Volatile evolution of long noncoding RNA repertoires: mechanisms and biological implications

•lncRNAs show weak selective constraint, even when clearly functional.•Gain and loss of lncRNA genes occurs at very high pace during evolution.•lncRNAs mostly evolve de novo.•Bidirectional promoters and transposable elements (TEs) promote the birth of lncRNAs.•Genomes rich in TEs may have more compl...

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Bibliographic Details
Published inTrends in genetics Vol. 30; no. 10; pp. 439 - 452
Main Authors Kapusta, Aurélie, Feschotte, Cédric
Format Journal Article
LanguageEnglish
Published England Elsevier Ltd 01.10.2014
Subjects
Animals
DNA Transposable Elements
Evolution, Molecular
Exons
Humans
Medical Education
Nucleic Acid Conformation
RNA, Long Noncoding - chemistry
RNA, Long Noncoding - metabolism
Transcription, Genetic
Online AccessGet full text

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Abstract •lncRNAs show weak selective constraint, even when clearly functional.•Gain and loss of lncRNA genes occurs at very high pace during evolution.•lncRNAs mostly evolve de novo.•Bidirectional promoters and transposable elements (TEs) promote the birth of lncRNAs.•Genomes rich in TEs may have more complex and malleable transcriptomes. Thousands of genes encoding long noncoding RNAs (lncRNAs) have been identified in all vertebrate genomes thus far examined. The list of lncRNAs partaking in arguably important biochemical, cellular, and developmental activities is steadily growing. However, it is increasingly clear that lncRNA repertoires are subject to weak functional constraint and rapid turnover during vertebrate evolution. We discuss here some of the factors that may explain this apparent paradox, including relaxed constraint on sequence to maintain lncRNA structure/function, extensive redundancy in the regulatory circuits in which lncRNAs act, as well as adaptive and non-adaptive forces such as genetic drift. We explore the molecular mechanisms promoting the birth and rapid evolution of lncRNA genes, with an emphasis on the influence of bidirectional transcription and transposable elements, two pervasive features of vertebrate genomes. Together these properties reveal a remarkably dynamic and malleable noncoding transcriptome which may represent an important source of robustness and evolvability.
AbstractList Thousands of genes encoding long noncoding RNAs (lncRNAs) have been identified in all vertebrate genomes thus far examined. The list of lncRNAs partaking in arguably important biochemical, cellular, and developmental activities is steadily growing. However, it is increasingly clear that lncRNA repertoires are subject to weak functional constraint and rapid turnover during vertebrate evolution. We discuss here some of the factors that may explain this apparent paradox, including relaxed constraint on sequence to maintain lncRNA structure/function, extensive redundancy in the regulatory circuits in which lncRNAs act, as well as adaptive and non-adaptive forces such as genetic drift. We explore the molecular mechanisms promoting the birth and rapid evolution of lncRNA genes, with an emphasis on the influence of bidirectional transcription and transposable elements, two pervasive features of vertebrate genomes. Together these properties reveal a remarkably dynamic and malleable noncoding transcriptome which may represent an important source of robustness and evolvability.Thousands of genes encoding long noncoding RNAs (lncRNAs) have been identified in all vertebrate genomes thus far examined. The list of lncRNAs partaking in arguably important biochemical, cellular, and developmental activities is steadily growing. However, it is increasingly clear that lncRNA repertoires are subject to weak functional constraint and rapid turnover during vertebrate evolution. We discuss here some of the factors that may explain this apparent paradox, including relaxed constraint on sequence to maintain lncRNA structure/function, extensive redundancy in the regulatory circuits in which lncRNAs act, as well as adaptive and non-adaptive forces such as genetic drift. We explore the molecular mechanisms promoting the birth and rapid evolution of lncRNA genes, with an emphasis on the influence of bidirectional transcription and transposable elements, two pervasive features of vertebrate genomes. Together these properties reveal a remarkably dynamic and malleable noncoding transcriptome which may represent an important source of robustness and evolvability.
