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Electrochemical Monitoring of ROS Influence on Seedlings And RSC Advances View Article Online PAPER View Journal | View Issue Electrochemical monitoring of ROS influence on seedlings and germination response to salinity Cite this: RSC Adv.,2019,9,17856 stress of three species of the tribe Inuleae† a a a Antonio Domenech-Carb´ o,´ * Paula Cervello-Bulls,´ Jose´ Miguel Gonzalez,´ b b a Pilar Soriano, Elena Estrelles and Noem´ı Montoya Solid-state electrochemical methods have been applied to the establishment of patterns of plant growth and response to saline stress using seedlings of Inula helenium L., Dittrichia viscosa (L.) Greuter (Inula viscosa (L.) Aiton), Limbarda crithmoides (L.) Dumort (Inula crithmoides L.). Upon in situ electrochemical generation of reactive oxygen species (ROS) the reactivity with such species was monitored using voltammetric signals associated to the oxidation of polyphenolic components of the plants. A simple kinetic model based on second-order reaction between ROS and polyphenolic components is applied to Received 4th April 2019 electrochemical data yielding apparent rate constants which can be correlated with the level of saline Accepted 28th May 2019 Creative Commons Attribution-NonCommercial 3.0 Unported Licence. stress revealing significant differences between the tested species. These results were contrasted with DOI: 10.1039/c9ra02556a the seed germination response to salt concentration in order to check potentiality of voltammetric rsc.li/rsc-advances techniques as analytical tools for evaluating salt stress tolerance in plants. Introduction and hydrogen peroxide (H2O2) can participate in a number of biochemical processes and, in particular, in adaptions associ- Soil salinity is one of the most important abiotic stresses in ated to both abiotic and biotic stress.8 plants determining success in germination and seedling ROS are involved in signaling events in normal cellular This article is licensed under a establishment. This factor induces alterations in the plant life metabolism and are produced from a variety of cytosolic cycle as a consequence of the effect on physiological and enzyme systems. However, at high concentrations, they produce biochemical attributes,1 and usually acts as a limiting factor toxic effects leading to the so-called “oxidative stress”, a condi- tion that disrupts redox signaling and control.9,10 Accordingly, Open Access Article. Published on 05 June 2019. Downloaded 9/26/2020 10:13:01 PM. that determines the distribution of species in salt marshes and other habitats where salt is present. plant cells have to be at least two mechanisms of ROS removing, Salt tolerance in plants is a result of the interaction of several the rst one controlling the ne modulation of their concen- factors that cover different aspects of plant physiology. These tration for signaling purposes, and the second to eliminate high aspects are linked to ion compartmentalization, osmolyte concentration levels of ROS in particular associated to the – production, osmotic adjustment, selective transport and uptake occurrence of hydric, saline, etc. stress.11 13 of ions, enzymatic and nonenzymatic antioxidant response to Due to the connection of oxidative stress with DNA muta- maintain the balance of reactive oxygen species (ROS), salt genesis14 and different diseases,15-17 there is an increasingly inclusion/excretion, and regulation of the expression levels of growing interest in evaluating the antioxidant effect of chem- different genes associated to salt tolerance.2–5 To reduce the icals, foods, vegetal extracts, etc.18 Although a variety of methods harmful effects of salt, plants use a series of morphological, have been proposed for this purpose, most of them are based on physiological and biochemical adaptations related to escape, chemical reactions with producers/scavengers of radicals (typi- avoidance and tolerance mechanisms.6 cally, 2,2-diphenyl-2-picrylhydrazyl (DPPHc), uorescein-AAPH 0 ROS play an important role in several biological processes (2,2 -azobis-2-methylpropanimidamide dihydrochloride)), and occurring in plants.7 Apart from hydroxyl radicals (HOc), monitoring Fenton-reaction, using 1,10-phenanthroline,18,19 cÀ c 20,21 superoxide radical anion (O ), hydroperoxide radical (HO2 ), these assays, including several electrochemical ones, measure a ‘global’, long time antioxidant activity of plant extracts (or individual plant components when these are iso- aDepartment of Analytical Chemistry, University of Valencia, Dr Moliner, 50, Burjassot, lated) but, as well as conventional HPLC studies,11–13,18,19 do not 46100, Valencia, Spain. E-mail: [email protected] provide direct mechanistic information on ROS reactivity with bICBiBE-Botanic Garden of the University of Valencia, Quart, 80, 46008, Valencia, the