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Plant transposable elements: where genetics meets genomics

Key Points

  • The analysis of unstable kernel phenotypes in maize led to the discovery and characterization of active class 2 DNA transposable elements (TEs).

  • These active elements are a very small fraction of the TEs found in plant genomes.

  • Access to all or part of the genomic sequence of an organism has led to the development of new techniques to analyse the life cycle of TEs and their interactions with the 'host' genome.

  • Two types of element — miniature inverted-repeat transposable elements (MITEs) and long terminal repeat (LTR) retrotransposons — predominate in plant genomes.

  • MITEs are non-autonomous class 2 elements, but most can now be connected with two superfamilies of transposases: Tc1/mariner and PIF/harbinger.

  • LTR retrotransposons are the single largest component of plant genomes and are responsible for the recent genome expansion in some plants.

  • Despite evidence of recent activity, TEs that are present in high copy numbers in plant genomes are almost universally found to be defective and/or epigenetically silenced.

  • Some LTR retrotransposons are transcriptionally activated by various biotic and abiotic stresses.

  • Availability of mutant backgrounds that are deficient in epigenetic regulation offers the promise of activating previously silenced TEs and revealing new facets of their biology.

Abstract

Transposable elements are the single largest component of the genetic material of most eukaryotes. The recent availability of large quantities of genomic sequence has led to a shift from the genetic characterization of single elements to genome-wide analysis of enormous transposable-element populations. Nowhere is this shift more evident than in plants, in which transposable elements were first discovered and where they are still actively reshaping genomes.

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Figure 1: Using kernel phenotypes to study transposon behaviour.
Figure 2: Model for the origin and amplification of MITEs.
Figure 3: Estimating the time of retrotransposon insertion.
Figure 4: Detection of new genomic insertions by transposon display.
Figure 5: Epigenetic silencing of transposable elements.

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Acknowledgements

We thank members of the Wessler lab, Z. Bao and E. Pritham for suggestions on the manuscript and stimulating discussions, and H. Cerrutti, S. Eddy, M.-A. Grandbastien, R. Martienssen, J. Tu and D. Voytas for providing helpful information and unpublished data. This work was supported by grants from the National Science Foundation (Plant Genome Initiative), the National Institute of Health, the Department of Energy and the University of Georgia Research Foundation to S.R.W.

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Correspondence to Susan R. Wessler.

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DATABASES

MaizeDB

Ac

adh1

Bs1

Ds

Hopscotch

Huck-2

Magellan

Mutator

Opie-2

Spm

Stonor

Stowaway

Tourist

The <i>Arabidopsis</i> Information Resource

ddm1

FURTHER INFORMATION

Encyclopedia of Life Sciences

Repetitive DNA: evolution

Transposons; eukaryotic

Barbara McClintock

Sue Wessler's lab

Zhijian Tu's web page

Glossary

ENDOSPERM

A triploid nutritive tissue in flowering plants.

EPIGENETIC

Any heritable change in gene expression that is not caused by a change in DNA sequence.

ORTHOLOGOUS GENES

Homologous genes that originated through speciation (for example, human and mouse β-globin).

PARALOGOUS GENES

Homologous genes that originated by gene duplication (for example, human α-globin and β-globin).

ABORTIVE GAP REPAIR

The double-stranded DNA break left at the site of excision of a class 2 transposon is repaired by the host machinery (gap repair). This gap is sometimes repaired by making an identical copy of the excised transposon, using the element still present on the sister chromatid or the homologous chromosome as a template. The process can be incomplete due to slippage and mispairing events. Such aberrant repairs are commonly responsible for the origin of an internally deleted copy of the excised transposon.

PROTOPLAST

A cell after the removal of its cell wall.

BREAKAGE–FUSION–BRIDGE CYCLE

In somatic cells, a cycle of chromosome breakage (at Ds, for example), DNA replication, chromatid fusion (forming a dicentric chromosome) and formation of a chromosome bridge occurs during mitotic anaphase. A new round follows when the chromosome breaks yet again as the two centromeres are pulled to opposite poles.

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Feschotte, C., Jiang, N. & Wessler, S. Plant transposable elements: where genetics meets genomics. Nat Rev Genet 3, 329–341 (2002). https://doi.org/10.1038/nrg793

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