Long noncoding RNAs contribute to DNA damage resistance in Arabidopsis thaliana

Abstract

Efficient repair of DNA lesions is essential for faithful transmission of genetic information between somatic cells and for genome integrity across generations. Plants have multiple, partially redundant and overlapping DNA repair pathways, probably due to the less constricted germline and the inevitable exposure to light including higher energy wavelengths. Many proteins involved in DNA repair and their mode of actions are well described. In contrast, a role for DNA damage-associated RNA components, evident from many other organisms, is less well understood. Here, we have challenged young Arabidopsis thaliana plants with two different types of genotoxic stress and performed de novo assembly and transcriptome analysis. We identified three long non-coding RNAs (lncRNAs) that are lowly or not expressed under regular conditions but up-regulated or induced by DNA damage. We generated CRISPR/Cas deletion mutants and found that the absence of the lncRNAs impairs the recovery capacity of the plants from genotoxic stress. The genetic loci are highly conserved among world-wide distributed Arabidopsis accessions and within related species in the Brassicaceae group. Together, these results suggest that the lncRNAs have a conserved function in connection with DNA damage and provide a basis for a mechanistic analysis of their role.

The long non‐coding RNALINDA restrains cellular collapse following DNA damage in Arabidopsis thaliana

“…Differently for Durut et al. (2023), we did not observe an effect on leaf development of Δlinda seedlings following zeocin treatment but noticed a severe cell death response in the root meristem. This increased cell death may account for the observed reduction in root growth recovery following transfer of the Δlinda seedlings from genotoxic to control conditions, compared to control plants.…”

“…We found LINDA to be strongly induced by different stresses inducing primarily DSBs, including zeocin and bleomycin, by UV‐C, which causes predominantly the formation of pyrimidine‐dimers, as well as by X‐rays (Wang et al., 2016) and gamma‐rays (Bourbousse et al., 2018). Similarly, LINDA was recently found in comparative RNA‐Seq analysis (Durut et al., 2023). The pyrimidine dimers caused by UV‐C can be either directly reversed by photoreactivation (Jiang et al., 1997) or removed by nucleotide excision repair (NER).…”

“…Additionally, the LINDA ORF is preceded by multiple start and stop codons. Moreover, single‐nucleotide polymorphism (SNP) analysis suggested a low conservation rate of LINDA in comparison to other lncRNAs (Durut et al., 2023). The low conservation rate argues against the translation of the ORF into a functional protein.…”

SPPiDDRs: a new gene family in dicot plants involved in DNA-Damage Response

“…Not only is LINDA needed for the regulation of its flanking gene, but also for the fine-tuning of the DDR after the occurrence of DNA double-strand breaks. Another study confirmed the involvement of LINDA in DDR and studied three additional lncRNAs in Arabidopsis 30 . One of these studied lncRNAs, annotated on Araport11 as a novel transcribed region (AT4G09215), was strongly upregulated by UV-C irradiation.…”

“…RLFS_026432 was found to be one of the most highly induced lncRNAs upon DNA damage caused by X-rays or UV-C 28,30 . To determine the optimal conditions for its induction by UV-C, different doses were tested and expression of RLFS_026432 was measured after 3 hours, the same time frame as in Wang et al (2016) 28 .…”