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Corresponding author: Michael Freeling, University of California, Berkeley, Department of Plant and Microbial Biology, 111 Koshland Hall, Berkeley, CA 94720., freeling{at}nature.berkeley.edu (E-mail)
Communicating editor: J. A. BIRCHLER
 | ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Insertions of Mutator transposons into maize genes can generate suppressible alleles. Mu suppression is when, in the absence of Mu activity, the phenotype of a mutant allele reverts to that of its progenitor. Here we present the characterization of five dominant Mu-suppressible alleles of the knox (knotted1-like homeobox) genes liguleless3 and rough sheath1, which exhibit neomorphic phenotypes in the leaves. RNA blot analysis suggests that Mu suppression affects only the neomorphic aspect of the allele, not the wild-type aspect. Additionally, Mu suppression appears to be exerting its effects at the level of transcription or transcript accumulation. We show that truncated transcripts are produced by three alleles, implying a mechanism for Mu suppression of 5' untranslated region insertion alleles distinct from that which has been described previously. Additionally, it is found that Mu suppression can be caused by at least three different types of Mutator elements. Evidence presented here suggests that whether an allele is suppressible or not may depend upon the site of insertion. We cite previous work on the knox gene kn1, and discuss our results in the context of interactions between Mu-encoded products and the inherently negative regulation of neomorphic liguleless3 and rough sheath1 transcription.
THE insertion of transposable elements into genes can have diverse consequences for gene regulation. Transposon-induced alleles, while often thought of as primarily resulting in loss-of-function "knock-outs," actually exhibit a fascinating array of regulatory alterations. These alterations include overexpression or misexpression of the gene, alterations in the start of transcription initiation, as well as commandeering the gene's expression completely through the interaction of trans-acting factors with the inserted element.
Insertions of the retrotransposons gypsy or copia in Drosophila can cause the overexpression of the gene into which they have inserted. Examples of this include the Dominant Hairy-Wing (Hw) alleles at the achaete-scute locus (
A transposon can also usurp entirely the promoter function of the gene into which it has inserted. high chlorophyll flourescence106 (hcf106), is a gene involved in the maize chloroplast electron transport pathway. hcf106::Mu1 is a recessive loss-of-function mutation caused by the insertion of a member of the Mutator (Mu) family of transposable elements (Mu1;
The Mutator system of transposons in maize is made up of at least five nonautonomous elements, all under the control of the system's autonomous regulator MuDR (
The knox genes knotted1, liguleless3, rough sheath1, gnarley1, and liguleless4 were first defined by a series of dominant mutations exhibiting similar, yet distinguishable, phenotypes in the leaf (Fig 1;
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Several of the Mutator-induced liguleless3 (lg3) and rough sheath1 (rs1) alleles identified are Mu suppressible. Mu-suppressible alleles are those alleles whose phenotypes are dependent upon whether they are in a Mu-active or -inactive background. More formally stated, Mu suppression occurs when the phenotype of the Mu-induced allele returns to that of its progenitor in the absence of Mu activity. hcf106::Mu1, discussed earlier, is an example of a Mu-suppressible allele. When Mu is active, hcf106::Mu1 transcripts fail to accumulate, and the plant appears mutant. When Mu is inactive, transcription once again resumes, restoring the phenotype to that of the progenitor (
The mechanism by which Mu activity is able to act as a switch, turning on and off the mutant phenotypes of suppressible alleles, is not well understood. Suppression of hcf106::Mu1 is postulated to be the result of a transcriptional block (
Suppression is found in other systems besides Mutator. Insertions of Suppressor-mutator (Spm), another maize transposable element system, can also result in suppressible alleles. When Spm is active, alleles containing the transposon display the null phenotypes. When Spm is inactive, if the element is inserted with its transcription unit opposite to that of the gene, it can be spliced out, and the mutant phenotype is suppressed (
