Differential Effects of Chromatin and Gcn4 on the 50-fold Range of Expression Among Individual Yeast Ty1 Retrotransposons

Overview

Journal Mol Cell Biol

Specialty Cell Biology

Date 2002 Mar 9

PMID 11884596

Citations 44

Authors

Antonin Morillon

Lionel Benard

Mathias Springer

Pascale Lesage

Affiliations

Soon will be listed here.

Abstract

Approximately 30 copies of the Ty1 retrotransposon are present in the genome of Saccharomyces cerevisiae. Previous studies gave insights into the global regulation of Ty1 transcription but provided no information on the behavior of individual genomic elements. This work shows that the expression of 31 individual Ty1 elements in S288C varies over a 50-fold range. Their transcription is repressed by chromatin structures, which are antagonized by the Swi/Snf and SAGA chromatin-modifying complexes in highly expressed Ty1 elements. These elements carry five potential Gcn4 binding sites in their promoter regions that are mostly absent in weakly expressed Ty1 copies. Consistent with this observation, Gcn4 activates the transcription of highly expressed Ty1 elements only. One of the potential Gcn4 binding sites acts as an upstream activating sequence in vivo and interacts with Gcn4 in vitro. Since Gcn4 has been shown to interact with Swi/Snf and SAGA, we predict that Gcn4 activates Ty1 transcription by targeting these complexes to specific Ty1 promoters.

Citing Articles

Template switching during DNA replication is a prevalent source of adaptive gene amplification.

Chuong J, Ben Nun N, Suresh I, Matthews J, De T, Avecilla G Elife. 2025; 13.

PMID: 39899365 PMC: 11790251. DOI: 10.7554/eLife.98934.

Template switching during DNA replication is a prevalent source of adaptive gene amplification.

Chuong J, Ben Nun N, Suresh I, Matthews J, De T, Avecilla G bioRxiv. 2024; .

PMID: 39464144 PMC: 11507740. DOI: 10.1101/2024.05.03.589936.

The Ty1 retrotransposon harbors a DNA region that performs dual functions as both a gene silencing and chromatin insulator.

Masumoto H, Muto H, Yano K, Kurosaki Y, Niki H Sci Rep. 2024; 14(1):16641.

PMID: 39025990 PMC: 11258251. DOI: 10.1038/s41598-024-67242-z.

Species-Specific Transcription Factors Associated with Long Terminal Repeat Promoters of Endogenous Retroviruses: A Comprehensive Review.

Hossain M, Nyame P, Monde K Biomolecules. 2024; 14(3).

PMID: 38540701 PMC: 10968565. DOI: 10.3390/biom14030280.

Evolution of a Restriction Factor by Domestication of a Yeast Retrotransposon.

Hannon-Hatfield J, Chen J, Bergman C, Garfinkel D Mol Biol Evol. 2024; 41(3).

PMID: 38442736 PMC: 10951436. DOI: 10.1093/molbev/msae050.

References

Gray W, Fassler J . Role of Saccharomyces cerevisiae Rap1 protein in Ty1 and Ty1-mediated transcription. Gene Expr. 1993; 3(3):237-51. PMC: 6081617. View

FULTON A, Rathjen P, Kingsman S, Kingsman A . Upstream and downstream transcriptional control signals in the yeast retrotransposon, TY. Nucleic Acids Res. 1988; 16(12):5439-58. PMC: 336777. DOI: 10.1093/nar/16.12.5439. View

Maftahi M, Gaillardin C, Nicaud J . Sticky-end polymerase chain reaction method for systematic gene disruption in Saccharomyces cerevisiae. Yeast. 1996; 12(9):859-68. DOI: 10.1002/(SICI)1097-0061(199607)12:9%3C859::AID-YEA978%3E3.0.CO;2-Q. View

Smith J, Boeke J . An unusual form of transcriptional silencing in yeast ribosomal DNA. Genes Dev. 1997; 11(2):241-54. DOI: 10.1101/gad.11.2.241. View

Bryk M, Banerjee M, Murphy M, Knudsen K, Garfinkel D, Curcio M . Transcriptional silencing of Ty1 elements in the RDN1 locus of yeast. Genes Dev. 1997; 11(2):255-69. DOI: 10.1101/gad.11.2.255. View

