Transposon-induced inversions activate gene expression in the maize pericarp

Abstract

Chromosomal inversions can have considerable biological and agronomic impacts including disrupted gene function, change in gene expression, and inhibited recombination. Here, we describe the molecular structure and functional impact of six inversions caused by Alternative Transpositions between p1 and p2 genes responsible for floral pigmentation in maize. In maize line p1-wwB54, the p1 gene is null and the p2 gene is expressed in anther and silk but not in pericarp, making the kernels white. By screening for kernels with red pericarp, we identified inversions in this region caused by transposition of Ac and fractured Ac (fAc) transposable elements. We hypothesize that these inversions place the p2 gene promoter near a p1 gene enhancer, thereby activating p2 expression in kernel pericarp. To our knowledge, this is the first report of multiple recurrent inversions that change the position of a gene promoter relative to an enhancer to induce ectopic expression in a eukaryote.

Complex chromosomal rearrangements induced by transposons in maize

“…The null allele p1-wwB54 has a white kernel pericarp phenotype, and the p2 gene is not expressed in the pericarp ( Sharma et al 2021 ). The p1-wwB54 allele retains the p1 enhancer downstream of p1 exon 3; as described above, there are 2 nearby copies of the fragment 15 enhancer, indicated by the 2 red boxes in Fig.…”

“…1a ). Some of the rearrangements previously studied are deletions ( Zhang et al 2006 ), inversions ( Sharma et al 2021 ), and Composite Insertions ( Su et al 2020 ). The model for the formation of Composite Insertion ( CI ) through DNA re-replication has been described previously in detail ( Zhang et al 2014 ; Su et al 2020 ).…”

“…Kernels from these red ears were sown, and genomic DNA was extracted from seedling leaves by a modified CTAB method ( Saghai-Maroof et al 1984 ). To detect structural rearrangements ( Su et al 2020 ; Sharma et al 2021 ), PCR was performed under standard conditions using Promega GoTaq Green Master Mix and primers specifically designed for the p1-wwB54 sequence (Supplementary Table 1). The models of RET predict that in rearrangements arising from the activity of Ac and fAc elements, each breakpoint will be expected to border a transposon involved in the reaction.…”

“…The p1-wwB54 allele retains p1 exon 3, the downstream enhancer, and the Ac and fAc elements in reversed orientation, separated by only 331 bp of DNA. These Ac / fAc termini can undergo frequent Reversed Ends Transposition (RET) events ( Zhang and Peterson 2004 ; Huang and Dooner 2008 ; Zhang et al 2009 ; Yu et al 2011 ), forming a variety of alleles including deletions ( Zhang and Peterson 2005b ; Zhang et al 2006 ), duplications ( Zhang et al 2013 ), Composite Insertions ( CIs ; Zhang et al 2014 ; Su et al 2018 , 2020 ), and inversions ( Zhang and Peterson 2004 ; Yu et al 2011 ; Sharma et al 2021 ). Here, we show how repeated RET events in maize can induce the formation of complex gene structures containing multiple rearrangements such as inversions, CIs , duplications and/or deletions.…”

Editorial: Innovative applications of sequencing technologies in plant science

“…This approach can be applied beyond the classical task of GW for genotyping studies in population genetics and as an alternative to amplified fragment length polymorphism (AFLP) ( Vos et al., 1995 ) or targeted next-generation sequencing. In this study, the utility of PST-PCR v.2 is used to analyze the variability associated with Ac transposon integration sites in the maize ( Zea mays ) genome ( Sharma et al., 2021 ).…”