Codon usage in twelve species of Drosophila
TLDR
The results suggest that natural selection has acted on codon usage in the genus Drosophila, at least often enough to leave a footprint of selection in modern genomes.Abstract:
Codon usage bias (CUB), the uneven use of synonymous codons, is a ubiquitous observation in virtually all organisms examined. The pattern of codon usage is generally similar among closely related species, but differs significantly among distantly related organisms, e.g., bacteria, yeast, and Drosophila. Several explanations for CUB have been offered and some have been supported by observations and experiments, although a thorough understanding of the evolutionary forces (random drift, mutation bias, and selection) and their relative importance remains to be determined. The recently available complete genome DNA sequences of twelve phylogenetically defined species of Drosophila offer a hitherto unprecedented opportunity to examine these problems. We report here the patterns of codon usage in the twelve species and offer insights on possible evolutionary forces involved. (1) Codon usage is quite stable across 11/12 of the species: G- and especially C-ending codons are used most frequently, thus defining the preferred codons. (2) The only amino acid that changes in preferred codon is Serine with six species of the melanogaster group favoring TCC while the other species, particularly subgenus Drosophila species, favor AGC. (3) D. willistoni is an exception to these generalizations in having a shifted codon usage for seven amino acids toward A/T in the wobble position. (4) Amino acids differ in their contribution to overall CUB, Leu having the greatest and Asp the least. (5) Among two-fold degenerate amino acids, A/G ending amino acids have more selection on codon usage than T/C ending amino acids. (6) Among the different chromosome arms or elements, genes on the non-recombining element F (dot chromosome) have the least CUB, while genes on the element A (X chromosome) have the most. (7) Introns indicate that mutation bias in all species is approximately 2:1, AT:GC, the opposite of codon usage bias. (8) There is also evidence for some overall regional bias in base composition that may influence codon usage. Overall, these results suggest that natural selection has acted on codon usage in the genus Drosophila, at least often enough to leave a footprint of selection in modern genomes. However, there is evidence in the data that random forces (drift and mutation) have also left patterns in the data, especially in genes under weak selection for codon usage for example genes in regions of low recombination. The documentation of codon usage patterns in each of these twelve genomes also aids in ongoing annotation efforts.read more
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Journal ArticleDOI
Evolution of genes and genomes on the Drosophila phylogeny.
