Distinct Patterns of Expression and Evolution of Intronless and Intron-Containing Mammalian Genes

Shabalina, Svetlana A.; Ogurtsov, Aleksey Y.; Spiridonov, Alexey N.; Novichkov, Pavel S.; Spiridonov, Nikolay A.; Koonin, Eugene V.

doi:10.1093/molbev/msq086

Title: Distinct Patterns of Expression and Evolution of Intronless and Intron-Containing Mammalian Genes

Journal Article · 01 April 2010 · Molecular Biology and Evolution

DOI: https://doi.org/10.1093/molbev/msq086 · OSTI ID:1625395

Shabalina, Svetlana A. ^[1]; Ogurtsov, Aleksey Y. ^[2]; Spiridonov, Alexey N. ^[3]; Novichkov, Pavel S. ^[4]; Spiridonov, Nikolay A. ^[5]; Koonin, Eugene V. ^[2]

National Institutes of Health (NIH), Bethesda, MD (United States). National Library of Medicine (NLM). National Center for Biotechnology Information; DOE/OSTI
National Institutes of Health (NIH), Bethesda, MD (United States). National Library of Medicine (NLM). National Center for Biotechnology Information
Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States). Dept. of Mathematics
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
U.S. Food and Drug Administration (FDA), Bethesda, MD (United States). Center for Drug Evaluation and Research. Division of Therapeutic Proteins

Comparison of expression levels and breadth and evolutionary rates of intronless and intron-containing mammalian genes shows that intronless genes are expressed at lower levels, tend to be tissue specific, and evolve significantly faster than spliced genes. By contrast, monomorphic spliced genes that are not subject to detectable alternative splicing and polymorphic alternatively spliced genes show similar statistically indistinguishable patterns of expression and evolution. Alternative splicing is most common in ancient genes, whereas intronless genes appear to have relatively recent origins. These results imply tight coupling between different stages of gene expression, in particular, transcription, splicing, and nucleocytosolic transport of transcripts, and suggest that formation of intronless genes is an important route of evolution of novel tissue-specific functions in animals.

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Research Organization:: Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1625395

Journal Information:: Molecular Biology and Evolution, Journal Name: Molecular Biology and Evolution Journal Issue: 8 Vol. 27; ISSN 0737-4038

