The impact of transposable elements in environmental adaptation

Transposable elements (TEs) play an important role in the responsive capacity of their hosts in the face of environmental challenges. The variety of mechanisms by which TEs influence the capacity of adaptation of the host is as large as the variety of TEs and host genomes. For example, TEs might directly affect the function of individual genes, provide a mechanism for rapidly acquiring new genetic material and disseminate regulatory elements that can lead to the creation of stress‐inducible regulatory networks. In this review, we summarize recent examples that are part of an increasing body of evidence suggesting a significant role of TEs in the host response to an ever‐changing environment, both in prokaryote and in eukaryote organisms. We argue that in the near future, the increasing availability of genome sequences and the development of new tools to discover and analyse TE insertions will further show the relevant role of TEs in environmental adaptation.

[1]  M. Syvanen,et al.  Evolutionary implications of horizontal gene transfer. , 2012, Annual review of genetics.

[2]  D. Fitzpatrick Horizontal gene transfer in fungi. , 2012, FEMS microbiology letters.

[3]  Lin-zhang Yang,et al.  Mechanisms of removing pollutants from aqueous solutions by microorganisms and their aggregates: a review. , 2012, Bioresource technology.

[4]  B. Daignan-Fornier,et al.  Tye7 regulates yeast Ty1 retrotransposon sense and antisense transcription in response to adenylic nucleotides stress , 2012, Nucleic acids research.

[5]  R. Slotkin,et al.  Gene Expression and Stress Response Mediated by the Epigenetic Regulation of a Transposable Element Small RNA , 2012, PLoS genetics.

[6]  A. Toussaint,et al.  Prokaryote genome fluidity: toward a system approach of the mobilome. , 2012, Methods in molecular biology.

[7]  Valer Gotea,et al.  Transposable elements and their identification. , 2012, Methods in molecular biology.

[8]  L. Yan,et al.  A Novel Retrotransposon Inserted in the Dominant Vrn-B1 Allele Confers Spring Growth Habit in Tetraploid Wheat (Triticum turgidum L.) , 2011, G3: Genes | Genomes | Genetics.

[9]  Francis M. Jiggins,et al.  Successive Increases in the Resistance of Drosophila to Viral Infection through a Transposon Insertion Followed by a Duplication , 2011, PLoS genetics.

[10]  C. Vieira,et al.  Evolvability, epigenetics and transposable elements , 2011, Biomolecular concepts.

[11]  Janice K. Wiedenbeck,et al.  Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. , 2011, FEMS microbiology reviews.

[12]  M. Low,et al.  Convergent evolution of two mammalian neuronal enhancers by sequential exaptation of unrelated retroposons , 2011, Proceedings of the National Academy of Sciences.

[13]  E. Danchin,et al.  Horizontal gene transfer in nematodes: a catalyst for plant parasitism? , 2011, Molecular plant-microbe interactions : MPMI.

[14]  R. Aminov Horizontal Gene Exchange in Environmental Microbiota , 2011, Front. Microbio..

[15]  M. Mergeay,et al.  Insertion sequence elements in Cupriavidus metallidurans CH34: distribution and role in adaptation. , 2011, Plasmid.

[16]  E. Bucher,et al.  An siRNA pathway prevents transgenerational retrotransposition in plants subjected to stress , 2011, Nature.

[17]  D. Schneider,et al.  Insertion Sequence-Driven Evolution of Escherichia coli in Chemostats , 2011, Journal of Molecular Evolution.

[18]  Kun Yang,et al.  Small RNAs from MITE-derived stem-loop precursors regulate abscisic acid signaling and abiotic stress responses in rice. , 2011, The Plant journal : for cell and molecular biology.

[19]  A. Hoffmann,et al.  Climate change and evolutionary adaptation , 2011, Nature.

[20]  T. Flutre,et al.  Considering Transposable Element Diversification in De Novo Annotation Approaches , 2011, PloS one.

[21]  D. Petrov,et al.  T-lex: a program for fast and accurate assessment of transposable element presence using next-generation sequencing data , 2010, Nucleic acids research.

