The Maize Genome Contains a Helitron Insertion

Abstract

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.

Helitrons: Their Impact on Maize Genome Evolution and Diversity

“…In contrast, no clear cut example of Helitron gene capture conditioning advantages to the Helitron or to the host organism is available. In fact, all characterized Helitron-captured maize genes are truncated and likely non-functional (Lal et al 2003;Gupta et al 2005, Lai et al 2005. Helitron capture of an almost intact copy of the maize gene encoding cytidine deaminase was recently reported (Xu and Messing, 2006).…”

“…The highly repetitive nature of genomic DNA hybridizing to Helitron termini (Lal et al 2003) suggests that there are hundreds to thousands of other family members. Accordingly, the terminal ends of the Helitrons have been used to effectively search for other family members in the maize genome database (Gupta et al 2005).…”

“…The gene pieces captured by Helitrons are often transcribed into eclectic transcripts conjoining coding regions of several different genes. These chimeric transcripts are sometimes alternatively spliced, generating several different transcripts via differential utilization of splice sites during pre-mRNA processing (Lal et al 2003;Morgante et al 2005;. For example, the Helitron insertion in maize mutant, sh2-7527 generates several, alternatively-spliced isoforms, at least two of which are caused by alternative retention of a wild type Sh2 intron (Lal et al 2003).…”

“…These include other plants, invertebrates, fungi and fish (Choi et al 2007;Kapitinov and Jurka 2001;Lal et al 2003;Poulter, Goodwin, Butler 2003). Massive abundance of Helitrons has been recently reported in a mammalian genome, the brown bat Myotis lucifugus, where they constitute ~3% of the genome (Pritham and Feschotte 2007 Kapitinov and Jurka 2007).…”

“…That Helitrons are active in modern genomes came from three recent reports of mutants caused by Helitron insertions. Two maize mutants, sh2-7527 and ba1-ref are caused by insertion of non-autonomous Helitrons (Lal, Giroux, Brendel, Vallejos, Hannah 2003;Gupta, Gallavotti, Stryker, Schmidt, Lal 2005). The mutants likely were caused by relatively recent Helitron insertions since (1) the insertion mutants do not contain any other alteration inactivating the gene (a signature of the evolutionary decay of functional genes) and (2) loss of Sh2 or Ba1 leads to germination and seed production deficiencies, respectively.…”