Genomic impact of stress-induced transposable element mobility in Arabidopsis

Abstract

Transposable elements (TEs) have long been known to be major contributors to plant evolution, adaptation and crop domestication. Stress-induced TE mobilization is of particular interest because it may result in novel gene regulatory pathways responding to stresses and thereby contribute to stress adaptation. Here, we investigated the genomic impacts of stress induced TE mobilization in wild type Arabidopsis plants. We find that the heat-stress responsive ONSEN TE displays an insertion site preference that is associated with specific chromatin states, especially those rich in H2A.Z histone variant and H3K27me3 histone mark. In order to better understand how novel ONSEN insertions affect the plant's response to heat stress, we carried out an in-depth transcriptomic analysis. We find that in addition to simple gene knockouts, ONSEN can produce a plethora of gene expression changes such as: constitutive activation of gene expression, alternative splicing, acquisition of heat-responsiveness, exonisation and genesis of novel non-coding and antisense RNAs. This report shows how the mobilization of a single TE-family can lead to a rapid rise of its copy number increasing the host's genome size and contribute to a broad range of transcriptomic novelty on which natural selection can then act.

Heat-induced transposition increases drought tolerance in Arabidopsis

“…To assess size variations between the hcLines, we analyzed the pixel counts of predicted vital areas before the appearance of necrotic leaves eight days after watering was suspended (Fig 1b, Fig 2a). Although heat stress and the AZ drug treatment have been shown to induce epi/genetic mutations 9,17,19 , we did not observe differences in growth among our five control lines. Yet, in accordance with the fact that transposition is predominantly associated with fitness loss of the host 17,20–22 , we found a significantly reduced number of vital pixels compared to the wt for four hcLines (Wilcoxon-test P<0.01, Fig 1b).…”

“…Although heat stress and the AZ drug treatment have been shown to induce epi/genetic mutations 9,17,19 , we did not observe differences in growth among our five control lines. Yet, in accordance with the fact that transposition is predominantly associated with fitness loss of the host 17,20–22 , we found a significantly reduced number of vital pixels compared to the wt for four hcLines (Wilcoxon-test P<0.01, Fig 1b). Notably, in some cases we also observed a strong size variation between hcLines originating from the same parent (e.g., hcLine37 and hcLine38 vs hcLine39) indicating genetic segregation of the lines (Fig 1b).…”

“…However, in some hcLines (e.g. hcLine9), no additional ONSEN copies were detectable by qPCR even though some were previously validated by sequencing (Roquis et al, 2021). As the hcLines were originally exposed to a combination of heat and the drugs zebularine (Z) and alpha-amanitin (A) (HS+AZ) (Thieme et al, 2017), we controlled for a potential ONSEN -independent phenotypic variation caused by epi/genetic changes induced by the heat-stress or the chemical demethylation.…”

“…We first used whole-genome re-sequencing data to locate all transposon-insertion polymorphisms (TIPs) of hcLine31 (Roquis et al, 2021). In accordance with its insertion bias towards actively transcribed regions in the A. thaliana genome (Quadrana et al, 2019; Roquis et al, 2021), six out of the ten ONSEN TIPs detected in hcLine31, were located in exons (Table S1). Notably, we detected a homozygous TIP in the ribose-5-phosphate-isomerase 2 ( RPI2, At2G01290 ), a gene involved in chloroplast photosynthetic capacity (Xiong et al, 2009).…”

Correction to ‘Genomic impact of stress-induced transposable element mobility in Arabidopsis’

“…The article ( 1 ) has been updated. The correction does not affect the results, discussion and conclusions presented in the article.…”