Effects of UV-B radiation on secondary metabolite production, antioxidant activity, photosynthesis and herbivory interactions in Nymphoides humboldtiana (Menyanthaceae)

https://doi.org/10.1016/j.jphotobiol.2020.112021Get rights and content

Highlights

  • UV-B treated plants responded by increasing the potential for the photosynthetic electron transport.

  • Changes observed in the flavonoid's metabolism of the UV-B treated plants were correlated with higher antioxidant activity.

  • Vsingle bondB treated plants responded by increasing the production of flavonoids.

  • Secondary metabolism changes of the UV-B treated plants did not alter herbivory by the gastropod Biomphalaria glabrata.

Abstract

Ultraviolet B-light (UV-B) can exert indirect effects on plant-herbivore interactions by inducing changes in constitutive and induced chemical defenses, since it modulates physiological aspects of plants. This study evaluated the action of UV-B radiation on photosynthesis and production of secondary metabolites in Nymphoides humboldtiana and the cascade effects on the relationship of this macrophyte with a generalist herbivore, the gastropod mollusk Biomphalaria glabrata. After 13 days of UV-B exposition under laboratory conditions, the floating macrophyte N. humboldtiana responded increasing its photosynthetic potential and the production of flavonoids with a correlated enhance in antioxidant activity. However, these changes observed in its metabolism were not enough to alter their palatability to consumption by B. glabrata verified through laboratory feeding choice experiments. Despite the known deleterious effects of exposure to UV-B on terrestrial plants, we found that N. humboldtiana does have physiological/biochemical mechanisms as a strategy or restorative response to this potencially adverse or impacting agent without changing its relationships with herbivores.

Introduction

Several environmental impacts are being imposed on the ecosystems around the world in the last decades, among them the increase of the ultraviolet (UV) indices attributed to rapid changes in climate conditions [1,2]. The UV radiation, distinguished according to their electromagnetic wavelength spectrum, can be classified into three distinct types: UV-C: 100-280 nm, UV-B: 280-320 nm, and UV-A: 320-400 nm [3]. Although representing less than 0.5% of total solar energy, UV-B photons are the most energetic wave that reach the earth's surface, and even small increases in its quantity can significantly affect important processes and attributes from organism to ecosystem levels [4]. At organism level, particularly those of a sessile habit and inevitably exposed to UV-B radiation, the exposure to high levels radiation is capable to influence growth, development, reproductive, as well as physiological, biochemical and genetic aspects [[5], [6], [7]]. Numerous reports revealed that photosynthetic organisms exposed to UV-B radiation can promote damage to photosynthetic machinery and photosystem II (PSII), leading to changes in photosynthetic rate, photoinhibition and photoprotection [7,8]. Furthermore, it is already agreed that UV-B radiation has enough energy to promote free radical overproduction and developing oxidative stress [9,10].

The direct effects of UV-B radiation on organisms can also unfold into effects on its ecological interactions in an ecosystem context and promote cascade changes in its distribution, abundance, and susceptibility and attractiveness to herbivores [2]. But the results are often variable and contradictory depending on the species and/or cultivation and growing conditions [11]. Considering that solar radiation is the primary energy source for plants, studies need to prioritize the complexity of natural systems in approach to understanding the impact of climate change in the context of plant responses to UV radiation [12].

However, as a result of intense studies of the effects of UV-B on plants in recent years, real progress has been made to understanding the conditions under which this radiation-type may be a stressor and perceived by organisms; but in recent years this perception of biological impact has changed for a broader environmental effects and not only restricted to negative impacts. For example, some experimental approaches revealed that UV-B radiation act more as a regulatory and acclimatizing factor in organisms, better than a limiting environmental stressor [4,13]. But the stress approach for UV-B radiation effect has also been used in the cultivation protocols as a strategy for better results for accumulation/biosynthesis of the interest phenolic compounds, as well as the ability to maintain the structural organization of PSII, especially for not introducing any taints in plant in vitro culture system [14,15]. Organisms have developed many physiological and biochemical strategies or mechanisms to repair or defense, such as induced biosynthesis and/or bioaccumulation of phenolic compounds [11,16], which comprise a wide variety of carbon skeletons and molecular structures, such as phenolic acids, coumarins, polyphenols and flavonoids [17]. These secondary metabolites have a broad-spectrum of ecological roles, such as enzyme modulators and enzymatic activity [14], allelopathic [18], protection against UV-absorbing [19], defense against herbivores [20], as well as antioxidant to neutralizing free radicals [15]. These multiple roles are likely to be responses to the various ecological processes that interactively model the costs of expression and adequacy of multifunctional defensive molecules [15].

