Chromosome Aberrations Induced during Storage in Barley and Pea Seeds

Dourado, A. M.; Roberts, Ε. H.

doi:10.1093/oxfordjournals.aob.a086849

Cited by 29 publications

(28 citation statements)

References 14 publications

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“…Seed aging is associated with an increasing incidence of chromosomal aberrations (Fig. 4 H-L), and even seed lots with high germination rates display levels of genome damage not seen at other stages of plant development (12,22). Consistent with this, during the early imbibition phase, seeds display a large and rapid induction of the ATM-mediated transcriptional DSB response (23).…”

Section: Discussionmentioning

confidence: 57%

“…Cytological studies have established a correlation between loss of vigor and viability on seed aging and accumulation of DNA damage, reporting increased frequencies of both chromosome breakage and rearrangements and abnormal, mutated seedlings on germination of aged seed (11). Significantly, even high-quality seeds display a background level of chromosomal breaks (i.e., DSBs) (12,22).…”

Section: Significancementioning

confidence: 99%

“…Reduced cellular maintenance in the quiescent state, in combination with cycle(s) of desiccation and rehydration, are associated with high levels of damage by reactive oxygen species, resulting in deterioration of proteins, DNA, and cellular structures (11). Genome damage is exacerbated by adverse environmental conditions (typically high temperature and relative humidity) that cause increased oxidative damage and seed aging (12)(13)(14)(15). This results in a loss of seed vigor, manifested as decreasing rapidity and uniformity of germination, leading to significant losses in yield in crop species (16), and ultimately culminates in loss of viability (17).…”

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confidence: 99%

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DNA damage checkpoint kinase ATM regulates germination and maintains genome stability in seeds

Waterworth

Footitt

Bray

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

101

113

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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.DNA repair | seed vigor | DNA damage response | dormancy cycling | soil seed bank M aintenance of genome integrity is indispensable for cellular survival and transmission of genetic information to the next generation; however, constant exposure of DNA to environmental and cellular oxidative stresses results in damage that can arrest growth and result in mutagenesis or cell death. Consequently, organisms have evolved powerful DNA repair and DNA damage signaling mechanisms. In plants, as in other eukaryotes, the cellular response to DNA damage is orchestrated by the phosphoinositide-3-kinase-related protein kinases (PIKKs) ATAXIA TELANGIECTASIA MUTATED (ATM) and ATM AND RAD3-RELATED (ATR) (1). In response to genotoxic stresses, these checkpoint kinases activate DNA repair factors, delay or halt cell cycle progression, and promote endocycles or programmed cell death (1-4). ATM is activated by double-strand DNA breaks (DSBs), a highly toxic form of DNA damage that results in chromosome fragmentation (1, 5), and plants mutated in ATM display hypersensitivity to DSBs induced by gamma radiation or radiomimetics (6). ATM also mediates a strong transcriptional up-regulation of hundreds of genes, including the SIAMESE/SIAMESE-RELATED cell cycle inhibitors ...

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Section: Discussionmentioning

confidence: 57%

Section: Significancementioning

confidence: 99%

mentioning

confidence: 99%

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DNA damage checkpoint kinase ATM regulates germination and maintains genome stability in seeds

Waterworth

Footitt

Bray

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

101

113

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“…Gunthardt et al (1953) and Nuti Ronchi and Martini (1962) reported the predominance of chromosome-type aberrations in the first mitotic divisions, while Corsi and Avanzi (1969) and Innocenti and Avanzi (1971) observed mainly chromatid type aberrations in their studies. Similarly in pea (Pisum sativum L.) D'Amato (1951) and Abdalla and Roberts (1968) reported chromosome-type aberrations, but Dourado and Roberts (1984) observed the predominance of chromatid-type aberrations. This controversy is partly attributable to the lack of synchronization of the mitotic divisions and to the hypothesis which is adopted for classification of the aberrations.…”

mentioning

confidence: 93%

“…However, their interpretations are based on the Classical Theory of chromosome breakage and reunion, proposed originally by Sax (1941). Recently, Dourado and Roberts (1984) suggested that chromosomal aberra tions in aged seeds are unlikely to be produced by direct breakage in the DNA strands since it requires high energy quanta, and the only known source of this during normal storage the background radiation-was discounted as the possible cause (Giles 1940, Gunthardt et al 1953. It was argued that the mechanism of production of chromosomal aberrations in aged seeds may well be similar to that induced by chemical mutagens; therefore, it is more appropriate to adopt the Exchange Hypothesis proposed by Revell (1959) for application to seed ageing problems (Dourado andRoberts 1984, Roberts 1988).…”

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confidence: 99%

Types of chromosomal aberrations at first mitosis in aged lettuce (lactuca sativa L.) seeds.

Rao

Roberts

1990

CYTOLOGIA

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Damage to the genome of the seeds induced during storage manifests as chromosomal aberrations in the first mitotic divisions during germination (see Roberts 1988) . By analogy with the work on ionising radiations in plants, many investigators in the past classified the ageing induced chromosomal aberrations observed in their studies into two broad categories chromosome and chromatid types, the former when the damage affected both the chromatids of the chromosome at the same location, and the latter when only one of the sister chromatids was affected at a given location. A survey of the literature on ageing-induced chromosomal aberrations in seeds shows that, even for the same species, the results are conflicting. For example, in wheat (Triticum spp.) Gunthardt et al. (1953) and Nuti Ronchi and Martini (1962) reported the predominance of chromosome-type aberrations in the first mitotic divisions, while Corsi and Avanzi (1969) and Innocenti and Avanzi (1971) observed mainly chromatid type aberrations in their studies. Similarly in pea (Pisum sativum L.) D'Amato (1951) and Abdalla and Roberts (1968) reported chromosome-type aberrations, but Dourado and Roberts (1984) observed the predominance of chromatid-type aberrations. This controversy is partly attributable to the lack of synchronization of the mitotic divisions and to the hypothesis which is adopted for classification of the aberrations. In addition, factors like seed age also affect the spectrum of aberrations scored in the first mitotic divisions. For example, Orlova (1967) and Orlova and Nikitina (1968) in Welsh onion (Allium fistulosum L.) and Sevov et al. (1973) in maize (Zea mays L.) found a relatively greater accumulation of the chromosome type aberrations with increased age of the seeds. Possibly differences in temperature and seed moisture content might also influence the type of chromosome damage induced during storage, but we are aware of no published information which sheds light on these possibilities.Recently, we found (Rao et al. 1987) a negative relationship between the seed moisture content and the amount of chromosome damage which accumulated for any given loss in viability in lettuce seeds; and this reinforces the possibility mentioned ahove that seed moisture content could also affect the type of damage induced in the genome during storage. The purpose of this paper is to examine the effect of moisture content of stored seeds on the Type of chromosome damage observed in the first mitotic anaphases of the surviving seeds. Materials and methodsAchenes (seeds) of lettuce (Lactuca sativa L.) cv. Trocadero Improved which had an initial viability of 98% were used in this study. These were conditioned to six moisture con tents, 3.3, 5.5, 8.1, 9.8, 13.0 and 18.1% [seed moisture content is described on wet weight basis and was determined according to ISTA Rules (ISTA 1985a, b)]. They were then sub-divided into samples of 500 or more seeds and sealed in laminated aluminium foil packets for storage

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