The origins of eukaryotic gene structure

Research output: Contribution to journalArticle

241 Citations (Scopus)

Abstract

Most of the phenotypic diversity that we perceive in the natural world is directly attributable to the peculiar structure of the eukaryotic gene, which harbors numerous embellishments relative to the situation in prokaryotes. The most profound changes include introns that must be spliced out of precursor mRNAs, transcribed but untranslated leader and trailer sequences (untranslated regions), modular regulatory elements that drive patterns of gene expression, and expansive intergenic regions that harbor additional diffuse control mechanisms. Explaining the origins of these features is difficult because they each impose an intrinsic disadvantage by increasing the genic mutation rate to defective alleles. To address these issues, a general hypothesis for the emergence of eukaryotic gene structure is provided here. Extensive information on absolute population sizes, recombination rates, and mutation rates strongly supports the view that eukaryotes have reduced genetic effective population sizes relative to prokaryotes, with especially extreme reductions being the rule in multicellular lineages. The resultant increase in the power of random genetic drift appears to be sufficient to overwhelm the weak mutational disadvantages associated with most novel aspects of the eukaryotic gene, supporting the idea that most such changes are simple outcomes of semi-neutral processes rather than direct products of natural selection. However, by establishing an essentially permanent change in the population-genetic environment permissive to the genome-wide repatterning of gene structure, the eukaryotic condition also promoted a reliable resource from which natural selection could secondarily build novel forms of organismal complexity. Under this hypothesis, arguments based on molecular, cellular, and/or physiological constraints are insufficient to explain the disparities in gene, genomic, and phenotypic complexity between prokaryotes and eukaryotes.

Original languageEnglish (US)
Pages (from-to)450-468
Number of pages19
JournalMolecular Biology and Evolution
Volume23
Issue number2
DOIs
StatePublished - Feb 1 2006
Externally publishedYes

Fingerprint

prokaryote
prokaryotic cells
gene
Genes
Genetic Selection
eukaryote
Mutation Rate
Population Density
Eukaryota
natural selection
genes
eukaryotic cells
mutation
harbor
population size
Untranslated Regions
Genetic Drift
trailers
Intergenic DNA
effective population size

Keywords

  • Complexity
  • Gene networks
  • Gene regulation
  • Gene structure
  • Genetic draft
  • Genome evolution
  • Introns
  • Modularity
  • Mutation
  • Natural selection
  • Pleiotropy
  • Population size
  • Random genetic drift
  • Recombination
  • Subfunctionalization
  • Transcription factors
  • UTR

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics

Cite this

The origins of eukaryotic gene structure. / Lynch, Michael.

In: Molecular Biology and Evolution, Vol. 23, No. 2, 01.02.2006, p. 450-468.

Research output: Contribution to journalArticle

@article{ba78120d7995474e8c85fb482d88dd84,
title = "The origins of eukaryotic gene structure",
abstract = "Most of the phenotypic diversity that we perceive in the natural world is directly attributable to the peculiar structure of the eukaryotic gene, which harbors numerous embellishments relative to the situation in prokaryotes. The most profound changes include introns that must be spliced out of precursor mRNAs, transcribed but untranslated leader and trailer sequences (untranslated regions), modular regulatory elements that drive patterns of gene expression, and expansive intergenic regions that harbor additional diffuse control mechanisms. Explaining the origins of these features is difficult because they each impose an intrinsic disadvantage by increasing the genic mutation rate to defective alleles. To address these issues, a general hypothesis for the emergence of eukaryotic gene structure is provided here. Extensive information on absolute population sizes, recombination rates, and mutation rates strongly supports the view that eukaryotes have reduced genetic effective population sizes relative to prokaryotes, with especially extreme reductions being the rule in multicellular lineages. The resultant increase in the power of random genetic drift appears to be sufficient to overwhelm the weak mutational disadvantages associated with most novel aspects of the eukaryotic gene, supporting the idea that most such changes are simple outcomes of semi-neutral processes rather than direct products of natural selection. However, by establishing an essentially permanent change in the population-genetic environment permissive to the genome-wide repatterning of gene structure, the eukaryotic condition also promoted a reliable resource from which natural selection could secondarily build novel forms of organismal complexity. Under this hypothesis, arguments based on molecular, cellular, and/or physiological constraints are insufficient to explain the disparities in gene, genomic, and phenotypic complexity between prokaryotes and eukaryotes.",
keywords = "Complexity, Gene networks, Gene regulation, Gene structure, Genetic draft, Genome evolution, Introns, Modularity, Mutation, Natural selection, Pleiotropy, Population size, Random genetic drift, Recombination, Subfunctionalization, Transcription factors, UTR",
author = "Michael Lynch",
year = "2006",
month = "2",
day = "1",
doi = "10.1093/molbev/msj050",
language = "English (US)",
volume = "23",
pages = "450--468",
journal = "Molecular Biology and Evolution",
issn = "0737-4038",
publisher = "Oxford University Press",
number = "2",

