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Chapter 36 : and Transposons

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Abstract:

A distinguishing feature of transposable elements (TEs) is their propensity to induce mutations. Among the most mutagenic of all TEs are the elements of maize. Lines carrying large numbers of these elements can exhibit mutation frequencies 50 to 100 times that of background ( ). This is due to a very high transposition frequency, which can exceed one new insertion per element per generation ( ), as well as a propensity to insert into or near genes ( ). Because they are so mutagenic, elements have been very useful in both forward and reverse genetic screens in maize and recent high-throughput methodologies have only made the system more so ( ). However, in addition to its utility, the system has also provided important clues as to the consequences of unrestrained TE activity, and the means by which active TEs are controlled by their host. This chapter will provide a review of the biology, regulation, evolution and uses of this remarkable transposon system, with an emphasis on recent developments in our understanding of the ways in which this TE system is recognized and epigenetically silenced.

Citation: Lisch D. 2015. and Transposons, p 803-828. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0032-2014
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Image of Figure 1
Figure 1

The transposon. (A) The structure of . Terminal inverted repeats (TIRs) at either end of the element are designated TIRA and TIRB. The two transcripts are indicated above and below. Exons are depicted as boxes. Introns are depicted as thin black lines. The third intron of is only infrequently spliced out. Domains identified within the MURA protein are as indicated. (B) The sequence of TIRA (top) and TIRB (bottom). The TIR sequences shows where the transposase binds and where and transcription are initiated are as shown. Note that TIRA and TIRB are identical for the first 158 nucleotides of each TIR. Differences between TIRA and TIRB are indicated by boxed residues.

Citation: Lisch D. 2015. and Transposons, p 803-828. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0032-2014
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Image of Figure 2
Figure 2

Structural features of nonautonomous elements in maize. Black triangles represent terminal inverted repeat (TIR) sequences. Shaded boxes represent captured host sequences, with each independent sequence indicated by a number. The cognate host genes are indicated here, along with the percent identity between the captured sequence and the host gene. and : (1) GRMZM2G117007, 94% identical (unknown function). : (2) GRMZM2G015352 (unknown function), 97% identical. (3) GRMZM2G542994 (putative mago nashi, protein), 94% identical. : (4) GRMZM2G177883 (putative receptor-like protein kinase 5 precursor), 97% identical. (5) GRMZM2G037164 (unknown function), 96% identical. : (6) GRMZM2G022945 (BRCA1 C Terminus domain containing protein), 98% identical. : (7) GRMZM2G315375 (P-glycoprotein 1), 99% identical. : (8) GRMZM2G317614 (putative nucleotide binding protein), 96% identical. : (9) GRMZM2G010000 (putative heat shock protein binding protein), 90% identical. (10) GRMZM2G120085 (subtilisin-like protease precursor), 94% identical. : (11) GRMZM2G181219 (unknown function), 96% identical. (12) AC196090.3 (putative xylem serine proteinase 1 precursor), 95% identical. (13) AC234154.1 (putative phospholipase A1), 95% identical. : (14) GRMZM2G001934 (putative receptor protein kinase TMK1 precursor), 95% identical. : (15) GRMZM2G029979 (TGACG-sequence-specific DNA-binding protein TGA-2), 97% identical (16) GRMZM2G331374 (unknown function), 100% identical (17) GRMZM2G148831 (unknown function), 97% identical. (18) GRMZM2G055809 (unknown function), 95% identical. (19) GRMZM2G126413 (VQ motif family protein), 87% identical. (20) GRMZM2G081406 (putative auxin response factor), 96% identical. (21) GRMZM2G152432 (putative calmodulin), 97% identical. (22) GRMZM2G106401 (putative xylem serine proteinase 1 precursor ), 96% identical. (23) GRMZM2G116908 (unknown fuction), 96% identical.

Citation: Lisch D. 2015. and Transposons, p 803-828. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0032-2014
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Figure 3

Examples of somatic excision of from in the seed (A), the sheath (B) and the anthers (C). Note that in each case, reversion events are uniformly late.

