation, we hypothesized that pseudogenes could shape human-specific phenotypes. To test this, we performed co-expression analyses and found that pseudogene exhibited tissue-specific expression, especially in the bone marrow. By incorporating genetic data, we identified a bone-marrow-specific duplicated pseudogene, HBBP1 (η-globin), which has been implicated in β-thalassemia. Extensive functional assays demonstrated that HBBP1 is essential for erythropoiesis by binding the RNA-binding protein (RBP), HNRNPA1, to upregulate TAL1, a key regulator of erythropoiesis. The HBBP1/TAL1 interaction contributes to a milder symptom in β-thalassemia patients. Comparative studies further indicated that the HBBP1/TAL1 interaction is human-specific. Genome-wide analyses showed that duplicated pseudogenes are often bound by RBPs and less commonly bound by microRNAs compared with retropseudogenes. Taken together, we not only demonstrate that pseudogenes can drive human evolution but also provide insights on their functional landscapes.
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http://dx.doi.org/10.1016/j.devcel.2020.12.019DOI Listing
February 2021

(p)ppGpp-Dependent Regulation of the Nucleotide Hydrolase PpnN Confers Complement Resistance in Salmonella enterica Serovar Typhimurium.

Infect Immun 2021 01 19;89(2). Epub 2021 Jan 19.

Department of Biochemistry & Biomedical Sciences, McMaster University, Hamilton, Ontario, Canada

The stringent response is an essential mechanism of metabolic reprogramming during environmental stress that is mediated by the nucleotide alarmones guanosine tetraphosphate and pentaphosphate [(p)ppGpp]. In addition to physiological adaptations, (p)ppGpp also regulates virulence programs in pathogenic bacteria, including serovar Typhimurium. Typhimurium is a common cause of acute gastroenteritis, but it may also spread to systemic tissues, resulting in severe clinical outcomes. During infection, Typhimurium encounters a broad repertoire of immune defenses that it must evade for successful host infection. Here, we examined the role of the stringent response in Typhimurium resistance to complement-mediated killing and found that the (p)ppGpp synthetase-hydrolase, SpoT, is required for bacterial survival in human serum. We identified the nucleotide hydrolase, PpnN, as a target of the stringent response that is required to promote bacterial fitness in serum. Using chromatography and mass spectrometry, we show that PpnN hydrolyzes purine and pyrimidine monophosphates to generate free nucleobases and ribose 5'-phosphate, and that this metabolic activity is required for conferring resistance to complement killing. In addition to PpnN, we show that (p)ppGpp is required for the biosynthesis of the very long and long O-antigen in the outer membrane, known to be important for complement resistance. Our results provide new insights into the role of the stringent response in mediating evasion of the innate immune system by pathogenic bacteria.
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http://dx.doi.org/10.1128/IAI.00639-20DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7822145PMC
January 2021

[Effects of soil water stress and atmospheric CO concentration on photosynthetic and post-photosynthetic fractionation].

Ying Yong Sheng Tai Xue Bao 2020 Jun;31(6):1800-1806

Ministry of Education Key Laboratory of Soil and Water Conservation and Desertification Combating, Beijing Forestry University, Beijing 100083, China.

Analysis of plant photosynthesis and post-photosynthetic fractionation can improve our understanding of plant physiology and water management. By measuring δC in the atmosphere, and δC of soluble compounds in leaves and branch phloem of Platycladus orientalis, we examined discrimination pattern, including atmosphere-leaf discrimination during photosynthesis (ΔC) and leaf-twig discrimination during post-photosynthesis (ΔC), in response to changes of soil water content (SWC) and atmospheric CO concentration (C). The results showed that ΔC reached a maximum of 13.06‰ at 95%-100% field water-holding capacity (FC) and C 400 μmol·mol, and a minimum of 8.63‰ at 35%-45% FC and C 800 μmol·mol. Both stomatal conductance and mesophyll cell conductance showed a significant linear positive correlation with ΔC, with a correlation coefficient of 0.43 and 0.44, respectively. ΔC was not affected by SWC and C. Our results provide mechanism of carbon isotopes fractionation and a theoretical basis for plant survival strategies in response to future climate change.
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http://dx.doi.org/10.13287/j.1001-9332.202006.024DOI Listing
June 2020

Gene expression across mammalian organ development.