[22]  A. Fuggi,et al.  Ttd1a promoter is involved in DNA–protein binding by salt and light stresses , 2011, Molecular Biology Reports.

[23]  P. Capy,et al.  The struggle for life of the genome's selfish architects , 2011, Biology Direct.

[24]  Jacques P. Bothma,et al.  Shadow Enhancers Foster Robustness of Drosophila Gastrulation , 2010, Current Biology.

[25]  Cédric Feschotte,et al.  Promiscuous DNA: horizontal transfer of transposable elements and why it matters for eukaryotic evolution. , 2010, Trends in ecology & evolution.

[26]  Ellen J. Pritham,et al.  Pervasive Horizontal Transfer of Rolling-Circle Transposons among Animals , 2010, Genome biology and evolution.

[27]  Yong Li,et al.  Profiling of cold-stress-responsive miRNAs in rice by microarrays. , 2010, Gene.

[28]  M. Goddard,et al.  Copy Number Variation and Transposable Elements Feature in Recent, Ongoing Adaptation at the Cyp6g1 Locus , 2010, PLoS genetics.

[29]  G. K. Davis,et al.  Phenotypic robustness conferred by apparently redundant transcriptional enhancers , 2010, Nature.

[30]  Daniel M. Stoebel,et al.  The Effect of Mobile Element IS10 on Experimental Regulatory Evolution in Escherichia coli , 2010, Molecular biology and evolution.

[31]  C. Vieira,et al.  Jumping genes and epigenetics: Towards new species. , 2010, Gene.

[32]  C. Feschotte,et al.  A role for host–parasite interactions in the horizontal transfer of transposons across phyla , 2010, Nature.

[33]  Philipp W. Messer,et al.  Genome-Wide Patterns of Adaptation to Temperate Environments Associated with Transposable Elements in Drosophila , 2010, PLoS genetics.

[34]  R. Lande,et al.  Adaptation, Plasticity, and Extinction in a Changing Environment: Towards a Predictive Theory , 2010, PLoS biology.

[35]  H. Levin,et al.  High-throughput sequencing of retrotransposon integration provides a saturated profile of target activity in Schizosaccharomyces pombe. , 2010, Genome research.

[36]  C. Bowler,et al.  Potential impact of stress activated retrotransposons on genome evolution in a marine diatom , 2009, BMC Genomics.

[37]  M. Lei,et al.  Stn1-Ten1 is an Rpa2-Rpa3-like complex at telomeres. , 2009, Genes & development.

[38]  D. Petrov,et al.  The adaptive role of transposable elements in the Drosophila genome. , 2009, Gene.

[39]  B. McClane,et al.  Characterization of Virulence Plasmid Diversity among Clostridium perfringens Type B Isolates , 2009, Infection and Immunity.

[40]  Hiroki Saito,et al.  Unexpected consequences of a sudden and massive transposon amplification on rice gene expression , 2009, Nature.

[41]  Karsten Hokamp,et al.  Compensatory Evolution of Gene Regulation in Response to Stress by Escherichia coli Lacking RpoS , 2009, PLoS genetics.

[42]  Hsin-Hung Chou,et al.  Fast Growth Increases the Selective Advantage of a Mutation Arising Recurrently during Evolution under Metal Limitation , 2009, PLoS genetics.

[43]  D. Petrov,et al.  A recent adaptive transposable element insertion near highly conserved developmental loci in Drosophila melanogaster. , 2009, Molecular biology and evolution.

[44]  A. Buzdin,et al.  Retroelements and their impact on genome evolution and functioning , 2009, Cellular and Molecular Life Sciences.

[45]  Baohui Liu,et al.  Adaptive Evolution Involving Gene Duplication and Insertion of a Novel Ty1/copia-Like Retrotransposon in Soybean , 2009, Journal of Molecular Evolution.

[46]  Yoichi Ishida,et al.  Transposable elements and an epigenetic basis for punctuated equilibria , 2009, BioEssays : news and reviews in molecular, cellular and developmental biology.