To better understand the mechanism of Mu suppression, we have characterized five suppressible alleles of lg3 and rs1. These alleles represent insertions into both introns and the 5'UTR of the genes. We have discovered that at least two mechanisms exist for Mu suppression caused by insertions into the 5'UTR, and these are likely to be distinct from how Mu suppression functions in intron insertions. Understanding the molecular basis of Mutator suppression is likely to contribute to our understanding not only of transposon biology, but also to our understanding of the spatial regulation of Lg3 and Rs1. There is evidence that one or more of the knox genes, including rs1, are subject to negative regulation by the MYB transcription factor RS2 (
| MATERIALS AND METHODS |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Genetic stocks:
Lg3-Or331, Lg3-Or422, and Lg3-Or1021 were isolated by J. Fowler in a Lg3-O revertant screen as described in
PCR:
For the determination of Mu insertion sites, the Mu D09242 (5' AGA GAA GCC AAC GCC AWC GCC TCY ATT TCGTC 3') primer was used coupled with either Lg3 R5'-1 (5' CTG GTA TTC TAG TAC GCC 3') for the Lg3 5'UTR insertions, Rs1-U6 (5' TGG AGT TCC TCA AGC GGG TG 3') for Rs1-Or11, or Lg3 cDNA F1 (5' CCC AAC CTC TCT CTC TCC CCC CTAG 3') for Lg3-Or211. Amplification conditions were 94° for 2 min, 35x [94° for 1 min, 60° for 30 sec, 72° for 1 min]. PCR products were electrophoresed, and then purified using the QIAquick gel extraction kit (QIAGEN, Chatsworth, CA). Purified PCR products were then direct sequenced at the University of California, Berkeley DNA sequencing facility using the double-stranded dye termination technique on an ABI sequencer (Applied Biosystems, Foster City, CA). To determine which Mu element was inserted into Rs1-Or11, PCR primers PBO9 (5' CGA TCC CAT CCA GCT TGT CACC 3') and Rs1-U6 were used with the Extend Long Template PCR kit (Roche) according to the manufacturer's instructions, and products were sequenced as described above. Alterations in the regions 3' of the Lg3-Or1021 allele were investigated using the MuDO9242 primer and and Lg3cDNA B1 (5' CGC CTG AAT GCT GCT CAG GAA CGAC 3') primer. Amplification conditions were the same as above, except extension time was increased to 1.5 min.
RT-PCR:
RT-PCR was performed according to
Rapid amplification of cDNA ends (RACE):
RACE reactions were performed according to manufacturer's instructions using the Marathon cDNA amplification kit (Clontech, Palo Alto, CA) with 1 µg poly(A)+ RNA from immature ear tissue and PCR primers Lg3-3' (5' CGC GGG ATC CAG TGG TGT ATG ATT CAG GGT CC 3') and Lg3-D3 (5' GAA GTA GAG TGT CGT CCC AGA AGA CCC ACC 3') as a nested amplification primer.
RNA blot analysis:
Total RNA was isolated from sheath or shoot of ~5-wk-old plants using TRIZOL reagent (Gibco BRL, Gaithersburg, MD) according to manufacturer's instructions. For analysis of rough sheath1 transcript, poly(A)+ RNA was iso-lated on oligo(dT) cellulose columns according to
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DNA gel blot analysis:
Genomic DNA isolation and DNA gel blot analysis were performed according to
| RESULTS |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Suppressible dominant alleles delineate two functions in the mutant; suppression affects only one:
The dominant Rs1 and Lg3 mutations are made up of two components, a wild-type component and a gain-of-function component. It is possible that Mu suppression acts as a general repressor of these genes. This would not be immediately distinguishable, as single mutant loss-of-function phenotypes for either of these genes probably do not exist (R. TYRES and M. FREELING in collaboration with Pioneer Hi-Bred Seed, Inc., unpublished results). Another possibility is that Mu suppression may act exclusively on the dominant ectopic function. To distinguish between these possibilities, we used RNA blot analysis to examine lg3 or rs1 expression in Mu-active, homozygous shoot tissue. In this experiment, because only the dominant allele was present, expression detected in this tissue would indicate that wild-type expression is not affected by suppression. This is precisely what we found (Fig 2). Total RNA from wild-type shoot tissue and shoot tissue from Mu-active, homozygous Lg3-Or331, Lg3-Or422, and Lg3-Or1021 plants was analyzed by RNA gel blot analysis, using the lg3 3'UTR region as a probe (see Fig 5). This region has been found to be unique by sequence comparisons with other knox genes (P. BAUER, unpublished results). While Mu activity is able to suppress the neomorphic leaf phenotype, wild-type expression is unaffected, as assayed by expression in the shoot (Fig 2).
