Literature DB >> 27892853

Structure of the germline genome of Tetrahymena thermophila and relationship to the massively rearranged somatic genome.

Eileen P Hamilton1, Aurélie Kapusta2, Piroska E Huvos3, Shelby L Bidwell4, Nikhat Zafar4, Haibao Tang4, Michalis Hadjithomas4, Vivek Krishnakumar4, Jonathan H Badger4, Elisabet V Caler4, Carsten Russ5, Qiandong Zeng5, Lin Fan5, Joshua Z Levin5, Terrance Shea5, Sarah K Young5, Ryan Hegarty5, Riza Daza5, Sharvari Gujja5, Jennifer R Wortman5, Bruce W Birren5, Chad Nusbaum5, Jainy Thomas2, Clayton M Carey2, Ellen J Pritham2, Cédric Feschotte2, Tomoko Noto6, Kazufumi Mochizuki6, Romeo Papazyan7, Sean D Taverna7, Paul H Dear8, Donna M Cassidy-Hanley9, Jie Xiong10, Wei Miao10, Eduardo Orias1, Robert S Coyne4.   

Abstract

The germline genome of the binucleated ciliate Tetrahymena thermophila undergoes programmed chromosome breakage and massive DNA elimination to generate the somatic genome. Here, we present a complete sequence assembly of the germline genome and analyze multiple features of its structure and its relationship to the somatic genome, shedding light on the mechanisms of genome rearrangement as well as the evolutionary history of this remarkable germline/soma differentiation. Our results strengthen the notion that a complex, dynamic, and ongoing interplay between mobile DNA elements and the host genome have shaped Tetrahymena chromosome structure, locally and globally. Non-standard outcomes of rearrangement events, including the generation of short-lived somatic chromosomes and excision of DNA interrupting protein-coding regions, may represent novel forms of developmental gene regulation. We also compare Tetrahymena's germline/soma differentiation to that of other characterized ciliates, illustrating the wide diversity of adaptations that have occurred within this phylum.

Entities:  

Keywords:  Tetrahymena thermophila; centromere; chromosome breakage; chromosomes; evolutionary biology; genes; genome rearrangement; genomics; intermal eliminated sequence; transposable element

Mesh:

Year:  2016        PMID: 27892853      PMCID: PMC5182062          DOI: 10.7554/eLife.19090

Source DB:  PubMed          Journal:  Elife        ISSN: 2050-084X            Impact factor:   8.140


  147 in total

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Authors:  Harmit S Malik; Steven Henikoff
Journal:  Curr Opin Genet Dev       Date:  2002-12       Impact factor: 5.578

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Journal:  Dev Genet       Date:  1992

3.  Identification and characterization of piggyBac-like elements in the genome of domesticated silkworm, Bombyx mori.

Authors:  Han-Fu Xu; Qing-You Xia; Chun Liu; Ting-Cai Cheng; Ping Zhao; Jun Duan; Xing-Fu Zha; Shi-Ping Liu
Journal:  Mol Genet Genomics       Date:  2006-05-10       Impact factor: 3.291

4.  Genetic consequences of programmed genome rearrangement.

Authors:  Jeramiah J Smith; Carl Baker; Evan E Eichler; Chris T Amemiya
Journal:  Curr Biol       Date:  2012-07-19       Impact factor: 10.834

5.  Strong sequence conservation of a 38 bp region near the center of the extrachromosomal rDNA palindrome in different Tetrahymena species.

Authors:  J Engberg
Journal:  Nucleic Acids Res       Date:  1983-07-25       Impact factor: 16.971

6.  Flanking regulatory sequences of the Tetrahymena R deletion element determine the boundaries of DNA rearrangement.

Authors:  D L Chalker; A La Terza; A Wilson; C D Kroenke; M C Yao
Journal:  Mol Cell Biol       Date:  1999-08       Impact factor: 4.272

7.  Macronuclear genetics of Tetrahymena. I. Random distribution of macronuclear genecopies in T. pyriformis, syngen 1.

Authors:  E Orias; M Flacks
Journal:  Genetics       Date:  1975-02       Impact factor: 4.562

8.  The architecture of a scrambled genome reveals massive levels of genomic rearrangement during development.

Authors:  Xiao Chen; John R Bracht; Aaron David Goldman; Egor Dolzhenko; Derek M Clay; Estienne C Swart; David H Perlman; Thomas G Doak; Andrew Stuart; Chris T Amemiya; Robert P Sebra; Laura F Landweber
Journal:  Cell       Date:  2014-08-28       Impact factor: 41.582

9.  Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote.