Nature 2019 07 26;571(7766):505-509. Epub 2019 Jun 26.

Department of Genetics, Stanford University School of Medicine, Stanford, CA, USA.

The evolution of gene expression in mammalian organ development remains largely uncharacterized. Here we report the transcriptomes of seven organs (cerebrum, cerebellum, heart, kidney, liver, ovary and testis) across developmental time points from early organogenesis to adulthood for human, rhesus macaque, mouse, rat, rabbit, opossum and chicken. Comparisons of gene expression patterns identified correspondences of developmental stages across species, and differences in the timing of key events during the development of the gonads. We found that the breadth of gene expression and the extent of purifying selection gradually decrease during development, whereas the amount of positive selection and expression of new genes increase. We identified differences in the temporal trajectories of expression of individual genes across species, with brain tissues showing the smallest percentage of trajectory changes, and the liver and testis showing the largest. Our work provides a resource of developmental transcriptomes of seven organs across seven species, and comparative analyses that characterize the development and evolution of mammalian organs.
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http://dx.doi.org/10.1038/s41586-019-1338-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6658352PMC
July 2019

Large-scale ruminant genome sequencing provides insights into their evolution and distinct traits.

Science 2019 06;364(6446)

Section for Computational and RNA Biology, Department of Biology, University of Copenhagen, DK-2100 Copenhagen, Denmark.

The ruminants are one of the most successful mammalian lineages, exhibiting morphological and habitat diversity and containing several key livestock species. To better understand their evolution, we generated and analyzed de novo assembled genomes of 44 ruminant species, representing all six Ruminantia families. We used these genomes to create a time-calibrated phylogeny to resolve topological controversies, overcoming the challenges of incomplete lineage sorting. Population dynamic analyses show that population declines commenced between 100,000 and 50,000 years ago, which is concomitant with expansion in human populations. We also reveal genes and regulatory elements that possibly contribute to the evolution of the digestive system, cranial appendages, immune system, metabolism, body size, cursorial locomotion, and dentition of the ruminants.
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http://dx.doi.org/10.1126/science.aav6202DOI Listing
June 2019

Topological evolution of coexpression networks by new gene integration maintains the hierarchical and modular structures in human ancestors.

Sci China Life Sci 2019 Apr 21;62(4):594-608. Epub 2019 Mar 21.

Department of Ecology and Evolution, The University of Chicago, Chicago, Illinois, 60637, USA.

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.
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http://dx.doi.org/10.1007/s11427-019-9483-6DOI Listing
April 2019

Water use efficiency and its influencing factors of Platycladus orientalis plantation in Beijing mountains area, China.

Ying Yong Sheng Tai Xue Bao 2019 Mar;30(3):727-734

Ministry of Education Key Laboratory of Soil and Water Conservation and Desertification Combating, Beijing Forestry University, Beijing 100083, China.

Water use efficiency (WUE) is an important index to evaluate plant drought resistance. Studying the dynamics of WUE and its influencing factors can provide reference for the vegetation restoration in Beijing mountainous area. We measured WUE of Platycladus orientalis in growing season and investigated the influence of meteorological factors, soil factors, and atmospheric CO concentration on WUE, based on the stable carbon isotope techniques. The results showed that: 1) The short-term WUE decreased and then increased in the growing season, with minimum value (2.69 mmol·mol) in July and maximum value (13.88 mmol·mol) in October. 2) The vapor pressure deficit (VPD) had the most significant impacts on WUE, followed by air temperature (T), soil moisture (M), relative humidity (RH), and atmospheric CO concentration (C), explaining 89.7% of the total variance. Solar radiation (R) and wind speed (W) had no impacts on WUE. 3) VPD and T are the most two important factors influencing short-term WUE, explaining 53.9% of the total variance. The effects of VPD on short-term WUE was higher than that of T. M and RH were the second important factors of the short-term WUE, explaining 25.4% of the total variance. The effects of M on short-term WUE was higher than that of RH. C had little effect on the short-term WUE and could explain 10.3% of the total variance.
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http://dx.doi.org/10.13287/j.1001-9332.201903.026DOI Listing
March 2019

Adaptation and Phenotypic Diversification in Arabidopsis through Loss-of-Function Mutations in Protein-Coding Genes.