Andrew G. Clark,Michael B. Eisen,Michael B. Eisen,Douglas Smith,Casey M. Bergman,Brian Oliver,Therese A. Markow,Thomas C. Kaufman,Manolis Kellis,Manolis Kellis,William M. Gelbart,Venky N. Iyer,Daniel A. Pollard,Timothy B. Sackton,Amanda M. Larracuente,Nadia D. Singh,José P. Abad,Dawn N. Abt,Boris Adryan,Montserrat Aguadé,Hiroshi Akashi,Wyatt W. Anderson,Charles F. Aquadro,David H. Ardell,Roman Arguello,Carlo G. Artieri,Daniel A. Barbash,Daniel Barker,Paolo Barsanti,Phil Batterham,Serafim Batzoglou,Dave Begun,Arjun Bhutkar,Arjun Bhutkar,Enrico Blanco,Stephanie Bosak,Robert K. Bradley,Adrianne Brand,Michael R. Brent,Angela N. Brooks,Randall H. Brown,Roger K. Butlin,Corrado Caggese,Brian R. Calvi,A. Bernardo Carvalho,Anat Caspi,Sergio Castrezana,Susan E. Celniker,Jean L. Chang,Charles Chapple,Sourav Chatterji,Sourav Chatterji,Asif T. Chinwalla,Alberto Civetta,Sandra W. Clifton,Josep M. Comeron,James C. Costello,Jerry A. Coyne,Jennifer Daub,Robert David,Arthur L. Delcher,Kim D. 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Remington,Tania Tassinari Rieger,Michael G. Ritchie,Charles Robin,Yu-Hui Rogers,Claudia Rohde,Julio Rozas,Marc Rubenfield,Alfredo Ruiz,Susan M. Russo,Steven L. Salzberg,Alejandro Sánchez-Gracia,Alejandro Sánchez-Gracia,David J. Saranga,Hajime Sato,Stephen W. Schaeffer,Michael C. Schatz,Todd A. Schlenke,Russell Schwartz,Carmen Segarra,Rama S. Singh,Laura K. Sirot,Marina Sirota,Nicholas Sisneros,Christopher D. Smith,Christopher D. Smith,Temple F. Smith,John Spieth,Deborah E. Stage,Alexander Stark,Alexander Stark,Wolfgang Stephan,Robert L. Strausberg,Sebastian Strempel,David Sturgill,Granger G. Sutton,Granger G. Sutton,Wei Tao,Sarah A. Teichmann,Yoshiko N. Tobari,Yoshihiko Tomimura,Jason M. Tsolas,Vera L. S. Valente,Eli Venter,J. Craig Venter,Saverio Vicario,Filipe G. Vieira,Albert J. Vilella,Alfredo Villasante,Brian P. Walenz,Jun Wang,Jun Wang,Marvin Wasserman,Thomas D. Watts,Derek Wilson,Richard K. Wilson,Rod A. Wing,Mariana F. Wolfner,Alex Wong,Gane Ka-Shu Wong,Gane Ka-Shu Wong,Chung-I Wu,Gabriel C. Wu,Daisuke Yamamoto,Hsiao Pei Yang,Shiaw Pyng Yang,James A. Yorke,Kiyohito Yoshida,Evgeny M. Zdobnov,Peili Zhang,Yu Zhang,Aleksey V. Zimin,Jennifer Baldwin,Amr Abdouelleil,Jamal Abdulkadir,Adal Abebe,Brikti Abera,Justin Abreu,St Christophe Acer,Lynne Aftuck,Allen Alexander,Peter An,Erica Anderson,Scott Anderson,Harindra Arachi,Marc Azer,Pasang Bachantsang,Andrew Barry,Tashi Bayul,Aaron M. Berlin,Daniel Bessette,Toby Bloom,Jason Blye,Leonid Boguslavskiy,Claude Bonnet,Boris Boukhgalter,Imane Bourzgui,Adam Brown,Patrick Cahill,Sheridon Channer,Yama Cheshatsang,Lisa Chuda,Mieke Citroen,Alville Collymore,Patrick Cooke,Maura Costello,Katie D'Aco,Riza M. Daza,Georgius De Haan,Stuart DeGray,Christina Demaso,Norbu Dhargay,Kimberly Dooley,Erin E. Dooley,Missole Doricent,Passang Dorje,Kunsang Dorjee,Alan Dupes,Richard Elong,Jill Falk,Abderrahim Farina,Susan Faro,Diallo Ferguson,Sheila Fisher,Chelsea D. 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TL;DR: These genome sequences augment the formidable genetic tools that have made Drosophila melanogaster a pre-eminent model for animal genetics, and will further catalyse fundamental research on mechanisms of development, cell biology, genetics, disease, neurobiology, behaviour, physiology and evolution.
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The nearly neutral theory of molecular evolution
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Evolution of genes and genomes on the Drosophila phylogeny.
