Mutator and MULE Transposons

The MuDR transposon. (A) The structure of MuDR. 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 mudrB 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 mudrA and mudrB 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.

Structural features of nonautonomous Mutator 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. Mu1 and Mu1.7: (1) GRMZM2G117007, 94% identical (unknown function). Mu3: (2) GRMZM2G015352 (unknown function), 97% identical. (3) GRMZM2G542994 (putative mago nashi, protein), 94% identical. Mu4: (4) GRMZM2G177883 (putative receptor-like protein kinase 5 precursor), 97% identical. (5) GRMZM2G037164 (unknown function), 96% identical. Mu7: (6) GRMZM2G022945 (BRCA1 C Terminus domain containing protein), 98% identical. Mu8: (7) GRMZM2G315375 (P-glycoprotein 1), 99% identical. Mu13: (8) GRMZM2G317614 (putative nucleotide binding protein), 96% identical. Mu14: (9) GRMZM2G010000 (putative heat shock protein binding protein), 90% identical. (10) GRMZM2G120085 (subtilisin-like protease precursor), 94% identical. Mu15: (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. Mu16: (14) GRMZM2G001934 (putative receptor protein kinase TMK1 precursor), 95% identical. Mu17: (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.

Examples of somatic excision of Mu1 from a1-mum2 in the seed (A), the sheath (B) and the anthers (C). Note that in each case, reversion events are uniformly late.

A model explaining the differences between late somatic and germinal Mutator element transposition. (A) In all tissues, Mutator 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.

A striking example of a position effect on the capacity for a MuDR element to cause somatic excision of a reporter element. (A) Somatic excisions caused by MuDR(p1) (left) and MuDR(p3) (right). (B) An example of likely transposition of MuDR(p3) during somatic development, resulting in a kernel sector with an increased level of somatic excision. (C) A rare ear sector in which MuDR(p3) has undergone a duplication during development, resulting in an ear sector in which MuDR(p3) and transposed copies of MuDR(p3) segregate. (D) Southern blot analysis of more typical, single kernel MuDR(p3) duplication events. Weakly spotted, pale and heavily spotted kernels were picked from a single ear and their DNA was examined for evidence of MuDR transposition. Analysis of the weakly spotted and pale kernels show that segregation of MuDR(p3) 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 MuDR(p3) and a transposed copy were present, while in others, only the transposed copy is available, suggesting that these transposition events occurred prior to meiosis.

Mu killer. (A) The Mu killer (Muk) locus. Mu killer is a rearranged MuDR element, derived from the single MuDR present in the minimal line [MuDR(p1)]. The rearrangement that gave rise to Muk 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 MuDR 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 Muk relative to a MuDR element. (C) The effect of Muk on MuDR in the first generation after a plant carrying Muk is crossed to a plant carrying MuDR. Heavily spotted kernels are those that inherit only MuDR. Weakly spotted kernels are those that carry both MuDR and Muk. Pale kernels lack MuDR.

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.

An illustration of the diversity of MULEs 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.