Large tandem duplications affect gene expression, 3D organization, and plant–pathogen response
- Ariadna Picart-Picolo1,2,
- Stefan Grob3,
- Nathalie Picault1,2,
- Michal Franek4,
- Christel Llauro1,2,
- Thierry Halter5,
- Tom R. Maier6,
- Edouard Jobet1,2,
- Julie Descombin1,2,
- Panpan Zhang2,7,
- Vijayapalani Paramasivan6,
- Thomas J. Baum6,
- Lionel Navarro5,
- Martina Dvořáčková4,
- Marie Mirouze2,7 and
- Frédéric Pontvianne1,2
- 1CNRS, LGDP UMR5096, Université de Perpignan, 66860 Perpignan, France;
- 2UPVD, LGDP UMR5096, Université de Perpignan, 66860 Perpignan, France;
- 3Institute of Plant and Microbial Biology, University of Zurich, CH-8008 Zurich, Switzerland;
- 4Mendel Centre for Plant Genomics and Proteomics, CEITEC, Masaryk University, 625 00 Brno, Czech Republic;
- 5ENS, IBENS, CNRS/INSERM, PSL Research University, 75005 Paris, France;
- 6Department of Plant Pathology and Microbiology, Iowa State University, Ames, Iowa 50011, USA;
- 7IRD, UMR232 DIADE, 34394 Montpellier, France
Abstract
Rapid plant genome evolution is crucial to adapt to environmental changes. Chromosomal rearrangements and gene copy number variation (CNV) are two important tools for genome evolution and sources for the creation of new genes. However, their emergence takes many generations. In this study, we show that in Arabidopsis thaliana, a significant loss of ribosomal RNA (rRNA) genes with a past history of a mutation for the chromatin assembly factor 1 (CAF1) complex causes rapid changes in the genome structure. Using long-read sequencing and microscopic approaches, we have identified up to 15 independent large tandem duplications in direct orientation (TDDOs) ranging from 60 kb to 1.44 Mb. Our data suggest that these TDDOs appeared within a few generations, leading to the duplication of hundreds of genes. By subsequently focusing on a line only containing 20% of rRNA gene copies (20rDNA line), we investigated the impact of TDDOs on 3D genome organization, gene expression, and cytosine methylation. We found that duplicated genes often accumulate more transcripts. Among them, several are involved in plant–pathogen response, which could explain why the 20rDNA line is hyper-resistant to both bacterial and nematode infections. Finally, we show that the TDDOs create gene fusions and/or truncations and discuss their potential implications for the evolution of plant genomes.
Footnotes
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[Supplemental material is available for this article.]
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Article published online before print. Article, supplemental material, and publication date are at http://www.genome.org/cgi/doi/10.1101/gr.261586.120.
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Freely available online through the Genome Research Open Access option.
- Received January 23, 2020.
- Accepted September 15, 2020.
This article, published in Genome Research, is available under a Creative Commons License (Attribution-NonCommercial 4.0 International), as described at http://creativecommons.org/licenses/by-nc/4.0/.
