Recombination rates between adjacent genic and retrotransposon regions in maize vary by 2 orders of magnitude

Abstract

Genetic map length and gene number in eukaryotes vary considerably less than genome size, giving rise to the hypothesis that recombination is restricted to genes. The complex genome of maize contains a large fraction of repetitive DNA, composed principally of retrotransposons arranged in clusters. Here, we assess directly the contribution of retrotransposon clusters and genes to genetic length. We first measured recombination across adjacent homozygous genetic intervals on either side of the bronze (bz) locus. We then isolated and characterized two bacterial artificial chromosome clones containing those intervals. Recombination was almost 2 orders of magnitude higher in the distal side, which is gene-dense and lacks retrotransposons, than in the proximal side, which is gene-poor and contains a large cluster of methylated retrotransposons. We conclude that the repetitive retrotransposon DNA in maize, which constitutes the bulk of the genome, most likely contributes little if any to genetic length.A lthough the amount of nuclear DNA in eukaryotes varies greatly, the total length of their genetic maps does not. This can be considered the genetic version of the C-value paradox, which states that the size of eukaryotic genomes bears little relationship to organismic complexity or number of genes (1). To account for the discrepancy between the sizes of genomes and genetic maps, Thuriaux hypothesized that meiotic recombination may be largely restricted to genes (2). Maize, with its large amount of repetitive DNA (3), is a particularly suitable organism for testing this hypothesis. One prediction of the hypothesis is that recombination within genes, expressed as the ratio of genetic to physical length (cM͞kb), should be much higher than the genome's average (4). Data from intragenic recombination experiments support that prediction (5-9). Recombination within the bronze (bz) locus, for example, is at least 100 times higher than the maize genome's average (5). A second prediction of the hypothesis is that repetitive DNA should not contribute significantly to genetic length, i.e., recombination across repetitive DNA should be much lower than across genic DNA. Here we analyze how this prediction holds around the bz locus, one of the regions of the maize genome where recombination has been studied in greatest detail (5, 10).Approximately 80% of the 2,500-megabase maize nuclear genome (11) is present in more than 100 copies (12). As in other plants with large genomes, much of this repetitive DNA consists of different families of retrotransposons (13-15). In maize, at least 50% of the repetitive DNA is made up of retrotransposon blocks dispersed throughout the gene-containing regions of the genome (16). We recently isolated a 240-kb bacterial artificial chromosome (BAC) contig centered around Bz-McC, one of the bz alleles used in the earlier intragenic recombination studies, and established that the bz gene is located in an unusually gene-dense region flanked at either end by retrotransposon blocks (17, 18). Thus, the bz geno...

Physical maps and recombination frequency of six rice chromosomes

“…Thuriaux (1977) hypothesized earlier that meiotic recombination in eukaryotes takes place mostly in the genic regions. Several genetic and molecular studies have found direct evidence that genomic repetitive sequences probably have a negative in¯uence on the chromosomal recombination rate in plants (Arabidopsis Genome Initiative, 2000;Fu et al, 2002;SanMiguel et al, 1996). To con®rm this, we used the ®nished genomic sequence data on chromosome 1 to examine the constitution and organization of sequences in 10 genomic regions showing mostly high (hotspot) or low (coldspot) recombination frequencies.…”

Caught Red-Handed:RcEncodes a Basic Helix-Loop-Helix Protein Conditioning Red Pericarp in Rice

“…Several previous studies have noted significant repression of recombination associated with the abundance of TEs and other repetitive sequences (Fu et al, 2002;Wu et al, 2003;Shah and Hassan, 2005). Therefore, we expected that the TEs themselves might contribute to the recombinational repression.…”

High-Resolution Mapping of Crossover Events in the Hexaploid Wheat Genome Suggests a Universal Recombination Mechanism

“…In sorghum, a similar correlation was observed with 97-98% of COs occurring in euchromatin regions (Paterson et al 2009). Similar studies aiming at deciphering recombination in maize (Fu et al 2001(Fu et al , 2002Yao and Schnable 2005) and wheat (Saintenac et al 2011) revealed the presence of small regions exhibiting high recombination rates. These authors evaluated intervals ranging from 380 to 11,600 bp where recombination varied from 22 to 132 cM/Mb compared to average chromosome values of 2.1 and 0.20 cM/Mb for maize and wheat, respectively.…”