Sharu Paul Sharma, Thomas Peterson

Genetics; 2023 Feb 9; 223(2):iyac124. doi: 10.1093/genetics/iyac124.

Abstract

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.

See https://pubmed.ncbi.nlm.nih.gov/36111993/

Fig. 1.

a) p1-wwB54: purple boxes represent the p2 gene with numbered exons 1, 2, and 3. The blue box is exon 3 of the p1 gene. Red boxes indicate 2 copies of fragment 15. Red arrows are Ac (2 arrowheads) and fAc (single arrowhead) elements. b) p1-wwB54-CI contains a CI at the site labeled a/b 6.79-kb downstream of p1 exon 3. This CI contains 1 copy of the enhancer region and exon 3 and is also present in 5 other rearrangement alleles. Corresponding pictures on the right show colorless pericarp phenotype in both alleles. The solid and spotted purple color is due to r1-m3::Ds activation in aleurone caused by Ac-induced excision of Ds.