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

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Additional file 1 of Genome-wide identification, expression analysis, and functional study of the GRAS transcription factor family and its response to abiotic stress in sorghum [Sorghum bicolor (L.) Moench] Fan, Yu; Yan, Jun; Lai, Dili figshare https://doi.org/10.6084/m9.figshare.14920929.v1	dataset	January 2021
Additional file 2 of Genome-wide identification, expression analysis, and functional study of the GRAS transcription factor family and its response to abiotic stress in sorghum [Sorghum bicolor (L.) Moench] Fan, Yu; Yan, Jun; Lai, Dili figshare https://doi.org/10.6084/m9.figshare.14920932	dataset	January 2021
Additional file 3 of Genome-wide identification, expression analysis, and functional study of the GRAS transcription factor family and its response to abiotic stress in sorghum [Sorghum bicolor (L.) Moench] Fan, Yu; Yan, Jun; Lai, Dili figshare https://doi.org/10.6084/m9.figshare.14920935.v1	dataset	January 2021
Additional file 4 of Genome-wide identification, expression analysis, and functional study of the GRAS transcription factor family and its response to abiotic stress in sorghum [Sorghum bicolor (L.) Moench] Fan, Yu; Yan, Jun; Lai, Dili figshare https://doi.org/10.6084/m9.figshare.14920938	dataset	January 2021
Additional file 5 of Genome-wide identification, expression analysis, and functional study of the GRAS transcription factor family and its response to abiotic stress in sorghum [Sorghum bicolor (L.) Moench] Fan, Yu; Yan, Jun; Lai, Dili figshare https://doi.org/10.6084/m9.figshare.14920941.v1	dataset	January 2021
Additional file 6 of Genome-wide identification, expression analysis, and functional study of the GRAS transcription factor family and its response to abiotic stress in sorghum [Sorghum bicolor (L.) Moench] Fan, Yu; Yan, Jun; Lai, Dili figshare https://doi.org/10.6084/m9.figshare.14920944	dataset	January 2021
Additional file 7 of Genome-wide identification, expression analysis, and functional study of the GRAS transcription factor family and its response to abiotic stress in sorghum [Sorghum bicolor (L.) Moench] Fan, Yu; Yan, Jun; Lai, Dili figshare https://doi.org/10.6084/m9.figshare.14920947.v1	dataset	January 2021
Additional file 8 of Genome-wide identification, expression analysis, and functional study of the GRAS transcription factor family and its response to abiotic stress in sorghum [Sorghum bicolor (L.) Moench] Fan, Yu; Yan, Jun; Lai, Dili figshare https://doi.org/10.6084/m9.figshare.14920950	dataset	January 2021
Additional file 9 of Genome-wide identification, expression analysis, and functional study of the GRAS transcription factor family and its response to abiotic stress in sorghum [Sorghum bicolor (L.) Moench] Fan, Yu; Yan, Jun; Lai, Dili figshare https://doi.org/10.6084/m9.figshare.14920953.v1	dataset	January 2021
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Additional file 2 of Genome-wide identification and expression profile analysis of trihelix transcription factor family genes in response to abiotic stress in sorghum [Sorghum bicolor (L.) Moench] Li, Kuiyin; Duan, Lili; Zhang, Yubo figshare https://doi.org/10.6084/m9.figshare.16815713	dataset	January 2021
Additional file 3 of Genome-wide identification and expression profile analysis of trihelix transcription factor family genes in response to abiotic stress in sorghum [Sorghum bicolor (L.) Moench] Li, Kuiyin; Duan, Lili; Zhang, Yubo figshare https://doi.org/10.6084/m9.figshare.16815716	dataset	January 2021
Additional file 4 of Genome-wide identification and expression profile analysis of trihelix transcription factor family genes in response to abiotic stress in sorghum [Sorghum bicolor (L.) Moench] Li, Kuiyin; Duan, Lili; Zhang, Yubo figshare https://doi.org/10.6084/m9.figshare.16815719	dataset	January 2021
