期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2022
卷号：119
期号：30
DOI：10.1073/pnas.2202172119
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：Significance
Successful germination underpins crop production and natural ecosystems. However, the desiccation-tolerant seed accumulates striking levels of genome damage in quiescence associated with seed aging. Here, we show that seeds display intrinsic resistance to genome stress, which is lost as seeds advance to germination. Seeds minimize meristem disruption and delay programmed cell death in response to seed aging to promote root growth early postgermination. This reveals distinct responses of seeds to DNA damage in terms of growth and transcriptional profiles, which support rapid seedling establishment at this crucial stage of the plant lifecycle. These findings advance our understanding of both plant DNA damage responses and seed longevity, important for crop yields and plant survival under changing climates.
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.