Mu suppression is independent of element type and can result from insertions at multiple sites:
To determine the context within which Mu suppression was functioning in Lg3 and Rs1, we determined where in each of the suppressible alleles the Mutator elements were inserted (Fig 3). We used gene-specific PCR primers coupled with a primer that amplifies from the end of all Mu elements to determine the sites of Mu insertions. We found that the Rs1-Or11 allele was caused by the insertion of a Mu element 154 bp into the third intron. The Lg3-Or211 allele was found to be inserted at the 3' intron/exon junction of the first intron. The Lg3-Or331, Lg3-Or422, and Lg3-Or1021 alleles were found to be caused by Mu insertions into the same site, +29, in the 5'UTR. These results show that Mu suppression can be caused by insertions into a variety of sites.
We found that Mu suppression of Lg3 and Rs1 could be caused by three types of Mu elements. PCR amplification followed by direct sequencing of the Mu element inserted into the Rs1-Or11 allele revealed it to be a deletion derivative of MuDR. The MuDR element undergoes frequent automutagenesis, likely as a result of interrupted double-stranded gap repair (
To determine which Mu elements were inserted into Lg3-Or331, Lg3-Or422, and Lg3–Or1021, plants from families segregating for these alleles were first genotyped by digesting genomic DNA from individual leaf tissue with XbaI and hybridizing with a lg3 5' (see Fig 5) probe, which reveals an ~6.9-kb band that segregates with the mutant phenotype (data not shown). These same blots were then stripped and reprobed with a Mu3-specific probe. This probe hybridized with the same segregating band as the lg3 5' probe did (Fig 4), suggesting that the polymorphism is due to the insertion of a Mu3 element. The same samples were also digested with EcoRI, which cuts once in Mu3 and once in lg3 (Fig 5), and were hybridized with the lg3 5' probe. This resulted in a 1.1-kb band consistent with the insertion of a Mu3 element into the site in the 5'UTR previously determined (data not shown). The element in Lg3-Or1021 is likely a Mu3-like element (Fig 4). This element cross-hybridizes with a Mu3 probe, but is polymorphic within the XbaI fragment containing it. This polymorphism is not due to any gross alterations within the XbaI fragment, EcoRI fragment, or in the region at least 1 kb 3' of the insertion as determined by PCR (data not shown), and is therefore likely to be due to alterations either 5' of the insertion or within the element itself. Each of these elements is in the same orientation, as indicated in Fig 5.
The Lg3-Or331 and Lg3-Or422 alleles are caused by insertions of the same Mu element into the same site in the 5'UTR and are monomorphic at the level of a Southern blot. Thus, it begs the question of whether these alleles represent independent reversion events or repeat isolations of the same event. Mutator mutagenesis for the screen that produced these revertant alleles occurred in the male parent, so a reversion event that takes place prior to meiosis I in the pollen cell lineage could result in a number of plants heterozygous for the same reversion event (
+90, while Lg3-Or422 has a slightly different deletion spanning +145 +96. Additionally, Lg3-Or211, which contains an insertion into the end of the first intron, is missing +140 +90. The deletions are not linked with suppressibility, however, because the nonsuppressible Lg3-Or81 allele also has a deletion from base pairs +140 +90. One possible mechanism for these strange incidences would be if each allele underwent a Mutator excision followed by exonuclease cleavage, followed by a subsequent reinsertion into either the intron or 5'UTR. Alternatively, the region in the 5'UTR where these deletions occurred is highly G + C rich and contains numerous direct repeats; therefore, it is possible that these deletions arose from strand slippage during replication.
