A Germline-limited PiggyBac Transposase Gene is Required for Precise Excision in Tetrahymena Genome Rearrangement

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2017 Sep 22

PMID 28934495

Citations 27

Authors

Lifang Feng

Guangying Wang

Eileen P Hamilton

Jie Xiong

Guanxiong Yan

Kai Chen

Xiao Chen

Wen Dui

Amber Plemens

Lara Khadr

Arjune Dhanekula

Mina Juma

Hung Quang Dang

Geoffrey M Kapler

Eduardo Orias

Wei Miao

Yifan Liu

Affiliations

Soon will be listed here.

Abstract

Developmentally programmed genome rearrangement accompanies differentiation of the silent germline micronucleus into the transcriptionally active somatic macronucleus in the ciliated protozoan Tetrahymena thermophila. Internal eliminated sequences (IES) are excised, followed by rejoining of MAC-destined sequences, while fragmentation occurs at conserved chromosome breakage sequences, generating macronuclear chromosomes. Some macronuclear chromosomes, referred to as non-maintained chromosomes (NMC), are lost soon after differentiation. Large NMC contain genes implicated in development-specific roles. One such gene encodes the domesticated piggyBac transposase TPB6, required for heterochromatin-dependent precise excision of IES residing within exons of functionally important genes. These conserved exonic IES determine alternative transcription products in the developing macronucleus; some even contain free-standing genes. Examples of precise loss of some exonic IES in the micronucleus and retention of others in the macronucleus of related species suggest an evolutionary analogy to introns. Our results reveal that germline-limited sequences can encode genes with specific expression patterns and development-related functions, which may be a recurring theme in eukaryotic organisms experiencing programmed genome rearrangement during germline to soma differentiation.

Citing Articles

Comprehensive genome annotation of the model ciliate Tetrahymena thermophila by in-depth epigenetic and transcriptomic profiling.

Ye F, Chen X, Li Y, Ju A, Sheng Y, Duan L Nucleic Acids Res. 2024; 53(2.

PMID: 39657783 PMC: 11754650. DOI: 10.1093/nar/gkae1177.

Programmed chromosome fragmentation in ciliated protozoa: multiple means to chromosome ends.

Betermier M, Klobutcher L, Orias E Microbiol Mol Biol Rev. 2023; 87(4):e0018422.

PMID: 38009915 PMC: 10732028. DOI: 10.1128/mmbr.00184-22.

Developmentally Programmed Switches in DNA Replication: Gene Amplification and Genome-Wide Endoreplication in .

Meng X, Dang H, Kapler G Microorganisms. 2023; 11(2).

PMID: 36838456 PMC: 9967165. DOI: 10.3390/microorganisms11020491.

MITE infestation accommodated by genome editing in the germline genome of the ciliate .

Seah B, Singh M, Emmerich C, Singh A, Woehle C, Huettel B Proc Natl Acad Sci U S A. 2023; 120(4):e2213985120.

PMID: 36669106 PMC: 9942856. DOI: 10.1073/pnas.2213985120.

Origins of genome-editing excisases as illuminated by the somatic genome of the ciliate .

Singh M, Seah B, Emmerich C, Singh A, Woehle C, Huettel B Proc Natl Acad Sci U S A. 2023; 120(4):e2213887120.

PMID: 36669098 PMC: 9942806. DOI: 10.1073/pnas.2213887120.

References

Smith J, Baker C, Eichler E, Amemiya C . Genetic consequences of programmed genome rearrangement. Curr Biol. 2012; 22(16):1524-9. PMC: 3427415. DOI: 10.1016/j.cub.2012.06.028. View

Stover N, Punia R, Bowen M, Dolins S, Clark T . Tetrahymena Genome Database Wiki: a community-maintained model organism database. Database (Oxford). 2012; 2012:bas007. PMC: 3308163. DOI: 10.1093/database/bas007. View

Arnaiz O, Mathy N, Baudry C, Malinsky S, Aury J, Denby Wilkes C . The Paramecium germline genome provides a niche for intragenic parasitic DNA: evolutionary dynamics of internal eliminated sequences. PLoS Genet. 2012; 8(10):e1002984. PMC: 3464196. DOI: 10.1371/journal.pgen.1002984. View

