Protein-Coding cis-Natural Antisense Transcripts Have High and Broad Expression in Arabidopsis

Shuhua Zhan,Lewis Lukens

doi:10.1104/pp.112.212100

Abstract

Pairs of genes within eukaryotic genomes are often located on opposite DNA strands such that transcription generates cis-natural sense antisense transcripts (cis-NATs). This orientation of genes has been associated with the biogenesis of splice variants and natural antisense small RNAs. Here, in an analysis of currently available data, we report that within Arabidopsis (Arabidopsis thaliana), protein-coding cis-NATs are also characterized by high abundance, high coexpression, and broad expression. Our results suggest that a permissive chromatin environment may have led to the proximity of these genes. Compared with other genes, cis-NAT-encoding genes have enriched low-nucleosome-density regions, high levels of histone H3 lysine-9 acetylation, and low levels of H3 lysine-27 trimethylation. Promoters associated with broadly expressed genes are preferentially found in the 5' regulatory sequences of cis-NAT-encoding genes. Our results further suggest that natural antisense small RNA production from cis-NATs is limited. Small RNAs sequenced from natural antisense small RNA biogenesis mutants including dcl1, dcl2, dcl3, and rdr6 map to cis-NATs as frequently as small RNAs sequenced from wild-type plants. Future work will investigate if the positive transcriptional regulation of overlapping protein-coding genes contributes to the prevalence of these genes within other eukaryotic genomes.

Highlights

Pairs of genes within eukaryotic genomes are often located on opposite DNA strands such that transcription generates cisnatural sense antisense transcripts
Promoter sequences of broadly expressed genes are highly represented in cis-NAT-encoding genes’ upstream regulatory regions, and the chromatin of cis-NAT-encoding genes is enriched for euchromatic marks. small RNAs (sRNAs) appear to play a limited role in cis-NAT regulation, as sRNAs sequenced from sRNA biogenesis mutants map to PC cis-NATs at a similar frequency as in wild-type plants
We found that PC cis-NATs are detected more frequently and at a higher abundance than transcripts from nonoverlapping PC genes (Figs. 1 and 2)

Summary

Introduction

Pairs of genes within eukaryotic genomes are often located on opposite DNA strands such that transcription generates cisnatural sense antisense transcripts (cis-NATs). A higher proportion of cis-NAT-encoding genes were expressed relative to non-cis-NAT-encoding genes in each condition (P , 0.001; Fig. 1).

Results

Conclusion