Effect of chronic β-radiation on long-distance electrical signals in wheat and their role in adaptation to heat stress
Graphical abstract
Introduction
The effects of ionizing radiation (IR) on living organisms, including plants, have been the subject of numerous studies. The reason for such attention is the variety of conditions under which plants can be exposed to a high level of radiation: lands with high background radiation due to natural and man-made sources, space stations, laboratories for the creation of new plant varieties. Currently, there is no doubt that the effects exerted on plants by IR are dose-time dependent (De Micco et al., 2011; Caplin and Willey, 2018; Gudkov et al., 2019). It is commonly believed that high doses of IR inhibit the growth and development of plants; however the low ones, on the contrary, have a stimulating effect. Irradiation in high doses inhibits the activity of a number of physiological processes, primarily photosynthesis, transport, leads to a decrease in pigment contents, inhibition of the biosynthesis of key metabolites, disruption of the cell cycle, the appearance of numerous mutations, etc., which causes suppression of plant growth and development (Marcu et al., 2013; Ahuja et al., 2014a; Van Hoeck et al., 2015). The observed disturbances are associated with increased oxidative processes that damage macromolecules and membranes (Esnault et al., 2010; Xie et al., 2019). When irradiated in low doses, an increase in such morphometric parameters as length, leaf area, fresh and dry weight, an accelerated development of plants are observed (Singh et al., 2013; Beyaz et al., 2016; Kumar et al., 2017). The stimulating effect of IR manifested in the growth of morphometric parameters is associated with the activation of a number of physiological processes, including photosynthesis, transpiration, etc. (Kim et al., 2004; Vanhoudt et al., 2014; Arena et al., 2019). As a key factor in stimulating the activity of physiological processes, activation of the antioxidant system is usually considered (De Micco et al., 2011).
The vast majority of works reporting the stimulating effect of low doses of IR take into account the influence of only one factor – the actual effects of IR. Plants, which are growing in areas with increased background radiation, along with radiation, are also affected by other adverse factors in the environment. However, the influence of environmental stress factors on irradiated plants has been studied on the very low level (Beresford et al., 2020).
It is known that irradiation in low doses can reduce the negative effect of a number of adverse factors, such as salt stress, heavy metals, drought, and lead to a partial restoration of morphometric and some physiological parameters of plants (Vanhoudt et al., 2010; Alikamanoglu et al., 2011; Macovei et al., 2014; Deng et al., 2017). In laboratory conditions, the combined effect of low doses of IR and stress factors is usually studied according to the following scheme: a single exposure of dry seeds to IR, then the chronic action of a stress factor. However, even the effect of equal low doses of IR differs for chronic and acute exposure modes, which, in particular, is expressed in the difference in gene expression profiles (Kovalchuk et al., 2007). In natural conditions, where there is a chronic exposure, the combined effect of IR and other stressors has virtually not been studied. There are only a few works reporting the effect of weather conditions such as temperature and humidity on a quality of seeds of plants, growing in areas with increased background radiation (Geras’kin et al., 2017; Pozolotina and Antonova, 2017). The detected increase in the resistance of irradiated plants to stress factors at the cell level is apparently resulted from the activation of the antioxidant system and the activation of the DNA repair systems (Kovalchuk et al., 2004; Culligan et al., 2006; Yoshiyama et al., 2014). An increase in genetic heterogeneity due to accelerated mutagenesis is suggested as a mechanism that works at the population level (Pozolotina and Antonova, 2017; Antonova et al., 2019). In addition to the listed, there may be other causes of altered stress resistance. At the level of the organism, an increase in resistance may be due to the modification of stress signaling under chronic IR exposure, which play an important role in the formation of a systemic adaptation under the influence of local and total stressors.
Due to the immobile lifestyle, plants developed an advanced system of stress signals, which have a different nature and are divided into chemical, hydraulic and electrical (Huber and Bauerle, 2016). Long-distance electrical signals of plants are represented by three main types of reactions: action potential, variation potential and system potential (Zimmermann et al., 2009; Vodeneev et al., 2015). Variation potential (VP) is of particular interest for several reasons. VP arises in response to a variety of rapidly growing adverse factors: a strong temperature rise, mechanical damage, an attack by leaf-eating insects, etc. (Vodeneev et al., 2017; Chatterjee et al., 2018). The VP is, apparently, a complex reaction, which includes, along with the depolarization wave, Ca2+ and ROS waves accelerated by the hydraulic pressure wave (Vodeneev et al., 2015; Choi et al., 2016; Gilroy et al., 2016). It is important to note that changes in Ca2+ and ROS concentrations and the pH shifts caused by them are the most important steps for activation of intracellular signaling systems, which are probably involved in the induction of functional responses triggered by an electric signal. Such responses include: transient inactivation of photosynthesis and transpiration, activation of respiration, changes in gene expression, etc. (Fromm and Lautner, 2007; Mousavi et al., 2013; Sukhov, 2016). In general, such functional responses, universal for impacts of various nature, allow forming adaptation of plants to rapidly growing environmental stress factors (Sukhov et al., 2014; Choi et al., 2016; Sukhov et al., 2019).
