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Chronic Ionizing Radiation of Plants: An Evolutionary Factor from Direct Damage to Non-Target Effects.

ABSTRACT: In present times, the levels of ionizing radiation (IR) on the surface of Earth are relatively low, posing no high challenges for the survival of contemporary life forms. IR derives from natural sources and naturally occurring radioactive materials (NORM), the nuclear industry, medical applications, and as a result of radiation disasters or nuclear tests. In the current review, we discuss modern sources of radioactivity, its direct and indirect effects on different plant species, and the scope of the radiation protection of plants. We present an overview of the molecular mechanisms of radiation responses in plants, which leads to a tempting conjecture of the evolutionary role of IR as a limiting factor for land colonization and plant diversification rates. The hypothesis-driven analysis of available plant genomic data suggests an overall DNA repair gene families' depletion in land plants compared to ancestral groups, which overlaps with a decrease in levels of radiation exposure on the surface of Earth millions of years ago. The potential contribution of chronic IR as an evolutionary factor in combination with other environmental factors is discussed.

SUBMITTER: Duarte GT

PROVIDER: S-EPMC10005729 | biostudies-literature | 2023 Mar

REPOSITORIES: biostudies-literature

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Chronic Ionizing Radiation of Plants: An Evolutionary Factor from Direct Damage to Non-Target Effects.

Duarte Gustavo Turqueto GT Volkova Polina Yu PY Fiengo Perez Fabricio F Horemans Nele N

Plants (Basel, Switzerland) 20230304 5

In present times, the levels of ionizing radiation (IR) on the surface of Earth are relatively low, posing no high challenges for the survival of contemporary life forms. IR derives from natural sources and naturally occurring radioactive materials (NORM), the nuclear industry, medical applications, and as a result of radiation disasters or nuclear tests. In the current review, we discuss modern sources of radioactivity, its direct and indirect effects on different plant species, and the scope o ...[more]

PMID: 36904038

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Project description:Understanding the effects of ionizing radiation (IR) on plants is important for environmental protection, for agriculture and horticulture, and for space science but plants have significant biological differences to the animals from which much relevant knowledge is derived. The effects of IR on plants are understood best at acute high doses because there have been; (a) controlled experiments in the field using point sources, (b) field studies in the immediate aftermath of nuclear accidents, and (c) controlled laboratory experiments. A compilation of studies of the effects of IR on plants reveals that although there are numerous field studies of the effects of chronic low doses on plants, there are few controlled experiments that used chronic low doses. Using the Bradford-Hill criteria widely used in epidemiological studies we suggest that a new phase of chronic low-level radiation research on plants is desirable if its effects are to be properly elucidated. We emphasize the plant biological contexts that should direct such research. We review previously reported effects from the molecular to community level and, using a plant stress biology context, discuss a variety of acute high- and chronic low-dose data against Derived Consideration Reference Levels (DCRLs) used for environmental protection. We suggest that chronic low-level IR can sometimes have effects at the molecular and cytogenetic level at DCRL dose rates (and perhaps below) but that there are unlikely to be environmentally significant effects at higher levels of biological organization. We conclude that, although current data meets only some of the Bradford-Hill criteria, current DCRLs for plants are very likely to be appropriate at biological scales relevant to environmental protection (and for which they were intended) but that research designed with an appropriate biological context and with more of the Bradford-Hill criteria in mind would strengthen this assertion. We note that the effects of IR have been investigated on only a small proportion of plant species and that research with a wider range of species might improve not only the understanding of the biological effects of radiation but also that of the response of plants to environmental stress.