Plant Cell 2019 05 18;31(5):1012-1025. Epub 2019 Mar 18.

State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China

According to the less-is-more hypothesis, gene loss is an engine for evolutionary change. Loss-of-function (LoF) mutations resulting in the natural knockout of protein-coding genes not only provide information about gene function but also play important roles in adaptation and phenotypic diversification. Although the less-is-more hypothesis was proposed two decades ago, it remains to be explored on a large scale. In this study, we identified 60,819 LoF variants in 1071 Arabidopsis () genomes and found that 34% of Arabidopsis protein-coding genes annotated in the Columbia-0 genome do not have any LoF variants. We found that nucleotide diversity, transposable element density, and gene family size are strongly correlated with the presence of LoF variants. Intriguingly, 0.9% of LoF variants with minor allele frequency larger than 0.5% are associated with climate change. In addition, in the Yangtze River basin population, 1% of genes with LoF mutations were under positive selection, providing important insights into the contribution of LoF mutations to adaptation. In particular, our results demonstrate that LoF mutations shape diverse phenotypic traits. Overall, our results highlight the importance of the LoF variants for the adaptation and phenotypic diversification of plants.
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http://dx.doi.org/10.1105/tpc.18.00791DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6533021PMC
May 2019

GenTree, an integrated resource for analyzing the evolution and function of primate-specific coding genes.

Genome Res 2019 04 12;29(4):682-696. Epub 2019 Mar 12.

Key Laboratory of Zoological Systematics and Evolution and State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.

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.
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http://dx.doi.org/10.1101/gr.238733.118DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6442393PMC
April 2019

Evolutionarily significant A-to-I RNA editing events originated through G-to-A mutations in primates.

Genome Biol 2019 02 4;20(1):24. Epub 2019 Feb 4.

Laboratory of Bioinformatics and Genomic Medicine, Beijing Key Laboratory of Cardiometabolic Molecular Medicine, Institute of Molecular Medicine, Peking University, Beijing, 100871, China.

Background: Recent studies have revealed thousands of A-to-I RNA editing events in primates, but the origination and general functions of these events are not well addressed.

Results: Here, we perform a comparative editome study in human and rhesus macaque and uncover a substantial proportion of macaque A-to-I editing sites that are genomically polymorphic in some animals or encoded as non-editable nucleotides in human. The occurrence of these recent gain and loss of RNA editing through DNA point mutation is significantly more prevalent than that expected for the nearby regions. Ancestral state analyses further demonstrate that an increase in recent gain of editing events contribute to the over-representation, with G-to-A mutation site as a favorable location for the origination of robust A-to-I editing events. Population genetics analyses of the focal editing sites further reveal that a portion of these young editing events are evolutionarily significant, indicating general functional relevance for at least a fraction of these sites.

Conclusions: Overall, we report a list of A-to-I editing events that recently originated through G-to-A mutations in primates, representing a valuable resource to investigate the features and evolutionary significance of A-to-I editing events at the population and species levels. The unique subset of primate editome also illuminates the general functions of RNA editing by connecting it to particular gene regulatory processes, based on the characterized outcome of a gene regulatory level in different individuals or primate species with or without these editing events.
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http://dx.doi.org/10.1186/s13059-019-1638-yDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6360793PMC
February 2019

Direct measurement of pervasive weak repression by microRNAs and their role at the network level.

BMC Genomics 2018 May 15;19(1):362. Epub 2018 May 15.

Key Laboratory of Genomic and Precision Medicine, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, 100101, China.

Background: A gene regulatory network (GRN) comprises many weak links that are often regulated by microRNAs. Since miRNAs rarely repress their target genes by more than 30%, doubts have been expressed about the biological relevance of such weak effects. These doubts raise the possibility of under-estimation as miRNA repression is usually estimated indirectly from equilibrium expression levels.

