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Mutator transposon activity alters the transcriptome and proteome of developing maize anthers

ABSTRACT: MuDR/Mu are a highly active transposon family moving by either cut only (or cut-and-paste) in strictly somatic tissues or net replicative transposition (absence of excision alleles) in reproductive tissues. Aside from the MuDR-encoded MURA and MURB proteins, other factors required for Mu transposition, particularly those contributing to the developmentally specific behavior, have yet to be identified. To address this question and assess the impact of a highly active transposon on the transcriptome, RNA was extracted from anthers at three developmental stages in Mu-active and -inactive stocks and compared on a 44,000 element oligonucleotide array. We found that approximately 30,000 unique genes are expressed at each stage. Of the ~10% (ca. 3000) differentially regulated transcripts per stage, there was approximately equal representation by the active or inactive individuals. Keywords: anther development, maize, Mu, transposon

ORGANISM(S): Zea mays

PROVIDER: GSE13118 | GEO | 2009/05/01

SECONDARY ACCESSION(S): PRJNA109655

REPOSITORIES: GEO

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Project description:Insertion sequences (IS) are compact and pervasive transposable elements found in bacteria, which encode only the genes necessary for their mobilization and maintenance. IS200/IS605 elements undergo ‘peel-and-paste’ transposition catalyzed by a TnpA transposase, but intriguingly, they also encode diverse, TnpB-family genes that are evolutionarily related to the CRISPR-associated effectors Cas9 and Cas12. Recent studies demonstrated that TnpB-family enzymes function as RNA-guided DNA endonucleases, but the broader biological role of this activity has remained enigmatic. Here we show that IscB and TnpB are essential to prevent loss of the donor IS element and potential transposon extinction as a consequence of the TnpA transposition mechanism. We first performed phylogenetic analysis of IscB/TnpB proteins and selected a family of related IS elements from Geobacillus stearothermophilus that we predicted would be mobilized by a common TnpA homolog. After reconstituting transposition using a heterologous expression system in E. coli, we found that IS elements were readily lost from the donor site due to the activity of TnpA in rejoining the flanking sequences back together upon excision. However, these IS elements also encode non-coding RNAs that guide TnpB and IscB nucleases to precisely recognize and cleave these excision products, leading either to elimination of the excision product or re-installation of the transposon through recombination. Indeed, under experimental conditions in which TnpA and TnpB-RNA complexes were co-expressed together with a genomically integrated IS element, transposon retention was significantly increased relative to conditions expressing TnpA alone. Remarkably, both TnpA and TnpB recognize the same AT-rich transposon-adjacent motif (TAM) during transposon excision and RNA-guided DNA cleavage, respectively, revealing a striking convergence in the evolution of DNA sequence specificity between transposase and nuclease. Collectively, our study reveals that RNA-guided DNA cleavage is a primal biochemical activity that arose to bias the selfish inheritance of transposable elements, which was later co-opted during the evolution of CRISPR-Cas adaptive immunity for antiviral defense.