Central International Journal of Plant Biology & Research

Special Issue on Plant Stress Biology Edited by: Qingmei Guan Department of Plant Science and Landscape Architecture, University of Maryland, USA

Mini Review *Corresponding author Anuluxshy Balasubramaniyam, Faculty of Engineering and Science, University of Greenwich, Medway Hormetic Dose Response as the Campus, Chatham Maritime, Kent, ME4 4TB, UK, Email:

Paradigm of Plant Response to Submitted: 05 March 2015 Accepted: 15 April 2015 Published: 19 April 2015 Stress ISSN: 2333-6668 Anuluxshy Balasubramaniyam* Copyright © 2015 Balasubramaniyam Faculty of Engineering and Science, University of Greenwich, UK OPEN ACCESS

Abstract The paradigm of the response of a biological organism to exposure to stressor agents is hormetic dose response, in which high doses of a stressor are toxic or harmful but low doses are beneficial. The exploitation of this biological characteristic could enable the efficient use of plants in the fields of phytoremediation and agriculture.

INTRODUCTION under stressful conditions, plants need to adapt themselves to Life on earth is surrounded by many challenges constantly through a series of molecular responses to cope with the adverse creating disturbances in the sensitive, dynamic equilibrium a conditions.their growth The environment integration that of many exposes transduced them to stress events factors, into a living organism inherently possesses and the delicate mutual comprehensive network of signalling pathways forms the basis relationship between the living being and its environment. The of the physiological processes for the molecular responses, challenges may come in the form of biotic stressors such as which enable the plants to adapt to the adverse conditions. Plant pathogenic microorganisms or abiotic factors such as drought hormones may act in conjunction with other signals to regulate arising from environmental perturbations. Thanks to cellular cellular processes such as division, elongation and differentiation. homeostasis, the internal system of an organism is well designed to sense changes in its environment, to adapt to stress situations the ecosystem, the mutual concerted relationship between plants and to restore the stable internal environment. andSince the stress environment factors are whichalso major presents ecological the cues factors or influencing stimuli for Unlike animals, higher plants, cannot escape from their the plants to evolve molecular mechanisms of stress signalling surroundings, as they are sessile, thereby their interactions pathways is fundamental. The plant signalling pathways and with their growth environment which may present stress sensor network as adaptive mechanisms to environmental respond to the stress conditions are critical. In order to grow sustainable development [1,2]. factors such as water deficiency and toxicity and how the plants stress are crucial in the contexts of agricultural environment and

Cite this article: Balasubramaniyam A (2015) Hormetic Dose Response as the Paradigm of Plant Response to Stress. Int J Plant Biol Res 3(2): 1037. Balasubramaniyam (2015) Email:

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in biological organisms. The delicate equilibrium between