[47]  Keith R. Oliver,et al.  Transposable elements: powerful facilitators of evolution , 2009, BioEssays : news and reviews in molecular, cellular and developmental biology.

[48]  M. Belfort,et al.  Global regulators orchestrate group II intron retromobility. , 2009, Molecular cell.

[49]  Hong Liu,et al.  A transposable class I composite transposon carrying mph (methyl parathion hydrolase) from Pseudomonas sp. strain WBC-3. , 2009, FEMS microbiology letters.

[50]  Marlen S. Clark,et al.  Repeated horizontal transfer of a DNA transposon in mammals and other tetrapods , 2008, Proceedings of the National Academy of Sciences.

[51]  H. Kazazian,et al.  Retrotransposons Revisited: The Restraint and Rehabilitation of Parasites , 2008, Cell.

[52]  Baohui Liu,et al.  Genetic Redundancy in Soybean Photoresponses Associated With Duplication of the Phytochrome A Gene , 2008, Genetics.

[53]  Josefa González,et al.  High Rate of Recent Transposable Element–Induced Adaptation in Drosophila melanogaster , 2008, PLoS biology.

[54]  F. Salamini,et al.  Retrotransposons and siRNA have a role in the evolution of desiccation tolerance leading to resurrection of the plant Craterostigma plantagineum. , 2008, The New phytologist.

[55]  J. Palmer,et al.  Horizontal gene transfer in eukaryotic evolution , 2008, Nature Reviews Genetics.

[56]  P. Davies,et al.  Lateral Transfer of a Lectin-Like Antifreeze Protein Gene in Fishes , 2008, PloS one.

[57]  G. Servant,et al.  Remodeling Yeast Gene Transcription by Activating the Ty1 Long Terminal Repeat Retrotransposon under Severe Adenine Deficiency , 2008, Molecular and Cellular Biology.

[58]  P. Capy,et al.  Revisiting horizontal transfer of transposable elements in Drosophila , 2008, Heredity.

[59]  J. Jurka,et al.  A universal classification of eukaryotic transposable elements implemented in Repbase , 2008, Nature Reviews Genetics.

[60]  C. Feschotte Transposable elements and the evolution of regulatory networks , 2008, Nature Reviews Genetics.

[61]  Marcel E Visser,et al.  Keeping up with a warming world; assessing the rate of adaptation to climate change , 2008, Proceedings of the Royal Society B: Biological Sciences.

[62]  Celso A. Espinoza,et al.  Human Alu RNA is a modular transacting repressor of mRNA transcription during heat shock. , 2008, Molecular cell.

[63]  J. Bennetzen,et al.  A unified classification system for eukaryotic transposable elements , 2007, Nature Reviews Genetics.

[64]  Rongcheng Lin,et al.  Transposase-Derived Transcription Factors Regulate Light Signaling in Arabidopsis , 2007, Science.

[65]  M. Low,et al.  Ancient Exaptation of a CORE-SINE Retroposon into a Highly Conserved Mammalian Neuronal Enhancer of the Proopiomelanocortin Gene , 2007, PLoS genetics.

[66]  I. Darboux,et al.  Transposon‐mediated resistance to Bacillus sphaericus in a field‐evolved population of Culex pipiens (Diptera: Culicidae) , 2007, Cellular microbiology.

[67]  D. Voytas,et al.  Phosphorylation regulates integration of the yeast Ty5 retrotransposon into heterochromatin. , 2007, Molecular cell.

[68]  J. Casacuberta,et al.  The promoter of the TLC1.1 retrotransposon from Solanum chilense is activated by multiple stress-related signaling molecules , 2007, Plant Cell Reports.

[69]  T. Samuelsson,et al.  Useful ‘junk’: Alu RNAs in the human transcriptome , 2007, Cellular and Molecular Life Sciences.

[70]  R. Martienssen,et al.  Transposable elements and the epigenetic regulation of the genome , 2007, Nature Reviews Genetics.

