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First published online January 17, 2003; 10.1105/tpc.008375 American Society of Plant Biologists The Maize Genome Contains a Helitron Insertion
a Program in Plant Molecular and Cellular Biology and Horticultural Sciences, University of Florida, Gainesville, Florida 32611-0690 3 To whom correspondence should be addressed. E-mail hannah{at}mail.ifas.ufl.edu; fax 352-392-6957
The maize mutation sh2-7527 was isolated in a conventional maize breeding program in the 1970s. Although the mutant contains foreign sequences within the gene, the mutation is not attributable to an interchromosomal exchange or to a chromosomal inversion. Hence, the mutation was caused by an insertion. Sequences at the two Sh2 borders have not been scrambled or mutated, suggesting that the insertion is not caused by a catastrophic reshuffling of the maize genome. The insertion is large, at least 12 kb, and is highly repetitive in maize. As judged by hybridization, sorghum contains only one or a few copies of the element, whereas no hybridization was seen to the Arabidopsis genome. The insertion acts from a distance to alter the splicing of the sh2 pre-mRNA. Three distinct intron-bearing maize genes were found in the insertion. Of most significance, the insertion bears striking similarity to the recently described DNA helicase–bearing transposable elements termed Helitrons. Like Helitrons, the inserted sequence of sh2-7527 is large, lacks terminal repeats, does not duplicate host sequences, and was inserted between a host dinucleotide AT. Like Helitrons, the maize element contains 5' TC and 3' CTRR termini as well as two short palindromic sequences near the 3' terminus that potentially can form a 20-bp hairpin. Although the maize element lacks sequence information for a DNA helicase, it does contain four exons with similarity to a plant DEAD box RNA helicase. A second Helitron insertion was found in the maize genomic database. These data strongly suggest an active Helitron in the present-day maize genome.
Transposable elements are entities that move within the genome (McClintock, 1949  , 1965). Phenotypically, they are recognized when they integrate into functional genes. Mutations associated with such insertions often are unstable, and the excision of the element can restore gene function. Historically, transposable elements were classified into two groups based on their structure and mechanistic mode of propagation. One group, represented by the classic maize transposable elements, have terminal inverted repeats, duplicate host sequences upon integration, and transpose via DNA (Engels, 1983; Fedoroff, 1989). These elements usually leave characteristic footprints after excision (Doring and Starlinger, 1986; Nevers et al., 1986; Jin and Bennetzen, 1989; Singer et al., 1993; Giroux et al., 1996; Kunze et al., 1997). The second group, the retroelements, move through an RNA copy, are related to retroviruses, and include long-terminal repeat and non-long-terminal repeat retrotransposons (Wessler et al., 1995). Long-terminal repeat retrotransposons possess long terminal repeats and encode all of the proteins required for transposition (Boeke and Corces, 1989; Grandbastien, 1992). Despite their diversity, these two classes of transposable elements share two common features. Both make duplications of host sequences upon entry, and the 3' end of the insertion is either a duplicate of the 5' terminus or a copy of a poly(A) tail.
Recently, a fundamentally different class of transposable elements, termed Helitrons, was proposed in eukaryotes (Feschotte and Wessler, 2001
Helitrons are quite large, ranging from
Like other transposable elements, Helitrons may be powerful tools for gene and genome expansion. They frequently capture cellular genes and multiply them during their journey through the genome. Furthermore, it is proposed that the transduced cellular genes that do not contribute to the replication of the Helitrons are destroyed by multiple mutations, whereas genes that provide selective advantage to the transposon are retained. These would exhibit obvious sequence similarity to their genes of origin (Kapitonov and Jurka, 2001
Many important questions remain to be answered concerning Helitron elements. How widespread are Helitrons, and do they all use the same cellular machinery for transposition? Most importantly, direct proof that these sequences are transposable elements has yet to be provided. Helitrons reported to date have been identified via computer-assisted reconstruction and are thought to have been "active in recent evolutionary history" (Kapitonov and Jurka, 2001
Here, we report a maize mutation that likely occurred in very recent times that has virtually all of the hallmarks of a Helitron. This mutation, sh2-7527, arose spontaneously in a conventional maize breeding program within the shrunken2 (Sh2) gene of maize. The locus encodes the large subunit of ADP-Glc pyrophosphorylase, a key regulatory enzyme in the starch biosynthetic pathway (Giroux et al., 1996
Transcripts of sh2-7527 Differ by Alternative Splicing within Sh2 and Contain Non-Sh2 Sequences Previous RNA gel blot analysis demonstrated that the mutant sh2-7527 produced at least two abundant transcripts: one larger and one smaller than the wild-type transcript (Giroux and Hannah, 1994 ). DNA gel blot analysis of the mutant genomic DNA suggested an insertion or rearrangement at the sh2 locus (data not shown). To further characterize sh2-7527, total RNA from mutant and wild-type developing endosperms was electrophoresed, blotted, and probed with different segments of the Sh2 cDNA. The full-length Sh2 cDNA hybridized to four transcripts of  1.8, 2.4, 3.5, and 5.5 kb in the mutant and to a single 2.2-kb transcript in the wild type (Figure 1A). A Sh2 cDNA probe containing exons 12 to 16 did not hybridize to any mutant transcripts (data not shown).
