Environmental variations mediate duckweed (Lemna minor L.) sensitivity to copper exposure through phenotypic plasticity

Roubeau Dumont, Eva; Larue, Camille; Pujol, Benoît; Lamaze, Thierry; Elger, Arnaud

doi:10.1007/s11356-019-04630-3

Research Article
Published: 10 March 2019

Environmental variations mediate duckweed (Lemna minor L.) sensitivity to copper exposure through phenotypic plasticity

Eva Roubeau Dumont ORCID: orcid.org/0000-0003-3355-4459^1,2,
Camille Larue¹,
Benoît Pujol^3,4,
Thierry Lamaze⁵ &
Arnaud Elger¹

Environmental Science and Pollution Research volume 26, pages 14106–14115 (2019)Cite this article

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Abstract

Environmentally mediated sensitivity of Lemna minor to copper (Cu) was evaluated for the first time in three experiments: the effects of two levels of nutrient concentration, light irradiance or Cu pre-exposure were tested. Various Cu concentrations (ranging from 0.05 to 0.25 mg/L) were used to assess the sensitivity of L. minor to this metal, using one common strain previously acclimatized to two different levels of light intensity, nutrient enrichment and Cu pre-exposure. Our results showed a phenotypic plastic response of the relative growth rates based on frond number and fresh mass production, and maximum quantum yield of photosystem II (F_v/F_m). Growth was affected by the three environmental conditions both prior and during Cu exposure, whereas F_v/F_m was mostly affected during Cu exposure. Copper significantly influenced all the parameters measured in the three experiments. Environmental conditions significantly modified L. minor sensitivity to Cu in all experiments, with up to twofold difference depending on the treatment. Growth rate was the parameter that was most impacted. Our study revealed for the first time the existence of phenotypic plasticity in L. minor sensitivity to chemical contamination, and implies that environmental context needs to be taken into account for a relevant risk assessment.