Project description:Purpose: Insulin-like growth factor-1 (IGF-1) stimulates epithelial regeneration but may also induce life-threatening hypoglycemia. In our study, we first assessed its safety. Subsequently, we examined the effect of IGF-1 administered in different dose regimens on gastrointestinal damage induced by high doses of gamma radiation. Material and methods: First, fasting C57BL/6 mice were injected subcutaneously with IGF-1 at a single dose of 0, 0.2, 1, and 2 mg/kg to determine the maximum tolerated dose (MTD). The glycemic effect of MTD (1 mg/kg) was additionally tested in non-fasting animals. Subsequently, a survival experiment was performed. Animals were irradiated (60Co; 14, 14.5, or 15 Gy; shielded head), and IGF-1 was administered subcutaneously at 1 mg/kg 1, 24, and 48 h after irradiation. Simultaneously, mice were irradiated (60Co; 12, 14, or 15 Gy; shielded head), and IGF-1 was administered subcutaneously under the same regimen. Jejunum and lung damage were assessed 84 h after irradiation. Finally, we evaluated the effect of six different IGF-1 dosage regimens administered subcutaneously on gastrointestinal damage and peripheral blood changes in mice 6 days after irradiation (60Co; 12 and 14 Gy; shielded head). The regimens differed in the number of doses (one to five doses) and the onset of administration (starting at 1 [five regimens] or 24 h [one regimen] after irradiation). Results: MTD was established at 1 mg/kg. MTD mitigated lethality induced by 14 Gy and reduced jejunum and lung damage caused by 12 and 14 Gy. However, different dosing regimens showed different efficacy, with three and four doses (administered 1, 24, and 48 h and 1, 24, 48, and 72 h after irradiation, respectively) being the most effective. The three-dose regimens supported intestinal regeneration even if the administration started at 24 h after irradiation, but its potency decreased. Conclusion: IGF-1 seems promising in the mitigation of high-dose irradiation damage. However, the selected dosage regimen affects its efficacy.

Project description:Ionizing radiation is a harsh environmental factor that could induce plant aging. We hypothesized that radiation-related aging remodels proteome, particularly triggering the accumulation of prion-like proteins in tissues. The object of this study, pea (Pisum sativum), is an agriculturally important legume. Research on the functional importance of amyloidogenic proteins was never performed on this species. Pea seeds were irradiated by 50 Gy of X-rays. Afterwards, Fourier-transform infrared spectroscopy (FTIR) was used to investigate changes in the secondary structure of proteins in germinated seedlings. Specifically, we evaluated the ratio between the amide I and II peaks. Next, we performed protein staining with Congo red to compare the presence of amyloids in the samples. In parallel, we profiled detergent-resistant proteome fraction by ultrahigh-performance liquid chromatography coupled to tandem mass spectrometry (UHPLC-MS). Differentially accumulated proteins were functionally analyzed in MapMan software, and the PLAAC tool was used to reveal putative prion-like proteins. We showed a reduced germination rate, yet higher plant height and faster appearance of reproductive organs in the irradiated group compared with the control; furthermore, we demonstrated more β-sheets and amyloid aggregates in the leaves of stressed plants. We detected 531 proteins in detergent-resistant fraction extracted from roots, and 62 were annotated as putative prion-like proteins. Notably, 29 proteins were significantly differentially abundant between the irradiated and the control groups. These proteins belong to several functional categories: amino acid metabolism, carbohydrate metabolism, cytoskeleton organization, regulatory processes, protein biosynthesis, and RNA processing. Thus, discovery proteomics provided deep data on novel aspects of plant stress biology. Our data hinted that protein accumulation stimulated seedlings' growth and affected the regulatory system, primarily through translation and RNA processing. Increased abundance of primary metabolism-related proteins points to more intensive metabolic processes triggered in germinating pea seeds upon X-ray exposure. The functional role of detected putative amyloidogenic proteins should be validated in overexpression or knockout follow-up studies.

Dataset Information

Chronic Ionizing Radiation of Plants: An Evolutionary Factor from Direct Damage to Non-Target Effects.

Publications

Chronic Ionizing Radiation of Plants: An Evolutionary Factor from Direct Damage to Non-Target Effects.

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