Improvement of Environmental Remediation by on-Site

May 13, 2014 - drates,2 as precursors of stress defense molecules, as providers of chemical energy and ... system development and stress tolerance. Be...
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Improvement of Environmental Remediation by on-Site Phytoremediating Greenhouses Cécile Sulmon, Fanny Ramel, Gwenola Gouesbet, and Ivan Couée* UMR 6553 Ecosystems-Biodiversity-Evolution Université de Rennes 1/CNRS Campus de Beaulieu, bâtiment 14A F-35042 Rennes Cedex, France regulation can activate expression of genes involved in transcription, stress defense, and xenobiotic conjugation and detoxification, such as genes encoding UDP-glucosyl-transferases, Glutathione-S-transferases and Cytochrome P450s2. The levels of endogenous soluble carbohydrates in plants have thus positive effects on underground exchange surfaces, on rhizospheric bacterial and fungal communities, on pollutant stress tolerance, on pollutant uptake and accumulation, and on pollutant molecular remediation (Figure 1). Analysis of natural

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ransfer of plant-driven soil depollution (phytoremediation) processes from controlled conditions (in vitro, growth chambers, greenhouses) to complex conditions in the field is often reported to be hampered by environmental factors,1 such as climatic conditions, soil properties, abiotic stress, or multipollution combinations (polycyclic aromatic hydrocarbons, solvents, explosives, pesticides, heavy metals). We wish to argue that there are important cases where difficulties of applying efficient phytoremediation protocols in the field could be lifted by the reversed approach of on-site installation of phytoremediating greenhouses. Plant phenotypic plasticity is an important leverage for meeting phytoremediation challenges. As integrators of nutrition, development and stress responses, endogenous soluble carbohydrates have major positive effects on physiological properties that are essential for phytoremediation: root growth, root-microorganisms interactions, growth of aerial organs, leafmicroorganisms interactions, pollutant uptake, stress tolerance, defense against oxidative stress, tolerance of pollutant accumulation, and pollutant chelation, conjugation or detoxification. These effects stem from direct metabolic action of carbohydrates,2 as precursors of stress defense molecules, as providers of chemical energy and reducing power, as precursors of chelators, and as providers of conjugation cosubstrates, glucose itself being involved in formation of glucosyl-xenobiotic conjugates.2 They also result from gene expression regulations that soluble sugars can exert as signaling molecules.2 Carbohydrate © 2014 American Chemical Society

Figure 1. Interactive effects of environmental factors, plant genotype, and plant endogenous carbon status on phytoremediation processes.

variation demonstrates significant correlations between endogenous levels of carbohydrates and tolerance to pollutant stress. The genetic diversity of plants provides a wealth of genotypedependent variation of carbon allocation, biomass increase, root system development and stress tolerance. Besides this genetic biodiversity, the dynamics of soluble carbohydrates is highly responsive to environmental conditions and highly plastic, thus implying that environmental drivers, such as exogenous carbohydrate amendment, temperature, CO2 levels, light, can increase endogenous sugar levels and enhance different aspects of phytoremediation potential (Figure 1). Moreover, the effects of soluble sugars are systemic, rather than pollutant-specific, and can be useful not only for single-pollution phytoremediaton, but also for multipollution phytoremediation. Nevertheless, environmental factors remain under the influence of bioclimatic and ecophysiological fluctuations, which are Received: April 3, 2014 Published: May 13, 2014 6055