Additional file 5 of Genome-wide identification and expression profile analysis of trihelix transcription factor family genes in response to abiotic stress in sorghum [Sorghum bicolor (L.) Moench] Li, Kuiyin; Duan, Lili; Zhang, Yubo figshare https://doi.org/10.6084/m9.figshare.16815722	dataset	January 2021
Additional file 6 of Genome-wide identification and expression profile analysis of trihelix transcription factor family genes in response to abiotic stress in sorghum [Sorghum bicolor (L.) Moench] Li, Kuiyin; Duan, Lili; Zhang, Yubo figshare https://doi.org/10.6084/m9.figshare.16815725.v1	dataset	January 2021
Additional file 7 of Genome-wide identification and expression profile analysis of trihelix transcription factor family genes in response to abiotic stress in sorghum [Sorghum bicolor (L.) Moench] Li, Kuiyin; Duan, Lili; Zhang, Yubo figshare https://doi.org/10.6084/m9.figshare.16815728	image	January 2021
Additional file 8 of Genome-wide identification and expression profile analysis of trihelix transcription factor family genes in response to abiotic stress in sorghum [Sorghum bicolor (L.) Moench] Li, Kuiyin; Duan, Lili; Zhang, Yubo figshare https://doi.org/10.6084/m9.figshare.16815731	image	January 2021
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Additional file 11 of Genome-wide investigation of the GRAS transcription factor family in foxtail millet (Setaria italica L.) Fan, Yu; Wei, Xiaobao; Lai, Dili figshare https://doi.org/10.6084/m9.figshare.16928757	image	January 2021
Additional file 12 of Genome-wide investigation of the GRAS transcription factor family in foxtail millet (Setaria italica L.) Fan, Yu; Wei, Xiaobao; Lai, Dili figshare https://doi.org/10.6084/m9.figshare.16928763.v1	image	January 2021
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Additional file 14 of Genome-wide investigation of the GRAS transcription factor family in foxtail millet (Setaria italica L.) Fan, Yu; Wei, Xiaobao; Lai, Dili figshare https://doi.org/10.6084/m9.figshare.16928769	image	January 2021
Additional file 15 of Genome-wide investigation of the GRAS transcription factor family in foxtail millet (Setaria italica L.) Fan, Yu; Wei, Xiaobao; Lai, Dili figshare https://doi.org/10.6084/m9.figshare.16928772.v1	image	January 2021
Additional file 1 of Genome-wide investigation of the GRAS transcription factor family in foxtail millet (Setaria italica L.) Fan, Yu; Wei, Xiaobao; Lai, Dili figshare https://doi.org/10.6084/m9.figshare.16928775.v1	dataset	January 2021
Additional file 2 of Genome-wide investigation of the GRAS transcription factor family in foxtail millet (Setaria italica L.) Fan, Yu; Wei, Xiaobao; Lai, Dili figshare https://doi.org/10.6084/m9.figshare.16928778.v1	dataset	January 2021
Additional file 3 of Genome-wide investigation of the GRAS transcription factor family in foxtail millet (Setaria italica L.) Fan, Yu; Wei, Xiaobao; Lai, Dili figshare https://doi.org/10.6084/m9.figshare.16928781.v1	dataset	January 2021
Additional file 4 of Genome-wide investigation of the GRAS transcription factor family in foxtail millet (Setaria italica L.) Fan, Yu; Wei, Xiaobao; Lai, Dili figshare https://doi.org/10.6084/m9.figshare.16928784	dataset	January 2021
Additional file 5 of Genome-wide investigation of the GRAS transcription factor family in foxtail millet (Setaria italica L.) Fan, Yu; Wei, Xiaobao; Lai, Dili figshare https://doi.org/10.6084/m9.figshare.16928787	dataset	January 2021
Additional file 6 of Genome-wide investigation of the GRAS transcription factor family in foxtail millet (Setaria italica L.) Fan, Yu; Wei, Xiaobao; Lai, Dili figshare https://doi.org/10.6084/m9.figshare.16928793.v1	dataset	January 2021
Additional file 7 of Genome-wide investigation of the GRAS transcription factor family in foxtail millet (Setaria italica L.) Fan, Yu; Wei, Xiaobao; Lai, Dili figshare https://doi.org/10.6084/m9.figshare.16928796.v1	dataset	January 2021
Additional file 8 of Genome-wide investigation of the GRAS transcription factor family in foxtail millet (Setaria italica L.) Fan, Yu; Wei, Xiaobao; Lai, Dili figshare https://doi.org/10.6084/m9.figshare.16928802.v1	dataset	January 2021
