Seeds and the Art of Genome Maintenance Waterworth, Wanda M; Bray, Clifford M; West, Christopher E
Frontiers in plant science,
05/2019, Volume:
10
Journal Article
Peer reviewed
Open access
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.
Genome integrity is crucial for cellular survival and the faithful transmission of genetic information. The eukaryotic cellular response to DNA damage is orchestrated by the DNA damage checkpoint ...kinases ATAXIA TELANGIECTASIA MUTATED (ATM) and ATM AND RAD3-RELATED (ATR). Here we identify important physiological roles for these sensor kinases in control of seed germination. We demonstrate that double-strand breaks (DSBs) are rate-limiting for germination. We identify that desiccation tolerant seeds exhibit a striking transcriptional DSB damage response during germination, indicative of high levels of genotoxic stress, which is induced following maturation drying and quiescence. Mutant atr and atm seeds are highly resistant to aging, establishing ATM and ATR as determinants of seed viability. In response to aging, ATM delays germination, whereas atm mutant seeds germinate with extensive chromosomal abnormalities. This identifies ATM as a major factor that controls germination in aged seeds, integrating progression through germination with surveillance of genome integrity. Mechanistically, ATM functions through control of DNA replication in imbibing seeds. ATM signaling is mediated by transcriptional control of the cell cycle inhibitor SIAMESE-RELATED 5, an essential factor required for the aging-induced delay to germination. In the soil seed bank, seeds exhibit increased transcript levels of ATM and ATR, with changes in dormancy and germination potential modulated by environmental signals, including temperature and soil moisture. Collectively, our findings reveal physiological functions for these sensor kinases in linking genome integrity to germination, thereby influencing seed quality, crucial for plant survival in the natural environment and sustainable crop production.
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.
Seeds are important to agriculture and conservation of plant biodiversity. In agriculture, seed germination performance is an important determinant of crop yield, in particular under adverse climatic ...conditions. Deterioration in seed quality is associated with the accumulation of cellular damage to macromolecules including lipids, protein, and DNA. Mechanisms that mitigate the deleterious cellular damage incurred in the quiescent state and in cycles of desiccation–hydration are crucial for the maintenance of seed viability and germination vigour. In early-imbibing seeds, damage to the embryo genome must be repaired prior to initiation of cell division to minimize growth inhibition and mutation of genetic information. Here we review recent advances that have established molecular links between genome integrity and seed quality. These studies identified that maintenance of genome integrity is particularly important to the seed stage of the plant lifecycle, revealing new insight into the physiological roles of plant DNA repair and recombination mechanisms. The high conservation of DNA repair and recombination factors across plant species underlines their potential as promising targets for the improvement of crop performance and development of molecular markers for prediction of seed vigour.
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.
Summary
DNA damage responses are crucial for plant growth under genotoxic stress. Accumulating evidence indicates that DNA damage responses differ between plant cell types. Here, quantitative shotgun ...phosphoproteomics provided high‐throughput analysis of the DNA damage response network in callus cells. MS analysis revealed a wide network of highly dynamic changes in the phosphoprotein profile of genotoxin‐treated cells, largely mediated by the ATAXIA TELANGIECTASIA MUTATED (ATM) protein kinase, representing candidate factors that modulate plant growth, development and DNA repair. A C‐terminal dual serine target motif unique to H2AX in the plant lineage showed 171‐fold phosphorylation that was absent in atm mutant lines. The physiological significance of post‐translational DNA damage signalling to plant growth and survival was demonstrated using reverse genetics and complementation studies of h2ax mutants, establishing the functional role of ATM‐mediated histone modification in plant growth under genotoxic stress. Our findings demonstrate the complexity and functional significance of post‐translational DNA damage signalling responses in plants and establish the requirement of H2AX phosphorylation for plant survival under genotoxic stress.
Significance Statement
This work demonstrates the central role for ATM in DNA damage signalling and establishes the functional requirement for H2AX phosphorylation in plant resistance to genotoxic stress. These results revealed the physiological significance of ATM‐dependent post‐translational protein modification in the plant DNA damage response in mitigating the deleterious cellular consequences of genome damage.
