Exceptional Diversity, Non-Random Distribution, and Rapid Evolution of Retroelements in the B73 Maize Genome

Abstract

Recent comprehensive sequence analysis of the maize genome now permits detailed discovery and description of all transposable elements (TEs) in this complex nuclear environment. Reiteratively optimized structural and homology criteria were used in the computer-assisted search for retroelements, TEs that transpose by reverse transcription of an RNA intermediate, with the final results verified by manual inspection. Retroelements were found to occupy the majority (>75%) of the nuclear genome in maize inbred B73. Unprecedented genetic diversity was discovered in the long terminal repeat (LTR) retrotransposon class of retroelements, with >400 families (>350 newly discovered) contributing >31,000 intact elements. The two other classes of retroelements, SINEs (four families) and LINEs (at least 30 families), were observed to contribute 1,991 and ∼35,000 copies, respectively, or a combined ∼1% of the B73 nuclear genome. With regard to fully intact elements, median copy numbers for all retroelement families in maize was 2 because >250 LTR retrotransposon families contained only one or two intact members that could be detected in the B73 draft sequence. The majority, perhaps all, of the investigated retroelement families exhibited non-random dispersal across the maize genome, with LINEs, SINEs, and many low-copy-number LTR retrotransposons exhibiting a bias for accumulation in gene-rich regions. In contrast, most (but not all) medium- and high-copy-number LTR retrotransposons were found to preferentially accumulate in gene-poor regions like pericentromeric heterochromatin, while a few high-copy-number families exhibited the opposite bias. Regions of the genome with the highest LTR retrotransposon density contained the lowest LTR retrotransposon diversity. These results indicate that the maize genome provides a great number of different niches for the survival and procreation of a great variety of retroelements that have evolved to differentially occupy and exploit this genomic diversity.

Improved maize reference genome with single-molecule technologies

“…Most of the maize Letter reSeArCH genome is derived from transposable elements 3, 21 , and careful study of a few regions has revealed a characteristic structure of sequentially nested retrotransposons 21,22 and the effect of deletions and recombina tion on retrotransposon evolution 23 . In the annotation of the original maize assembly, however, fewer than 1% of long terminal repeat (LTR) retrotransposon copies were intact 24 . By applying a new homology independent annotation pipeline to our assembly (Extended Data Table 3), we identified 1,268 Mb (130,604 copies) of structurally intact retrotransposons, of which 661 Mb (70,035 copies) are nested retro transposon copies disrupted by the insertion of other transposable elements, 8.7 Mb (14,041 copies) are DNA terminal inverted repeat transposons, and 76 Mb (21,095 copies) are helitrons.…”

The dynamics of LTR retrotransposon accumulation across 25 million years of panicoid grass evolution

“…For Zea, where repeat sequences have been well-characterized, the repeat groups were then annotated using Cross_Match and five repeat databases (MAGI v3.1, TIGR v2.0 (Ouyang and Buell, 2004), TREP release 7, and the Maize Transposable Element database (Baucom et al, 2009) (http://maizetedb. org/Bmaize/)).…”

“…In most angiosperm genomes, the LTR retrotransposons are the most significant contributor to genome size, contributing over 75% of the nuclear DNA to even moderate-sized genomes like maize (Schnable et al, 2009). Most LTR retrotransposons families exist in low copy numbers (SanMiguel and Bennetzen, 1998;Baucom et al, 2009), but the amplification of a few families that individually contribute 4100 Mb of DNA to a genome are the major causes of 'genomic obesity' (Bennetzen and Kellogg, 1997) in plants. LTR retrotransposon amplifications by only one or a few families are sufficient to more than double genome size in a just a few million years, as shown for Oryza australiensis (Piegu et al, 2006).…”

Transposable elements contribute to activation of maize genes in response to abiotic stress

“…While TEs only account for ,10% of the Arabidopsis genome [32] or ,32% of the rice genome [33], they contribute ,85% to the maize genome [34]- [35]. Many TEs are located in pericentromeric regions and heterochromatic maize knobs [34], [36], but there are also many TE insertions interspersed between maize genes [37]- [39].…”