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Chapter 24 : The and CACTA Superfamilies of Plant Transposons

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Abstract:

This chapter focuses primarily on what is known about the and superfamilies of plant mobile elements. It discusses features of their biology and their transposition mechanisms that have become known in the past decade. While sequences that structurally resemble these element families have been found in a variety of plant species, the authors deal only with those that are known to transpose. Control of transposition is complex, intimately tied to the developmental processes in the host maize plant, and has been the subject of genetically elegant and fascinating studies that date back half a century. was isolated as a 17-kb insertion in the highly unstable allele of . The genetic properties and molecular structure indicate that is an autonomous member of the CACTA superfamily. also shows some of the genetic characteristics of , most notably the ability to have both suppressor and mutator functions. Transposons have proven to be powerful mutagens that enable selection for disruptions of virtually any gene. Since their molecular isolation, plant transposons have been used extensively as probes to isolate genes mutagenized in exactly this manner. Two general approaches have been taken in plants: tagging with endogenous elements where they are available and well-characterized (primarily in maize, in petunia, and in Antirrhinum), and tagging with transposons from heterologous systems.

Citation: Kunze R, Weil C. 2002. The and CACTA Superfamilies of Plant Transposons, p 565-610. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch24

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Figures

Image of Figure 1.
Figure 1.

Autonomous plant elements. The diagram below shows the domains found within the TPase protein. b, basic regions; x, N-terminal fragment that can be removed without loss of TPase function; m, middle region where the reactive residues are likely to occur; N1, N2+3, nuclear localization signals; PQ, Pro-Glx repeat region essential for transposition; DNA, DNA binding domain; DIM, dimerization domain: hAT1, hAT2, hAT3, regions of strong sequence similarity among family TPase proteins, including those in animals and fungi. Introns are indicated by white bars within transcribed (hatched) region.

Citation: Kunze R, Weil C. 2002. The and CACTA Superfamilies of Plant Transposons, p 565-610. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch24
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Image of Figure 2.
Figure 2.

Mechanisms suggested for formation of defective elements. (A) Formation of internally deleted transposons in plants can occur following an excision event. (B) Synthesis-dependent strand annealing (SDSA). Once each new strand acquires a copy of sequence that can base pair with the other newly synthesized DNA, a new duplex is formed and the remaining “flaps” are removed by an exonuclease. (C) Similar to SDSA, except that one template being copied to repair the excision site is from an ectopic site. Resolution is again through sequences that can anneal; however, the new DNA is heteroduplex for an extensive region and this ectopic sequence can become incorporated into the transposon. (D) DNA synthesis errors such as slipped mispairing can create deletions. (E) These deletions can also be repaired using “filler DNA” sequences taken from a nearby sequence that is fortuitously similar to the sequence on both sides of the deletion breakpoint.

Citation: Kunze R, Weil C. 2002. The and CACTA Superfamilies of Plant Transposons, p 565-610. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch24
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Image of Figure 3.
Figure 3.

dosage and excision frequency. A likely explanation for variations in transposition frequency in maize, as well as in other plants, is that the concentration of TPase must fall within an optimum range. Too little produces inefficient transposition and too much creates nonfunctional TPase complexes.

Citation: Kunze R, Weil C. 2002. The and CACTA Superfamilies of Plant Transposons, p 565-610. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch24
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Image of Figure 4.
Figure 4.

Hemimethylation and transposition. Following DNA replication, the TPase binding sites in each daughter element are hemimethylated differently, such that one daughter is more competent to transpose, in this case, the element shown on the left.

Citation: Kunze R, Weil C. 2002. The and CACTA Superfamilies of Plant Transposons, p 565-610. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch24
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Image of Figure 5.
Figure 5.

Aberrant transposition and /-induced chromosome breakage. The hemimethylation model in Fig. 4 has important implications for chromosome breakage and rearrangement. (A) Transposase attempting to utilize the transposition-competent left end and right end of the same element can result in element excision and transposition, with the excision site rejoined in a characteristic transposon footprint. (B) Transposase interacting with the transposition-competent left end of one element and the transposition-competent right end of a second element can lead to large-scale rearrangements. When the two elements involved are in opposite orientations, the two element ends in the aberrant transposition lie on opposite sister chromatids. Repair of the “excision site” forms a typical transposon footprint, but also produces a dicentric chromosome (centromere indicated by “C”). (C) Elements can be inserted one into the other, or can be nearby, but must be in opposite orientation with respect to one another. By the hemimethylation model, the transposition-competent daughter element for each of the two transposons would be on opposite sister chromatids.

