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Eukaryotic genomes are large and complex, and gene expression can be affected by multiple regulatory elements and their positions within the dynamic chromatin architecture. Transposable elements are known to play important roles in genome evolution, yet questions remain as to how transposable elements alter genome structure and affect gene expression. Previous studies have shown that genome rearrangements can be induced by Reversed Ends Transposition involving termini of Activator and related transposable elements in maize and other plants. Here, we show that complex alleles can be formed by the rapid and progressive accumulation of Activator-induced duplications and rearrangements. The p1 gene enhancer in maize can induce ectopic expression of the nearby p2 gene in pericarp tissue when placed near it via different structural rearrangements. By screening for p2 expression, we identified and studied 5 cases in which multiple sequential transposition events occurred and increased the p1 enhancer copy number. We see active p2 expression due to multiple copies of the p1 enhancer present near p2 in all 5 cases. The p1 enhancer effects are confirmed by the observation that loss of p2 expression is correlated with transposition-induced excision of the p1 enhancers. We also performed a targeted Chromosome Conformation Capture experiment to test the physical interaction between the p1 enhancer and p2 promoter region. Together, our results show that transposon-induced rearrangements can accumulate rapidly and progressively increase genetic variation important for genomic evolution., Competing Interests: Conflicts of interest: None declared., (© The Author(s) 2022. Published by Oxford University Press on behalf of Genetics Society of America.)

Transposable elements (TEs) are DNA sequences that can mobilize and proliferate throughout eukaryotic genomes. Previous studies have shown that in plant genomes, TEs can influence gene expression in various ways, such as inserting in introns or exons to alter transcript structure and content, and providing novel promoters and regulatory elements to generate new regulatory patterns. Furthermore, TEs can also regulate gene expression at the epigenetic level by modifying chromatin structure, changing DNA methylation status, and generating small RNAs. In this study, we demonstrated that Ac/ fractured Ac (fAc ) TEs are able to induce ectopic gene expression by duplicating and shuffling enhancer elements. Ac/fAc elements belong to the hAT family of class II TEs. They can undergo standard transposition events, which involve the two termini of a single transposon, or alternative transposition events that involve the termini of two different nearby elements. Our previous studies have shown that alternative transposition can generate various genome rearrangements such as deletions, duplications, inversions, translocations, and composite insertions (CIs). We identified >50 independent cases of CIs generated by Ac/fAc alternative transposition and analyzed 10 of them in detail. We show that these CIs induced ectopic expression of the maize pericarp color 2 ( p2 ) gene, which encodes a Myb-related protein. All the CIs analyzed contain sequences including a transcriptional enhancer derived from the nearby p1 gene, suggesting that the CI-induced activation of p2 is affected by mobilization of the p1 enhancer. This is further supported by analysis of a mutant in which the CI is excised and p2 expression is lost. These results show that alternative transposition events are not only able to induce genome rearrangements, but also generate CIs that can control gene expression., (Copyright © 2020 by the Genetics Society of America.)