Andrew G. Clark,Michael B. Eisen,Michael B. Eisen,Douglas Smith,Casey M. Bergman,Brian Oliver,Therese A. Markow,Thomas C. Kaufman,Manolis Kellis,Manolis Kellis,William M. Gelbart,Venky N. Iyer,Daniel A. Pollard,Timothy B. Sackton,Amanda M. Larracuente,Nadia D. Singh,José P. Abad,Dawn N. Abt,Boris Adryan,Montserrat Aguadé,Hiroshi Akashi,Wyatt W. Anderson,Charles F. Aquadro,David H. Ardell,Roman Arguello,Carlo G. Artieri,Daniel A. Barbash,Daniel Barker,Paolo Barsanti,Phil Batterham,Serafim Batzoglou,Dave Begun,Arjun Bhutkar,Arjun Bhutkar,Enrico Blanco,Stephanie Bosak,Robert K. Bradley,Adrianne Brand,Michael R. Brent,Angela N. Brooks,Randall H. Brown,Roger K. Butlin,Corrado Caggese,Brian R. Calvi,A. Bernardo Carvalho,Anat Caspi,Sergio Castrezana,Susan E. Celniker,Jean L. Chang,Charles Chapple,Sourav Chatterji,Sourav Chatterji,Asif T. Chinwalla,Alberto Civetta,Sandra W. Clifton,Josep M. Comeron,James C. Costello,Jerry A. Coyne,Jennifer Daub,Robert David,Arthur L. Delcher,Kim D. Delehaunty,Chuong B. Do,Heather Ebling,Kevin A. Edwards,Thomas H. Eickbush,Jay D. Evans,Alan Filipski,Sven Findeiß,Sven Findeiß,Eva Freyhult,Lucinda Fulton,Robert S. Fulton,Ana Cristina Lauer Garcia,Anastasia Gardiner,David A. Garfield,Barry E. Garvin,Greg Gibson,Don Gilbert,Sante Gnerre,Jennifer Godfrey,Robert T. Good,Valer Gotea,Brenton Gravely,Anthony J. Greenberg,Sam Griffiths-Jones,Sam Griffiths-Jones,Samuel R. Gross,Roderic Guigó,Erik Gustafson,Wilfried Haerty,Matthew W. Hahn,Daniel L. Halligan,Aaron L. Halpern,Gillian M. Halter,Mira V. Han,Andreas Heger,LaDeana W. Hillier,Angie S. Hinrichs,Ian Holmes,Roger A. Hoskins,Melissa J. Hubisz,Dan Hultmark,Melanie A. Huntley,David B. Jaffe,Santosh Jagadeeshan,William R. Jeck,Justin Johnson,Corbin D. Jones,William C. Jordan,Gary H. Karpen,Gary H. Karpen,Eiko Kataoka,Peter D. Keightley,Pouya Kheradpour,Ewen F. Kirkness,Leonardo Koerich,Karsten Kristiansen,Dave Kudrna,Rob J. Kulathinal,Sudhir Kumar,Roberta Kwok,Eric S. Lander,Charles H. Langley,Richard T. Lapoint,Brian P. Lazzaro,So Jeong Lee,Lisa Levesque,Ruiqiang Li,Ruiqiang Li,Chiao-Feng Lin,Michael F. Lin,Michael F. Lin,Kerstin Lindblad-Toh,Ana Llopart,Manyuan Long,Lloyd Low,Elena R. Lozovsky,Jian Lu,Meizhong Luo,Carlos A. Machado,Wojciech Makalowski,Mar Marzo,Muneo Matsuda,Luciano M. Matzkin,Bryant F. McAllister,Carolyn S. McBride,Brendan McKernan,Kevin McKernan,Maria Mendez-Lago,Patrick Minx,Michael U. Mollenhauer,Kristi L. Montooth,Stephen M. Mount,Xu Mu,Eugene W. Myers,Bárbara Negre,Stuart J. Newfeld,Rasmus Nielsen,Mohamed A. F. Noor,Patrick M. O’Grady,Lior Pachter,Montserrat Papaceit,Matthew J. Parisi,Michael Parisi,Leopold Parts,Jakob Skou Pedersen,Jakob Skou Pedersen,Graziano Pesole,Adam M. Phillippy,Chris P. Ponting,Mihai Pop,Damiano Porcelli,Jeffrey R. Powell,Sonja J. Prohaska,Kim D. Pruitt,Marta Sabariego Puig,Hadi Quesneville,Kristipati Ravi Ram,David M. Rand,Matthew D. Rasmussen,Laura K. Reed,Robert A. Reenan,Amy Denise Reily,Karin A. Remington,Tania Tassinari Rieger,Michael G. Ritchie,Charles Robin,Yu-Hui Rogers,Claudia Rohde,Julio Rozas,Marc Rubenfield,Alfredo Ruiz,Susan M. Russo,Steven L. Salzberg,Alejandro Sánchez-Gracia,Alejandro Sánchez-Gracia,David J. Saranga,Hajime Sato,Stephen W. Schaeffer,Michael C. Schatz,Todd A. Schlenke,Russell Schwartz,Carmen Segarra,Rama S. Singh,Laura K. Sirot,Marina Sirota,Nicholas Sisneros,Christopher D. Smith,Christopher D. Smith,Temple F. Smith,John Spieth,Deborah E. Stage,Alexander Stark,Alexander