}

TY - JOUR

T1 - The origins of eukaryotic gene structure

AU - Lynch, Michael

PY - 2006/2/1

Y1 - 2006/2/1

N2 - Most of the phenotypic diversity that we perceive in the natural world is directly attributable to the peculiar structure of the eukaryotic gene, which harbors numerous embellishments relative to the situation in prokaryotes. The most profound changes include introns that must be spliced out of precursor mRNAs, transcribed but untranslated leader and trailer sequences (untranslated regions), modular regulatory elements that drive patterns of gene expression, and expansive intergenic regions that harbor additional diffuse control mechanisms. Explaining the origins of these features is difficult because they each impose an intrinsic disadvantage by increasing the genic mutation rate to defective alleles. To address these issues, a general hypothesis for the emergence of eukaryotic gene structure is provided here. Extensive information on absolute population sizes, recombination rates, and mutation rates strongly supports the view that eukaryotes have reduced genetic effective population sizes relative to prokaryotes, with especially extreme reductions being the rule in multicellular lineages. The resultant increase in the power of random genetic drift appears to be sufficient to overwhelm the weak mutational disadvantages associated with most novel aspects of the eukaryotic gene, supporting the idea that most such changes are simple outcomes of semi-neutral processes rather than direct products of natural selection. However, by establishing an essentially permanent change in the population-genetic environment permissive to the genome-wide repatterning of gene structure, the eukaryotic condition also promoted a reliable resource from which natural selection could secondarily build novel forms of organismal complexity. Under this hypothesis, arguments based on molecular, cellular, and/or physiological constraints are insufficient to explain the disparities in gene, genomic, and phenotypic complexity between prokaryotes and eukaryotes.

AB - Most of the phenotypic diversity that we perceive in the natural world is directly attributable to the peculiar structure of the eukaryotic gene, which harbors numerous embellishments relative to the situation in prokaryotes. The most profound changes include introns that must be spliced out of precursor mRNAs, transcribed but untranslated leader and trailer sequences (untranslated regions), modular regulatory elements that drive patterns of gene expression, and expansive intergenic regions that harbor additional diffuse control mechanisms. Explaining the origins of these features is difficult because they each impose an intrinsic disadvantage by increasing the genic mutation rate to defective alleles. To address these issues, a general hypothesis for the emergence of eukaryotic gene structure is provided here. Extensive information on absolute population sizes, recombination rates, and mutation rates strongly supports the view that eukaryotes have reduced genetic effective population sizes relative to prokaryotes, with especially extreme reductions being the rule in multicellular lineages. The resultant increase in the power of random genetic drift appears to be sufficient to overwhelm the weak mutational disadvantages associated with most novel aspects of the eukaryotic gene, supporting the idea that most such changes are simple outcomes of semi-neutral processes rather than direct products of natural selection. However, by establishing an essentially permanent change in the population-genetic environment permissive to the genome-wide repatterning of gene structure, the eukaryotic condition also promoted a reliable resource from which natural selection could secondarily build novel forms of organismal complexity. Under this hypothesis, arguments based on molecular, cellular, and/or physiological constraints are insufficient to explain the disparities in gene, genomic, and phenotypic complexity between prokaryotes and eukaryotes.

KW - Complexity

KW - Gene networks

KW - Gene regulation

KW - Gene structure

KW - Genetic draft

KW - Genome evolution

KW - Introns

KW - Modularity

KW - Mutation

KW - Natural selection

KW - Pleiotropy

KW - Population size

KW - Random genetic drift

KW - Recombination

KW - Subfunctionalization

KW - Transcription factors

KW - UTR

UR - http://www.scopus.com/inward/record.url?scp=30744475434&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=30744475434&partnerID=8YFLogxK

U2 - 10.1093/molbev/msj050

DO - 10.1093/molbev/msj050

M3 - Article

C2 - 16280547

AN - SCOPUS:30744475434

VL - 23

SP - 450

EP - 468

JO - Molecular Biology and Evolution

JF - Molecular Biology and Evolution

SN - 0737-4038

IS - 2

ER -