DNA-binding specificity of rice mariner-like transposases and interactions with Stowaway MITEs
Nucleic Acids Research
DNA-binding specificity of rice mariner-like transposases and interactions with Stowaway MITEs
Ce´ dric Feschotte 0 1
Mark T. Osterlund 1
Ryan Peeler 1
Susan R. Wessler 1
0 Department of Biology, University of Texas at Arlington , Arlington, TX 76019 , USA
1 Department of Plant Biology, University of Georgia , Athens, GA 30602 , USA
*To whom correspondence should be addressed. Tel: +1 706 542 1870; Fax: +1 706 542 1805; Email: Correspondence may also be addressed to Ce´dric Feschotte. Tel: +1 817 272 2426; Fax: +1 817 272 2855; Email:
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Mariner-like elements (MLEs) are DNA transposons
found throughout the plant and animal kingdoms.
A previous computational survey of the rice (Oryza
sativa) genome sequence revealed 34 full length
MLEs (Osmars) belonging to 25 distinct families.
This survey, which also identified sequence
similarities between the Osmar elements and the Stowaway
superfamily of MITEs, led to the formulation of a
hypothesis whereby Stowaways are mobilized by
OSMAR transposases. Here we investigate the
DNAbinding activities and specificities of two OSMAR
transposases, OSMAR5 and OSMAR10. Like other
mariner-like transposases, the OSMARs bind
specifically to the terminal inverted repeat (TIR) sequences
of their encoding transposons. OSMAR5 binds DNA
through a bipartite N-terminal domain containing
two functionally separable helix-turn-helix motifs,
resembling the paired domain of Tc1-like
transposases and PAX transcription factors in metazoans.
Furthermore, binding of the OSMARs is not limited
to their own TIRs; OSMAR5 transposase can also
interact in vitro with TIRs from closely related Osmar
elements and with consensus TIRs of several
Stowaway families mined from the rice genome
sequence. These results provide the first
biochemical evidence for a functional relationship between
Osmar elements and Stowaway MITEs and lead us
to suggest that there is extensive cross-talk among
related but distinct transposon families co-existing
in a single eukaryote genome.
Transposable elements make up the largest fraction of many
eukaryotic genomes. They are divided into two classes based
on their mechanism of transposition (1–3). Class 1 elements
(retrotransposons) transpose by means of an RNA
intermediate in a reaction involving several enzymes, including reverse
transcriptase and integrase. In contrast, class 2 elements (DNA
transposons) move directly via DNA and the transposition
reaction is catalyzed by an element-encoded enzyme called
transposase. During transposition of class 2 elements,
transposase molecules bind to the transposon in a sequence-specific
manner and catalyze both the DNA cleavage and strand
transfer steps of the so-called ‘cut-and-paste’ reaction (3).
Nonautonomous DNA transposons do not encode
transposase, but can still undergo transposition using transposase
encoded by an autonomous element [for a review, see (2)].
Because nonautonomous elements are often internal deletion
derivatives of autonomous elements, they retain the terminal
binding sites necessary to interact with transposase. A
seemingly distinct class of nonautonomous elements, called
miniature-inverted repeat elements (MITEs), was first
identified in plant genomes (4–7) and was subsequently identified
in a wide range of animal genomes, including those of
nematodes, mosquitoes, sea squirt, zebrafish, frogs and humans [for a
review, see (6)]. Elements structurally reminiscent of MITEs
were also described in eubacteria and archaea (8–10). Like most
other nonautonomous transposons, MITEs have no coding
capacity and thus must rely on transposase encoded in trans
by autonomous elements. MITE families are distinguished from
other nonautonomous DNA transposons by their high copy
numbers and structural homogeneity. These features are
consistent with the initial amplification of one or a few MITEs.
Because MITEs do not encode transposase, their initial
classification was based on similarities in noncoding sequences
The authors wish it to be known that, in their opinion, the first two authors should be regarded as joint First Authors
including the terminal inverted repeat (TIR) and target site
duplication (TSD). Using these criteria, most plant MITEs
were assigned to one of two groups, Tourist or Stowaway
[for a review, see (6,7)]. Subsequently, sequence similarity
was detected between the TIRs and TSDs of MITEs and
of transposase-encoding elements in the same genome. For
example, Tourist MITEs share sequence similarity with the
TIRs of the transpoase-encoding PIF/Harbinger superfamily
(11–13), while the TIR and TSD of Stowaway MITEs are
similar to the TIR and TSD of Tc1/mariner elements (5,14,15).
In a recent genome-wide analysis of rice, the sequences of
virtually all Stowaway MITEs and mariner-like elements
(MLEs) (called Osmars) were identified and compared (16).
More than 22 000 Stowaway MITEs were classified into
36 families, while 34 different Osmars were found to group
into three major clades (...truncated)