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References

Arshid S, Wani AA (2013) Phenotypic plasticity, clonal architecture and biomass partitioning in Myriophyllum spicatum L across different lentic and lotic. Ecosyst Kashmir 12:2618–2623. https://doi.org/10.5897/AJB2013.12062
Article Google Scholar
Barko JW, Smart RM (1981) Comparative influences of light and temperature on the growth and metabolism of selected submersed freshwater macrophytes. Ecol Monogr 51:219–236
Article Google Scholar
Barrett SCH, Eckert CG, Husband BC (1993) Evolutionary processes in aquatic plant populations. Aquat Bot 44:105–145. https://doi.org/10.1016/0304-3770(93)90068-8
Article Google Scholar
Bornette G, Puijalon S (2011) Response of aquatic plants to abiotic factors: a review. Aquat Sci 73:1–14. https://doi.org/10.1007/s00027-010-0162-7
Article CAS Google Scholar
Boxall A, Fogg L, Ashauer R et al (2013) Effects of repeated pulsed herbicide exposures on the growth of aquatic macrophytes. Environ Toxicol Chem 32:193–200. https://doi.org/10.1002/etc.2040
Article CAS Google Scholar
Brogan WR, Relyea RA (2015) Submerged macrophytes mitigate direct and indirect insecticide effects in freshwater communities. PLoS One 10:e0126677. https://doi.org/10.1371/journal.pone.0126677
Article CAS Google Scholar
Cao JJ, Wang Y, Zhu ZL (2012) Growth response of the submerged macrophyte Myriophyllum spicatum to sediment nutrient levels and water-level fluctuations. Aquat Biol 17:295–303. https://doi.org/10.3354/ab00484
Article Google Scholar
Chambers PA, Lacoul P, Murphy KJ, Thomaz SM (2008) Global diversity of aquatic macrophytes in freshwater. Hydrobiologia 595:9–26. https://doi.org/10.1007/s10750-007-9154-6
Article Google Scholar
Coutris C, Merlina G, Silvestre J, Pinelli E, Elger A (2011) Can we predict community-wide effects of herbicides from toxicity tests on macrophyte species? Aquat Toxicol 101:49–56. https://doi.org/10.1016/j.aquatox.2010.08.017
Article CAS Google Scholar
Eichelmann H, Oja V, Rasulov B et al (2005) Adjustement of leaf photosynthesis to chade in a natural canopy: reallocation of nitrogen. Plant Cell Environ 28:389–401. https://doi.org/10.1111/j.1365-3040.2004.01275.x
Article CAS Google Scholar
Eissa AE, Zaki MM (2011) The impact of global climatic changes on the aquatic environment. Procedia Environ Sci 4:251–259. https://doi.org/10.1016/j.proenv.2011.03.030
Article CAS Google Scholar
Elger A, Willby NJ (2003) Leaf dry matter content as an integrative expression of plant palatability: the case of freshwater macrophytes. Funct Ecol 17(1):58-65
Evans JR (1989) Photosynthesis and nitrogen relationship in leaves of C3 plants. Oecologia 78:9–19. https://doi.org/10.1007/BF00377192
Article Google Scholar
Fairchild JF, Ruessler DS, Ron A (1998) Comparative sensitivity of five species of macrophytes and six species of algae to atrazine, metribuzin, alachlor, and metolachlor. Environ Toxicol Chem 17:1830–1834
Article CAS Google Scholar
Fritioff Å, Kautsky L, Greger M (2005) Influence of temperature and salinity on heavy metal uptake by submersed plants. Environ Pollut 133:265–274. https://doi.org/10.1016/j.envpol.2004.05.036
Article CAS Google Scholar
Ghalambor CK, McKay JK, Carroll SP, Reznick DN (2007) Adaptive versus non-adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct Ecol 21:394–407. https://doi.org/10.1111/j.1365-2435.2007.01283.x
Article Google Scholar
Gibbin EM, Massamba N’Siala G, Chakravarti LJ, Jarrold MD, Calosi P (2017) The evolution of phenotypic plasticity under global change. Sci Rep 7:1–8. https://doi.org/10.1038/s41598-017-17554-0
Article CAS Google Scholar
Going B, Simpson J, Even T (2008) The influence of light on the growth of watercress (Nasturtium officinale R. Br.). Hydrobiologia 607:75–85. https://doi.org/10.1007/s10750-008-9368-2
Article CAS Google Scholar
Gratani L (2014) Plant phenotypic plasticity in response to environmental factors. Adv Bot 2014:17. https://doi.org/10.1155/2014/208747
Article Google Scholar
Gupta M, Sinha S, Chandra P (1996) Copper-induced toxicity in aquatic macrophyte, Hydrilla verticillata: effect of pH. Ecotoxicology 5:23–33. https://doi.org/10.1007/BF00116321
Article CAS Google Scholar
Hussner A, Meyer C, Busch J (2009) The influence of water level and nutrient availability on growth and root system development of Myriophyllum aquaticum. Weed Res 49:73–80
Article CAS Google Scholar
Jackrel SL, Morton TC (2018) Inducible phenotypic plasticity in plants regulates aquatic ecosystem functioning. Oecologia 186:895–906. https://doi.org/10.1007/s00442-018-4094-6
Article Google Scholar
Khellaf N, Zerdaoui M (2010) Growth, photosynthesis and respiratory response to copper in Lemna minor: a potential use of duckweed in biomonitoring. Iran J Environ Heal Sci Eng 7:299–306
CAS Google Scholar
Khellaf N, Zerdaoui M (2013) Phytoaccumulation of zinc using the duckweed Lemna gibba L.: effect of temperature, pH and metal source. Desalin Water Treat 51:5755–5760. https://doi.org/10.1080/19443994.2012.761162
Article CAS Google Scholar
van Kleunen M, Fischer M (2005) Constraints on the evolution of adaptive phenotypic plasticity in plants. New Phytol 166:49–60. https://doi.org/10.1111/j.1469-8137.2004.01296.x
Article Google Scholar
Knauer K, Vervliet-Scheebaum M, Dark RJ, Maund SJ (2006) Methods for assessing the toxicity of herbicides to submersed aquatic plants. Pest Manag Sci 65:715–722. https://doi.org/10.1002/ps.1226
Article CAS Google Scholar
Landis WG, Durda JL, Brooks ML, Chapman PM, Menzie CA, Stahl RG Jr, Stauber JL (2013) Ecological risk assessment in the context of global climate change. Environ Toxicol Chem 32:79–92. https://doi.org/10.1002/etc.2047
Article CAS Google Scholar
Leblebici Z, Aksoy A (2011) Growth and lead accumulation capacity of Lemna minor and Spirodela polyrhiza (Lemnaceae): interactions with nutrient enrichment. Water Air Soil Pollut 214:175–184. https://doi.org/10.1007/s11270-010-0413-1
Article CAS Google Scholar
Li G, Xue P, Yan C, Li Q (2010) Copper biosorption by Myriophyllum spicatum: effects of temperature and pH. Korean J Chem Eng 27:1239–1245. https://doi.org/10.1007/s11814-010-0183-x
Article CAS Google Scholar
Li L, Barrett SCH, Song Z, Chen J (2019) Sex-specific plasticity of reproductive allocation in response to water depth in a clonal, dioecious macrophyte. Am J Bot 106:42–50. https://doi.org/10.1002/ajb2.1218
Article Google Scholar
Madsen JD (2013) Influences of light intensity variations on growth characteristics of Myriophyllum aquaticum. J Freshw Ecol 28:147–164. https://doi.org/10.1080/02705060.2012.722067