Results: To measure miRNA repression directly, we inhibited transcript synthesis in Drosophila larvae and collected time-course data on mRNA abundance, the decline of which reflects transcript degradation. The rate of target degradation in the absence of miR310s, a moderately expressed miRNA family, was found to decrease by 5 to 15%. A conventional analysis that does not remove transcript synthesis yields an estimate of 6.5%, within the range of the new estimates. These data permit further examinations of the repression mechanisms by miRNAs including seed matching types, APA (alternative polyadenylation) sites, effects of other highly-expressed miRNAs and the length of 3'UTR. Our direct measurements suggest the latter two factors have a measurable effect on decay rate.

Conclusion: The direct measurement confirms pervasive weak repression by miRNAs, supporting the conclusions based on indirect assays. The confirmation suggests that this weak repression may indeed be miRNAs' main function. In this context, we discuss the recent proposal that weak repression is "cumulatively powerful" in stabilizing GRNs.
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http://dx.doi.org/10.1186/s12864-018-4757-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5952853PMC
May 2018

[Variations and determinants of CO concentration and δC in Platycladus orientalis plantation in Beijing mountainous area, China].

Ying Yong Sheng Tai Xue Bao 2017 Jul;28(7):2164-2170

Beijing Forestry University, Beijing 100083, China.

This research employed off-axis integrated cavity output spectroscopy technique to observe CO concentration and δC values of planted Platycladus orientalis in Beijing mountainous area. We compared the variation between CO concentration and δC values in the plantation at different heights observed by every 0.5 h to explore how the CO concentration and δC values responded to the meteorological factors. The results showed that the CO concentration showed the pattern of "first decreased and then increased" after sunrise. The lowest value (352.5 μmol·mol) appeared at 16:00-16:30, while the maximum value (402.0 μmol·mol) was observed at about 5:00. However, the change of δC value was not significant and regular, which increased firstly and then decreased in the surface layer while opposite for the canopy. Atmospheric CO concentration decreased with the increasing height. In the height of 0, 2, 5, 8, 12.5 and 18 m, the average daily value was 386.5, 369.9, 368.2, 367.8, 367.9 and 367.9 μmol·mol, respectively. In contrast, the δC values tended to rise correspondingly with height with the average daily value being -16.0‰, -13.7‰, -13.5‰, -13.5‰, -13.1‰ and -13.3% at 0, 2, 5, 8, 12.5 and 18 m, respectively. The stepwise regression analysis showed that temperature and humidity were the main factors for the changes of atmospheric CO concentration and δC values. The saturated vapor pressure difference (VPD) affected the concentration of CO in the forest and wind speed could affect it on the canopy. However, soil moisture, soil electric conductivity and net solar radiation affected the CO concentration and δC values in surface layer. All these environmental factors influenced CO concentration and δC values through their influences on the photosynthesis and respiration.
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http://dx.doi.org/10.13287/j.1001-9332.201707.014DOI Listing
July 2017

[Foliar water use efficiency of Platycladus orientalis sapling under different soil water contents].

Ying Yong Sheng Tai Xue Bao 2017 Jul;28(7):2149-2154

Ministry of Education Key Laboratory of Soil & Water Conservation and Desertification Combating, Beijing Forestry University, Beijing 100083, China.

The determination of plant foliar water use efficiency will be of great value to improve our understanding about mechanism of plant water consumption and provide important basis of regional forest ecosystem management and maintenance, thus, laboratory controlled experiments were carried out to obtain Platycladus orientalis sapling foliar water use efficiency under five different soil water contents, including instantaneous water use efficiency (WUE) derived from gas exchange and short-term water use efficiency (WUE) caculated using carbon isotope model. The results showed that, controlled by stomatal conductance (g), foliar net photosynthesis rate (P) and transpiration rate (T) increased as soil water content increased, which both reached maximum va-lues at soil water content of 70%-80% field capacity (FC), while WUE reached a maximum of 7.26 mmol·m·s at the lowest soil water content (35%-45% FC). Both δC of water-soluble leaf and twig phloem material achieved maximum values at the lowest soil water content (35%-45% FC). Besides, δC values of leaf water-soluble compounds were significantly greater than that of phloem exudates, indicating that there was depletion in C in twig phloem compared with leaf water-soluble compounds and no obvious fractionation in the process of water-soluble material transportation from leaf to twig. Foliar WUE also reached a maximum of 7.26 mmol·m·s at the lowest soil water content (35%-45% FC). There was some difference between foliar WUE and WUE under the same condition, and the average difference was 0.52 mmol·m·s. The WUE had great space-time variability, by contrast, WUE was more representative. It was concluded that P. orientalis sapling adapted to drought condition by increasing water use efficiency and decreasing physiological activity.
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http://dx.doi.org/10.13287/j.1001-9332.201707.020DOI Listing
July 2017