components of vegetal matter. Spain † Electronic supplementary information (ESI) available. See DOI: In this context, we have developed a solid-state electro- 10.1039/c9ra02556a chemical methodology for studying the interaction between 17856 | RSC Adv.,2019,9,17856–17867 This journal is © The Royal Society of Chemistry 2019 View Article Online Paper RSC Advances vegetal matter and electrochemically generated ROS aimed to Experimental monitor the reactivity of polyphenolic components of fruits22 and possible ROS relation with gynodioecy.23 This methodology Selection of the studied taxa exploits the possibility of electrochemical generation of ROS by The research was carried out using three different species of the applying reductive potential inputs to air-saturated aqueous genera Inula, Dittrichia and Limbarda. These species were solutions,24–26 combined with the voltammetry of immobilized previously included in the same genus, Inula, of the family particles (VIMP), a solid state technique developed by Scholz Asteraceae (¼Compositae): Inula helenium L., Dittrichia viscosa et al.27,28 which provides analytical information on sparingly (L.) Greuter, (Inula viscosa (L.) Aiton), and Limbarda crithmoides soluble solids attached to inert electrodes in contact with suit- (L.) Dumort, (Inula crithmoides L.). However, currently they are able electrolytes.29 The VIMP was previously applied to deter- considered three different genera within the tribe Inuleae, mine antioxidant capabilities of vegetal products30,31 and for belonging to the family Asteroidae.45 The selection took into electro-chemotaxonomic purposes32,33 and monitoring plant account the taxonomic proximity between genera and their defense against external stressors.34 distribution in different type of habitats, subjected to very The current work reports the application of this method- different salt stress levels. ology to monitor the interaction of ROS with the components of Dittrichia viscosa is a species widespread throughout the extracts from seedlings of Inula helenium L., Dittrichia viscosa Mediterranean areas, generally living in altered and anthrop- (L.) Greuter, and Limbarda crithmoides (L.) Dumort, three ized areas like abandoned crop elds, debris storage areas or species of the tribe Inuleae. This is a large tribe, belonging the altered road edges.46 Limbarda crithmoides is a succulent Asteraceae family, that comprises more than 50 genera whose perennial species distributed in Western Europe, and Mediter- species are widespread in temperate regions of Europe, Asia and ranean basin, mainly in coastal areas, living in salt marshes, North of Africa. Its genera are a good example of habitat halophilous reedbeds, coastal sands, shingle banks and mari- diversity so that the salt tolerance varies between species, even time cliffs.47 Inula helenium is a perennial species, it is widely 47 Creative Commons Attribution-NonCommercial 3.0 Unported Licence. of the same genus, according to the ecological characteristics of distributed in Europe, East Asia and North America, growing their habitat. in woodland margins, roadsides, meadows, usually close to The voltammetric method exploits the electroactive char- cultivated elds and inhabited areas. It is a widely cultivated acter of polyphenolic compounds, (lignins, avonoids, avo- species by its high ornamental value. nols, avones, ..) abundantly represented in the leaves of the 35–40 tribe. Most of these components display well-known Germination experiments oxidations of o-catechol units to the corresponding o- To check seed germination tolerance to salt, seeds were sowed quinones highly sensitive to the overall molecular struc- on increasing salt concentrations: 50, 100, 150, 200, 300, and ture.20–23,30–34,41,42 Ultimately, the current work was aimed to This article is licensed under a 400 mM of NaCl, in order to compare the response to a control provide an analytical tool to be used in the botanic science without salt in the medium. The substrate with the different salt frame to acquire ‘direct’ mechanistic information on ROS solutions was prepared with agar 0.6%, and germination was reactivity and its relation with biochemical processes that is conducted at 25 C, temperature previously established as Open Access Article. Published on 05 June 2019. Downloaded 9/26/2020 10:13:01 PM. unavailable from the usual HPLC methodologies. As an illus- À À optimal, with a 12/12 h photoperiod (100 mmol m 2 s 1) with trativeexample,herewecomparethesalttoleranceofthe uorescent daylight tubes, during 30 days. Aer this testing previously mentioned species in germination phase. The use period, no germinated seeds in the plates with salt concentra- of the proposed electrochemical methodology, although does tion from 100 mM were transferred to 0.6% agar substrate not provide
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