Reactive oxygen species (ROS) are produced in the presence act as damaging or signalling molecule [3]. Evolving effective of oxygen as a product of cellular metabolism, but exposure to ROS production and scavenging determines whether ROS will any stress factor results in the excessive production of ROS stress that inversely correlates with lifespan in a variety of triggerwhich maya cascade result of inevents oxidative that leads stress to conferment which is a of deleterious tolerance antioxidant defence responses is critical in resisting oxidative toprocess. various Despite environmental their destructive stresses activity,[3]. More ROS often are than also not, able this to renders an organism the capability to resist tougher challenges. organisms [15] including plants. stress have been widely reported in the literature [16-19]. The protective effects of soluble sugars against oxidative to stress promotes destruction or resilience [4]. Biphasic dose- sugars at high Here dose is the criterion that determines whether exposure In addition to functioning as antioxidants, entering the concentrations (sucrose, fructans, sugar-like compounds)2 2 may formsresponse the basis (hormesis), for the adaptive in which responses high doses of a living of a organism substance/ to vacuole [19], producing sugar radicals. A study conducted by directly scavenge ROS derived from excess H O stressstressor conditions agent are [4-6]. toxic/ Biphasic harmful responses but low doseshave been are beneficial, reported in organisms ranging from bacteria to human, but to date, showed that the abundance of glucose, galactose, UDP-glucose, Balasubramaniyam and Harvey (2014b) [20] on tall fescue [4]. To date, only a limited number of studies on the occurrence naphthalene-treated roots when compared to the controls. The ribose, sucrose and trehalose was significantly higher in of‘hormesis’ hormesis has in beenplants primarily have been associated conducted. with An only understanding human toxins of high increase of glucose concentration in contaminated plant the relationship between hormesis and biological plasticity of roots shown in the study of Balasubramaniyam and Harvey plants is of importance in improving crop yield under stressful input biotechnology approach to clean up contaminated soils and stress.(2014b) Sucrose [20] particularly is required highlight for the production the importance of anthocyanins of glucose waters.conditions This and paper the efficiency reviews of the phytoremediation, potential and newly which emerging is a low signalling and ROS scavenging in plant defence against oxidative application of hormesis underpinning the adaptive responses which play an important role in ROS scavenging and antioxidant phytoremediation. defence [15]; hence the increased levels of sucrose in treated of plants to stressful conditions, in the fields of agriculture and roots would effectively contribute to the stress tolerance [20]. OXIDATIVE STRESS RESPONSES IN PLANTS gravitropismROS also [21]. plays In a a role study in conducted gravitropism by Balasubramaniyam and it has been demonstrated that scavenging of ROS by antioxidants inhibited during the electron transport activities in the chloroplast et al [14], tall fescue roots grown in sand contaminated with petroleum andUnder mitochondria normal conditions or as a by-product ROS are formed of various in plant metabolic cells and Harvey (2014 a)-1 [22] and Balasubramaniyam (2015)-1 activities localized in different cellular compartments [7-11]. sand Environmental stresses such as drought, salinity, chilling, crude oil (10.8 g kg sand dw) or naphthalene (0.8 g kg dw) showed deviations from normal root orientation response chemical toxicity, UV radiation and pathogens disrupt cellular to gravity, turning away from the contaminated soil matrix back homeostasis and lead to an excessive production of ROS in into the top layer of clean sand, indicating scavenging of ROS by antioxidants.A strong dependence of plants on photosynthesis when the [3].plant In cells.a study At carried high concentrations out on Arabidopsis ROS thaliana, are harmful cell death to plants was and would lead to oxidative stress and programmed cell death demonstrated in leaves of the plants grown on Murashige and Balasubramaniyam et al growthroots are was exposed not affected to stress in has 3 weeksbeen illustrated old tall fescue in the grown study inof Arabidopsis leaves to phenanthrene was (2015) [14] that showed-1 that the shoot Skoog (MS) medium supplemented with 0.5mM phenanthrene 2 2 their root growth was severely inhibited when compared to the [12][12]. which The exposure is known of to mediate cell death. Additionally, Zacchi naphthalene-contaminated sand (0.8g kg sand dw) whereas etshown al to induce localized hydrogen peroxide (H O ) production than that of the reducing equivalents in fungal cells caused gross controls. The roots exposed to the toxic chemicals were able to . (2000) [13] had shown that the greater abundance of ROS ofgrow these into roots the contaminatedrevealed enhanced matrix thickening without restrictions in the endodermis at later the electron micrographs of the roots of tall fescue Festuca stages and the scanning electron and fluorescence micrographs arundinaceadisorganisationgrown of cellular in drought ultra-structure. and naphthalene-contaminated On the other hand, -1 ( and greater suberization [14,20], whereas the expression of ) While these also suggest the tentatively identified compound indole acetic acid (IAA) (0.8 g kg sand dw |dry weight|) environment illustrated H either programmed cell death or gross disorganization of cellular was2 2 subdued in the stressed root and shoot tissues [20]. Since distortions in the root cortex [14]. to enhanced thickening and greater suberization [3] as well as O , an ROS, is a substrate for enhanced lignification that leads similar in appearance to lysigenous aerenchyma formation. Here lysigenousstructure in aerenchyma stressed plant denotes roots, air the spaces distorted in a cortex soft plant cells tissue were stress.peroxidase Here catalysed the greatly IAA thickenedoxidation [23-26], endodermis the results and suberized of these studies demonstrate adaptive responses of plants to oxidative diffusion within the tissue. formed by lysis triggered by deficiency of oxygen to facilitate gas exodermis could also be plant root adaptations, helping with prevention of toxic contaminants from reaching the inner core It is important to note that ROS also have a role as secondary of the roots [14], whereas the IAA oxidation could be related to a messengers/ signalling molecules promoting adaptive response contaminant-detoxification pathway [25]. Int J Plant Biol Res 3(2): 1037 (2015) 2/5 Balasubramaniyam (2015) Email:

