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      New genes often acquire male-specific functions but rarely become essential in Drosophila

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          Abstract

          In this study, Kondo et al. performed large-scale CRISPR/Cas9 mutagenesis of “conserved, essential” and “young, RNAi-lethal” genes and confirmed the lethality of conserved genes but not young genes. Additionally, two young gene mutants resulted in spermatogenesis and/or male sterility, indicating that young genes have a preferential impact on male reproductive system function.

          Abstract

          Relatively little is known about the in vivo functions of newly emerging genes, especially in metazoans. Although prior RNAi studies reported prevalent lethality among young gene knockdowns, our phylogenomic analyses reveal that young Drosophila genes are frequently restricted to the nonessential male reproductive system. We performed large-scale CRISPR/Cas9 mutagenesis of “conserved, essential” and “young, RNAi-lethal” genes and broadly confirmed the lethality of the former but the viability of the latter. Nevertheless, certain young gene mutants exhibit defective spermatogenesis and/or male sterility. Moreover, we detected widespread signatures of positive selection on young male-biased genes. Thus, young genes have a preferential impact on male reproductive system function.

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          Most cited references28

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          Genome-wide midrange transcription profiles reveal expression level relationships in human tissue specification.

          Genes are often characterized dichotomously as either housekeeping or single-tissue specific. We conjectured that crucial functional information resides in genes with midrange profiles of expression. To obtain such novel information genome-wide, we have determined the mRNA expression levels for one of the largest hitherto analyzed set of 62 839 probesets in 12 representative normal human tissues. Indeed, when using a newly defined graded tissue specificity index tau, valued between 0 for housekeeping genes and 1 for tissue-specific genes, genes with midrange profiles having 0.15 50% of all expression patterns. We developed a binary classification, indicating for every gene the I(B) tissues in which it is overly expressed, and the 12-I(B) tissues in which it shows low expression. The 85 dominant midrange patterns with I(B)=2-11 were found to be bimodally distributed, and to contribute most significantly to the definition of tissue specification dendrograms. Our analyses provide a novel route to infer expression profiles for presumed ancestral nodes in the tissue dendrogram. Such definition has uncovered an unsuspected correlation, whereby de novo enhancement and diminution of gene expression go hand in hand. These findings highlight the importance of gene suppression events, with implications to the course of tissue specification in ontogeny and phylogeny. All data and analyses are publically available at the GeneNote website, http://genecards.weizmann.ac.il/genenote/ and, GEO accession GSE803. doron.lancet@weizmann.ac.il Four tables available at the above site.
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            Origins, evolution, and phenotypic impact of new genes.

            Ever since the pre-molecular era, the birth of new genes with novel functions has been considered to be a major contributor to adaptive evolutionary innovation. Here, I review the origin and evolution of new genes and their functions in eukaryotes, an area of research that has made rapid progress in the past decade thanks to the genomics revolution. Indeed, recent work has provided initial whole-genome views of the different types of new genes for a large number of different organisms. The array of mechanisms underlying the origin of new genes is compelling, extending way beyond the traditionally well-studied source of gene duplication. Thus, it was shown that novel genes also regularly arose from messenger RNAs of ancestral genes, protein-coding genes metamorphosed into new RNA genes, genomic parasites were co-opted as new genes, and that both protein and RNA genes were composed from scratch (i.e., from previously nonfunctional sequences). These mechanisms then also contributed to the formation of numerous novel chimeric gene structures. Detailed functional investigations uncovered different evolutionary pathways that led to the emergence of novel functions from these newly minted sequences and, with respect to animals, attributed a potentially important role to one specific tissue--the testis--in the process of gene birth. Remarkably, these studies also demonstrated that novel genes of the various types significantly impacted the evolution of cellular, physiological, morphological, behavioral, and reproductive phenotypic traits. Consequently, it is now firmly established that new genes have indeed been major contributors to the origin of adaptive evolutionary novelties.
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              Diversity and dynamics of the Drosophila transcriptome

              Animal transcriptomes are dynamic, each cell type, tissue and organ system expressing an ensemble of transcript isoforms that give rise to substantial diversity. We identified new genes, transcripts, and proteins using poly(A)+ RNA sequence from Drosophila melanogaster cultured cell lines, dissected organ systems, and environmental perturbations. We found a small set of mostly neural-specific genes has the potential to encode thousands of transcripts each through extensive alternative promoter usage and RNA splicing. The magnitudes of splicing changes are larger between tissues than between developmental stages, and most sex-specific splicing is gonad-specific. Gonads express hundreds of previously unknown coding and long noncoding RNAs (lncRNAs) some of which are antisense to protein-coding genes and produce short regulatory RNAs. Furthermore, previously identified pervasive intergenic transcription occurs primarily within newly identified introns. The fly transcriptome is substantially more complex than previously recognized arising from combinatorial usage of promoters, splice sites, and polyadenylation sites.
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                Author and article information

                Journal
                Genes Dev
                Genes Dev
                genesdev
                genesdev
                GAD
                Genes & Development
                Cold Spring Harbor Laboratory Press
                0890-9369
                1549-5477
                15 September 2017
                : 31
                : 18
                : 1841-1846
                Affiliations
                [1 ]Invertebrate Genetics Laboratory, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan;
                [2 ]Department of Developmental Biology, Sloan-Kettering Institute, New York, New York 10065, USA;
                [3 ]Department of Biological Statistics and Computational Biology, Cornell University, Ithaca, New York 14853, USA;
                [4 ]Tri-Institutional Training Program in Computational Biology and Medicine, New York, New York 10021, USA;
                [5 ]Department of Biology, Yeshiva University, New York, New York 10033, USA;
                [6 ]Simons Center for Quantitative Biology, Cold Spring Harbor Laboratory, Cold Spring Harbor, New York 11724, USA
                Author notes
                [7]

                These authors contributed equally to this work.

                Article
                8711660
                10.1101/gad.303131.117
                5695085
                29051389
                2f81792e-87ea-455c-9a33-2edd68977dad
                © 2017 Kondo et al.; Published by Cold Spring Harbor Laboratory Press

                This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genesdev.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.

                History
                : 11 June 2017
                : 12 September 2017
                Page count
                Pages: 6
                Funding
                Funded by: Mochida Memorial Foundation for Medical and Pharmaceutical Research , open-funder-registry 10.13039/501100005865;
                Award ID: R01-GM102192
                Award ID: NIH R15-HD080511
                Funded by: National Institutes of Health (NIH) , open-funder-registry 10.13039/100000002;
                Award ID: R01-NS083833
                Award ID: R01-GM083300
                Funded by: Memorial Sloan-Kettering Core
                Award ID: P30-CA008748
                Categories
                Research Communication

                drosophila,gene evolution,spermatogenesis,testis
                drosophila, gene evolution, spermatogenesis, testis

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