Transposable Elements Contribute to Activation of Maize Genes in Response to Abiotic Stress

Abstract

Transposable elements (TEs) account for a large portion of the genome in many eukaryotic species. Despite their reputation as “junk” DNA or genomic parasites deleterious for the host, TEs have complex interactions with host genes and the potential to contribute to regulatory variation in gene expression. It has been hypothesized that TEs and genes they insert near may be transcriptionally activated in response to stress conditions. The maize genome, with many different types of TEs interspersed with genes, provides an ideal system to study the genome-wide influence of TEs on gene regulation. To analyze the magnitude of the TE effect on gene expression response to environmental changes, we profiled gene and TE transcript levels in maize seedlings exposed to a number of abiotic stresses. Many genes exhibit up- or down-regulation in response to these stress conditions. The analysis of TE families inserted within upstream regions of up-regulated genes revealed that between four and nine different TE families are associated with up-regulated gene expression in each of these stress conditions, affecting up to 20% of the genes up-regulated in response to abiotic stress, and as many as 33% of genes that are only expressed in response to stress. Expression of many of these same TE families also responds to the same stress conditions. The analysis of the stress-induced transcripts and proximity of the transposon to the gene suggests that these TEs may provide local enhancer activities that stimulate stress-responsive gene expression. Our data on allelic variation for insertions of several of these TEs show strong correlation between the presence of TE insertions and stress-responsive up-regulation of gene expression. Our findings suggest that TEs provide an important source of allelic regulatory variation in gene response to abiotic stress in maize.

Author Summary

Transposable elements are mobile DNA elements that are a prevalent component of many eukaryotic genomes. While transposable elements can often have deleterious effects through insertions into protein-coding genes they may also contribute to regulatory variation of gene expression. There are a handful of examples in which specific transposon insertions contribute to regulatory variation of nearby genes, particularly in response to environmental stress. We sought to understand the genome-wide influence of transposable elements on gene expression responses to abiotic stress in maize, a plant with many families of transposable elements located in between genes. Our analysis suggests that a small number of maize transposable element families may contribute to the response of nearby genes to abiotic stress by providing stress-responsive enhancer-like functions. The specific insertions of transposable elements are often polymorphic within a species. Our data demonstrate that allelic variation for insertions of the transposable elements associated with stress-responsive expression can contribute to variation in the regulation of nearby genes. Thus novel insertions of transposable elements provide a potential mechanism for genes to acquire cis-regulatory influences that could contribute to heritable variation for stress response.