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HORMETIC RESPONSES IN PLANTS position behind the root tip, and this could have conferred Herbicide-related hormesis has been demonstrated by many droughtexodermis resilience which to was naphthalene-treated absent in control plants roots [14]. at theJupp same and authors [27-36]. Cedergreen et al hormesis in four species: the aquatic plant Lemna minor, the micro-alga Pseudokirchneriella . subcapitata (2007) [36] and demonstrated the two Newman (1987) [38] reported that a well-developed exodermis, terrestrial plants Tripleurospermum inodorum and Stellaria if in place in grass roots, prevents cortex cells from drying out media from water deficit conditions. Additionally, tall fescue roots aexposed disaccharide to naphthalene that retains contamination water retention that also properties confers drought and is exposed to nine herbicides and one fungicide and frequency and the magnitude of the hormetic response depended accountablestress to plants for contained the resurrection a greater of abundance Selaginella of which trehalose grows [20], in a mixture of both. Their study demonstrated that both the on the endpoint being measured: dry weight at harvest showed desert and mountainous areas [39]. Furthermore, a microcosm a higher frequency and a larger hormetic response compared to cattail and clover showed an accumulation of novel dehydrins, stressstudy carriedproteins out that to protectdetermine plants the againsteffect of drought oil sands in effluent the plants on relative growth rates. Viewed from an evolutionary perspective, a trade-off between traits to minimise fitness reduction could be The study by Balasubramaniyam et al developingexpected of hormetic alternative responses contaminant in plants barriers [36]. Limiting such as the shedding extent grown in the impacted site [40]. of cell wall thickening in response to contaminant exposure by (2015) [14] also showed that tall fescue roots exposed to naphthalene stress withstood root hairs and possessing an increased cortex zone was evident in uptake of Nile red, a hydrophobic, fluorescent dye beyond the tall fescue roots exposed to crude oil contamination in the study of between prevention of contaminant entry and admittance of endodermis, demonstrating resistance to hydrophobic xenobiotic Balasubramaniyam and Harvey (2014a) [22], reflecting a balance shoot-ward movement of contaminants. The ability of plant roots the desired substances such as water and nutrients across the uptake into the xylem that represent the predominant route for endodermis into the steel, which is the central core of the root protects the process of photosynthesis from being disturbed. consisting of the vascular tissue and associated supporting tissue, to withhold harmful substances from entering the root xylem and this too demonstrates a trade-off between traits. Moreover, the results of the study by Balasubramaniyam Furthermore, Huang et al and Harvey (2014b) [20] indicate that the shoot tissues of o . (1991) [37] demonstrated smaller naphthalene-treated plants are protected from chemical toxicity, andplants fewer resisted metaxylem drought vessels stress at in later seminal stages, wheat and roots this count exposed as whilst echoing some of the oxidative stress responses of their toa hormetic high temperature response. Moreover, (40 C) and the study showed of Balasubramaniyam that the stressed roots such as under-expression of IAA and the presence of et al fructans. Vacuolar fructans has the function of stabilising cell treated sand which presented a drought environment for the membranes under stress conditions [15], hence stabilizing plants (2015) resisted [14] drought showed stress that tall after fescue the grown acclimatisation in naphthalene- period accumulationleaf cell membrane in treated against shoots, oxidative presumably stress whereas due to foliar the root IAA of three months better than the control plants. In this study, todegradation shoot communication in treated plants via stress-mediated could suggest response sugar signalling to ROS the naphthalene-treated roots contained a well-developed

pathways [20].

Control Protective effect Adverse effect R e s p o n s e

No stressor agent Dose of stressor agent

Figure 1

Illustration of hormetic responses of plants. Exposure to low-doses of a stressor agent produces a postulated protective response, enabling the plant to resist tougher challenges (middle). Increased-doses produce an oppositely postulated adverse response (right). Adpated from Hayes, 2007 [1]. Int J Plant Biol Res 3(2): 1037 (2015) 3/5 Balasubramaniyam (2015) Email:

