Ordered Structure of the Transcription Network Inherited from the Yeast Whole-genome Duplication

Overview

Journal BMC Syst Biol

Publisher Biomed Central

Specialty Biology

Date 2010 Jun 8

PMID 20525287

Citations 7

Authors

Diana Fusco

Luigi Grassi

Bruno Bassetti

Michele Caselle

Marco Cosentino Lagomarsino

Affiliations

Soon will be listed here.

Abstract

Background: Gene duplication, a major evolutionary path to genomic innovation, can occur at the scale of an entire genome. One such "whole-genome duplication" (WGD) event among the Ascomycota fungi gave rise to genes with distinct biological properties compared to small-scale duplications.

Results: We studied the evolution of transcriptional interactions of whole-genome duplicates, to understand how they are wired into the yeast regulatory system. Our work combines network analysis and modeling of the large-scale structure of the interactions stemming from the WGD.

Conclusions: The results uncover the WGD as a major source for the evolution of a complex interconnected block of transcriptional pathways. The inheritance of interactions among WGD duplicates follows elementary "duplication subgraphs", relating ancestral interactions with newly formed ones. Duplication subgraphs are correlated with their neighbours and give rise to higher order circuits with two elementary properties: newly formed transcriptional pathways remain connected (paths are not broken), and are preferentially cross-connected with ancestral ones. The result is a coherent and connected "WGD-network", where duplication subgraphs are arranged in an astonishingly ordered configuration.

Citing Articles

The genetic consequences of range expansion and its influence on diploidization in polyploids.

Booker W, Schrider D bioRxiv. 2023; .

PMID: 37905020 PMC: 10614938. DOI: 10.1101/2023.10.18.562992.

The impact of whole genome duplications on the human gene regulatory networks.

Mottes F, Villa C, Osella M, Caselle M PLoS Comput Biol. 2021; 17(12):e1009638.

PMID: 34871317 PMC: 8675932. DOI: 10.1371/journal.pcbi.1009638.

Using digital organisms to study the evolutionary consequences of whole genome duplication and polyploidy.

Yao Y, Carretero-Paulet L, Van de Peer Y PLoS One. 2019; 14(7):e0220257.

PMID: 31365541 PMC: 6668904. DOI: 10.1371/journal.pone.0220257.

Living Organisms Author Their Read-Write Genomes in Evolution.

Shapiro J Biology (Basel). 2017; 6(4).

PMID: 29211049 PMC: 5745447. DOI: 10.3390/biology6040042.

Polyploidy and the evolution of complex traits.

Huminiecki L, Conant G Int J Evol Biol. 2012; 2012:292068.

PMID: 22900230 PMC: 3413983. DOI: 10.1155/2012/292068.

References

Byrne K, Wolfe K . The Yeast Gene Order Browser: combining curated homology and syntenic context reveals gene fate in polyploid species. Genome Res. 2005; 15(10):1456-61. PMC: 1240090. DOI: 10.1101/gr.3672305. View

Guan Y, Dunham M, Troyanskaya O . Functional analysis of gene duplications in Saccharomyces cerevisiae. Genetics. 2006; 175(2):933-43. PMC: 1800624. DOI: 10.1534/genetics.106.064329. View

Otto S . The evolutionary consequences of polyploidy. Cell. 2007; 131(3):452-62. DOI: 10.1016/j.cell.2007.10.022. View

Dietrich F, Voegeli S, Brachat S, Lerch A, Gates K, Steiner S . The Ashbya gossypii genome as a tool for mapping the ancient Saccharomyces cerevisiae genome. Science. 2004; 304(5668):304-7. DOI: 10.1126/science.1095781. View

Maslov S, Sneppen K, Eriksen K, Yan K . Upstream plasticity and downstream robustness in evolution of molecular networks. BMC Evol Biol. 2004; 4:9. PMC: 385226. DOI: 10.1186/1471-2148-4-9. View

Aury J, Jaillon O, Duret L, Noel B, Jubin C, Porcel B . Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia. Nature. 2006; 444(7116):171-8. DOI: 10.1038/nature05230. View

Conant G, Wolfe K . Turning a hobby into a job: how duplicated genes find new functions. Nat Rev Genet. 2008; 9(12):938-50. DOI: 10.1038/nrg2482. View

Wolfe K, Shields D . Molecular evidence for an ancient duplication of the entire yeast genome. Nature. 1997; 387(6634):708-13. DOI: 10.1038/42711. View

Teichmann S, Babu M . Gene regulatory network growth by duplication. Nat Genet. 2004; 36(5):492-6. DOI: 10.1038/ng1340. View

10.

McLysaght A, Hokamp K, Wolfe K . Extensive genomic duplication during early chordate evolution. Nat Genet. 2002; 31(2):200-4. DOI: 10.1038/ng884. View

11.

Torres E, Sokolsky T, Tucker C, Chan L, Boselli M, Dunham M . Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science. 2007; 317(5840):916-24. DOI: 10.1126/science.1142210. View

12.

Balaji S, Babu M, Iyer L, Luscombe N, Aravind L . Comprehensive analysis of combinatorial regulation using the transcriptional regulatory network of yeast. J Mol Biol. 2006; 360(1):213-27. DOI: 10.1016/j.jmb.2006.04.029. View

13.

Sellerio A, Bassetti B, Isambert H, Cosentino Lagomarsino M . A comparative evolutionary study of transcription networks. The global role of feedback and hierachical structures. Mol Biosyst. 2009; 5(2):170-9. DOI: 10.1039/b815339f. View

14.

Maslov S, Krishna S, Pang T, Sneppen K . Toolbox model of evolution of prokaryotic metabolic networks and their regulation. Proc Natl Acad Sci U S A. 2009; 106(24):9743-8. PMC: 2701025. DOI: 10.1073/pnas.0903206106. View

15.

Kellis M, Birren B, Lander E . Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature. 2004; 428(6983):617-24. DOI: 10.1038/nature02424. View

16.

Evlampiev K, Isambert H . Conservation and topology of protein interaction networks under duplication-divergence evolution. Proc Natl Acad Sci U S A. 2008; 105(29):9863-8. PMC: 2481380. DOI: 10.1073/pnas.0804119105. View

17.

Dujon B, Sherman D, Fischer G, Durrens P, Casaregola S, Lafontaine I . Genome evolution in yeasts. Nature. 2004; 430(6995):35-44. DOI: 10.1038/nature02579. View

18.

Koszul R, Fischer G . A prominent role for segmental duplications in modeling eukaryotic genomes. C R Biol. 2009; 332(2-3):254-66. DOI: 10.1016/j.crvi.2008.07.005. View

19.

Jeong J, Berman P . On cycles in the transcription network of Saccharomyces cerevisiae. BMC Syst Biol. 2008; 2:12. PMC: 2275720. DOI: 10.1186/1752-0509-2-12. View

20.

Babu M, Luscombe N, Aravind L, Gerstein M, Teichmann S . Structure and evolution of transcriptional regulatory networks. Curr Opin Struct Biol. 2004; 14(3):283-91. DOI: 10.1016/j.sbi.2004.05.004. View