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

Abstract

Successful germination and seedling establishment are important determinants of crop yields and plant survival in natural environments. Germination potential is compromised by suboptimal environmental conditions that result in seed ageing and high levels of genome damage. However, the mutagenic and growth inhibitory potential of DNA damage accumulated in seeds on subsequent seedling growth remains largely unknown. Arabidopsis seeds deficient in the chromosomal break repair factors DNA LIGASE 4 and DNA LIGASE 6 exhibited hypersensitivity to the effects of natural ageing, with reduced germination vigour and seedling biomass relative to wild type seed. Here we identify that aged Arabidopsis seed display elevated levels of programmed cell death (PCD) in the root meristem which persists into seedling establishment, with higher levels of cell death in lines deficient in DNA double strand break repair. Reporter lines determined the effects of seed ageing on mutation levels and intrachromosomal recombination frequencies. Seed deterioration resulted in strikingly elevated levels of frameshift mutations and genome instability in germinated seedlings. Thus, elevated levels genome damage incurred in the seed stage of the plant life cycle potentially impacts significantly on subsequent plant development. Furthermore, the mutagenic effects of seed ageing has potentially long-term implications on the genome stability of plant populations and ecosystem fitness. Collectively, we identify genome damage accumulated in suboptimal quality seed impacts on subsequent plant growth and genome stability, with associated implications for crop yields and plant survival under changing climates.

Seed longevity and genome damage

“…Similarly, mutation in NHEJ pathway factors DNA LIGASE 4 (LIG4), DNA LIGASE 6 (LIG6) and KU80 results in hypersensitivity to accelerated ageing, indicating essential functions in maintaining genome integrity in germination [ 78 , 87 ]. Arabidopsis lig6 lig4 double mutants also displayed hypersensitivity to natural seed ageing for 10 years under ambient conditions [ 89 ]. The naturally aged DNA ligase deficient lines displayed significantly elevated frequencies of programmed cell death (PCD) in the apical meristem of roots three days post-germination.…”

“…The naturally aged DNA ligase deficient lines displayed significantly elevated frequencies of programmed cell death (PCD) in the apical meristem of roots three days post-germination. This indicates that DNA repair activities are required for recovery from seed ageing under both natural (long-term, dry ageing) storage conditions and after accelerated ageing at elevated temperature and humidity [ 78 , 89 ].…”

“…The factors that lead to poor seedling growth after seed ageing remain obscure at the molecular level. However, low vigour seeds germinate to produce seedlings with high levels of genome instabilty, resulting in extensive chromosomal abnormalies and increased intra-chromosomal recombination [ 72 , 77 , 89 ].…”

“…Seeds minimize the impact of genome damage observed at later stages of plant growth by reducing meristem disruption and delaying SOG1-dependent programmed cell death in response to genotoxic stress [ 87 ]. SOG1 activation of cell death in the RAM is delayed several days post-germination in response to both X-irradiation and natural seed ageing [ 87 , 89 ]. Thus, seeds promote post-germinative root growth to enable rapid seedling establishment and transition to independent resource acquisition and autotrophy.…”

“…The mutagenic potential of DNA damage accumulated in seeds on subsequent plant growth remains largely unknown. Analysis of genome instability in seedlings germinated from ageing Arabidopsis seeds identified striking increases in both frameshift mutations (using a microsatellite stability reporter line) and genome stability (using an intrachromosomal recombination reporter) as germination vigour declined [ 89 ]. Thus, elevated levels of genome damage incurred in the seed stage of the plant life cycle potentially impact on subsequent plant development.…”