To elucidate the nature of the sh2-7527 mutation and resulting transcripts, cDNA and genomic libraries were constructed from the mutant and screened with a full-length Sh2 cDNA. Sequence analysis of 28 resulting cDNA clones identified two classes of Sh2 transcripts (Figure 1E). The two classes, consisting of 12 and 16 members, differed only by the presence or absence of Sh2 intron 9. In addition, an extraneous 1.2-kb sequence, not of Sh2 origin, was positioned exactly at the 3' terminus of exon 11 in all 28 clones. This sequence then terminated with a poly(A) tail. Based on the wild-type Sh2 sequence and the sh2-7527 foreign cDNA insertion, the calculated lengths of these clones (2372 and 2440 bp) likely correspond to that of the 2.4-kb mutant transcript doublet shown in Figure 1A. When the 3' non-Sh2 sequence was used as a probe on RNA gel blots, a single transcript of low abundance was detected in wild-type RNA (Figure 1B). Some but not all of the non-Sh2 sequences isolated from the mutant cDNAs are highly repetitive in the maize genome, as judged by genomic DNA gel blot analysis (Figure 1C). When the 3' segment of the insertion isolated from a genomic clone was used as a probe, only one or two hybridizing fragments were detected in both mutant and wild-type genomic DNA (Figure 1D).
The Extraneous Sequence Is Spliced into the sh2-7527 Transcript from an Insertion Located within Intron 11 of Sh2 Sequencing of 6.87 kb from the 5' end and 3.88 kb from the 3' terminus of the insertion identified the placement of the insertion within Sh2. The insertion lies within intron 11; hence, the covalent attachment of the inserted sequences to Sh2 exon 11 of the mutant transcript comes about by pre-mRNA splicing. The insertion lies within the dinucleotide AT 139 bp from the 5' terminus of Sh2 intron 11, starts with 5' TC, ends with 3' CTAG, and contains two short palindromic sequences near its 3' terminus. These features give it the potential of forming a 20-bp hairpin (Figure 2).
The Removal of Introns from Mosaic Sh2-Insertion Pre-mRNA Follows Conventional Rules of RNA Splicing Comparison of the insertion's genomic sequence with the processed Sh2 mosaic transcript identified 12 exons. Splicing follows conventional rules for nuclear genes (Simpson and Filipowicz, 1996 ). With one exception, all introns begin with GT and end with AG. The last intron begins with GC. A GC donor site occurs in 0.5% of Arabidopsis introns (Simpson et al., 1993; Korning et al., 1996).
Some introns of the insertion are large, and the 1.2-kb mature sequence in the chimeric Sh2 transcript is spread over a 6.5-kb genomic fragment (Figure 3A). The first intron, separating exon 11 of Sh2 and the first exon of the insertion, is 2388 bp and contains an
The Insertion in sh2-7527 Alters Sh2 Splicing from a Distance The complexity of the pre-mRNA splicing process is made evident by the splicing pattern of sh2-7527. Although the insertion lies in intron 11 and sequences from exons 7 to 11 are wild type, intron 9 is excised from only approximately half of the mature transcripts, even though the closer intron 10 is removed faithfully in these transcripts. Whether other mutant transcripts noted on RNA gel blots represent additional distortions in splicing is unknown, because clones that correspond to them were not isolated. Although not common, mutations that affect the splicing of distant introns have been described in vertebrates and plants (McNellis et al., 1994 ; Marillonnet and Wessler, 1997; Lal et al., 1999b).