[Foliar water use efficiency of Platycladus orientalis of different canopy heights in Beijing western mountains area, China].

Ying Yong Sheng Tai Xue Bao 2017 Jul;28(7):2143-2148

Ministry of Education Key Laboratory of Soil & Water Conservation and Desertification Combating, Beijing Forestry University, Beijing 100083, China.

In this study, we focused on Platycladus orientalis, a widely distributed tree species in Beijing western mountains area, and precisely determined its foliar water use efficiency (including instantaneous water use efficiency derived from gas exchange and short-term water use efficiency obtained on carbon isotope model) by carefully considering the discrepancies of meteorological factors and atmosphere CO concentration and δC among different canopy heights, hoping to provide theoretical basis for carbon sequestration and water loss in regional forest ecosystem, and offer technical support for regional forest management and maintenance. The results showed that the foliar instan-taneous water use efficiency tended to increase with the increasing canopy height, following the order of the upper canopy > the middle canopy > the lower canopy. A variety of meteorological factors synergistically influenced stomatal movement, and stomatal conductance would in turn have an effect on foliar instantaneous water use efficiency. Foliar short-term water use efficiency also increased with increasing canopy height, following the order of the upper canopy > the middle canopy > the lower canopy. The differences of foliar short-term water use efficiency among different heights could be explained by discrepancies of environmental drivers and atmosphere CO concentration and δC. Platycladus orientalis leaves in upper canopy adapted to ambient condition by improving water use efficiency.
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http://dx.doi.org/10.13287/j.1001-9332.201707.015DOI Listing
July 2017

Evolution of beak morphology in the Ground Tit revealed by comparative transcriptomics.

Front Zool 2017 21;14:58. Epub 2017 Dec 21.

Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101 China.

Background: Beak morphology exhibits considerable adaptive plasticity in birds, which results in highly varied or specialized forms in response to variations in ecology and life history. As the only parid species endemic to the Qinghai-Tibet Plateau, the Ground Tit () has evolved a distinctly long and curved beak from other parids. An integration of morphometrics, phylogenetics, transcriptomics and embryology allows us to address the evolutionary and developmental mechanisms of the adaptive beak structure observed in the Ground Tit.

Results: A morphometric approach quantified that the Ground Tit has a comparatively longer and more decurved upper beaks than other parids. We estimated that the ancestor of the Ground Tit likely had a short straight upper beak similar to most current recognized parid species using an ancestral state reconstruction. This morphological specialization is considered an adaptation to its ground-oriented behavior on the high plateau. To identify genetic mechanisms behind this adaptive change, a comparative transcriptomic analysis was applied between the Ground Tit and its closely related species, the Great Tit (). We detected that 623 genes were significantly differentially expressed in embryonic upper beaks between the two species, 17 of which were functionally annotated to correlate with bone development and morphogenesis, although genes related to bone development were not found to undergo accelerated evolution in the Ground Tit. RT-qPCR validation confirmed differential expression of five out of eight genes that were selected from the 17 genes. Subsequent functional assays in chicken embryos demonstrated that two of these genes, and , may affect beak morphology by modulating levels of osteoblasts and osteoclasts.

Conclusions: Our results provide preliminary evidence that development of the long decurved beak of the Ground Tit is likely regulated by transcriptional activities of multiple genes coordinating osteoblasts and osteoclasts. The integration of multiple approaches employed here sheds light on ecological and genetic mechanisms in the evolution of avian morphology.
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http://dx.doi.org/10.1186/s12983-017-0245-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5740785PMC
December 2017

Expressed Structurally Stable Inverted Duplicates in Mammalian Genomes as Functional Noncoding Elements.