Additional file 9 of Genome-wide investigation of the GRAS transcription factor family in foxtail millet (Setaria italica L.) Fan, Yu; Wei, Xiaobao; Lai, Dili figshare https://doi.org/10.6084/m9.figshare.16928805	dataset	January 2021
Additional file 3 of Genome-wide identification and expression analysis of the bZIP transcription factor family genes in response to abiotic stress in Nicotiana tabacum L. Duan, Lili; Mo, Zejun; Fan, Yue figshare https://doi.org/10.6084/m9.figshare.19634924.v1	dataset	January 2022
Additional file 4 of Genome-wide identification and expression analysis of the bZIP transcription factor family genes in response to abiotic stress in Nicotiana tabacum L. Duan, Lili; Mo, Zejun; Fan, Yue figshare https://doi.org/10.6084/m9.figshare.19634927.v1	dataset	January 2022
Additional file 5 of Genome-wide identification and expression analysis of the bZIP transcription factor family genes in response to abiotic stress in Nicotiana tabacum L. Duan, Lili; Mo, Zejun; Fan, Yue figshare https://doi.org/10.6084/m9.figshare.19634930.v1	dataset	January 2022
Additional file 6 of Genome-wide identification and expression analysis of the bZIP transcription factor family genes in response to abiotic stress in Nicotiana tabacum L. Duan, Lili; Mo, Zejun; Fan, Yue figshare https://doi.org/10.6084/m9.figshare.19634933	dataset	January 2022
Additional file 7 of Genome-wide identification and expression analysis of the bZIP transcription factor family genes in response to abiotic stress in Nicotiana tabacum L. Duan, Lili; Mo, Zejun; Fan, Yue figshare https://doi.org/10.6084/m9.figshare.19634936	dataset	January 2022
Additional file 10 of Genome-wide survey and expression analysis of GRAS transcription factor family in sweetpotato provides insights into their potential roles in stress response Zhang, Chengbin; Liu, Siyuan; Liu, Delong figshare https://doi.org/10.6084/m9.figshare.19728166.v1	dataset	January 2022
Additional file 11 of Genome-wide survey and expression analysis of GRAS transcription factor family in sweetpotato provides insights into their potential roles in stress response Zhang, Chengbin; Liu, Siyuan; Liu, Delong figshare https://doi.org/10.6084/m9.figshare.19728169.v1	dataset	January 2022
Additional file 5 of Genome-wide survey and expression analysis of GRAS transcription factor family in sweetpotato provides insights into their potential roles in stress response Zhang, Chengbin; Liu, Siyuan; Liu, Delong figshare https://doi.org/10.6084/m9.figshare.19728184.v1	dataset	January 2022
Additional file 6 of Genome-wide survey and expression analysis of GRAS transcription factor family in sweetpotato provides insights into their potential roles in stress response Zhang, Chengbin; Liu, Siyuan; Liu, Delong figshare https://doi.org/10.6084/m9.figshare.19728187	dataset	January 2022
Additional file 7 of Genome-wide survey and expression analysis of GRAS transcription factor family in sweetpotato provides insights into their potential roles in stress response Zhang, Chengbin; Liu, Siyuan; Liu, Delong figshare https://doi.org/10.6084/m9.figshare.19728190.v1	dataset	January 2022
Additional file 1 of Genome-wide identification and characterization of the SPL gene family and its expression in the various developmental stages and stress conditions in foxtail millet (Setaria italica) Lai, Dili; Fan, Yue; Xue, Guoxing figshare https://doi.org/10.6084/m9.figshare.19807937	dataset	January 2022
Additional file 2 of Genome-wide identification and characterization of the SPL gene family and its expression in the various developmental stages and stress conditions in foxtail millet (Setaria italica) Lai, Dili; Fan, Yue; Xue, Guoxing figshare https://doi.org/10.6084/m9.figshare.19807940.v1	dataset	January 2022
Additional file 3 of Genome-wide identification and characterization of the SPL gene family and its expression in the various developmental stages and stress conditions in foxtail millet (Setaria italica) Lai, Dili; Fan, Yue; Xue, Guoxing figshare https://doi.org/10.6084/m9.figshare.19807943	dataset	January 2022