The parameters underlying this complexity are unknown. Possibly, the insertion-induced change in the environment surrounding intron 9 is causal, as is the case with the splicing of the transposable element Ds (Lal and Hannah, 1999
The sh2-7527 Insertion Contains Putative Pseudogenes
The concatenation of apparently unrelated ORFs and the lack of similarity over the entire lengths of the corresponding proteins suggest that the sh2-7527 insertion encodes either highly diverged proteins or pseudogenes. To investigate these possibilities more closely, we determined significantly matching ESTs by spliced alignment using the GeneSeqer World Wide Web service (http://bioinformatics.iastate.edu/cgi-bin/gs.cgi) (Usuka et al., 2000
The EST spliced alignment revealed an additional potential exon 5' to exon 1 in the insertion (Figure 3B). Spliced alignment with the Arabidopsis RNA helicase encoded by At4g00660 using the SplicePredictor World Wide Web service (http://bioinformatics.iastate.edu/cgi-bin/sp.cgi) (Usuka and Brendel, 2000 ) suggests that this exon is part of a predicted pseudogene with similarity to a maize RNA helicase. The alignment is shown in Figure 5. Although the similarity at the amino acid level is highly significant, multiple nonsense mutations and frameshift-inducing small insertions clearly identify this segment as a remnant of an RNA helicase–encoding gene that no longer encodes a full-length protein. Alignment of the sorting nexin protein to the distal exons displays a similar pattern of nonsense mutations and insertions/deletions (data not shown).
In contrast to vertebrates and yeast, the U content of plant introns is much higher than that of their flanking exons (Brendel et al., 1998 ). This difference has been implicated in defining splice sites (Goodall and Filipowicz, 1989; Simpson and Brown, 1993; Luehrsen and Walbot, 1994; Brown and Simpson, 1998). As noted, the first exon of the RNA helicase gene predicted by EST and protein evidence is retained in the mutant intron and is not spliced from the primary transcript. We postulate that the change in the strategic location of this exon in the context of the Sh2 sequence interferes with its recognition, leading to exon skipping. Exon skipping was demonstrated recently in two mutants of maize and several mutants of Arabidopsis (Brown, 1996; Brown and Simpson, 1998; Simpson et al., 1998; Lal et al., 1999a, 1999b). The 3' sequenced part of the sh2-7527 insertion has similarity to several ESTs (http://gremlin1.zool.iastate.edu/~volker/v3html/). A three-exon structure close to the 3' end (Figure 3A) shows significant similarity to the Arabidopsis protein At1g04010 of unknown function.
The Foreign Sequence within Sh2 Is Attributable to an Insertion and Not to a Chromosomal Rearrangement PCR primers for each of the two Sh2–foreign insertion borders were used to analyze genomic DNA from each of 16 plants derived from mutant seeds of the cross described above. Both borders were found in all plants. We conclude that viable duplication-deficient gametes do not occur and that the sh2-7527 mutant is not the result of an interchromosomal rearrangement.
Next, we determined whether an intrachromosomal rearrangement gave rise to sh2-7527. Intrachromosomal exchanges could have occurred in either the direct or the inverted orientation. In the first case, the centromere distal portion of Sh2 would be placed on an acentric chromosomal ring, whereas the centromere proximal portion of Sh2 would remain on chromosome 3. Chromosomal rings are mitotically unstable and are maintained only by selection (McClintock, 1938 The hypothesis that an intrachromosomal rearrangement involving a nonhomologous exchange in the inverted orientation gave rise to sh2-7527 also was tested. In this case, all of chromosome 3 remains attached to the centromere. The sequence between the two breakpoints would be inverted, and the distal portion of Sh2 would not be lost. In this scenario, the two sequences abutting Sh2 would lie adjacent to each other before the rearrangement event occurred. As a direct test, primers complementary to the two borders were used in PCR experiments with wild-type DNA. If an inversion were causal, a PCR product of 532 bp would be predicted. An amplified product was not produced. We conclude that the foreign sequence within Sh2 is attributable to an insertion and not to a chromosomal rearrangement.
