Abstract
The ancestral centromeres of maize contain long stretches of the tandemly arranged CentC repeat. The abundance of tandem DNA repeats and centromeric retrotransposons (CR) has presented a significant challenge to completely assembling centromeres using traditional sequencing methods. Here, we report a nearly complete assembly of the 1.85 Mb maize centromere 10 from inbred B73 using PacBio technology and BACs from the reference genome project. The error rates estimated from overlapping BAC sequences are 7 × 10−6 and 5 × 10−5 for mismatches and indels, respectively. The number of gaps in the region covered by the reassembly was reduced from 140 in the reference genome to three. Three expressed genes are located between 92 and 477 kb from the inferred ancestral CentC cluster, which lies within the region of highest centromeric repeat density. The improved assembly increased the count of full-length CR from 5 to 55 and revealed a 22.7 kb segmental duplication that occurred approximately 121,000 years ago. Our analysis provides evidence of frequent recombination events in the form of partial retrotransposons, deletions within retrotransposons, chimeric retrotransposons, segmental duplications including higher order CentC repeats, a deleted CentC monomer, centromere-proximal inversions, and insertion of mitochondrial sequences. Double-strand DNA break (DSB) repair is the most plausible mechanism for these events and may be the major driver of centromere repeat evolution and diversity. In many cases examined here, DSB repair appears to be mediated by microhomology, suggesting that tandem repeats may have evolved to efficiently repair frequent DSBs in centromeres.
Highlights
Centromeres are required for the faithful segregation of chromosomes during cell division in higher organisms and are usually visible as a primary constriction on the chromosome
By sequencing a centromere 10 region (CEN10) CentC segment in another inbred we identified a homology-mediated recombination that resulted in the deletion of one CentC monomer and the creation of a new CentC variant
CentC regions of C1 and C2 are separated by 2.6 Mb, can be visualized as two distinct Fluorescence in situ hybridization (FISH) signals and likely are the result of a hemicentric inversion (Lamb et al, 2007b)
Summary
Centromeres are required for the faithful segregation of chromosomes during cell division in higher organisms and are usually visible as a primary constriction on the chromosome. Centromere-proximal DSBs of the kind that can lead to deletion and recombination are well documented and are detectable as paracentric chromosome arm inversions (e.g., tomato Tanksley et al, 1992), centric fusion (Robertsonian) translocations (e.g., human Jacobs, 1981) and nested chromosome fusions (e.g., Brachypodium Murat et al, 2010; The International Brachypodium Initiative, 2010), as well as breakdown of sorghum-rice colinearity near centromeres (Bowers et al, 2005). Centromere-specific retrotransposons (CRs) and long tandem arrays of the 156 nt CentC repeat are key DNA components of maize centromeres (Jiang et al, 2003). Maize diverged from rice around 50 million years ago, CentC is similar to the rice CentO in length and sequence (Lee et al, 2005), indicating that these repeats have been retained at their respective centromeres for a very long time. Domesticated maize shows reduced CentC levels compared to its wild teosinte relatives (Albert et al, 2010; Hufford et al, 2012; Bilinski et al, 2015)
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