Cheng C, Young J, Lin C, Chao J, Malik H, Yao M . The piggyBac transposon-derived genes TPB1 and TPB6 mediate essential transposon-like excision during the developmental rearrangement of key genes in Tetrahymena thermophila. Genes Dev. 2017; 30(24):2724-2736. PMC: 5238731. DOI: 10.1101/gad.290460.116. View

Eisen J, Coyne R, Wu M, Wu D, Thiagarajan M, Wortman J . Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biol. 2006; 4(9):e286. PMC: 1557398. DOI: 10.1371/journal.pbio.0040286. View

Mochizuki K, Fine N, Fujisawa T, Gorovsky M . Analysis of a piwi-related gene implicates small RNAs in genome rearrangement in tetrahymena. Cell. 2002; 110(6):689-99. DOI: 10.1016/s0092-8674(02)00909-1. View

Orias E, Flacks M . Macronuclear genetics of Tetrahymena. I. Random distribution of macronuclear genecopies in T. pyriformis, syngen 1. Genetics. 1975; 79(2):187-206. PMC: 1213266. DOI: 10.1093/genetics/79.2.187. View

Bryant S, Herdy J, Amemiya C, Smith J . Characterization of Somatically-Eliminated Genes During Development of the Sea Lamprey (Petromyzon marinus). Mol Biol Evol. 2016; 33(9):2337-44. PMC: 4989109. DOI: 10.1093/molbev/msw104. View

Chen X, Bracht J, Goldman A, Dolzhenko E, Clay D, Swart E . The architecture of a scrambled genome reveals massive levels of genomic rearrangement during development. Cell. 2014; 158(5):1187-1198. PMC: 4199391. DOI: 10.1016/j.cell.2014.07.034. View

10.

Smith J, Antonacci F, Eichler E, Amemiya C . Programmed loss of millions of base pairs from a vertebrate genome. Proc Natl Acad Sci U S A. 2009; 106(27):11212-7. PMC: 2708698. DOI: 10.1073/pnas.0902358106. View

11.

Liao Y, Smyth G, Shi W . The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote. Nucleic Acids Res. 2013; 41(10):e108. PMC: 3664803. DOI: 10.1093/nar/gkt214. View

12.

Stargell L, Gorovsky M . TATA-binding protein and nuclear differentiation in Tetrahymena thermophila. Mol Cell Biol. 1994; 14(1):723-34. PMC: 358421. DOI: 10.1128/mcb.14.1.723-734.1994. View

13.

Langmead B, Salzberg S . Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012; 9(4):357-9. PMC: 3322381. DOI: 10.1038/nmeth.1923. View

14.

Iwamoto M, Mori C, Kojidani T, Bunai F, Hori T, Fukagawa T . Two distinct repeat sequences of Nup98 nucleoporins characterize dual nuclei in the binucleated ciliate tetrahymena. Curr Biol. 2009; 19(10):843-7. DOI: 10.1016/j.cub.2009.03.055. View

15.

Nowacki M, Higgins B, Maquilan G, Swart E, Doak T, Landweber L . A functional role for transposases in a large eukaryotic genome. Science. 2009; 324(5929):935-8. PMC: 3491810. DOI: 10.1126/science.1170023. View

16.

Mitra R, Fain-Thornton J, Craig N . piggyBac can bypass DNA synthesis during cut and paste transposition. EMBO J. 2008; 27(7):1097-109. PMC: 2323262. DOI: 10.1038/emboj.2008.41. View

17.

Stein L . Using GBrowse 2.0 to visualize and share next-generation sequence data. Brief Bioinform. 2013; 14(2):162-71. PMC: 3603216. DOI: 10.1093/bib/bbt001. View

18.

Nikiforov M, Smothers J, Gorovsky M, Allis C . Excision of micronuclear-specific DNA requires parental expression of pdd2p and occurs independently from DNA replication in Tetrahymena thermophila. Genes Dev. 1999; 13(21):2852-62. PMC: 317139. DOI: 10.1101/gad.13.21.2852. View

19.

Yao M, Yao C, Monks B . The controlling sequence for site-specific chromosome breakage in Tetrahymena. Cell. 1990; 63(4):763-72. DOI: 10.1016/0092-8674(90)90142-2. View

20.

Allis C, Dennison D . Identification and purification of young macronuclear anlagen from conjugating cells of Tetrahymena thermophila. Dev Biol. 1982; 93(2):519-33. DOI: 10.1016/0012-1606(82)90139-7. View