Additional file 4 of Genome-wide identification and characterization of the SPL gene family and its expression in the various developmental stages and stress conditions in foxtail millet (Setaria italica) Lai, Dili; Fan, Yue; Xue, Guoxing figshare https://doi.org/10.6084/m9.figshare.19807946.v1	dataset	January 2022
Additional file 5 of Genome-wide identification and characterization of the SPL gene family and its expression in the various developmental stages and stress conditions in foxtail millet (Setaria italica) Lai, Dili; Fan, Yue; Xue, Guoxing figshare https://doi.org/10.6084/m9.figshare.19807952.v1	dataset	January 2022
Additional file 6 of Genome-wide identification and characterization of the SPL gene family and its expression in the various developmental stages and stress conditions in foxtail millet (Setaria italica) Lai, Dili; Fan, Yue; Xue, Guoxing figshare https://doi.org/10.6084/m9.figshare.19807955	dataset	January 2022
Additional file 7 of Genome-wide identification and characterization of the SPL gene family and its expression in the various developmental stages and stress conditions in foxtail millet (Setaria italica) Lai, Dili; Fan, Yue; Xue, Guoxing figshare https://doi.org/10.6084/m9.figshare.19807958.v1	dataset	January 2022
Additional file 8 of Genome-wide identification and characterization of the SPL gene family and its expression in the various developmental stages and stress conditions in foxtail millet (Setaria italica) Lai, Dili; Fan, Yue; Xue, Guoxing figshare https://doi.org/10.6084/m9.figshare.19807964.v1	dataset	January 2022
Additional file 9 of Genome-wide identification and characterization of the SPL gene family and its expression in the various developmental stages and stress conditions in foxtail millet (Setaria italica) Lai, Dili; Fan, Yue; Xue, Guoxing figshare https://doi.org/10.6084/m9.figshare.19807967	dataset	January 2022
Additional file 10 of Genome-wide identification, phylogenetic analysis, and expression profiles of trihelix transcription factor family genes in quinoa (Chenopodium quinoa Willd.) under abiotic stress conditions Li, Kuiyin; Fan, Yue; Zhou, Guangyi figshare https://doi.org/10.6084/m9.figshare.20282176	dataset	January 2022
Additional file 1 of Genome-wide identification, phylogenetic analysis, and expression profiles of trihelix transcription factor family genes in quinoa (Chenopodium quinoa Willd.) under abiotic stress conditions Li, Kuiyin; Fan, Yue; Zhou, Guangyi figshare https://doi.org/10.6084/m9.figshare.20282179	dataset	January 2022
Additional file 2 of Genome-wide identification, phylogenetic analysis, and expression profiles of trihelix transcription factor family genes in quinoa (Chenopodium quinoa Willd.) under abiotic stress conditions Li, Kuiyin; Fan, Yue; Zhou, Guangyi figshare https://doi.org/10.6084/m9.figshare.20282182	dataset	January 2022
Additional file 5 of Genome-wide identification, phylogenetic analysis, and expression profiles of trihelix transcription factor family genes in quinoa (Chenopodium quinoa Willd.) under abiotic stress conditions Li, Kuiyin; Fan, Yue; Zhou, Guangyi figshare https://doi.org/10.6084/m9.figshare.20282191.v1	dataset	January 2022
Additional file 7 of Genome-wide identification, phylogenetic analysis, and expression profiles of trihelix transcription factor family genes in quinoa (Chenopodium quinoa Willd.) under abiotic stress conditions Li, Kuiyin; Fan, Yue; Zhou, Guangyi figshare https://doi.org/10.6084/m9.figshare.20282197.v1	dataset	January 2022
Additional file 8 of Genome-wide identification, phylogenetic analysis, and expression profiles of trihelix transcription factor family genes in quinoa (Chenopodium quinoa Willd.) under abiotic stress conditions Li, Kuiyin; Fan, Yue; Zhou, Guangyi figshare https://doi.org/10.6084/m9.figshare.20282203	dataset	January 2022
