Seed DNA damage responses promote germination and growth inArabidopsis thaliana

Abstract

The desiccated, quiescent state of seeds confers extended survival of the embryonic plant. However, accumulation of striking levels of genome damage in quiescence impairs germination and threatens plant survival. The mechanisms by which seeds mitigate this damage remain unclear. Here, we reveal that imbibed Arabidopsis seeds display high resistance to DNA damage, which is lost as seeds advance to germination, coincident with increasing cell cycle activity. In contrast to seedlings, we show that seeds minimize the impact of DNA damage by reducing meristem disruption and delaying SOG1-dependent programmed cell death. This promotes root growth early postgermination. In response to naturally accumulated DNA damage in aging seeds, SOG1 activates cell death postgermination. SOG1 activities are also important for promoting successful seedling establishment. These distinct cellular responses of seeds and seedlings are reflected by different DNA damage transcriptional profiles. Comparative analysis of DNA repair mutants identifies roles of the major genome maintenance pathways in germination but that the repair of cytotoxic chromosomal breaks is the most important for seed longevity. Collectively, these results indicate that high levels of DNA damage incurred in seeds are countered by low cell cycle activity, cell cycle checkpoints, and DNA repair, promoting successful seedling establishment. Our findings reveal insight into both the physiological significance of plant DNA damage responses and the mechanisms which maintain seed longevity, important for survival of plant populations in the natural environment and sustainable crop production under changing climates.

Integrative Transcriptomics Data Mining to Explore the Functions of TDP1α and TDP1β Genes in the Arabidopsis thaliana Model Plant

“…When considering the types of cellular mortality, IR induced the enhanced accumulation of programmed cell death (PCD) and necrotic nuclei in Col0, while these were more pronounced in the sog1 mutant gene in the absence of stress ( Figure 6 c). These results prove once more that the SOG1 gene deficiency is strongly correlated with defects in DNA repair activation and PCD induction [ 49 , 92 , 93 , 94 ]. When looking at the gene expression data, the first observation that can be made in our system is that the TDP1β gene seems to be more expressed in the sog1 mutant compared to the Col0 line in the absence of IR treatment, whereas the TDP1α gene is similarly expressed in both genotypes ( Figure 6 d, CTRL samples).…”

Genome damage accumulated in seed ageing leads to plant genome instability and growth inhibition

“…Our previous work found that seeds were surprisingly resistant to X-ray induced DNA damage [ 16 ]. In particular, seeds maintained post-germinative growth after irradiation, with levels of programmed cell death (PCD) that were both delayed and attenuated relative to irradiated seedlings.…”

“…As a result, genome maintenance mechanisms in plant cells are important not only for growth and development, but also in preserving the longer term stability of plant germplasm at the level of populations and species. Previously we demonstrated that experimental application of stresses to seeds, including X-irradiation or accelerated ageing (at 35°C and 83% relative humidity), resulted in PCD in early post-germination [ 16 ]. We hypothesised that similar effects occur in natural seed ageing and that cell death persists throughout seedling establishment, indicative of genome instability carried over from DNA damage incurred in the seed.…”

ATM and ATR, two central players of the DNA damage response, are involved in the induction of systemic acquired resistance by extracellular DNA, but not the plant wound response

“…Even the NPR1-independent SAR induction via the ‘Dong-pathway’ requires SA as the DNA-damaging agent. Moreover, most studies assign partly overlapping, additive or even redundant functions to ATM and ATR ( 162 , 163 ), mainly because both kinases signal through the shared SUPPRESSOR OF GAMMA RESPONSE 1 (SOG1) ( 80 , 139 , 164 , 165 ). With exception of the sterility of double mutants of atm and atr ( 163 ), it seems difficult to envision a strictly ATM – and ATR-dependent process as it is indicated by our data for the DNA-induced increased in SA ( Figure 4C ).…”