The plant DNA polymerase theta is essential for the repair of replication-associated DNA damage

Safeguarding of genome integrity is a key process in all living organisms. Due to their sessile lifestyle, plants are particularly exposed to all kinds of stress conditions that could induce DNA damage. However, very few genes involved in the maintenance of genome integrity are indispensable to plants' viability. One remarkable exception is the POLQ gene, which encodes DNA polymerase theta (Pol theta), a non-replicative polymerase involved in trans-lesion synthesis during DNA replication and double-strand break (DSB) repair. The Arabidopsis tebichi (teb) mutants, deficient in Pol theta, have been reported to display severe developmental defects, leading to the conclusion that Pol theta is required for normal plant development. However, this essential role of Pol theta in plants is challenged by contradictory reports regarding the phenotypic defects of teb mutants and the recent finding that rice (Oryza sativa) null mutants develop normally. Here we show that the phenotype of teb mutants is highly variable. Taking advantage of hypomorphic mutants for the replicative DNA polymerase eta, which display constitutive replicative stress, we show that Pol theta allows maintenance of meristem activity when DNA replication is partially compromised. Furthermore, we found that the phenotype of Pol theta mutants can be aggravated by modifying their growth conditions, suggesting that environmental conditions impact the basal level of replicative stress and providing evidence for a link between plants' responses to adverse conditions and mechanisms involved in the maintenance of genome integrity.

Automated summary

Protecting genome integrity is crucial for all organisms, with plants being particularly susceptible due to their immobile lifestyle and exposure to various stressors. While POLQ gene plays a vital role in maintaining genome integrity in plants, its significance is subject to variability among mutants. Recent studies suggest that Pol theta helps preserve meristem activity in plants under conditions of partial DNA replication impairment, and the phenotypic expression of Pol theta mutants can be influenced by environmental factors. This underscores a connection between plants' responses to adverse conditions and mechanisms involved in genome integrity maintenance.