It is known that acute irradiation in high doses of by itself can induce long-distance signals in plants (Esch et al., 1964; Wang et al., 2011). Chronic irradiation of the whole organism in low doses, apparently, does not cause long-distance signals, but, probably, changes the status of signaling systems. To date, the information about the effect of IR on individual components of distant signaling in plants is fragmentary. Thus, IR influences the hormonal status of plants and modifies the hormone-response paths: at low IR doses, the contribution of stimulating hormones, such as indolylacetic acid (IAA), cytokinins, gibberellins, increases (Latif et al., 2011; Bitarishvili et al., 2018). A change in the parameters of the electric signals by type of action potential, due to the modification of the activity of ion channels on isolated cells of irradiated characea was shown (Sevriukova et al., 2014). Analysis of gene expression revealed modified gene expression of proteins that are involved in the ROS-Ca2+ signaling in irradiated plants (Kim et al., 2012; Goh et al., 2014; Qi et al., 2015), which may be important not only for intracellular, but also for distance signals. On the whole, the data available are insufficient to form a complete picture of the IR impact on long-distance signaling and the role of signals in plant adaptation to stressors.
The aim of the work was to study the effect of chronic irradiation in low doses on the change in plant resistance to rapidly growing stressors induced by electrical signals. The work simulates a situation when plants growing under high background radiation are subjected to additional stressor (high temperature) and form resistance to heat stress. We studied the effect of IR on (1) morphometric parameters and activity of some physiological processes in unstressed plants, (2) parameters of electrical signals, (3) responses of physiological processes induced by electrical signals, (4) formation of plant resistance to heat stress.
Section snippets
Plant growth and β-irradiation conditions
Studies were conducted on 15−16-day-old seedlings of wheat (Triticum aestivum L.), variety "Daria". The seeds were germinated for 3 days in distilled water, after which the seedlings were transplanted into vessels with sand. Plants grow at 24 °C with a 16-h light/8-h dark cycle.
Irradiation was conducted using a sealed 90Sr-90Y-source with an activity of 0.1 MBq. The source design is a disc 27 mm in diameter, in the center of which there is an active spot (5 mm in diameter), sealed with two
The effect of ionizing radiation on the morphofunctional state of plants
To evaluate the effect of IR on plants at resting state, we examined morphometric parameters, photosynthesis and transpiration activity, membrane potential, and measured the degree of lipid oxidation and the activity of antioxidant enzymes.
No significant differences in the morphometric parameters of irradiated and control wheat seedlings were found (Fig. 2). There is a tendency for an increase in the length and fresh weight of irradiated plants (39.8 ± 0.9 cm and 280 ± 10 mg in the control,
Discussion
It is well known that the IR action on living organisms is mediated mainly by ROS generated during the radiolysis of water (Ward, 1988; Bruskov et al., 2012). At the same time long-term effects of IR are based on the damage of biomolecules and the formation of "secondary" ROS, which can be formed due to changes in the activity of signaling ROS-producing systems, and also due to disruption of electron transport chains (ETC) as a result of IR (Gudkov et al., 2019). Depending on the absorbed dose
Conclusion
Chronic low-doses β-irradiation modifies distant signaling of wheat plants exposed to stress factor. Both the signals’ parameters and functional responses induced by them are undergoing quantitative changes with preserved direction of the stress driven reaction. The changes, however, can lead to qualitative alterations in resulted resistance to stress factor. The phenomenon was demonstrated for the heat stress resistance of wheat plant induced by local heating of the tip of one of the leaves.
Author contributions
Conception and design – M.G., S.G., V.V.; collection and assembly of data – M.G., E.G., Yu. S.; analysis and interpretation of the data – M.G., S.G., Yu. S., V.S, V.V.; drafting of the article – M.G., I.B., V.V.; final approval of the article – M.G., V.V.
Declaration of Competing Interest
The authors declare no conflicts of interest.
Acknowledgements
This work was supported by the Russian Foundation for Basic Research (No 19-04-01141, 17-29-08026) and Ministry of Science and Higher Education of the Russian Federation (contract no. 0729-2020-0061).
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