[71]  L. Anderson,et al.  Repetitive DNA elements as mediators of genomic change in response to environmental cues. , 2007, Biological reviews of the Cambridge Philosophical Society.

[72]  L. Yan,et al.  The wheat and barley vernalization gene VRN3 is an orthologue of FT , 2006, Proceedings of the National Academy of Sciences.

[73]  S. Wessler,et al.  Dramatic amplification of a rice transposable element during recent domestication , 2006, Proceedings of the National Academy of Sciences.

[74]  M. Batzer,et al.  Emergence of primate genes by retrotransposon-mediated sequence transduction , 2006, Proceedings of the National Academy of Sciences.

[75]  Christian Biémont,et al.  Genetics: Junk DNA as an evolutionary force , 2006, Nature.

[76]  J. Volff Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes , 2006, BioEssays : news and reviews in molecular, cellular and developmental biology.

[77]  Didier Mazel,et al.  Integrons: agents of bacterial evolution , 2006, Nature Reviews Microbiology.

[78]  P. Bennett,et al.  ISCR Elements: Novel Gene-Capturing Systems of the 21st Century? , 2006, Microbiology and Molecular Biology Reviews.

[79]  J. Häsler,et al.  Alu RNP and Alu RNA regulate translation initiation in vitro , 2006, Nucleic acids research.

[80]  A. Reymond,et al.  Emergence of Young Human Genes after a Burst of Retroposition in Primates , 2005, PLoS biology.

[81]  Laura S. Frost,et al.  Mobile genetic elements: the agents of open source evolution , 2005, Nature Reviews Microbiology.

[82]  M. Springer,et al.  Severe Adenine Starvation Activates Ty1 Transcription and Retrotransposition in Saccharomyces cerevisiae , 2005, Molecular and Cellular Biology.

[83]  M. Morgante,et al.  Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize , 2005, Nature Genetics.

[84]  D. Petrov,et al.  References and Notes Materials and Methods Tables S1 and S2 References and Notes Pesticide Resistance via Transposition-mediated Adaptive Gene Truncation in Drosophila , 2022 .

[85]  M. Van Sluys,et al.  Stress activation and genomic impact of Tnt1 retrotransposons in Solanaceae , 2005, Cytogenetic and Genome Research.

[86]  Sophie Brachat,et al.  Contribution of Horizontal Gene Transfer to the Evolution of Saccharomyces cerevisiae , 2005, Eukaryotic Cell.

[87]  Bernard B. Suh,et al.  The genome of the protist parasite Entamoeba histolytica , 2005, Nature.

[88]  J. D. de Visser,et al.  Insertion-Sequence-Mediated Mutations Isolated During Adaptation to Growth and Starvation in Lactococcus lactis , 2004, Genetics.

[89]  S. Wessler,et al.  Using rice to understand the origin and amplification of miniature inverted repeat transposable elements (MITEs). , 2004, Current opinion in plant biology.

[90]  K. Anamthawat-jónsson,et al.  Retrotransposon BARE-1 is a major, dispersed component of the barley (Hordeum vulgare L.) genome , 1996, Plant Molecular Biology.

[91]  M. Grandbastien,et al.  The expression of the tobacco Tnt1 retrotransposon is linked to plant defense responses , 2004, Genetica.

[92]  E. Eichler,et al.  An Alu transposition model for the origin and expansion of human segmental duplications. , 2003, American journal of human genetics.

[93]  V. Wood,et al.  Retrotransposons and their recognition of pol II promoters: a comprehensive survey of the transposable elements from the complete genome sequence of Schizosaccharomyces pombe. , 2003, Genome research.

[94]  D. Voytas,et al.  Controlling integration specificity of a yeast retrotransposon , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[95]  R. ffrench-Constant,et al.  A Single P450 Allele Associated with Insecticide Resistance in Drosophila , 2002, Science.

[96]  S. Shimada,et al.  OARE-1, a Ty1-copia retrotransposon in oat activated by abiotic and biotic stresses. , 2001, Plant & cell physiology.