Citation: Lisch D. 2015. and Transposons, p 803-828. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0032-2014
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Figure 4

A model explaining the differences between late somatic and germinal element transposition. (A) In all tissues, element excision produces a double-stranded gap. What is hypothesized to vary is how that gap is repaired. (B) In germinal (and early somatic) lineages the gap is repaired using the sister chromatid, which requires that excision occurs primarily after DNA synthesis. Occasional strand slippage, mediated by short stretches of sequence homology, can result in deletions within the element. (C) In contrast, during the last few rounds of cell division in somatic tissue, the double-stranded gap is repaired using nonhomologous end joining, resulting in a characteristic set of “footprints.” In each case, the excised element can insert at a new location, but in the germinal lineage, sister-chromatid-mediated repair restores an element at the original position.

Citation: Lisch D. 2015. and Transposons, p 803-828. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0032-2014
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Figure 5

A striking example of a position effect on the capacity for a element to cause somatic excision of a reporter element. (A) Somatic excisions caused by (left) and (right). (B) An example of likely transposition of during somatic development, resulting in a kernel sector with an increased level of somatic excision. (C) A rare ear sector in which has undergone a duplication during development, resulting in an ear sector in which and transposed copies of segregate. (D) Southern blot analysis of more typical, single kernel duplication events. Weakly spotted, pale and heavily spotted kernels were picked from a single ear and their DNA was examined for evidence of transposition. Analysis of the weakly spotted and pale kernels show that segregation of correlates with the weak spotting phenotype. Analysis of the heavily spotted kernels shows that in each case, a new fragment, consistent with a transposition event, appeared. Note that in some cases both and a transposed copy were present, while in others, only the transposed copy is available, suggesting that these transposition events occurred prior to meiosis.

Citation: Lisch D. 2015. and Transposons, p 803-828. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0032-2014
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Figure 6

. (A) The () locus. is a rearranged element, derived from the single present in the minimal line []. The rearrangement that gave rise to also caused the complet deletion of one gene and the deletion of portions of two other genes, as well as a duplication and inversion of a portion of the 5′ end of the element. Triangles represent the TIR. Boxes represent coding sequences. Transcriptional start sites for genes are as indicated. (B) The structure of the hairpin transcript derived from relative to a element. (C) The effect of on in the first generation after a plant carrying is crossed to a plant carrying . Heavily spotted kernels are those that inherit only . Weakly spotted kernels are those that carry both and . Pale kernels lack .

Citation: Lisch D. 2015. and Transposons, p 803-828. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0032-2014
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Figure 7

Maize development. (A) An illustration of the major components of an adult maize plant. Leaves are produced sequentially as the maize plant develops, with juvenile and adult leaves being distinguished by presence of epicuticular wax (a juvenile trait) and epidermal hairs (an adult trait). Transition leaves have patches of tissue with either adult or juvenile traits. Ears and tassels are only produced once adult leaves are produced. Each maize plant can be crossed as a male, or a female, or to itself. (B) A cartoon of a maize seed, showing the location of the embryo, endosperm (a terminally differentiated nutritive tissue), and the aleurone, which is the outer cell layer of the endosperm that is competent to express color. (C) A cartoon of a mature pollen grain, which contains three nuclei. The vegetative nucleus is responsible for the development of the pollen tube, and will not contribute to the next generation. Of the two sperm cells, one will fertilize the two polar nuclei to give rise to the triploid endosperm, and one of which will fertilize the egg cell to give rise to the embryo. In each part of the plant illustrated here, tissues and cells in which a relaxation of TE silencing has been observed are indicated by red asterisks.

Citation: Lisch D. 2015. and Transposons, p 803-828. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0032-2014
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Figure 8

An illustration of the diversity of in a wide variety of species. In each case, triangles represent TIRs of various lengths. Boxes represent putative coding sequences. Black boxes represent putative transposases. All models are to scale. Names marked with one asterisks indicate elements that have been shown to be mobile. Those with two asterisks have been demonstrated to be autonomous.

Citation: Lisch D. 2015. and Transposons, p 803-828. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0032-2014
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