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.

CNRS LGDP UMR5096 Université de Perpignan 66860 Perpignan France

Department of Plant Pathology and Microbiology Iowa State University Ames Iowa 50011 USA

ENS IBENS CNRS INSERM PSL Research University 75005 Paris France

Institute of Plant and Microbial Biology University of Zurich CH 8008 Zurich Switzerland

IRD UMR232 DIADE 34394 Montpellier France

Mendel Centre for Plant Genomics and Proteomics CEITEC Masaryk University 625 00 Brno Czech Republic

UPVD LGDP UMR5096 Université de Perpignan 66860 Perpignan France

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