Additional file 9 of Genome-wide identification, phylogenetic analysis, and expression profiles of trihelix transcription factor family genes in quinoa (Chenopodium quinoa Willd.) under abiotic stress conditions Li, Kuiyin; Fan, Yue; Zhou, Guangyi figshare https://doi.org/10.6084/m9.figshare.20282206	dataset	January 2022
Additional file 1 of Genome-wide identification and expression analysis of the SPL transcription factor family and its response to abiotic stress in Quinoa (Chenopodium quinoa) Ren, Yanyan; Ma, Rui; Fan, Yue figshare https://doi.org/10.6084/m9.figshare.21628954.v1	image	January 2022
Additional file 2 of Genome-wide identification and expression analysis of the SPL transcription factor family and its response to abiotic stress in Quinoa (Chenopodium quinoa) Ren, Yanyan; Ma, Rui; Fan, Yue figshare https://doi.org/10.6084/m9.figshare.21628957.v1	dataset	January 2022
Additional file 3 of Genome-wide identification and expression analysis of the SPL transcription factor family and its response to abiotic stress in Quinoa (Chenopodium quinoa) Ren, Yanyan; Ma, Rui; Fan, Yue figshare https://doi.org/10.6084/m9.figshare.21628960	dataset	January 2022
Additional file 4 of Genome-wide identification and expression analysis of the SPL transcription factor family and its response to abiotic stress in Quinoa (Chenopodium quinoa) Ren, Yanyan; Ma, Rui; Fan, Yue figshare https://doi.org/10.6084/m9.figshare.21628963	dataset	January 2022
Additional file 5 of Genome-wide identification and expression analysis of the SPL transcription factor family and its response to abiotic stress in Quinoa (Chenopodium quinoa) Ren, Yanyan; Ma, Rui; Fan, Yue figshare https://doi.org/10.6084/m9.figshare.21628966	dataset	January 2022
Additional file 6 of Genome-wide identification and expression analysis of the SPL transcription factor family and its response to abiotic stress in Quinoa (Chenopodium quinoa) Ren, Yanyan; Ma, Rui; Fan, Yue figshare https://doi.org/10.6084/m9.figshare.21628969	dataset	January 2022
Additional file 7 of Genome-wide identification and expression analysis of the SPL transcription factor family and its response to abiotic stress in Quinoa (Chenopodium quinoa) Ren, Yanyan; Ma, Rui; Fan, Yue figshare https://doi.org/10.6084/m9.figshare.21628972	dataset	January 2022
Additional file 8 of Genome-wide identification and expression analysis of the SPL transcription factor family and its response to abiotic stress in Quinoa (Chenopodium quinoa) Ren, Yanyan; Ma, Rui; Fan, Yue figshare https://doi.org/10.6084/m9.figshare.21628975	dataset	January 2022
Additional file 1 of Splicing complexity as a pivotal feature of alternative exons in mammalian species Zhao, Feiyang; Yan, Yubin; Wang, Yaxi figshare https://doi.org/10.6084/m9.figshare.22619834	dataset	January 2023
Additional file 2 of Splicing complexity as a pivotal feature of alternative exons in mammalian species Zhao, Feiyang; Yan, Yubin; Wang, Yaxi figshare https://doi.org/10.6084/m9.figshare.22619837.v1	dataset	January 2023
Additional file 1 of Genome-wide identification, comparative analysis and functional roles in flavonoid biosynthesis of cytochrome P450 superfamily in pear (Pyrus spp.) Zhang, Wei; Li, Hongxiang; Li, Qionghou figshare https://doi.org/10.6084/m9.figshare.24240104	dataset	January 2023
Additional file 1 of Genome-wide identification, expression analysis, and functional study of the bZIP transcription factor family and its response to hormone treatments in pea (Pisum sativum L.) Wu, Xiaozong; Cheng, Changhe; Ma, Rui figshare https://doi.org/10.6084/m9.figshare.24628079.v1	dataset	January 2023
Additional file 1 of Genome-wide identification and expression pattern analysis of the kiwifruit GRAS transcription factor family in response to salt stress Zhu, Ling; Yin, Tuo; Zhang, Mengjie figshare https://doi.org/10.6084/m9.figshare.24934186	dataset	January 2024
Introns and gene expression: Cellular constraints, transcriptional regulation, and evolutionary consequences: Prospects & Overviews Heyn, Patricia; Kalinka, Alex T.; Tomancak, Pavel BioEssays, Vol. 37, Issue 2 https://doi.org/10.1002/bies.201400138	journal	November 2014
