Haplotype structure strongly affects recombination in a maize genetic interval polymorphic for Helitron and retrotransposon insertions

Abstract

We have asked here how the remarkable variation in maize haplotype structure affects recombination. We compared recombination across a genetic interval of 9S in 2 highly dissimilar heterozygotes that shared 1 parent. The genetic interval in the common haplotype is Ϸ100 kb long and contains 6 genes interspersed with gene-fragment-bearing Helitrons and retrotransposons that, together, comprise 70% of its length. In one heterozygote, most intergenic insertions are homozygous, although polymorphic, enabling us to determine whether any recombination junctions fall within them. In the other, most intergenic insertions are hemizygous and, thus, incapable of homologous recombination. Our analysis of the frequency and distribution of recombination in the interval revealed that: (i) Most junctions were circumscribed to the gene space, where they showed a highly nonuniform distribution. In both heterozygotes, more than half of the junctions fell in the stc1 gene, making it a clear recombination hotspot in the region. However, the genetic size of stc1 was 2- Ac ͉ bz locus ͉ genome ͉ hotspots ͉ methylation T here is ample evidence that most recombination in maize takes place in or around genes (1-3) and that little, if any, recombination takes place in the repetitive and methylated retrotransposon DNA that makes up the bulk of the genome (4, 5). The evidence that retrotransposons are largely recombinationally inert is 2-fold: (i) when homozygous, the standard situation in inbreds, they do not contribute significantly to genetic length (4), and (ii) when hemizygous, a common situation in hybrids, no recombination junctions fall in intervals containing them (5).The unprecedented haplotype diversity recently discovered in maize (6-8) raises several questions regarding the effect of local structural polymorphisms on recombination. In a recent pairwise comparison of 8 bz1 haplotypes, each one consisting of 8 genes spread over a stretch of DNA that averaged Ϸ90 kb, the percentage of shared sequences ranged from 25% to 84% (9). The lines differed by the existence of many polymorphic insertions in introns and intergenic regions, the main ones being LTR retrotransposons, often arranged in nests (10), miniature inverted repeat transposable elements (MITEs) (11), and Helitron transposons carrying fragments of several genes (12, 13). In addition, high SNP and indel heterozygosity would occur in most intergenic regions of hybrids made from those lines.This level of structural polymorphisms could affect recombination in multiple ways and, thus, contribute to the 2-to 3-fold variation in estimates of map distances for single genetic intervals that has been reported in different maize mapping populations (14-16). For example, the highly methylated retrotransposon clusters are probably heterochromatic, so retrotransposon hemizygosity could reduce recombination in adjacent genes; the level of small insertion and SNP affects overall sequence homology and, thus, could determine whether recombination occurs in intergenic regions lacking retrotra...

Polarized gene conversion at the bz locus of maize

“…As discussed above, the degree of NCO gene conversion appears to be a function of the percent identity of the recombining sequences, so we can expect it to vary both at the gene level within a species and at the genome level between species. Another caveat in extrapolating genome-wide results from one species to another is that in some species, like Arabidopsis, most recombination events occur in intergenic regions (13,43,45), whereas in others, like maize, most recombination is intragenic (17,46). The latter observation is not surprising given the high degree of intergenic gross structural polymorphism in maize (36,47).…”

Recombination in diverse maize is stable, predictable, and associated with genetic load

“…Earlier studies of kernel phenotypes have noted high recombination variability between lines (23)(24)(25)(26). In particular, several earlier studies demonstrate that heavily methylated TEs can suppress recombination within and around the repetitive region in heterozygotes (23,27,28).…”

Helitrons , the Eukaryotic Rolling-circle Transposable Elements

“…Indeed, He and Dooner reported that no recombination events could be detected in a 100-kb space containing multiple Helitron insertions and that recombination was inversely correlated with a pattern of dense Helitron methylation (168).…”