Thousands of genes encoding long noncoding RNAs (lncRNAs) have been identified in all vertebrate genomes thus far examined. The list of lncRNAs partaking in arguably important biochemical, cellular, and developmental activities is steadily growing. However, it is increasingly clear that lncRNA repertoires are subject to weak functional constraint and rapid turnover during vertebrate evolution. We discuss here some of the factors that may explain this apparent paradox, including relaxed constraint on sequence to maintain lncRNA structure/function, extensive redundancy in the regulatory circuits in which lncRNAs act, as well as adaptive and non-adaptive forces such as genetic drift. We explore the molecular mechanisms promoting the birth and rapid evolution of lncRNA genes, with an emphasis on the influence of bidirectional transcription and transposable elements, two pervasive features of vertebrate genomes. Together these properties reveal a remarkably dynamic and malleable noncoding transcriptome which may represent an important source of robustness and evolvability.
Thousands of genes encoding long noncoding RNAs (lncRNAs) have been identified in all vertebrate genomes thus far examined. The list of lncRNAs partaking in arguably important biochemical, cellular, and developmental activities is steadily growing. However, it is increasingly clear that lncRNA repertoires are subject to weak functional constraint and rapid turnover during vertebrate evolution. Here we discuss some of the factors that may explain this apparent paradox, including relaxed constraint on sequence to maintain lncRNA structure/function, extensive redundancy in the regulatory circuits in which lncRNAs act, as well as adaptive and non-adaptive forces such as genetic drift. We explore the molecular mechanisms promoting the birth and rapid evolution of lncRNA genes with an emphasis on the influence of bidirectional transcription and transposable elements, two pervasive features of vertebrate genomes. Together these properties reveal a remarkably dynamic and malleable noncoding transcriptome, which may represent an important source of robustness and evolvability.
•lncRNAs show weak selective constraint, even when clearly functional.•Gain and loss of lncRNA genes occurs at very high pace during evolution.•lncRNAs mostly evolve de novo.•Bidirectional promoters and transposable elements (TEs) promote the birth of lncRNAs.•Genomes rich in TEs may have more complex and malleable transcriptomes. Thousands of genes encoding long noncoding RNAs (lncRNAs) have been identified in all vertebrate genomes thus far examined. The list of lncRNAs partaking in arguably important biochemical, cellular, and developmental activities is steadily growing. However, it is increasingly clear that lncRNA repertoires are subject to weak functional constraint and rapid turnover during vertebrate evolution. We discuss here some of the factors that may explain this apparent paradox, including relaxed constraint on sequence to maintain lncRNA structure/function, extensive redundancy in the regulatory circuits in which lncRNAs act, as well as adaptive and non-adaptive forces such as genetic drift. We explore the molecular mechanisms promoting the birth and rapid evolution of lncRNA genes, with an emphasis on the influence of bidirectional transcription and transposable elements, two pervasive features of vertebrate genomes. Together these properties reveal a remarkably dynamic and malleable noncoding transcriptome which may represent an important source of robustness and evolvability.
Highlights • lncRNAs show weak selective constraint, even when clearly functional. • Gain and loss of lncRNA genes occurs at very high pace during evolution. • lncRNAs mostly evolve de novo. • Bidirectional promoters and transposable elements (TEs) promote the birth of lncRNAs. • Genomes rich in TEs may have more complex and malleable transcriptomes.
Author Feschotte, Cédric
Kapusta, Aurélie
Author_xml – sequence: 1
  givenname: Aurélie
  surname: Kapusta
  fullname: Kapusta, Aurélie
  email: aurelie.kapusta@gmail.com
– sequence: 2
  givenname: Cédric
  surname: Feschotte
  fullname: Feschotte, Cédric
  email: cedric@genetics.utah.edu
BackLink https://www.ncbi.nlm.nih.gov/pubmed/25218058$$D View this record in MEDLINE/PubMed
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Snippet •lncRNAs show weak selective constraint, even when clearly functional.•Gain and loss of lncRNA genes occurs at very high pace during evolution.•lncRNAs mostly...
Highlights • lncRNAs show weak selective constraint, even when clearly functional. • Gain and loss of lncRNA genes occurs at very high pace during evolution. •...
Thousands of genes encoding long noncoding RNAs (lncRNAs) have been identified in all vertebrate genomes thus far examined. The list of lncRNAs partaking in...
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SubjectTerms Animals
DNA Transposable Elements
Evolution, Molecular
Exons
Humans
Medical Education
Nucleic Acid Conformation
RNA, Long Noncoding - chemistry
RNA, Long Noncoding - metabolism
Transcription, Genetic
Title Volatile evolution of long noncoding RNA repertoires: mechanisms and biological implications
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https://www.clinicalkey.es/playcontent/1-s2.0-S0168952514001346
https://dx.doi.org/10.1016/j.tig.2014.08.004
https://www.ncbi.nlm.nih.gov/pubmed/25218058
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https://pubmed.ncbi.nlm.nih.gov/PMC4464757
Volume 30
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