Genome Biol Evol 2017 Apr;9(4):981-992

Department of Ecology and Evolution, University of Chicago.

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.
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http://dx.doi.org/10.1093/gbe/evx054DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5398296PMC
April 2017

LTR-mediated retroposition as a mechanism of RNA-based duplication in metazoans.

Genome Res 2016 12 20;26(12):1663-1675. Epub 2016 Oct 20.

Key Laboratory of Zoological Systematics and Evolution and State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.

In a broad range of taxa, genes can duplicate through an RNA intermediate in a process mediated by retrotransposons (retroposition). In mammals, L1 retrotransposons drive retroposition, but the elements responsible for retroposition in other animals have yet to be identified. Here, we examined young retrocopies from various animals that still retain the sequence features indicative of the underlying retroposition mechanism. In Drosophila melanogaster, we identified and de novo assembled 15 polymorphic retrocopies and found that all retroposed loci are chimeras of internal retrocopies flanked by discontinuous LTR retrotransposons. At the fusion points between the mRNAs and the LTR retrotransposons, we identified shared short similar sequences that suggest the involvement of microsimilarity-dependent template switches. By expanding our approach to mosquito, zebrafish, chicken, and mammals, we identified in all these species recently originated retrocopies with a similar chimeric structure and shared microsimilarities at the fusion points. We also identified several retrocopies that combine the sequences of two or more parental genes, demonstrating LTR-retroposition as a novel mechanism of exon shuffling. Finally, we found that LTR-mediated retrocopies are immediately cotranscribed with their flanking LTR retrotransposons. Transcriptional profiling coupled with sequence analyses revealed that the sense-strand transcription of the retrocopies often lead to the origination of in-frame proteins relative to the parental genes. Overall, our data show that LTR-mediated retroposition is highly conserved across a wide range of animal taxa; combined with previous work from plants and yeast, it represents an ancient and ongoing mechanism continuously shaping gene content evolution in eukaryotes.
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http://dx.doi.org/10.1101/gr.204925.116DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5131818PMC
December 2016

Divergent DNA Methylation Provides Insights into the Evolution of Duplicate Genes in Zebrafish.

G3 (Bethesda) 2016 Nov 8;6(11):3581-3591. Epub 2016 Nov 8.

The Key Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Sciences, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, Hubei, People's Republic of China

The evolutionary mechanism, fate and function of duplicate genes in various taxa have been widely studied; however, the mechanism underlying the maintenance and divergence of duplicate genes in remains largely unexplored. Whether and how the divergence of DNA methylation between duplicate pairs is associated with gene expression and evolutionary time are poorly understood. In this study, by analyzing bisulfite sequencing (BS-seq) and RNA-seq datasets from public data, we demonstrated that DNA methylation played a critical role in duplicate gene evolution in zebrafish. Initially, we found promoter methylation of duplicate genes generally decreased with evolutionary time as measured by synonymous substitution rate between paralogous duplicates (Ks). Importantly, promoter methylation of duplicate genes was negatively correlated with gene expression. Interestingly, for 665 duplicate gene pairs, one gene was consistently promoter methylated, while the other was unmethylated across nine different datasets we studied. Moreover, one motif enriched in promoter methylated duplicate genes tended to be bound by the transcription repression factor FOXD3, whereas a motif enriched in the promoter unmethylated sequences interacted with the transcription activator Sp1, indicating a complex interaction between the genomic environment and epigenome. Besides, body-methylated genes showed longer length than body-unmethylated genes. Overall, our results suggest that DNA methylation is highly important in the differential expression and evolution of duplicate genes in zebrafish.
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http://dx.doi.org/10.1534/g3.116.032243DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5100857PMC
November 2016

LINE-1-like retrotransposons contribute to RNA-based gene duplication in dicots.

Sci Rep 2016 Apr 21;6:24755. Epub 2016 Apr 21.

Key Laboratory of the Zoological Systematics and Evolution &State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.

