High quality maize centromere 10 sequence reveals evidence of frequent recombination events

The ancestral centromeres of maize contain long stretches of the tandemly arranged CentC repeat. The abundance of tandem DNA repeats and centromeric retrotransposons (CR) have presented a significant challenge to completely assembling centromeres using traditional sequencing methods. Here we report...

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Main Authors: Thomas Kai Wolfgruber, Megan M Nakashima, Kevin L Schneider, Anupma eSharma, Zidian eXie, Patrice S Albert, Ronghui eXu, Paul eBilinski, R. Kelly Dawe, Jeffrey eRoss-Ibarra, James A. Birchler, Gernot ePresting
Format: Article
Language:English
Published: Frontiers Media S.A. 2016-03-01
Series:Frontiers in Plant Science
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Online Access:http://journal.frontiersin.org/Journal/10.3389/fpls.2016.00308/full
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spelling doaj-1e8e729466fb413f9c19365823ff47322020-11-24T22:44:52ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2016-03-01710.3389/fpls.2016.00308179024High quality maize centromere 10 sequence reveals evidence of frequent recombination eventsThomas Kai Wolfgruber0Megan M Nakashima1Kevin L Schneider2Anupma eSharma3Zidian eXie4Patrice S Albert5Ronghui eXu6Paul eBilinski7R. Kelly Dawe8Jeffrey eRoss-Ibarra9Jeffrey eRoss-Ibarra10James A. Birchler11Gernot ePresting12University of HawaiiUniversity of HawaiiUniversity of HawaiiUniversity of HawaiiUniversity of HawaiiUniversity of MissouriUniversity of HawaiiUniversity of CaliforniaUniversity of GeorgiaUniversity of CaliforniaUniversity of CaliforniaUniversity of MissouriUniversity of HawaiiThe ancestral centromeres of maize contain long stretches of the tandemly arranged CentC repeat. The abundance of tandem DNA repeats and centromeric retrotransposons (CR) have 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 x 10-6 and 5 x 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 of the inferred ancestral CentC cluster, which lies within the region of highest centromeric repeat density. The improved assembly increased the count of full-length centromeric retrotransposons 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. This repair appears to be mediated by microhomology, suggesting that tandem repeats may have evolved to facilitate the repair of frequent DSBs in centromeres.http://journal.frontiersin.org/Journal/10.3389/fpls.2016.00308/fullDNA damage repairIllegitimate recombinationcentromere evolutionDNA loss at centromereshemicentric inversion
collection DOAJ
language English
format Article
sources DOAJ
author Thomas Kai Wolfgruber
Megan M Nakashima
Kevin L Schneider
Anupma eSharma
Zidian eXie
Patrice S Albert
Ronghui eXu
Paul eBilinski
R. Kelly Dawe
Jeffrey eRoss-Ibarra
Jeffrey eRoss-Ibarra
James A. Birchler
Gernot ePresting
spellingShingle Thomas Kai Wolfgruber
Megan M Nakashima
Kevin L Schneider
Anupma eSharma
Zidian eXie
Patrice S Albert
Ronghui eXu
Paul eBilinski
R. Kelly Dawe
Jeffrey eRoss-Ibarra
Jeffrey eRoss-Ibarra
James A. Birchler
Gernot ePresting
High quality maize centromere 10 sequence reveals evidence of frequent recombination events
Frontiers in Plant Science
DNA damage repair
Illegitimate recombination
centromere evolution
DNA loss at centromeres
hemicentric inversion
author_facet Thomas Kai Wolfgruber
Megan M Nakashima
Kevin L Schneider
Anupma eSharma
Zidian eXie
Patrice S Albert
Ronghui eXu
Paul eBilinski
R. Kelly Dawe
Jeffrey eRoss-Ibarra
Jeffrey eRoss-Ibarra
James A. Birchler
Gernot ePresting
author_sort Thomas Kai Wolfgruber
title High quality maize centromere 10 sequence reveals evidence of frequent recombination events
title_short High quality maize centromere 10 sequence reveals evidence of frequent recombination events
title_full High quality maize centromere 10 sequence reveals evidence of frequent recombination events
title_fullStr High quality maize centromere 10 sequence reveals evidence of frequent recombination events
title_full_unstemmed High quality maize centromere 10 sequence reveals evidence of frequent recombination events
title_sort high quality maize centromere 10 sequence reveals evidence of frequent recombination events
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2016-03-01
description The ancestral centromeres of maize contain long stretches of the tandemly arranged CentC repeat. The abundance of tandem DNA repeats and centromeric retrotransposons (CR) have 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 x 10-6 and 5 x 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 of the inferred ancestral CentC cluster, which lies within the region of highest centromeric repeat density. The improved assembly increased the count of full-length centromeric retrotransposons 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. This repair appears to be mediated by microhomology, suggesting that tandem repeats may have evolved to facilitate the repair of frequent DSBs in centromeres.
topic DNA damage repair
Illegitimate recombination
centromere evolution
DNA loss at centromeres
hemicentric inversion
url http://journal.frontiersin.org/Journal/10.3389/fpls.2016.00308/full
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