Article Google Scholar
Maltby L, Arnold D, Arts G et al (2009) Aquatic macrophyte risk assessment for pesticides. Taylor & Francis Group, London, New York
Book Google Scholar
Matesanz S, Gianoli E, Valladares F (2010) Global change and the evolution of phenotypic plasticity in plants. Ann N Y Acad Sci 1206:35–55. https://doi.org/10.1111/j.1749-6632.2010.05704.x
Article Google Scholar
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence - a practical guide. J Exp Bot 51:659–668
Article CAS Google Scholar
Molina-Montenegro MA, Salgado-Luarte C, Oses R, Torres-Díaz C (2013) Is physiological performance a good predictor for fitness? Insights from an invasive plant species. PLoS One 8:1–9. https://doi.org/10.1371/journal.pone.0076432
Article CAS Google Scholar
Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot 64:3983–3998. https://doi.org/10.1093/jxb/ert208
Article CAS Google Scholar
Nuttens A, Gross EM (2017) Sucrose modifies growth and physiology in axenically grown Myriophyllum spicatum with potential effects on the response to pollutants. Environ Toxicol Chem 36:969–975. https://doi.org/10.1002/etc.3610
Article CAS Google Scholar
OECD (2006) OECD 221 guidelines for testing of chemicals: Lemna sp. Growth inhibition test
Olesen B, Madsen TV (2000) Growth and physiological acclimation to temperature and inorganic carbon availability by two submerged aquatic macrophyte species, Callitriche cophocarpa and Elodea canadensis. Funct Ecol 14:252–260. https://doi.org/10.1046/j.1365-2435.2000.00412.x
Article Google Scholar
Onaindia M, Amezaga I, Garbisu C, García-Bikuña B (2005) Aquatic macrophytes as biological indicators of environmental conditions of rivers in north-eastern Spain. Ann Limnol Int J Limnol 41:175–182. https://doi.org/10.1051/limn:20054130175
Article Google Scholar
Rai PK (2009) Heavy metal phytoremediation from aquatic ecosystems with special reference to macrophytes. Crit Rev Environ Sci Technol 39:697–753. https://doi.org/10.1080/10643380801910058
Article CAS Google Scholar
R Core Team (2018). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Razinger J, Dermastia M, Drinovec L, Drobne D, Zrimec A, Dolenc Koce J (2007) Antioxidative responses of duckweed (Lemna minor L.) to short-term copper exposure. Env Sci Pollut Res Res 14:194–201. https://doi.org/10.1065/espr2006.11.364
Article CAS Google Scholar
Sultan SE (1995) Phenotypic plasticity and plant adaptation. Acta Bot Neerl 44:363–383. https://doi.org/10.1111/j.1438-8677.1995.tb00793.x
Article Google Scholar
Szabó S, Peeters ETHM, Várbíró G, Borics G, Lukács BA (2018) Phenotypic plasticity as a clue for invasion success of the submerged aquatic plant Elodea nuttallii. Plant Biol 21:54–63. https://doi.org/10.1111/plb.12918
Article Google Scholar
Thomas G, Stärk HJ, Wellenreuther G, Dickinson BC, Küpper H (2013) Effects of nanomolar copper on water plants-comparison of biochemical and biophysical mechanisms of deficiency and sublethal toxicity under environmentally relevant conditions. Aquat Toxicol 140–141:27–36. https://doi.org/10.1016/j.aquatox.2013.05.008
Article CAS Google Scholar
Thomas G, Andresen E, Mattusch J, Hubáček T, Küpper H (2016) Deficiency and toxicity of nanomolar copper in low irradiance—a physiological and metalloproteomic study in the aquatic plant Ceratophyllum demersum. Aquat Toxicol 177:226–236. https://doi.org/10.1016/j.aquatox.2016.05.016
Article CAS Google Scholar
Thomaz SM, Esteves FA, Murphy KJ, et al (2008) Aquatic macrophytes in the tropics: ecology of populations and communities, impacts of invasions and use by man. In: Del-Claro K, Scarano F, Luettge H (eds) Encyclopedia of life system support. UNESCO, pp 1252–1280
Üçüncü E, Tunca E, Fikirdeşici Ş, Özkan AD, Altındağ A (2013) Phytoremediation of Cu, Cr and Pb mixtures by Lemna minor. Bull Environ Contam Toxicol 91:600–604. https://doi.org/10.1007/s00128-013-1107-3
Article CAS Google Scholar
Vasseur L, Aarssen LW (1992) Phenotypic plasticity in Lemna minor (Lemnaceae). Plant Syst Evol 180:205–219. https://doi.org/10.1007/BF00941151
Article Google Scholar
Vasseur L, Aarssen LW, Lefebvre DD (1994) Plasticity of morphological and isozymic traits in response to short-term environmental variation in Lemna minor L. Ecoscience 1:249–254. https://doi.org/10.1080/11956860.1994.11682249
Article Google Scholar
Verma R, Suthar S (2015) Lead and cadmium removal from water using duckweed - Lemna gibba L.: impact of pH and initial metal load. Alexandria Eng J 54:1297–1304. https://doi.org/10.1016/j.aej.2015.09.014
Article Google Scholar
Vitasse Y, Bresson CC, Kremer A, Michalet R, Delzon S (2010) Quantifying phenological plasticity to temperature in two temperate tree species. Funct Ecol 24:1211–1218. https://doi.org/10.1111/j.1365-2435.2010.01748.x
Article Google Scholar
Wells CL, Pigliucci M (2000) Adaptive phenotypic plasticity: the case of heterophylly in aquatic plants. Perspect Plant Ecol Evol Syst 3:1–18. https://doi.org/10.1078/1433-8319-00001
Article Google Scholar
Woodward G, Bonada N, Brown LE, Death RG, Durance I, Gray C, Hladyz S, Ledger ME, Milner AM, Ormerod SJ, Thompson RM, Pawar S (2016) The effects of climatic fluctuations and extreme events on running water ecosystems. Philos Trans R Soc B 371:20150274. https://doi.org/10.1098/rstb.2015.0274
Article Google Scholar
Xie D, Yu D (2011) Size-related auto-fragment production and carbohydrate storage in auto-fragment of Myriophyllum spicatum L. in response to sediment nutrient and plant density. Hydrobiologia 658:221–231. https://doi.org/10.1007/s10750-010-0475-5
Article CAS Google Scholar
Xing W, Huang W, Liu G (2009) Effect of excess iron and copper on physiology of aquatic plant Spirodela polyrrhiza (L.) Schleid. Environ Toxicol 25:103–112. https://doi.org/10.1002/tox.20480
Article CAS Google Scholar
Yang Y, Yu D, Li Y, Xie Y, Geng X (2004) Phenotypic plasticity of two submersed plants in response to flooding. J Freshw Ecol 19:69–76. https://doi.org/10.1080/02705060.2004.9664514
Article Google Scholar
Yang L, Wen KS, Ruan X et al (2018) Response of plant secondary metabolites to environmental factors. Molecules 23:1–26. https://doi.org/10.3390/molecules23040762
CAS Article Google Scholar
Younginger BS, Sirová D, Cruzan MB, Ballhorn DJ (2017) Is biomass a reliable estimate of plant fitness? Appl Plant Sci 5:1600094. https://doi.org/10.3732/apps.1600094
Article Google Scholar
Ziegler JP, Solomon CT, Finney BP, Gregory-Eaves I (2015) Macrophyte biomass predicts food chain length in shallow lakes. Ecosphere 6:art5. https://doi.org/10.1890/ES14-00158.1
Article Google Scholar