RNA-based duplicated genes or functional retrocopies (retrogenes) are known to drive phenotypic evolution. Retrogenes emerge via retroposition, which is mainly mediated by long interspersed nuclear element 1 (LINE-1 or L1) retrotransposons in mammals. By contrast, long terminal repeat (LTR) retrotransposons appear to be the major player in plants, although an L1-like mechanism has also been hypothesized to be involved in retroposition. We tested this hypothesis by searching for young retrocopies, as these still retain the sequence features associated with the underlying retroposition mechanism. Specifically, we identified polymorphic retrocopies (retroCNVs) by analyzing public Arabidopsis (Arabidopsis thaliana) resequencing data. Furthermore, we searched for recently originated retrocopies encoded by the reference genome of Arabidopsis and Manihot esculenta. Across these two datasets, we found cases with L1-like hallmarks, namely, the expected target site sequence, a polyA tail and target site duplications. Such data suggest that an L1-like mechanism could operate in plants, especially dicots.
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http://dx.doi.org/10.1038/srep24755DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4838847PMC
April 2016

Divergent lncRNAs Regulate Gene Expression and Lineage Differentiation in Pluripotent Cells.

Cell Stem Cell 2016 05 17;18(5):637-52. Epub 2016 Mar 17.

Tsinghua-Peking Center for Life Sciences, School of Medicine, Tsinghua University, Beijing 100084, China. Electronic address:

Divergent lncRNAs that are transcribed in the opposite direction to nearby protein-coding genes comprise a significant proportion (∼20%) of total lncRNAs in mammalian genomes. Through genome-wide analysis, we found that the distribution of this lncRNA class strongly correlates with essential developmental regulatory genes. In pluripotent cells, divergent lncRNAs regulate the transcription of nearby genes. As an example, the divergent lncRNA Evx1as promotes transcription of its neighbor gene, EVX1, and regulates mesendodermal differentiation. At a single-cell level, early broad expression of Evx1as is followed by a rapid, high-level transcription of EVX1, supporting the idea that Evx1as plays an upstream role to facilitate EVX1 transcription. Mechanistically, Evx1as RNA binds to regulatory sites on chromatin, promotes an active chromatin state, and interacts with Mediator. Based on our analyses, we propose that the biological function of thousands of uncharacterized lncRNAs of this class may be inferred from the role of their neighboring adjacent genes.
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http://dx.doi.org/10.1016/j.stem.2016.01.024DOI Listing
May 2016

Underrepresentation of active histone modification marks in evolutionarily young genes.

Insect Sci 2017 Apr 8;24(2):174-186. Epub 2016 Mar 8.

State Key Laboratory of Integrated Management of Pest Insects and Rodents & Key Laboratory of the Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.

It is known that evolutionarily new genes can rapidly evolve essential roles in fundamental biological processes. Nevertheless, the underlying molecular mechanism of how they acquire their novel transcriptional pattern is less characterized except for the role of cis-regulatory evolution. Epigenetic modification offers an alternative possibility. Here, we examined how histone modifications have changed among different gene age groups in Drosophila melanogaster by integrative analyses of an updated new gene dataset and published epigenomic data. We found a robust pattern across various datasets where both the coverage and intensity of active histone modifications, histone 3 lysine 4 trimethylation and lysine 36 trimethylation, increased with evolutionary age. Such a temporal correlation is negative and much weaker for the repressive histone mark, lysine 9 trimethylation, which is expected given its major association with heterochromatin. By further comparison with neighboring old genes, the depletion of active marks of new genes could be only partially explained by the local epigenetic context. All these data are consistent with the observation that older genes bear relatively higher expression levels and suggest that the evolution of histone modifications could be implicated in transcriptional evolution after gene birth.
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http://dx.doi.org/10.1111/1744-7917.12299DOI Listing
April 2017

Correlated expression of retrocopies and parental genes in zebrafish.

Mol Genet Genomics 2016 Apr 11;291(2):723-37. Epub 2015 Nov 11.

The Key Laboratory of Aquatic Biodiversity and Conservation of Chinese Academy of Sciences, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan, 430072, Hubei, People's Republic of China.