Stark,Wolfgang Stephan,Robert L. Strausberg,Sebastian Strempel,David Sturgill,Granger G. Sutton,Granger G. Sutton,Wei Tao,Sarah A. Teichmann,Yoshiko N. Tobari,Yoshihiko Tomimura,Jason M. Tsolas,Vera L. S. Valente,Eli Venter,J. Craig Venter,Saverio Vicario,Filipe G. Vieira,Albert J. Vilella,Alfredo Villasante,Brian P. Walenz,Jun Wang,Jun Wang,Marvin Wasserman,Thomas D. Watts,Derek Wilson,Richard K. Wilson,Rod A. Wing,Mariana F. Wolfner,Alex Wong,Gane Ka-Shu Wong,Gane Ka-Shu Wong,Chung-I Wu,Gabriel C. Wu,Daisuke Yamamoto,Hsiao Pei Yang,Shiaw Pyng Yang,James A. Yorke,Kiyohito Yoshida,Evgeny M. Zdobnov,Peili Zhang,Yu Zhang,Aleksey V. Zimin,Jennifer Baldwin,Amr Abdouelleil,Jamal Abdulkadir,Adal Abebe,Brikti Abera,Justin Abreu,St Christophe Acer,Lynne Aftuck,Allen Alexander,Peter An,Erica Anderson,Scott Anderson,Harindra Arachi,Marc Azer,Pasang Bachantsang,Andrew Barry,Tashi Bayul,Aaron M. Berlin,Daniel Bessette,Toby Bloom,Jason Blye,Leonid Boguslavskiy,Claude Bonnet,Boris Boukhgalter,Imane Bourzgui,Adam Brown,Patrick Cahill,Sheridon Channer,Yama Cheshatsang,Lisa Chuda,Mieke Citroen,Alville Collymore,Patrick Cooke,Maura Costello,Katie D'Aco,Riza M. Daza,Georgius De Haan,Stuart DeGray,Christina Demaso,Norbu Dhargay,Kimberly Dooley,Erin E. Dooley,Missole Doricent,Passang Dorje,Kunsang Dorjee,Alan Dupes,Richard Elong,Jill Falk,Abderrahim Farina,Susan Faro,Diallo Ferguson,Sheila Fisher,Chelsea D. Foley,Alicia Franke,Dennis C. Friedrich,Loryn Gadbois,Gary Gearin,Christina R. Gearin,Georgia Giannoukos,Tina Goode,Joseph Graham,Edward Grandbois,Sharleen Grewal,Kunsang Gyaltsen,Nabil Hafez,Birhane Hagos,Jennifer L. Hall,Charlotte Henson,Andrew Hollinger,Tracey Honan,Monika D. Huard,Leanne Hughes,Brian Hurhula,M. Erii Husby,Asha Kamat,Ben Kanga,Seva Kashin,Dmitry Khazanovich,Peter Kisner,Krista Lance,Marcia Lara,William Lee,Niall J. Lennon,Frances Letendre,Rosie Levine,Alex Lipovsky,Xiaohong Liu,Jinlei Liu,Shangtao Liu,Tashi Lokyitsang,Yeshi Lokyitsang,Rakela Lubonja,Annie Lui,Pen MacDonald,Vasilia Magnisalis,Kebede Maru,Charles Matthews,William McCusker,Susan McDonough,Teena Mehta,James Meldrim,Louis Meneus,Oana Mihai,Atanas Mihalev,Tanya Mihova,Rachel Mittelman,Valentine Mlenga,Anna Montmayeur,Leonidas Mulrain,Adam Navidi,Jerome Naylor,Tamrat Negash,Thu Nguyen,Nga Nguyen,Robert Nicol,Choe Norbu,Nyima Norbu,Nathaniel Novod,Barry O'Neill,Sahal Osman,Eva Markiewicz,Otero L. Oyono,Christopher Patti,Pema Phunkhang,Fritz Pierre,Margaret Priest,Sujaa Raghuraman,Filip Rege,Rebecca Reyes,Cecil Rise,Peter Rogov,Keenan Ross,Elizabeth P. Ryan,Sampath Settipalli,Terry Shea,Ngawang Sherpa,Lu Shi,Diana Shih,Todd Sparrow,Jessica Spaulding,John Stalker,Nicole Stange-Thomann,Sharon Stavropoulos,Catherine Stone,Christopher Strader,Senait Tesfaye,Talene Thomson,Yama Thoulutsang,Dawa Thoulutsang,Kerri Topham,Ira Topping,Tsamla Tsamla,Helen Vassiliev,Andy Vo,Tsering Wangchuk,Tsering Wangdi,Michael Weiand,Jane Wilkinson,Adam Wilson,Shailendra Yadav,Geneva Young,Qing Yu,Lisa Zembek,Danni Zhong,Andrew Zimmer,Zac Zwirko,Pablo Alvarez,William Brockman,Jonathan Butler,Cheewhye Chin,Manfred Grabherr,Michael Kleber,Evan Mauceli,Iain MacCallum +429 more
The codon Adaptation Index--a measure of directional synonymous codon usage bias, and its potential applications.
Paul M. Sharp,Wen-Hsiung Li +1 more