Intergenic ORFs As Elementary Structural Modules of De Novo Gene Birth and Protein Evolution

Overview

Journal Genome Res

Specialty Genetics

Date 2021 Nov 23

PMID 34810219

Citations 17

Authors

Chris Papadopoulos

Isabelle Callebaut

Jean-Christophe Gelly

Isabelle Hatin

Olivier Namy

Maxime Renard

Olivier Lespinet

Anne Lopes

Affiliations

Soon will be listed here.

Abstract

The noncoding genome plays an important role in de novo gene birth and in the emergence of genetic novelty. Nevertheless, how noncoding sequences' properties could promote the birth of novel genes and shape the evolution and the structural diversity of proteins remains unclear. Therefore, by combining different bioinformatic approaches, we characterized the fold potential diversity of the amino acid sequences encoded by all intergenic open reading frames (ORFs) of with the aim of (1) exploring whether the structural states' diversity of proteomes is already present in noncoding sequences, and (2) estimating the potential of the noncoding genome to produce novel protein bricks that could either give rise to novel genes or be integrated into pre-existing proteins, thus participating in protein structure diversity and evolution. We showed that amino acid sequences encoded by most yeast intergenic ORFs contain the elementary building blocks of protein structures. Moreover, they encompass the large structural state diversity of canonical proteins, with the majority predicted as foldable. Then, we investigated the early stages of de novo gene birth by reconstructing the ancestral sequences of 70 yeast de novo genes and characterized the sequence and structural properties of intergenic ORFs with a strong translation signal. This enabled us to highlight sequence and structural factors determining de novo gene emergence. Finally, we showed a strong correlation between the fold potential of de novo proteins and one of their ancestral amino acid sequences, reflecting the relationship between the noncoding genome and the protein structure universe.

Citing Articles

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References

Schavemaker P, Smigiel W, Poolman B . Ribosome surface properties may impose limits on the nature of the cytoplasmic proteome. Elife. 2017; 6. PMC: 5726854. DOI: 10.7554/eLife.30084. View

Wilson B, Foy S, Neme R, Masel J . Young Genes are Highly Disordered as Predicted by the Preadaptation Hypothesis of Gene Birth. Nat Ecol Evol. 2017; 1(6):0146-146. PMC: 5476217. DOI: 10.1038/s41559-017-0146. View

Berezovsky I . Towards descriptor of elementary functions for protein design. Curr Opin Struct Biol. 2019; 58:159-165. DOI: 10.1016/j.sbi.2019.06.010. View

Hocker B . Design of proteins from smaller fragments-learning from evolution. Curr Opin Struct Biol. 2014; 27:56-62. DOI: 10.1016/j.sbi.2014.04.007. View

Radhakrishnan A, Chen Y, Martin S, Alhusaini N, Green R, Coller J . The DEAD-Box Protein Dhh1p Couples mRNA Decay and Translation by Monitoring Codon Optimality. Cell. 2016; 167(1):122-132.e9. PMC: 5635654. DOI: 10.1016/j.cell.2016.08.053. View

Langenberg T, Gallardo R, van der Kant R, Louros N, Michiels E, Duran-Romana R . Thermodynamic and Evolutionary Coupling between the Native and Amyloid State of Globular Proteins. Cell Rep. 2020; 31(2):107512. PMC: 7175379. DOI: 10.1016/j.celrep.2020.03.076. View

Wu D, Irwin D, Zhang Y . De novo origin of human protein-coding genes. PLoS Genet. 2011; 7(11):e1002379. PMC: 3213175. DOI: 10.1371/journal.pgen.1002379. View

Ganesan A, Siekierska A, Beerten J, Brams M, Van Durme J, De Baets G . Structural hot spots for the solubility of globular proteins. Nat Commun. 2016; 7:10816. PMC: 4770091. DOI: 10.1038/ncomms10816. View

Papaleo E, Saladino G, Lambrughi M, Lindorff-Larsen K, Gervasio F, Nussinov R . The Role of Protein Loops and Linkers in Conformational Dynamics and Allostery. Chem Rev. 2016; 116(11):6391-423. DOI: 10.1021/acs.chemrev.5b00623. View

10.

Meszaros B, Erdos G, Dosztanyi Z . IUPred2A: context-dependent prediction of protein disorder as a function of redox state and protein binding. Nucleic Acids Res. 2018; 46(W1):W329-W337. PMC: 6030935. DOI: 10.1093/nar/gky384. View

11.

Namy O, Duchateau-Nguyen G, Hatin I, Denmat S, Termier M, Rousset J . Identification of stop codon readthrough genes in Saccharomyces cerevisiae. Nucleic Acids Res. 2003; 31(9):2289-96. PMC: 154216. DOI: 10.1093/nar/gkg330. View

12.

Bornberg-Bauer E, Alba M . Dynamics and adaptive benefits of modular protein evolution. Curr Opin Struct Biol. 2013; 23(3):459-66. DOI: 10.1016/j.sbi.2013.02.012. View

13.

Faure G, Callebaut I . Comprehensive repertoire of foldable regions within whole genomes. PLoS Comput Biol. 2013; 9(10):e1003280. PMC: 3812050. DOI: 10.1371/journal.pcbi.1003280. View

14.

Wolf Y, Novichkov P, P Karev G, Koonin E, Lipman D . The universal distribution of evolutionary rates of genes and distinct characteristics of eukaryotic genes of different apparent ages. Proc Natl Acad Sci U S A. 2009; 106(18):7273-80. PMC: 2666616. DOI: 10.1073/pnas.0901808106. View

15.

Postic G, Ghouzam Y, Chebrek R, Gelly J . An ambiguity principle for assigning protein structural domains. Sci Adv. 2017; 3(1):e1600552. PMC: 5235333. DOI: 10.1126/sciadv.1600552. View

16.

Langmead B, Trapnell C, Pop M, Salzberg S . Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009; 10(3):R25. PMC: 2690996. DOI: 10.1186/gb-2009-10-3-r25. View

17.

Zhang L, Ren Y, Yang T, Li G, Chen J, Gschwend A . Rapid evolution of protein diversity by de novo origination in Oryza. Nat Ecol Evol. 2019; 3(4):679-690. DOI: 10.1038/s41559-019-0822-5. View

18.

Lumb K, Kim P . A buried polar interaction imparts structural uniqueness in a designed heterodimeric coiled coil. Biochemistry. 1995; 34(27):8642-8. DOI: 10.1021/bi00027a013. View

19.

Bartonek L, Braun D, Zagrovic B . Frameshifting preserves key physicochemical properties of proteins. Proc Natl Acad Sci U S A. 2020; 117(11):5907-5912. PMC: 7084103. DOI: 10.1073/pnas.1911203117. View

20.

Knowles D, McLysaght A . Recent de novo origin of human protein-coding genes. Genome Res. 2009; 19(10):1752-9. PMC: 2765279. DOI: 10.1101/gr.095026.109. View