Previous studies of the function and evolution of retrocopies in plants, Drosophila and non-mammalian chordates provided new insights into the origin of novel genes. However, little is known about retrocopies and their parental genes in teleosts, and it remains obscure whether there is any correlation between them. The present study aimed to characterize the spatial and temporal expression profiles of retrogenes and their parental genes based on RNA-Seq data from Danio rerio embryos and tissues from adult. Using a modified pipeline, 306 retrocopies were identified in the zebrafish genome, most of which exhibited ancient retroposition, and 76 of these showed a Ks < 2.0. Expression of a retrocopy is generally expected to present no correlation with its parental gene, as regulatory regions are not part of the retroposition event. Here, this assumption was tested based on RNA-Seq data from eight stages and thirteen tissue types of zebrafish. However, the result suggested that retrocopies displayed correlated expression with their parental genes. The level of correlation was found to decrease during embryogenesis, but to increase slightly within a tissue using Ks as the proxy for the divergence time. Tissue specificity was also observed: retrocopies were found to be expressed at a more specific level compared with their parental genes. Unlike Drosophila, which has sex chromosomes, zebrafish do not show testis-biased expression. Our study elaborated temporal and spatial patterns of expression of retrocopies in zebrafish, examined the correlation between retrocopies and parental genes and analyzed potential source of regulated elements of retrocopies, which lay a foundation for further functional study of retrocopies.
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http://dx.doi.org/10.1007/s00438-015-1140-5DOI Listing
April 2016

Genetic responses to seasonal variation in altitudinal stress: whole-genome resequencing of great tit in eastern Himalayas.

Sci Rep 2015 Sep 25;5:14256. Epub 2015 Sep 25.

Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China.

Species that undertake altitudinal migrations are exposed to a considerable seasonal variation in oxygen levels and temperature. How they cope with this was studied in a population of great tit (Parus major) that breeds at high elevations and winters at lower elevations in the eastern Himalayas. Comparison of population genomics of high altitudinal great tits and those living in lowlands revealed an accelerated genetic selection for carbohydrate energy metabolism (amino sugar, nucleotide sugar metabolism and insulin signaling pathways) and hypoxia response (PI3K-akt, mTOR and MAPK signaling pathways) in the high altitudinal population. The PI3K-akt, mTOR and MAPK pathways modulate the hypoxia-inducible factors, HIF-1α and VEGF protein expression thus indirectly regulate hypoxia induced angiogenesis, erythropoiesis and vasodilatation. The strategies observed in high altitudinal great tits differ from those described in a closely related species on the Tibetan Plateau, the sedentary ground tit (Parus humilis). This species has enhanced selection in lipid-specific metabolic pathways and hypoxia-inducible factor pathway (HIF-1). Comparative population genomics also revealed selection for larger body size in high altitudinal great tits.
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http://dx.doi.org/10.1038/srep14256DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4585896PMC
September 2015

Integrative analyses of RNA editing, alternative splicing, and expression of young genes in human brain transcriptome by deep RNA sequencing.

J Mol Cell Biol 2015 Aug 17;7(4):314-25. Epub 2015 Jul 17.

State Key Laboratory of Genetic Resources and Evolution, Yunnan Laboratory of Molecular Biology of Domestic Animals, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming 650223, China Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming 650204, China Laboratory for Conservation and Utilization of Bio-resource, Yunnan University, Kunming 650091, China

Next-generation RNA sequencing has been successfully used for identification of transcript assembly, evaluation of gene expression levels, and detection of post-transcriptional modifications. Despite these large-scale studies, additional comprehensive RNA-seq data from different subregions of the human brain are required to fully evaluate the evolutionary patterns experienced by the human brain transcriptome. Here, we provide a total of 6.5 billion RNA-seq reads from different subregions of the human brain. A significant correlation was observed between the levels of alternative splicing and RNA editing, which might be explained by a competition between the molecular machineries responsible for the splicing and editing of RNA. Young human protein-coding genes demonstrate biased expression to the neocortical and non-neocortical regions during evolution on the lineage leading to humans. We also found that a significantly greater number of young human protein-coding genes are expressed in the putamen, a tissue that was also observed to have the highest level of RNA-editing activity. The putamen, which previously received little attention, plays an important role in cognitive ability, and our data suggest a potential contribution of the putamen to human evolution.
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http://dx.doi.org/10.1093/jmcb/mjv043DOI Listing
August 2015
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