[97]  M. Grandbastien,et al.  Three Tnt1 subfamilies show different stress-associated patterns of expression in tobacco. Consequences for retrotransposon control and evolution in plants. , 2001, Plant physiology.

[98]  S. Wessler,et al.  Treasures in the attic: Rolling circle transposons discovered in eukaryotic genomes , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[99]  W. Miller,et al.  The evolutionary life history of P transposons: from horizontal invaders to domesticated neogenes , 2001, Chromosoma.

[100]  J. Hacker,et al.  Ecological fitness, genomic islands and bacterial pathogenicity , 2001, EMBO reports.

[101]  F. Blattner,et al.  Complete DNA Sequence and Analysis of the Large Virulence Plasmid of Shigella flexneri , 2001, Infection and Immunity.

[102]  P. Nordmann,et al.  Characterization of In53, a Class 1 Plasmid- and Composite Transposon-Located Integron of Escherichia coli Which Carries an Unusual Array of Gene Cassettes , 2001, Journal of bacteriology.

[103]  J. Hayles,et al.  Fission yeast retrotransposon Tf1 integration is targeted to 5' ends of open reading frames. , 2000, Nucleic acids research.

[104]  C. Buchrieser,et al.  The virulence plasmid pWR100 and the repertoire of proteins secreted by the type III secretion apparatus of Shigella flexneri , 2000, Molecular microbiology.

[105]  R. Lenski,et al.  Long-term experimental evolution in Escherichia coli. IX. Characterization of insertion sequence-mediated mutations and rearrangements. , 2000, Genetics.

[106]  C. Biémont,et al.  Stress and transposable elements: co-evolution or useful parasites? , 2000, Heredity.

[107]  Carl T. Bergstrom,et al.  Bacteria are different: observations, interpretations, speculations, and opinions about the mechanisms of adaptive evolution in prokaryotes. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[108]  B. Young,et al.  The most frequent constitutional translocation in humans, the t(11;22)(q23;q11) is due to a highly specific alu-mediated recombination. , 2000, Human molecular genetics.

[109]  H. Ochman,et al.  Lateral gene transfer and the nature of bacterial innovation , 2000, Nature.

[110]  H. Hirochika,et al.  A 13-bp cis-regulatory element in the LTR promoter of the tobacco retrotransposon Tto1 is involved in responsiveness to tissue culture, wounding, methyl jasmonate and fungal elicitors. , 1999, The Plant journal : for cell and molecular biology.

[111]  J. Bennetzen,et al.  Plant retrotransposons. , 1999, Annual review of genetics.

[112]  L. Brown,et al.  Reconstructing hominid Y evolution: X-homologous block, created by X-Y transposition, was disrupted by Yp inversion through LINE-LINE recombination. , 1998, Human molecular genetics.

[113]  S. Wessler Plant retrotransposons: Turned on by stress , 1996, Current Biology.

[114]  S. Wessler Turned on by stress. Plant retrotransposons. , 1996, Current biology : CB.

[115]  D. Petrov,et al.  Diverse transposable elements are mobilized in hybrid dysgenesis in Drosophila virilis. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[116]  R M Hall,et al.  Expression of antibiotic resistance genes in the integrated cassettes of integrons , 1995, Antimicrobial agents and chemotherapy.

[117]  P. Nordmann,et al.  Analysis of a carbapenem-hydrolyzing class A beta-lactamase from Enterobacter cloacae and of its LysR-type regulatory protein. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[118]  R M Hall,et al.  Site‐specific insertion of gene cassettes into integrons , 1993, Molecular microbiology.

[119]  B. Mcclintock,et al.  The significance of responses of the genome to challenge. , 1984, Science.

[120]  R. Paro,et al.  The molecular basis of I-R hybrid Dysgenesis in drosophila melanogaster: Identification, cloning, and properties of the I factor , 1984, Cell.

[121]  G. Rubin,et al.  The molecular basis of P-M hybrid dysgenesis: The role of the P element, a P-strain-specific transposon family , 1982, Cell.