Finally, we note that the wild-type Sh2 sequences, albeit divided, remained unaltered in this mutant. Chromosomal rearrangements involving the rejoining of nonhomologous breaks in plant DNA normally are associated with the loss of sequences at the breakpoints or with the addition of filler DNA (Gorbunova and Levy, 1997
The sh2-7527 Insertion Is Not a Repetitive Sequence in Closely Related Sorghum
The Maize Mutation sh2-7527 Most Likely Was Caused by a Helitron Recently, a novel family of eukaryotic transposable elements, termed Helitrons, was discovered by computer-assisted genome analysis (Kapitonov and Jurka, 2001 ). Helitrons presumably transpose through a mechanism that is fundamentally different from those of other eukaryotic transposable elements and involves catalysis by a DNA helicase. Because the structures of these recently identified elements are based on inactive copies, it is unknown whether an active autonomous element exists in a modern genome. If Helitrons are active in present-day genomes, then one would expect to observe movement of a Helitron into sequences known to lack the element. Analysis of the maize mutant sh2-7527 strongly suggests that Helitrons are present and active in the modern maize genome. Like Helitrons, the insert of sh2-7527 is large, lacks terminal repeats, does not duplicate host sequences, was inserted within a host AT dinucleotide, contains 5' TC and 3' CTRR termini, and contains two palindromic sequences at its 3' terminus. We suggest that Helitrons are functional in the modern maize genome. A search of maize sequences identified the presence of another Helitron element. This element resides in BAC clone gi:(gi|13606087|gb| AF090447.2| AF090447) and is 17,749 bp in length, starting at position 4408 and ending at position 22,158. It bears sequence similarity to the sh2-7527 element only in the last 20 bp of each terminus. Twelve pseudogenes are located randomly throughout its length. Five of the 12 genes are composed of more than one exon. Based on a comparison of the insertion site with maize ESTs, this Helitron insertion lies in an active gene within a host AT dinucleotide.
The Helitron insertion of sh2-7527 contains many features typical of transposable elements. It is highly repetitive in its host genome but has only single/low copy numbers in the close relative sorghum. Second, it apparently collects host sequences, as was noted with the second maize Helitron element described above. Sequence analysis of the 5' and 3' regions of the sh2-7527 insertion revealed similarity to three distinct intron-bearing maize genes. The capture and movement of cellular genes by retroelements are well documented in vertebrates and to some extent in plants. For instance,
The presence of sequences similar to part of an RNA helicase rather than a DNA helicase gene in this maize element raises a number of interesting possibilities. At present, we do not know whether it is a remnant of a cellular gene captured by the element or whether the complete RNA helicase gene in an autonomous Helitron element plays a role in transposition. RNA helicase activity has been invoked in many functions, including RNA unwinding, RNA splicing, RNA editing, translation initiation, and rRNA processing (Luking et al., 1998
As noted, the sh2-7527 Helitron element contains sequences similar to coding sequences of a sorting nexin. This family of proteins is involved in intracellular vesicle protein trafficking (Haft et al., 1998
We also note that some of the structural features of the sh2-7527 insertion resemble those of the Y' family of repeated DNA elements in yeast. Like the sh2-7527 insertion, these elements lack direct repeats, and unlike known class 1 and 2 transposable elements, they appear to move via recombination. Of most significance, a Y' ORF encodes an RNA helicase that presumably is required for its maintenance (Louis and Haber, 1992
The Capture of Genes by Transposable Elements Likely Plays an Important Role in Evolution
Plant Material Maize (Zea mays) plants were grown in the field or in the greenhouse at the University of Florida. The mutant sh2-7527, kindly provided by the late Oliver Nelson (University of Wisconsin, Madison), was described previously (Giroux and Hannah, 1994 ). The wild-type Sh2 allele used in this study was isolated originally from McClintock's a1-m3 stock (Giroux et al., 1996).
Construction and Screening of Genomic and cDNA Libraries
A cDNA library was constructed from RNA extracted from sh2-7527 endosperms at 20 days after pollination using a cDNA synthesis kit (
RNA Isolation and RNA Gel Blot Analysis
Genomic DNA Isolation and DNA Gel Blot Analysis
PCR Amplification of the sh2-7527 Sequence Upon request, all novel materials described in this article will be made available in a timely manner for noncommercial research purposes.
Accession Numbers
We thank Tom Peterson, Don McCarty, and Rob Ferl for helpful comments. We thank Maureen Clancy for assistance with manuscript preparation and Gabrielle Stryker for her help with the figures. This research was supported by National Science Foundation Grants IBN-9316887 and MCB-9420422 and U.S. Department of Agriculture Competitive Grants 94-37300-453, 97-36306-4461, 95-37301-2080, and 98-01006. This is Florida Agricultural Experiment Station Journal Series No. R-07881.
Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.008375.
1 Current address: Department of Biological Sciences, Oakland University, Rochester, MI 48309-4401.
2 Current address: Plant Science and Plant Pathology, Montana State University, Bozeman, MT 50717-3150. Received October 7, 2002; accepted November 11, 2002.
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Abstract
INTRODUCTION
library was screened with a full-length Sh2 cDNA clone. Although clones containing the two Sh2-insertion borders were isolated, we were unable to isolate single or overlapping clones that contained the entire insertion. 