Grant P, Duggan L, Cote J, Roberts S, Brownell J, Candau R . Yeast Gcn5 functions in two multisubunit complexes to acetylate nucleosomal histones: characterization of an Ada complex and the SAGA (Spt/Ada) complex. Genes Dev. 1997; 11(13):1640-50. DOI: 10.1101/gad.11.13.1640. View

Baur M, Esch R, Errede B . Cooperative binding interactions required for function of the Ty1 sterile responsive element. Mol Cell Biol. 1997; 17(8):4330-7. PMC: 232286. DOI: 10.1128/MCB.17.8.4330. View

TURKEL S, Liao X, Farabaugh P . GCR1-dependent transcriptional activation of yeast retrotransposon Ty2-917. Yeast. 1997; 13(10):917-30. DOI: 10.1002/(SICI)1097-0061(199708)13:10<917::AID-YEA148>3.0.CO;2-G. View

Chambers S, Prior S, Barstow D, Minton N . The pMTL nic- cloning vectors. I. Improved pUC polylinker regions to facilitate the use of sonicated DNA for nucleotide sequencing. Gene. 1988; 68(1):139-49. DOI: 10.1016/0378-1119(88)90606-3. View

10.

Moye-Rowley W, Harshman K, Parker C . Yeast YAP1 encodes a novel form of the jun family of transcriptional activator proteins. Genes Dev. 1989; 3(3):283-92. DOI: 10.1101/gad.3.3.283. View

11.

Sikorski R, Hieter P . A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989; 122(1):19-27. PMC: 1203683. DOI: 10.1093/genetics/122.1.19. View

12.

Fink G, Arndt K . BAS1 has a Myb motif and activates HIS4 transcription only in combination with BAS2. Science. 1989; 246(4932):931-5. DOI: 10.1126/science.2683089. View

13.

Curcio M, Hedge A, Boeke J, Garfinkel D . Ty RNA levels determine the spectrum of retrotransposition events that activate gene expression in Saccharomyces cerevisiae. Mol Gen Genet. 1990; 220(2):213-21. DOI: 10.1007/BF00260484. View

14.

Laloux I, Dubois E, Dewerchin M, Jacobs E . TEC1, a gene involved in the activation of Ty1 and Ty1-mediated gene expression in Saccharomyces cerevisiae: cloning and molecular analysis. Mol Cell Biol. 1990; 10(7):3541-50. PMC: 360789. DOI: 10.1128/mcb.10.7.3541-3550.1990. View

15.

Curcio M, Garfinkel D . Single-step selection for Ty1 element retrotransposition. Proc Natl Acad Sci U S A. 1991; 88(3):936-40. PMC: 50929. DOI: 10.1073/pnas.88.3.936. View

16.

Happel A, Swanson M, Winston F . The SNF2, SNF5 and SNF6 genes are required for Ty transcription in Saccharomyces cerevisiae. Genetics. 1991; 128(1):69-77. PMC: 1204454. DOI: 10.1093/genetics/128.1.69. View

17.

Ciriacy M, Freidel K, Lohning C . Characterization of trans-acting mutations affecting Ty and Ty-mediated transcription in Saccharomyces cerevisiae. Curr Genet. 1991; 20(6):441-8. DOI: 10.1007/BF00334769. View

18.

Winston F, Carlson M . Yeast SNF/SWI transcriptional activators and the SPT/SIN chromatin connection. Trends Genet. 1992; 8(11):387-91. DOI: 10.1016/0168-9525(92)90300-s. View

19.

Hirschhorn J, Brown S, Clark C, Winston F . Evidence that SNF2/SWI2 and SNF5 activate transcription in yeast by altering chromatin structure. Genes Dev. 1992; 6(12A):2288-98. DOI: 10.1101/gad.6.12a.2288. View

20.

Errede B . MCM1 binds to a transcriptional control element in Ty1. Mol Cell Biol. 1993; 13(1):57-62. PMC: 358884. DOI: 10.1128/mcb.13.1.57-62.1993. View