Gene movement by Helitron transposons contributes to the haplotype variability of maize

Abstract

(1, 2), a line that had been used extensively in genetic analyses, with that of the unrelated standard inbred B73 (3) revealed unexpected differences between them. First, retrotransposon clusters, which make up the bulk of the maize genome (4-6), differed in composition and location relative to the genes in the region so that the two sequences could be aligned only at the genes they had in common. Second, and most strikingly, some genes present in McC were absent from B73, indicating that genetic colinearity was violated within the species. Noncolinear haplotypes were also found in a comparison of the genomic intervals containing the z1C zein gene cluster in B73 and BSSS53, inbred lines derived from the same synthetic population (7). The lengths of the z1C regions in the two inbreds varied by 50% because of differences in the number of zein and other genes and in the sizes of the retrotransposon clusters flanking them. Similar extensive nonhomologies were reported between the allelic regions of inbreds B73 and Mo17 at three additional chromosomal locations in the genome (8). That study established that more than one-third of the predicted genes were present in just one inbred at the loci examined, although many of the unshared genes appeared to be truncated. The observation that genes not shared between inbreds violate the maize-rice colinearity usually displayed by shared genes prompted the authors to speculate that unshared genes originated from insertions of a yet-unknown nature rather than deletions.High intraspecific haplotype variability is not restricted to maize, having been recently described in barley, another species with a large amount of repetitive DNA. A comparison of the Rph7 locus in two barley cultivars established that colinearity was restricted to Ͻ35% of the two sequences, principally because of differences in retrotransposon blocks (9). Interestingly, a gene encoding a truncated helicase was present in only one of the two cultivars. On the other hand, no cases of gene acquisition or loss were found in a comparison of two different orthologous regions between rice subspecies (10, 11). This finding suggests that the type of variation detected in maize and barley may not be a general feature of plant genomes. The functional significance of the ''plus-minus'' type of variation is also unclear, because the genes that vary among accessions of the same species are present in multiple copies (3), and many of them are clearly pseudogenes or gene fragments (8, 9). Independent of its generality or functional significance, the described variation raises an important question: How did it arise? Evidence presented here indicates that the apparent intraspecific violations of genetic colinearity in maize and, probably, barley, arise from the movement of genes or gene fragments by Helitrons, a recently discovered type of eukaryotic transposon (12).Helitrons were found by computational analysis of genomic sequences from Arabidopsis, rice, and Caenorhabditis elegans (12) and were later reported to be the caus...

A Helitron-Like Transposon Superfamily from Lepidoptera Disrupts (GAAA)n Microsatellites and is Responsible for Flanking Sequence Similarity within a Microsatellite Family

“…A BLASTn search of the GenBank nr database with positions 25,211-27,159 of the ABC transporter (query sequence containing (GAAA) n microsatellite through the beginning of exon 3) resulted in a ''hit'' to the B. mori BAC clone 048C11 (GenBank accession AP009015.1; positions 30, 194). Sequence alignment indicates the two genomic regions share 99% similarity over 1.83 kb that terminates after a 3 0 GTAA nucleotide motif, which suggests that BmMINE-1 Helitrons may terminate at 3 0 GTRR motifs compared to the 3 0 -CTRR Helitron motif (Kapitonov and Jurka 2001;Lai et al 2005). Additionally, an internal ORF on the antisense strand was predicted to encode a 520 residue peptide called BMMINE-1p_1 that contains a non-LTR-like reverse transcriptase domain (RT; hit E-value 4e -36 ; cd01650; Marchler-Bauer et al 2009) from residues 61-325 ( Fig.…”

“…Similar to MITEs, non-autonomous Helitron elements exist and were predicted to represent all known Helitron-like Drosophila interspersed elements (DINE-1s) in the D. melanogaster genome (Kapitonov and Jurka 2007a). Helitrons have been described from Aradidopsis thaiana, Oriza sativa, Caenorhabditis elegans, and Zea maize (Gupta et al 2005;Lai et al 2005), and might be related to Geminiviruses that have integrated into plant genomes (Kapitonov and Jurka 2007b).…”

The Contribution of Transposable Elements to Expressed Coding Sequence in Arabidopsis thaliana

“…For example, reverse transcription of mRNA transcripts by class I transposons has generated more than 1000 retroposed genes in rice, many of which have recruited exons from flanking regions to produce functional genes (Wang et al 2006). TEs also capture and shuffle gene fragments (Jiang et al 2004;Brunner et al 2005;Lai et al 2005). Maize helitrons, for example, capture and move gene fragments to the extent that *20% of genes (or gene fragments) differ in location between two maize lines (Lai et al 2005;Morgante et al 2005).…”

“…TEs also capture and shuffle gene fragments (Jiang et al 2004;Brunner et al 2005;Lai et al 2005). Maize helitrons, for example, capture and move gene fragments to the extent that *20% of genes (or gene fragments) differ in location between two maize lines (Lai et al 2005;Morgante et al 2005). Additionally, in A. thaliana, helitrons proliferated after the acquisition of exon fragments (Hollister and Gaut 2007).…”

“…Additionally, in A. thaliana, helitrons proliferated after the acquisition of exon fragments (Hollister and Gaut 2007). Many of the gene fragments captured by TEs are expressed (Jiang et al 2004;Brunner et al 2005;Lai et al 2005), fueling speculation that TE-mediated gene shuffling can lead to novel genes. While it is clear that TEs can capture gene fragments, there are few direct examples that TE sequences have contributed to functional plant genes.…”