The impacts of UV-B radiation have been widely investigated on terrestrial photosynthetic organisms over the last 30 years, with intense research efforts following the discovery of the Antarctic Ozone hole due to the climate change scenario [12]. But its effect on coastal freshwater ecosystems has received relatively little attention and immediate and long-term damage have not yet been accounted [1,21]. However, these ecosystems are extremely relevant for studying the acclimation responses of organisms to high UV-B radiation, since aquatic plants exhibit great phenotypic plasticity as response to strong gradients and environmental pressures of this ecosystem [22]. In fact, the complexity of biotic-abiotic interactions in freshwater environments, its interactions with secondary metabolite production and the consequences on species and on its ecological interactions remain unclear and in need of further investigation [23].

Some questions have been postulated as crucial in the context of plant responses to UV-B radiation [12], such as: What response mechanisms can be integrated into a coherent conceptual model to explains the roles of UV-B radiation in plant adaptation and acclimation? What contribution do these responses make to the effects of UV-B radiation on vegetation composition and ecosystem function? The present study was conducted to evaluate the effect of increased UV-B radiation at organism level and potential consumers, encompassing its effect on the photosynthetic efficiency, chemical profile of secondary metabolites and antioxidant response of the floating macrophyte Nymphoides humboldtiana. Nymphoides humboldtiana (Menyanthaceae) is a fixed perennial aquatic plant with floating leaves naturally exposed to environmental enemies. Like other freshwater macrophytes, it has an important ecological role in structuring freshwater ecosystems since it colonizes large areas, possesses high rates of primary production and provides food and shelter for many invertebrate and vertebrate animals [22]. In addition, structurally diverse arrays of chemicals, such as fatty acids and phenols have been isolated from Menyanthaceae species [24,25], and presumably compounds of the same chemical nature can also be produced by N. humboldtiana. The gastropod mollusk Biomphalaria glabrata is a generalist herbivore [26], broadly distributed in freshwater bodies, mainly close to Brazilian littoral [27], and commonly living associated to macrophytes banks.

Specifically, here we used the floating macrophyte Nymphoides humboldtiana to address the following questions: How does UV radiation affect two physiological aspects (photosynthetic performance and secondary metabolite production) and do these traits alter the resistance of this aquatic plant to consumption by the generalist gastropod mollusk Biomphalaria glabrata.

Section snippets

Collection Sites and Organisms

Specimens of N. humboldtiana and B. glabrata were collected in the vicinities of the Restinga de Jurubatiba (PNRJ) National Park, Rio de Janeiro State, Brazil. Individuals of N. humboldtiana were collected at the margin of the Comprida lagoon (22° 16’ 51.30“ S 41° 39’ 19.80” W) in February 2012. After collection, they were packed and transported to the laboratory (NUPEM/UFRJ, Macaé city, Rio de Janeiro), where they were maintained in glass bottles with sediment from the lagoon and under a

Chlorophyll a Fluorescence Analysis

Measurements of potential quantum yield of PSII (Fv/fm) in the field specimens of N. humbolditiana verified a slight reduction (0.78 ± 0.03, 1 h of dark adaptation) from the maximal expected range (0.80–0.83) [41], indicating that the exposition to full sun light promotes a small deactivation of PSII in this macrophyte.

In the laboratory, the analysis of RLCs showed that the UV-B treated plants of N. humboldtiana enhanced their overall potential for the photosynthetic electron transport in

Discussion

The effect of increased UV-B radiation on physiology of aquatic plants and their ecological interactions can help to understand how this cause-effect relationship can affect life of plants in freshwater environments. Here, the UV-B radiation increased the photosynthetic performance in N. humboldtiana and also the production of flavonoids, which consequently increased the antioxidant activity of extracts of this plant. However, these observed changes in chemical profile of specimens maintained

Declaration of Competing Interest

None.

Acknowledgements

This research was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação Carlos Chagas de Amapro à Pesquisa do Estado do Rio de Janeiro (FAPERJ) and the Programa de Pesquisas Ecológicas de Longa Duração (PELD)/CNPq. R.C.P. and A.R.S. thanks CNPq for Research Productivity fellowships. NN thanks Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for a Master degree fellowship. We also thank João Marcelo S. de Sousa and Lilian Bento for general

Author statement

Nocchi N., Duarte H.M., Pereira R.C. and Soares A.R. conceived the ideas, designed the methodology, collected, and analyzed the data. Nocchi, N., Duarte, H.M., Pereira R.C., Konno T.U.P. and Soares A.R. wrote the manuscript. Konno, T.U.P. identified N. humboldtiana. Soares A.R. acquired the funding.

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