How important are transposons for plant evolution?

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Key Points

  • Transposable elements (TEs) are the single most variable components of plant genomes. Even closely related plants can harbour widely different populations of TEs.

  • TEs can cause a broad array of changes in gene composition and function. These changes range from simple insertional mutations to genetic reprogramming, gene movement and the evolution of novel functional protein-coding sequences.

  • To restrain TE activity, plants have a potent response that results in epigenetic silencing of these elements. This can in turn result in epigenetic as well as genetic variation in plant gene function.

  • The changes caused by TEs are a potentially rich source of variation on which selection can operate. Given the large numbers of plant TEs on evidence for ongoing activity of these selfish genetic elements, it is a reasonable hypothesis that TEs have played an important part in plant adaptation.

  • Despite the possibilities raised by experimental evidence of the kinds of changes that TEs can cause, there is only limited and anecdotal evidence that TEs have in fact been important players in adaptive evolution of plants.

  • Recent advances in genomics and phenomics have made it possible systematically to assess the part that TEs have played. It is only through the systematic identification of large numbers of alleles with important effects on phenotype that it will be possible to determine the relative role that TEs have had in the generation of meaningful genetic variation in plants.

  • Domesticated plant species provide us with an ideal model for understanding this process. These species have been under strong, recent directional selection, often have well-characterized TEs, have been extensively characterized with respect to trait variation and can be readily compared to wild relatives.

Abstract

For decades, transposable elements have been known to produce a wide variety of changes in plant gene expression and function. This has led to the idea that transposable element activity has played a key part in adaptive plant evolution. This Review describes the kinds of changes that transposable elements can cause, discusses evidence that those changes have contributed to plant evolution and suggests future strategies for determining the extent to which these changes have in fact contributed to plant adaptation and evolution. Recent advances in genomics and phenomics for a range of plant species, particularly crops, have begun to allow the systematic assessment of these questions.

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Figure 1: Structural and functional changes that can be caused by transposable elements.
Figure 2: Transposable element insertions associated with changes in grape colour.
Figure 3: Effects of transposable element insertions on expression tissue specificity and cold inducibility.
Figure 4: Retroposition of the IQD12 gene at the SUN locus results in ectopic expression in the fruit.
Figure 5: Epigenetic regulation of plant genes.

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Acknowledgements

The author apologizes to the many authors whose work he was unable to include owing to space constraints. The author is supported by a grant from the US National Science Foundation (DBI 031726).

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Damon Lisch is supported by a grant from the US National Science Foundation (DBI 031726).

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1001 Genomes Project

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International Rice Functional Genomics Consortium

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Sequenced plant genomes — CoGePedia

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Glossary

Transposable elements

(TEs). Stretches of DNA that are competent to integrate into new positions in the genome, that are competent to increase their copy number over time and that rely on one or more enzymatic function provided by an autonomous element.

Epigenetic variation

Heritable differences in the expression of a gene in the absence of changes in the DNA sequence of that gene. It is often associated with changes in cytosine methylation and histone modification. Cryptic epigenetic variation refers to epigenetic variation that is only manifest under specific conditions.

Phenomics

The objective and systematic acquisition of high-quality phenotypic data, allowing for phenotypic features to be analysed on a continuum together with molecular data, such as gene expression profiles or causative genomic mutations.

Class I elements

A transposable element that uses a 'copy-and-paste' transposition mechanism involving an RNA intermediate.

Class II elements

A transposable element that transposes via a 'cut-and-paste' mechanism in which the DNA of the element is physically transposed from one position in the genome to another.

Comparative genomics

The discipline devoted to comparing related genomes, focusing on large-scale changes in the overall structure and composition of genomes, chromosomal segments and genes.

Recombinant inbred lines

(RILs). Strains that are derived from crosses between two or more parental strains, followed by recombination of chromosomes and inbreeding to homozygosity. Typically, RILs are carefully genotyped at many loci. A panel of RILs can be a stable resource for quantitative trait locus mapping.

Exaptation

The process by which a trait takes on a new function. For a transposable element, this would imply a shift from facilitating replication of the transposable element to providing an adaptive function for the host.

Retroposition

The process by which mRNA from a gene is reverse-transcribed by a retrotransposon-encoded reverse transcriptase and then integrated at a new position by a retrotransposon-encoded integrase. Typically, this process involves the loss of intron sequences and the presence of a new insertion flanked by short target site duplications.

Transduplication

The process by which a transposable element incorporates a gene or gene fragment and duplicates and transposes it to a new position.

Helitron

A class of transposable element that transposes by a 'rolling circle' mechanism, a process that is frequently associated with the capture of short portions of host coding sequence.

Retrogenes

Genes that have arisen through the reverse transcription of an mRNA.

KA/KS

KA and KS are the rates of substitution at nonsynonymous sites and synonymous sites, respectively. The ratio KA/KS is often used to infer selection: KA/KS <1 indicates a functional constraint; KA/KS = 1 indicates a lack of functional constraint; and KA/KS >1 indicates positive Darwinian selection.

Transposase

An enzyme that is encoded by a gene carried by an autonomous class II transposable element and that catalyses the transposition reaction.

Syntenic

A term that describes the presence of collinear homologous DNA sequences in related chromosomal regions, implying a common ancestor. The presence of syntenic, conserved sequences over long periods of time suggests continued function, particularly in plants, which exhibit a high rate of DNA elimination.

Autonomous element

A transposable element that encodes the genes necessary for its own transposition.

Epialleles

Alternative chromatin states at a given locus, defined with respect to individuals in the population for a given time point and tissue type. Epialleles vary greatly in their stability and they affect gene expression levels or patterns rather than gene products.

Genome-wide association study

A study in which associations between genetic variation and a phenotype or trait of interest are identified by genotyping cases and controls for a set of genetic variants that capture variation across the entire genome.

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Lisch, D. How important are transposons for plant evolution?. Nat Rev Genet 14, 49–61 (2013) doi:10.1038/nrg3374

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