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stresses and amelioration of defense systems in plants. Foyer CH, photosynthetic electron transport. In: Causes of photooxidative productionCalabrese of etdefence al. [4] molecules documented within that the low organism levels and of toxins once or other stressors produce beneficial effects by triggering the formed, these defence molecules not only deal with the immediate Mullineaux P, editors. Boca Raton (Fla): CRC Press; 1994. threat but also increase resistance to other threats. Tall fescue In: Molecular biology of free radical scavenging systems. Scandalios J, grown in naphthalene-contaminated sand showed remarkably 8. Foyer CH. Oxygen metabolism and electron transportin photosynthesis. 9. editor.del Río (NY): LA, SandalioCold Spring LM, Harbor Corpas Laboratory FJ, Palma Press; JM, Barroso 1997. pp. JB. 587–621. Reactive well-expressed hormetic responses such as resilience to drought phytoremediationstress and restrictions and agrochemistry. to the entry of xenobiotic uptake [14], oxygen species and reactive nitrogen species in peroxisomes. indicating promising applications of ‘hormesis’ to the fields of Production, scavenging, and role in cell signaling. Plant Physiol. 2006; The application of ‘hormesis’ can be of use in overcoming 141: 330-335. plant mitochondria: origin and redundant regulatory systems. Physiol drought which is one of the most serious world-wide problems 10. Blokhina O, Fagerstedt KV. Reactive oxygen species and nitric oxide in moderate water stress could induce changes in the biochemical 11. Plant. 2010; 138: 447-462. pathwaysfor agriculture in plants, and is making looming them by day. adapted Intermittent to grow exposure effectively to Heyno E, Mary V, Schopfer P, Krieger-Liszkay A. Oxygen activation at in drought conditions. Allowing plants to evolve changes in the plasma membrane: relation between superoxide and hydroxyl biochemical pathways and gene composition to suit the drought 12. radicalAlkio M, production Tabuchi TM,by isolated Wang X,membranes. Colón-Carmona Planta. A. 2011; Stress 234: responses 35-45. conditions will take time, and some plants may not be able to to polycyclic aromatic hydrocarbons in Arabidopsis include growth survive the stress. Still, the surviving plants could become greatly adapted to not only moderate drought stress but other severe inhibition and hypersensitive response-like symptoms. J Exp Bot. stresses too. 13. 2005;Zacchi 56: L, 2983-2994. Morris I, Harvey PJ. Disordered ultrastructure in lignin- However, the genetic composition, i.e. the species of plant is crucial in taking advantage of ‘hormesis’ in phytoremediation peroxidase-secreting hyphae of the white-rot fungus Phanerochaete and agriculture. This is evident in the study of Balasubramaniyam 14. chrysosporium.Balasubramaniyam Microbiology. A, Chapman 2000; MM, 146 Harvey : 759-765. PJ. Responses of tall

-1 fescue (Festuca arundinacea) to growth in naphthalene-contaminated stimulatory(2012) [41] responses that showed in tall the fescue dose ofwas petroleum damaging hydrocarbon for parsnip, sand: xenobiotic stress versus water stress. Environ Sci Pollut R. 2015. contamination (10.8 g kg sand dw) that triggered adaptive/ carrot, beetroot and brown top bent. 15. Bolouri-Moghaddam MR, Le Roy K, Xiang L, Rolland F, Van den Ende W. Sugar signalling and antioxidant network connections in plant CONCLUSIONS 16. cells.Weber FEBS AP, J.Schwacke 2010; 277: R, 2022-2037.Flügge UI. Solute transporters of the plastid to stressors in their growth environment. Certain plants are 17. envelope membrane. Annu Rev Plant Biol. 2005; 56: 133-164. ablePlants to overcome are exposed the stress to many below challenges a certain arising threshold from level.exposure The induction of the anthocyanin biosynthetic pathway in Arabidopsis. Solfanelli C, Poggi A, Loreti E, Alpi A, Perata P. Sucrose-specific hormetic responses of plants to stress help overcome not only Plant Physiol. 2006; 140: 637-646. tougher challenges as well. The application of hormesis merits alS. Are small GTPases signal hubs in sugar-mediated induction of attentionthe stress inthe making plants plantsare exposed more droughtto, but help resistant the plants and inwithstand the safe 18. Ritsema T, Brodmann D, Diks SH, Bos CL, Nagaraj V, Pieterse CM, et

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Cite this article Balasubramaniyam A (2015) Hormetic Dose Response as the Paradigm of Plant Response to Stress. Int J Plant Biol Res 3(2): 1037.

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