Seeds and the Art of Genome Maintenance

Abstract

Successful germination represents a crucial developmental transition in the plant lifecycle and is important both for crop yields and plant survival in natural ecosystems. However, germination potential decreases during storage and seed longevity is a key determinant of crop production. Decline in germination vigor is initially manifest as an increasing delay to radicle emergence and the completion of germination and eventually culminating in loss of seed viability. The molecular mechanisms that determine seed germination vigor and viability remain obscure, although deterioration in seed quality is associated with the accumulation of damage to cellular structures and macromolecules including lipids, protein, and nucleic acids. In desiccation tolerant seeds, desiccation/rehydration cycles and prolonged periods in the dry quiescent state are associated with remarkable levels of stress to the embryo genome which can result in mutagenesis of the genetic material, inhibition of transcription and replication and delayed growth and development. An increasing number of studies are revealing DNA damage accumulated in the embryo genome, and the repair capacity of the seed to reverse this damage, as major factors that determine seed vigor and viability. Recent findings are now establishing important roles for the DNA damage response in regulating germination, imposing a delay to germination in aged seed to minimize the deleterious consequences of DNA damage accumulated in the dry quiescent state. Understanding the mechanistic basis of seed longevity will underpin the directed improvement of crop varieties and support preservation of plant genetic resources in seed banks.

Keywords: DNA repair; aging; germination; priming; seeds.

Figure 1

DNA damage lesions and their DNA repair pathways in seeds. Nucleotide excision repair (NER) repairs damage on a single strand of the duplex, with specificity for bulky adducts and forms of damage that block RNA polymerase. Base excision repair (BER) removes damaged bases and repairs single strand breaks (SSBs). DNA double strand breaks (DSBs) are repaired by homologous recombination (HR), non-homologous end joining (NHEJ), or alternative NHEJ. Oxo G is 8-oxoguanine.

Figure 2

The DNA damage response (DDR) in seeds. The DNA damage response executes a coordinated network of responses in order to minimize the consequences of genome damage to the cell, including activation of cell cycle checkpoints, DNA repair factors, and programmed cell death (PCD). The master kinases ATAXIA TELANGIECTASIA MUTATED (ATM) and ATM AND RAD3-RELATED (ATR) control the cellular response to DNA damage in eukaryotes through activation of downstream responses at the transcriptional and post-transcriptional levels. ATM controls advancement of germination in aged seeds, in part through transcriptional control of the cell cycle inhibitor SIAMESE RELATED 5 (SMR5). Both ATM and ATR influence seed viability but the molecular mechanism is unknown. In plants the transcriptional DDR encompasses hundreds of genes encoding proteins involved in DNA repair, chromatin remodeling and DNA metabolism. In the early stages of imbibition, seeds exhibit a large and rapid ATM-dependent transcriptional DNA damage response early in imbibition. DNA repair synthesis is detectable from the earliest stages of imbibition. As seed aging progresses and radicle emergence is delayed, this lag phase to germination is accompanied by an ATM-mediated delay of cell cycle activation in the root apical meristem (RAM) and extension of DNA repair activities.