Mu activity abolishes ectopic transcript accumulation resulting in a mutant plant appearing indistinguishable from wild type:
Each of the suppressible lg3 and rs1 alleles discussed here appears identical to wild type when they are in a Mutator-active background. The mutant phenotype manifests itself only when Mu is inactive. We wanted to know whether this was due to an absence of ectopic transcripts or whether Mu activity was acting post-transcriptionally. To investigate this, we used RNA blot analysis to examine RNA accumulation in sheath tissue of Mu-active heterozygous plants, using the lg3 3'UTR as a probe (Fig 5). RNA blot analysis indicated that for each of the alleles, when Mu was active and the plants appeared wild type, transcripts failed to accumulate (data not shown) as shown for the Lg3-Or211 allele (Fig 6). These results suggest that suppression is operating at the level of transcription. Because we did not perform transcription run-on assays, it remains possible that transcripts are initiated but are unstable.
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Suppressible intronic insertions mediate normal transcription from a distance:
Previous work on Mu suppression of hcf106 had shown that Mu is able to function as an outward-reading promoter (
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Lg3-Or331, Lg3-Or422, and Lg3–Or1021 produce altered transcripts:
Lg3-Or331, Lg3-Or422, and Lg3–Or1021 are caused by insertions into the 5'UTR, so we thought these alleles might be likely candidates for using Mu as an outward-reading promoter. Instead, we found that when Mu is inactive, these alleles produce a transcript that is significantly shorter than that of wild type (Fig 8A). These transcripts appear too short to be explained by transcripts initiating from the end of the inserted element. These truncated transcripts are seen ectopically expressed in the leaf, as well as where lg3 is normally expressed in shoot meristematic tissue. Transcripts identical in size were also detected associated with the Lg3-Or331 allele (data not shown). To characterize these transcripts further, we made a RACE library using tissue from Mu-inactive, homozygous Lg3-Or422 immature ears. From this library, we cloned the cDNA corresponding to Lg3-Or422 transcript, and found it to start 187 bp downstream of the inserted element (Fig 8B), a truncation of the transcript that is in the range predicted by the size discrepancy seen on the RNA blot.
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To further support our finding that the 5' region of these transcripts was altered, we performed RT-PCR using gene-specific primers, one of which primed off of sequences contained within the region we believe to be absent in transcripts from these altered alleles. We prepared cDNA from wild-type sheath, which is not expected to ectopically express lg3, as a negative control, and wild-type shoot as a positive control. We used ubiquitin primers to ensure the integrity of the template as well as lg3 gene-specific primers that span an intron to verify template source. The lg3 primers were determined to be gene specific for this RT-PCR assay by sequence comparison with the other knox genes. Using this assay, we found that while we successfully amplified a band of the expected size from wild-type shoot, no product is seen using cDNA from Lg3-Or422/+ Mu-inactive sheath tissue, consistent with the deletion of the region that includes the binding site for the 5' PCR primer (Fig 8C). In summary, three lg3 alleles caused by Mu insertions into the 5'UTR repress ectopic transcription in the presence of Mu activity. When Mu is inactive, they exhibit a normal expression pattern, although they are associated with truncated transcripts.