Authors:  Jonathan A Eisen; Robert S Coyne; Martin Wu; Dongying Wu; Mathangi Thiagarajan; Jennifer R Wortman; Jonathan H Badger; Qinghu Ren; Paolo Amedeo; Kristie M Jones; Luke J Tallon; Arthur L Delcher; Steven L Salzberg; Joana C Silva; Brian J Haas; William H Majoros; Maryam Farzad; Jane M Carlton; Roger K Smith; Jyoti Garg; Ronald E Pearlman; Kathleen M Karrer; Lei Sun; Gerard Manning; Nels C Elde; Aaron P Turkewitz; David J Asai; David E Wilkes; Yufeng Wang; Hong Cai; Kathleen Collins; B Andrew Stewart; Suzanne R Lee; Katarzyna Wilamowska; Zasha Weinberg; Walter L Ruzzo; Dorota Wloga; Jacek Gaertig; Joseph Frankel; Che-Chia Tsao; Martin A Gorovsky; Patrick J Keeling; Ross F Waller; Nicola J Patron; J Michael Cherry; Nicholas A Stover; Cynthia J Krieger; Christina del Toro; Hilary F Ryder; Sondra C Williamson; Rebecca A Barbeau; Eileen P Hamilton; Eduardo Orias
Journal:  PLoS Biol       Date:  2006-09       Impact factor: 8.029

10.  The Paramecium germline genome provides a niche for intragenic parasitic DNA: evolutionary dynamics of internal eliminated sequences.

Authors:  Olivier Arnaiz; Nathalie Mathy; Céline Baudry; Sophie Malinsky; Jean-Marc Aury; Cyril Denby Wilkes; Olivier Garnier; Karine Labadie; Benjamin E Lauderdale; Anne Le Mouël; Antoine Marmignon; Mariusz Nowacki; Julie Poulain; Malgorzata Prajer; Patrick Wincker; Eric Meyer; Sandra Duharcourt; Laurent Duret; Mireille Bétermier; Linda Sperling
Journal:  PLoS Genet       Date:  2012-10-04       Impact factor: 5.917

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2.  Diversification of small RNA amplification mechanisms for targeting transposon-related sequences in ciliates.

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5.  Genome analyses of the new model protist Euplotes vannus focusing on genome rearrangement and resistance to environmental stressors.

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Review 6.  Insights into transgenerational epigenetics from studies of ciliates.

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7.  The Hippo Pathway Maintains the Equatorial Division Plane in the Ciliate Tetrahymena.

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Journal:  Genetics       Date:  2017-04-16       Impact factor: 4.562

8.  Setting boundaries for genome-wide heterochromatic DNA deletions through flanking inverted repeats in Tetrahymena thermophila.

Authors:  Chih-Yi Gabriela Lin; Ju-Lan Chao; Huai-Kuang Tsai; Douglas Chalker; Meng-Chao Yao
Journal:  Nucleic Acids Res       Date:  2019-06-04       Impact factor: 16.971

9.  Two Antagonistic Hippo Signaling Circuits Set the Division Plane at the Medial Position in the Ciliate Tetrahymena.

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Journal:  Genetics       Date:  2018-12-28       Impact factor: 4.562

10.  Comprehensive Chromosome End Remodeling during Programmed DNA Elimination.

Authors:  Jianbin Wang; Giovana M B Veronezi; Yuanyuan Kang; Maxim Zagoskin; Eileen T O'Toole; Richard E Davis
Journal:  Curr Biol       Date:  2020-07-16       Impact factor: 10.834

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