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Frequent spontaneous structural rearrangements promote rapid genome diversification in a Brassica napus F1 generation

Mauricio Orantes-Bonilla, Manar Makhoul, HueyTyng Lee, Harmeet Singh Chawla, Paul Vollrath, Anna Langstroff, Fritz J. Sedlazeck, Jun Zou, Rod J. Snowdon
doi: https://doi.org/10.1101/2022.06.27.497715
Mauricio Orantes-Bonilla
1Department of Plant Breeding, IFZ Research Centre for Biosystems, Land Use and Nutrition, Justus Liebig University, Giessen, Germany
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Manar Makhoul
1Department of Plant Breeding, IFZ Research Centre for Biosystems, Land Use and Nutrition, Justus Liebig University, Giessen, Germany
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HueyTyng Lee
1Department of Plant Breeding, IFZ Research Centre for Biosystems, Land Use and Nutrition, Justus Liebig University, Giessen, Germany
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Harmeet Singh Chawla
2Department of Plant Sciences, Crop Development Centre, University of Saskatchewan, Saskatoon, SK, Canada
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Paul Vollrath
1Department of Plant Breeding, IFZ Research Centre for Biosystems, Land Use and Nutrition, Justus Liebig University, Giessen, Germany
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Anna Langstroff
1Department of Plant Breeding, IFZ Research Centre for Biosystems, Land Use and Nutrition, Justus Liebig University, Giessen, Germany
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Fritz J. Sedlazeck
3Human Genome Sequencing Center, Baylor College of Medicine, Houston, TX, United States of America
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Jun Zou
4National Key Laboratory of Crop Genetic Improvement, College of Plant Science & Technology, Huazhong Agricultural University, Wuhan, People’s Republic of China
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Rod J. Snowdon
1Department of Plant Breeding, IFZ Research Centre for Biosystems, Land Use and Nutrition, Justus Liebig University, Giessen, Germany
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  • For correspondence: Rod.Snowdon@agrar.uni-giessen.de
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Abstract

In a cross between two homozygous Brassica napus plants of synthetic and natural origin, we demonstrate that novel structural genome variants from the synthetic parent cause immediate genome diversification among F1 offspring. Long read sequencing in twelve F1 sister plants revealed five large-scale structural rearrangements where both parents carried different homozygous alleles but the heterozygous F1 genomes were not identical heterozygotes as expected. Such spontaneous rearrangements were part of homoeologous exchanges or segmental deletions and were identified in different, individual F1 plants. The variants caused deletions, gene copy-number variations, diverging methylation patterns and other structural changes in large numbers of genes and may have been causal for unexpected phenotypic variation between individual F1 sister plants, for example strong divergence of plant height and leaf area. This example supports the hypothesis that spontaneous de novo structural rearrangements after de novo polyploidization can rapidly overcome intense allopolyploidization bottlenecks to re-expand crops genetic diversity for ecogeographical expansion and human selection. The findings imply that natural genome restructuring in allopolyploid plants from interspecific hybridization, a common approach in plant breeding, can have a considerably more drastic impact on genetic diversity in agricultural ecosystems than extremely precise, biotechnological genome modifications.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Results section on large-scale rearrangement and Table S3 were updated to clarify differences between mid-sized and large-scale structural rearrangements. Introduction and discussion were revised and title and abstract were modified accordingly.

  • https://www.ncbi.nlm.nih.gov/sra/PRJNA837580

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted September 30, 2022.
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Frequent spontaneous structural rearrangements promote rapid genome diversification in a Brassica napus F1 generation
Mauricio Orantes-Bonilla, Manar Makhoul, HueyTyng Lee, Harmeet Singh Chawla, Paul Vollrath, Anna Langstroff, Fritz J. Sedlazeck, Jun Zou, Rod J. Snowdon
bioRxiv 2022.06.27.497715; doi: https://doi.org/10.1101/2022.06.27.497715
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Frequent spontaneous structural rearrangements promote rapid genome diversification in a Brassica napus F1 generation
Mauricio Orantes-Bonilla, Manar Makhoul, HueyTyng Lee, Harmeet Singh Chawla, Paul Vollrath, Anna Langstroff, Fritz J. Sedlazeck, Jun Zou, Rod J. Snowdon
bioRxiv 2022.06.27.497715; doi: https://doi.org/10.1101/2022.06.27.497715

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