Three Independent Determinants of Protein Evolutionary Rate Choi, Sun Shim; Hannenhalli, Sridhar Journal of Molecular Evolution, Vol. 76, Issue 3 https://doi.org/10.1007/s00239-013-9543-6	journal	February 2013
Deep intronic mutations and human disease Vaz-Drago, Rita; Custódio, Noélia; Carmo-Fonseca, Maria Human Genetics, Vol. 136, Issue 9 https://doi.org/10.1007/s00439-017-1809-4	journal	May 2017
Alternative Splicing of the Delta-Opioid Receptor Gene Suggests Existence of New Functional Isoforms Piltonen, Marjo; Parisien, Marc; Grégoire, Stéphanie Molecular Neurobiology, Vol. 56, Issue 4 https://doi.org/10.1007/s12035-018-1253-z	journal	July 2018
Expansion of a bitter taste receptor family in a polyphagous insect herbivore Xu, Wei; Papanicolaou, Alexie; Zhang, Hui-Jie Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep23666	journal	April 2016
Export and stability of naturally intronless mRNAs require specific coding region sequences and the TREX mRNA export complex Lei, H.; Dias, A. P.; Reed, R. Proceedings of the National Academy of Sciences, Vol. 108, Issue 44 https://doi.org/10.1073/pnas.1113076108	journal	October 2011
Genome structure and metabolic features in the red seaweed Chondrus crispus shed light on evolution of the Archaeplastida Collen, J.; Porcel, B.; Carre, W. Proceedings of the National Academy of Sciences, Vol. 110, Issue 13 https://doi.org/10.1073/pnas.1221259110	journal	March 2013
Sounds of silence: synonymous nucleotides as a key to biological regulation and complexity Shabalina, S. A.; Spiridonov, N. A.; Kashina, A. Nucleic Acids Research, Vol. 41, Issue 4 https://doi.org/10.1093/nar/gks1205	journal	January 2013
Genome-wide features of introns are evolutionary decoupled among themselves and from genome size throughout Eukarya Lozada-Chávez, Irma; Stadler, Peter F.; Prohaska, Sonja J. https://doi.org/10.1101/283549	posted_content	March 2018
Antagonistic relationships between intron content and codon usage bias of genes in three mosquito species: functional and evolutionary implications Behura, Susanta K.; Singh, Brajendra K.; Severson, David W. Evolutionary Applications, Vol. 6, Issue 7 https://doi.org/10.1111/eva.12088	journal	July 2013
Why eukaryotic cells use introns to enhance gene expression: Splicing reduces transcription-associated mutagenesis by inhibiting topoisomerase I cutting activity Niu, Deng-Ke; Yang, Yu-Fei Biology Direct, Vol. 6, Issue 1 https://doi.org/10.1186/1745-6150-6-24	journal	January 2011
Phylogenetic and genomic analyses of the ribosomal oxygenases Riox1 (No66) and Riox2 (Mina53) provide new insights into their evolution Bräuer, Katharina E.; Brockers, Kevin; Moneer, Jasmin BMC Evolutionary Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s12862-018-1215-0	journal	June 2018
Evolution of intron splicing towards optimized gene expression is based on various Cis- and Trans-molecular mechanisms Frumkin, Idan; Yofe, Ido; Bar-Ziv, Raz PLOS Biology, Vol. 17, Issue 8 https://doi.org/10.1371/journal.pbio.3000423	journal	August 2019
Enhancement of Transcription by a Splicing-Competent Intron Is Dependent on Promoter Directionality Agarwal, Neha; Ansari, Athar PLOS Genetics, Vol. 12, Issue 5 https://doi.org/10.1371/journal.pgen.1006047	journal	May 2016
Genome-wide investigation of superoxide dismutase (SOD) gene family and their regulatory miRNAs reveal the involvement in abiotic stress and hormone response in tea plant (Camellia sinensis) Zhou, Chengzhe; Zhu, Chen; Fu, Haifeng PLOS ONE, Vol. 14, Issue 10 https://doi.org/10.1371/journal.pone.0223609	journal	October 2019
Molecular Evolution and Functional Diversification of Replication Protein A1 in Plants Aklilu, Behailu B.; Culligan, Kevin M. Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.00033	journal	January 2016
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Title: Distinct Patterns of Expression and Evolution of Intronless and Intron-Containing Mammalian Genes

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