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Acknowledgments

We thank David Baqué (R&D Engineer in ICP-OES and ICP-MS analysis techniques) for his support for ICP-OES metal analyses and Olivier Berseille for technical assistance during preliminary experiments.

Funding

This research was funded by the EC2CO program from the National Institute of Sciences of the Universe (CNRS/INSU), granted to the VIRMA project, and by the French Ministry of research and higher education through a Doctoral Fellowship awarded to ER.

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Authors and Affiliations

EcoLab, CNRS, Université de Toulouse, Toulouse, France
Eva Roubeau Dumont, Camille Larue & Arnaud Elger
EcoLab, Campus INPT-ENSAT, Avenue de l’Agrobiopole – BP 32607, 31326, Castanet Tolosan Cedex, France
Eva Roubeau Dumont
Laboratoire Évolution & Diversité Biologique (EDB UMR 5174), CNRS, IRD, UPS, Université Fédérale de Toulouse Midi-Pyrénées, Toulouse, France
Benoît Pujol
EPHE, CNRS, UPVD, PSL Research University, USR 3278 CRIOBE, F-66360, Perpignan, France
Benoît Pujol
Laboratoire CESBIO, CNRS, IRD, CNES, UPS, Université de Toulouse, Toulouse, France
Thierry Lamaze

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Eva Roubeau Dumont
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Camille Larue
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Benoît Pujol
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Thierry Lamaze
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Arnaud Elger
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Correspondence to Eva Roubeau Dumont.

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Roubeau Dumont, E., Larue, C., Pujol, B. et al. Environmental variations mediate duckweed (Lemna minor L.) sensitivity to copper exposure through phenotypic plasticity. Environ Sci Pollut Res 26, 14106–14115 (2019). https://doi.org/10.1007/s11356-019-04630-3

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Received: 06 June 2018
Accepted: 19 February 2019
Published: 10 March 2019
Issue Date: 01 May 2019
DOI: https://doi.org/10.1007/s11356-019-04630-3

Keywords

Aquatic macrophyte
Lemna minor
Risk assessment
Ecotoxicology
Environmental fluctuations
Abiotic factors