DNA damage threatens the integrity of the genome and has potentially lethal consequences for the organism. Plant DNA is under continuous assault from endogenous and environmental factors and ...effective detection and repair of DNA damage are essential to ensure the stability of the genome. One of the most cytotoxic forms of DNA damage are DNA double-strand breaks (DSBs) which fragment chromosomes. Failure to repair DSBs results in loss of large amounts of genetic information which, following cell division, severely compromises daughter cells that receive fragmented chromosomes. This review will survey recent advances in our understanding of plant responses to chromosomal breaks, including the sources of DNA damage, the detection and signalling of DSBs, mechanisms of DSB repair, the role of chromatin structure in repair, DNA damage signalling and the link between plant recombination pathways and transgene integration. These mechanisms are of critical importance for maintenance of plant genome stability and integrity under stress conditions and provide potential targets for the improvement of crop plants both for stress resistance and for increased precision in the generation of genetically improved varieties.
DNA repair is important for maintaining genome integrity. In plants, DNA damage accumulated in the embryo of seeds is repaired early in imbibition, and is important for germination performance and ...seed longevity. An essential step in most repair pathways is the DNA ligase-mediated rejoining of single- and double-strand breaks. Eukaryotes possess multiple DNA ligase enzymes, each having distinct roles in cellular metabolism. Here, we report the characterization of DNA LIGASE VI, which is only found in plant species. The primary structure of this ligase shows a unique N-terminal region that contains a β-CASP motif, which is found in a number of repair proteins, including the DNA double-strand break (DSB) repair factor Artemis. Phenotypic analysis revealed a delay in the germination of atlig6 mutants compared with wild-type lines, and this delay becomes markedly exacerbated in the presence of the genotoxin menadione. Arabidopsis atlig6 and atlig6 atlig4 mutants display significant hypersensitivity to controlled seed ageing, resulting in delayed germination and reduced seed viability relative to wild-type lines. In addition, atlig6 and atlig6 atlig4 mutants display increased sensitivity to low-temperature stress, resulting in delayed germination and reduced seedling vigour upon transfer to standard growth conditions. Seeds display a rapid transcriptional DNA DSB response, which is activated in the earliest stages of water imbibition, providing evidence for the accumulation of cytotoxic DSBs in the quiescent seed. These results implicate AtLIG6 and AtLIG4 as major determinants of Arabidopsis seed quality and longevity.
WHIRLY protein functions in plants Taylor, Rachel E.; West, Christopher E.; Foyer, Christine H.
Food and energy security,
March 2023, Volume:
12, Issue:
2
Journal Article
Peer reviewed
Open access
Environmental stresses pose a significant threat to food security. Understanding the function of proteins that regulate plant responses to biotic and abiotic stresses is therefore pivotal in ...developing strategies for crop improvement. The WHIRLY (WHY) family of DNA‐binding proteins are important in this regard because they fulfil a portfolio of important functions in organelles and nuclei. The WHY1 and WHY2 proteins function as transcription factors in the nucleus regulating phytohormone synthesis and associated growth and stress responses, as well as fulfilling crucial roles in DNA and RNA metabolism in plastids and mitochondria. WHY1, WHY2 (and WHY3 proteins in Arabidopsis) maintain organelle genome stability and serve as auxiliary factors for homologous recombination and double‐strand break repair. Our understanding of WHY protein functions has greatly increased in recent years, as has our knowledge of the flexibility of their localization and overlap of functions but there is no review of the topic in the literature. Our aim in this review was therefore to provide a comprehensive overview of the topic, discussing WHY protein functions in nuclei and organelles and highlighting roles in plant development and stress responses. In particular, we consider areas of uncertainty such as the flexible localization of WHY proteins in terms of retrograde signalling connecting mitochondria, plastids, and the nucleus. Moreover, we identify WHY proteins as important targets in plant breeding programmes designed to increase stress tolerance and the sustainability of crop yield in a changing climate.
WHY proteins serve important roles in plant development and stress tolerance. They function as transcription factors in the nucleus, as well as fulfilling crucial roles in DNA and RNA metabolism in chloroplasts and mitochondria. They are excellent potential targets for plant breeding strategies aiming to improve sustainable agriculture.
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