Citation: Kunze R, Weil C. 2002. The and CACTA Superfamilies of Plant Transposons, p 565-610. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch24
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Image of Figure 6.
Figure 6.

Excision and reinsertion models for elements. (A) Template-switching model based on / elements in maize. Black triangles indicate positions of TPase cleavage.Transposon ends are synapsedby interactionsamongboundTPase molecules, indicated by dashed lines. DNA repair synthesis of flanking DNA is indicated below the synapsed element as a solid line for the DNA at one end of the element and a hatched line for the other. Template switches are indicated among some of the available templates; however, synthesis is not known to read into the transposon itself. (B) The hairpin model. Positioning of the TPase cleavage events (black triangles) is based on transposon footprints for each case, the bases adjacent to the transposon for , as well as for / and other elements in plants. Hairpin formation in the host DNA is by the direct transesterification of one strand by the other following TPase cleavage. Prior to rejoining, the excision site may be exposed to exonuclease degradation, as shown. (C) element reinsertion. The free 3′ OH group at the ends of the transposon may perform a similar attack on the target site DNA as the trans-esterification proposed in hairpin formation. The TPase molecules bound to the transposon could space the 3′ OH groups at a distance that causes them to attack a target on opposite sugar-phosphate backbones at positions separated by 8 bp, as indicated. The 8-bp gaps created are then filled in to create the target-site duplication.

Citation: Kunze R, Weil C. 2002. The and CACTA Superfamilies of Plant Transposons, p 565-610. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch24
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Image of Figure 7.
Figure 7.

CACTA elements. Elements from this family are arranged to maximize the similarities within their coding regions (see text). Terminal-inverted repeats are represented as closed triangles and subterminal repeat regions are stippled. The most consistent similarity is in the crosshatched region corresponding to the gene for the putative TPase in /.

Citation: Kunze R, Weil C. 2002. The and CACTA Superfamilies of Plant Transposons, p 565-610. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch24
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Image of Figure 8.
Figure 8.

Subterminal repeat regions for CACTA elements. Each end of the indicated transposon is shown as a thick arrow representing the TIR and two thin lines. Subterminal repeats are shown as black arrowheads where they match the consensus sequence exactly or where they are mismatched at only one position. Hatched arrowheads indicate sites degenerate by two or more bases. Other shapes represent potential protein binding at the invariant nucleotides within each repeat. The filled shape in front of the arrowhead represents a protein on the face of the helix facing the reader, and the arrowhead in front of the shape represents contact would occur on the opposite face of the helix. Potential interactions between proteins are indicated by filled arcs, and possible interactions with proteins bound to more degenerate sites are indicated by open arcs. The sequences diagrammed are from sequencing results only; no evidence for their movement has been reported.

Citation: Kunze R, Weil C. 2002. The and CACTA Superfamilies of Plant Transposons, p 565-610. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch24
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Image of Figure 9.
Figure 9.

Model for the / transposome complex. TIRs indicated by large filled triangles. Subterminal repeats that make up TNPA binding sites are indicated by smaller filled triangles ( ) and stippled triangles ( ). TNPA molecules are represented as striped ovals, and TNPD molecules are represented as crosshatched boxes bound near the ends of the element.

Citation: Kunze R, Weil C. 2002. The and CACTA Superfamilies of Plant Transposons, p 565-610. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch24
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Image of Figure 10.
Figure 10.

Screening plant populations for insertion mutants by PCR. (A) Primer x within the gene of interest is tested against a primer y specific for the transposon. In theory, only in those samples where a transposon has inserted in or near the gene of interest should a product be possible. (B) Identification of potential candidates involves the use of large pools of samples from randomly transposon-mutagenized populations. By creating a three-dimensional grid of individual samples, pools can be created that will allow the screening of many samples quickly. If a positive result is obtained from pools II, 3, and d in the sample shown, only one plant is common to all three.

Citation: Kunze R, Weil C. 2002. The and CACTA Superfamilies of Plant Transposons, p 565-610. In Craig N, Craigie R, Gellert M, Lambowitz A (ed), Mobile DNA II. ASM Press, Washington, DC. doi: 10.1128/9781555817954.ch24
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