Genomic features shaping the landscape of meiotic double-strand-break hotspots in maize

Yan He, Minghui Wang, Stefanie Dukowic-Schulze, Adele Zhou, Choon Lin Tiang, Shay Shilo, Gaganpreet K. Sidhu, Steven Eichten, Peter Bradbury, Nathan M. Springer, Edward S. Buckler, Avraham A. Levy, Qi Sun, Jaroslaw Pillardy, Penny M.A. Kianian, Shahryar F. Kianian, Changbin Chen, Wojciech P. Pawlowski

Research output: Contribution to journalArticle

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Abstract

Meiotic recombination is the most important source of genetic variation in higher eukaryotes. It is initiated by formation of double-strand breaks (DSBs) in chromosomal DNA in early meiotic prophase. The DSBs are subsequently repaired, resulting in crossovers (COs) and noncrossovers (NCOs). Recombination events are not distributed evenly along chromosomes but cluster at recombination hotspots. How specific sites become hotspots is poorly understood. Studies in yeast and mammals linked initiation of meiotic recombination to active chromatin features present upstream from genes, such as absence of nucleosomes and presence of trimethylation of lysine 4 in histone H3 (H3K4me3). Core recombination components are conserved among eukaryotes, but it is unclear whether this conservation results in universal characteristics of recombination landscapes shared by a wide range of species. To address this question, we mapped meiotic DSBs in maize, a higher eukaryote with a large genome that is rich in repetitive DNA. We found DSBs in maize to be frequent in all chromosome regions, including sites lacking COs, such as centromeres and pericentromeric regions. Furthermore, most DSBs are formed in repetitive DNA, predominantly Gypsy retrotransposons, and only one-quarter of DSB hotspots are near genes. Genic and nongenic hotspots differ in several characteristics, and only genic DSBs contribute to crossover formation. Maize hotspots overlap regions of low nucleosome occupancy but show only limited association with H3K4me3 sites. Overall, maize DSB hotspots exhibit distribution patterns and characteristics not reported previously in other species. Understanding recombination patterns in maize will shed light on mechanisms affecting dynamics of the plant genome.

Original languageEnglish (US)
Pages (from-to)12231-12236
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume114
Issue number46
DOIs
StatePublished - Nov 14 2017

Fingerprint

Genetic Recombination
Zea mays
Eukaryota
Nucleosomes
DNA
Chromosomes
Plant Genome
Chromosome Breakage
Prophase
Retroelements
Centromere
Histones
Genes
Lysine
Chromatin
Mammals
Yeasts
Genome

Keywords

  • Chromosomes
  • Double-strand breaks
  • Maize
  • Meiosis
  • Recombination

Cite this

Genomic features shaping the landscape of meiotic double-strand-break hotspots in maize. / He, Yan; Wang, Minghui; Dukowic-Schulze, Stefanie; Zhou, Adele; Tiang, Choon Lin; Shilo, Shay; Sidhu, Gaganpreet K.; Eichten, Steven; Bradbury, Peter; Springer, Nathan M.; Buckler, Edward S.; Levy, Avraham A.; Sun, Qi; Pillardy, Jaroslaw; Kianian, Penny M.A.; Kianian, Shahryar F.; Chen, Changbin; Pawlowski, Wojciech P.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 114, No. 46, 14.11.2017, p. 12231-12236.

Research output: Contribution to journalArticle

He, Y, Wang, M, Dukowic-Schulze, S, Zhou, A, Tiang, CL, Shilo, S, Sidhu, GK, Eichten, S, Bradbury, P, Springer, NM, Buckler, ES, Levy, AA, Sun, Q, Pillardy, J, Kianian, PMA, Kianian, SF, Chen, C & Pawlowski, WP 2017, 'Genomic features shaping the landscape of meiotic double-strand-break hotspots in maize', Proceedings of the National Academy of Sciences of the United States of America, vol. 114, no. 46, pp. 12231-12236. https://doi.org/10.1073/pnas.1713225114
He, Yan ; Wang, Minghui ; Dukowic-Schulze, Stefanie ; Zhou, Adele ; Tiang, Choon Lin ; Shilo, Shay ; Sidhu, Gaganpreet K. ; Eichten, Steven ; Bradbury, Peter ; Springer, Nathan M. ; Buckler, Edward S. ; Levy, Avraham A. ; Sun, Qi ; Pillardy, Jaroslaw ; Kianian, Penny M.A. ; Kianian, Shahryar F. ; Chen, Changbin ; Pawlowski, Wojciech P. / Genomic features shaping the landscape of meiotic double-strand-break hotspots in maize. In: Proceedings of the National Academy of Sciences of the United States of America. 2017 ; Vol. 114, No. 46. pp. 12231-12236.
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AU - Shilo, Shay

AU - Sidhu, Gaganpreet K.

AU - Eichten, Steven

AU - Bradbury, Peter

AU - Springer, Nathan M.

AU - Buckler, Edward S.

AU - Levy, Avraham A.

AU - Sun, Qi

AU - Pillardy, Jaroslaw

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