dx.doi.org/10.1021/es502041a | Environ. Sci. Technol. 2014, 48, 6055−6056

Environmental Science & Technology

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liable to dampen positive effects on phytoremediation.1 In contrast, on-site greenhouse facilities covering canopies of phytoremediating plants should greatly improve efficiency and speed of phytoremediation processes. Proper management of greenhouse conditions (light, temperature, humidity, watering, CO2) can yield severalfold increases of plant carbon gain and biomass accumulation relatively to field or stress conditions. Such semicontrolled and protected conditions should enhance phytoremediation under adverse climatic conditions, such as northern conditions, where plant biological activity is restricted by seasonality and where natural pollutant dynamics is decreased. Setting up on-site phytoremediation greenhouses will also enhance plant tolerance to pollutants, root development and uptake efficiency, phytoremediation efficiency, and phytoremediation turnover (Figure 1). Finally, given the nonspecific effects of endogenous soluble sugars, this approach could facilitate growth and activity of spontaneous plant communities in the polluted site or enhance establishment, growth and activity of introduced phytoremediating plants. Design of transgenic plants bearing microbial detoxifying genes and association of plants with detoxifying microorganisms provide novel means to broaden and systematize the scope of phytoremediation. On-site greenhouses with adapted containment systems that comply with biosafety regulations could extend the use of non-native species, invasive weeds, or genetically engineered plants, in phytoremediation protocols. The size of current greenhouses, from a few m2 to 100 000 m2 complexes, could completely cover small-size or medium-size polluted plots. It has been estimated that, in the United Kingdom alone, there are 120 000 small-size contaminated petrol station sites with potential remediation costs amounting to 2.5 billions of pounds.3 At a wider scale, oil production plants1 or mine tailings sites4,5 can vary in size from several hundred m2 to tens of thousands m2. Mine tailings are estimated to correspond to thousands of sites worldwide, with several hundred cases of major incidents during the 20th century.4 An important arsenic and cadmium tailing dam in China was recently rehabilitated by a phytoremediation project, where plants accumulating heavy metals in their biomass were shown to reduce significantly ecological and health risks.5 The 6200 m2 of this soil-covered tailing dam5 could have been amenable to installation of a phytoremediating greenhouse, in order to counter-act adverse seasonal effects, and enhance at least plant biomass gain and therefore global metal uptake by the plant community, thus improving heavy metal removal within the time scale of the project. Alternatively, wherever complete coverage of contaminated surfaces cannot be achieved, on-site phytoremediating greenhouses could cover polluted hotspots within larger areas of pollution. Overall costs and final choices for implementation of on-site phytoremediation greenhouses must depend on the size of contaminated sites, on environmental and human health risks, and on economical, cultural, or patrimonial, value of land reclaim. There are already depollution situations where expensive installations are built on-site for pump-and-treat chemical or bacterial remediation of groundwater contaminations. Moreover, greenhouse construction costs widely vary, and greenhouse technology is a field of active research and continuous improvement. Glazing materials, sustainable energy for warming or lighting, light-emitting diodes, intracanopy lighting, automation systems, and plant architecture are being investigated for improving plant carbohydrate production and plant growth. Costs will be lowering, and extended choice of plants for

phytoremediating greenhouses could take into account properties for biomass, fiber, or biofuel accumulation in aerial organs, which may be processed, as part of postmanagement of pollutant-laden plants, to contribute to sustainable energy management of the greenhouse. It is therefore timely that greenhouse technology and plant physiology knowledge on phytoremediation converge to improve the efficiency and time scale of phytoremediation, and that on-site phytoremediating greenhouses be considered as important options for expanding the use of phytoremediation in soil depollution, in a global context where reclaim of polluted arable land and environmental protection are burning issues.



AUTHOR INFORMATION

Corresponding Author

*Phone: 33-223235123; fax: 33-223235026; e-mail: Ivan.Couee@ univ-rennes1.fr. Notes

The authors declare no competing financial interest.



REFERENCES

(1) Schwitzguébel, J.-P.; Comino, E.; Plata, N.; Khaltavi, M. Is phytoremediation a sustainable and reliable approach to clean-up contaminated water and soil in Alpine areas? Environ. Sci. Pollut. Res. 2011, 18 (6), 842−856, DOI: 10.1007/s11356-011-0498-0. (2) Ramel, F.; Sulmon, C.; Cabello-Hurtado, F.; Taconnat, L.; Martin-Magniette, M. L.; Renou, J. P.; El Amrani, A.; Couée, I.; Gouesbet, G. Genome-wide interacting effects of sucrose and herbicide-mediated-stress in Arabidopsis thaliana: novel insights into atrazine toxicity and sucrose-induced tolerance. BMC Genomics 2007, 8, 450 DOI: 10.1186/1471-2164-8-450. (3) Collins, C. D. Implementing phytoremediation of petroleum hydrocarbons. In Phytoremediation: Methods and Reviews; Willey, N., Ed; Humana Press: Toronto, 2007; pp 99−108. (4) Rico, M.; Benito, G.; Díez-Herrero, A. Floods from tailings dam failures. J. Hazard Mater. 2008, 154, 79−87, DOI: 10.1016/ j.jhazmat.2007.09.110. (5) Zhu, Y.-M.; Wei, C.-Y.; Yang, L.-S. Rehabilitation of a tailing dam at Shimen County, Hunan Province: Effectiveness assessment. Acta Ecol. Sin. 2010, 30, 178−183, DOI: 10.1016/j.chnaes.2010.04.009.

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dx.doi.org/10.1021/es502041a | Environ. Sci. Technol. 2014, 48, 6055−6056