| DISCUSSION |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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We have presented the characterization of the Mutator-suppressible Liguleless3-0 and Rough Sheath1-0 alleles: Lg3-Or331, Lg3-Or422, Lg3-Or1021, Lg3-Or211, and Rs1-Or11. These alleles represent Mutator insertions into introns as well as into the 5'UTR. Analysis of the 5'UTR insertions suggests an additional mechanism for Mu suppression of 5' insertions distinct from that described for hcf106 (
We have found that suppressible alleles can be caused by three types of Mutator elements: Mu1, Mu3, and MuDR. Based upon work by Greene and co-workers that describes suppressible knotted1 alleles caused by Mu1 insertions in both orientations (
The suppressible intron insertions we describe (Lg3-Or211 and Rs1-Or11) both produce a wild-type size transcript when Mu is inactive. These results support the idea that transcription through Mutator transposons is not the limiting factor affecting insertion alleles. It has been found that some Mutator insertions into introns can be spliced out along with surrounding sequences (
When Mu is inactive, the Lg3-Or331, Lg3-Or422, and Lg3-Or1021 5'UTR insertion alleles produce a transcript that initiates 216 bp downstream of the normal site and 187 bp downstream of the inserted Mu element. Our results show that when Mu is off, the Mu element appears to redirect the start of transcription, although we cannot formally exclude the possibility that the effect is post-transcriptional. A similar example of transposon-induced alteration of transcription initiation has been found in Antirrhinum majus (snapdragons) at the Tam1-induced allele niv-5311 (
So how is it that some Mu insertions result in suppressible alleles while others do not? Any model that attempts to explain Mu suppression of these alleles must take into account that the lg3- and rs1-suppressible alleles were identified as revertants of their reference alleles, Lg3-O and Rs1-O, which are both gain-of-function mutations with as yet undescribed lesions.
Our results, taken with evidence from work on knotted1 suppressible alleles (
Another possibility is that Mu insertions into critical sites of Lg3-O or Rs1-O could function, in an activity-dependent manner, to recruit novel silencing complexes "seeded" by the transposon-encoded proteins, to quench the dominant phenotype. It has been shown in Drosophila that Dorsal-mediated repression at the ventral silencer requires the formation of a multiprotein complex (
We have considerable evidence that at least three class I knox genes, including rs1 and lg3, are under negative regulation. rough sheath2, which encodes a member of the MYB family of transcription factors, has been found to negatively regulate lg3, rs1, and kn1 (
Other plant gene introns have been found also to contain regulatory sites. Insertion of a Tam3 element into the intron of plena in Antirrhinum, the homolog of AGAMOUS in Arabadopsis, results in a gain-of-function ovulata phenotype in which sterile floral organs are replaced by sex organs due to ectopic expression of plena (
While our work does not implicate directly a molecular mechanism that describes Mu suppression of Lg3-O and Rs1-O ectopic transcription, it does set constraints upon the contributing factors. The variety of effects that transposons can have on the genes they insert into is still not completely understood. The absence of a clearly understood mechanism for Mu suppression has not, however, prevented it from being utilized as a genetic tool. Mu suppression has been used successfully to turn genes on and off in marked sectors at various developmental times (
| FOOTNOTES |
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1 Present address: California Institute of Technology, Division of Biology 156-29, Pasadena, CA 91125. 
| ACKNOWLEDGMENTS |
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We thank David Braun and Albert Erives for critically reading the manuscript and Sarah Hake for helping us interpret some of the data. We also thank Richard Schneeberger for the Rs1-Or11 pictures in Fig 1. The authors also thank Gary Muehlbauer, Richard Schneeberger, and Petra Bauer for contributory discussions and stocks, Randall Tyers for PCR technical advice, and Barbara Kloeckner-Gruissem for her invaluable consultations. This work was supported by National Science Foundation grant no. MCB 9603119 to M.F.
Manuscript received August 24, 1999; Accepted for publication September 28, 1999.
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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B. Shen, C. Li, Z. Min, R. B. Meeley, M. C. Tarczynski, and O.-A. Olsen sal1 determines the number of aleurone cell layers in maize endosperm and encodes a class E vacuolar sorting protein PNAS, May 27, 2003; 100(11): 6552 - 6557. [Abstract] [Full Text] [PDF]
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X. Cui, A.-P. Hsia, F. Liu, D. A. Ashlock, R. P. Wise, and P. S. Schnable Alternative Transcription Initiation Sites and Polyadenylation Sites Are Recruited During Mu Suppression at the rf2a Locus of Maize Genetics, February 1, 2003; 163(2): 685 - 698. [Abstract] [Full Text] [PDF]
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