Bioaccumulation and physiological traits qualify Pistia stratiotes as a suitable species for phytoremediation and bioindication of iron-contaminated water.

Serious concerns have recently been raised regarding the association of Fe excess with neurodegenerative diseases in mammals and nutritional and oxidative disorders in plants. Therefore, the current study aimed to understand the physiological changes induced by Fe excess in Pistia stratiotes, a species often employed in phytoremediation studies. P. stratiotes were subjected to five concentrations of Fe: 0.038 (control), 1.0, 3.0, 5.0 and 7.0 mM. Visual symptoms of Fe-toxicity such as bronzing of leaf edges in 5.0 and 7.0 mM-grown plants were observed after 5 days. Nevertheless, no major changes were observed in photosynthesis-related parameters at this time-point. In contrast, plants growing for 10 days in high Fe concentrations showed decreased chlorophyll concentrations and lower net CO2 assimilation rate. Notwithstanding, P. stratiotes accumulated high amounts of Fe, especially in roots (maximum of 10,000 µg g-1 DW) and displayed a robust induction of the enzymatic antioxidant system. In conclusion, we demonstrated that P. stratiotes can be applied to clean up Fe-contaminated water, as the species displays high Fe bioaccumulation, mostly in root apoplasts, and can maintain physiological processes under Fe excess. Our results further revealed that by monitoring visual symptoms, P. stratiotes could be applied for bioindication purposes.

[1]  M. Aschner,et al.  Iron overload and neurodegenerative diseases: What can we learn from Caenorhabditis elegans? , 2022, Toxicology research and application.

[2]  Yan Li,et al.  Physiological defense and metabolic strategy of Pistia stratiotes in response to zinc-cadmium co-pollution. , 2022, Plant physiology and biochemistry : PPB.

[3]  P. H. Gorni,et al.  Iron toxicity: effects on the plants and detoxification strategies , 2022, Acta Botanica Brasilica.

[4]  Aguiar,et al.  The impact of trace metals in marine sediments after a tailing dam failure: the Fundão dam case (Brazil) , 2021, Environmental Earth Sciences.

[5]  G. Kirk,et al.  Below-ground plant-soil interactions affecting adaptations of rice to iron toxicity. , 2021, Plant, cell & environment.

[6]  R. Paul,et al.  Lead phytoremediation potentials of four aquatic macrophytes under hydroponic cultivation , 2021, International journal of phytoremediation.

[7]  S. K. Pradhan,et al.  Population genetic structure and association mapping for iron toxicity tolerance in rice , 2021, PloS one.

[8]  M. Das,et al.  Performance and efficiency services for the removal of hexavalent chromium from water by common macrophytes , 2021, International journal of phytoremediation.

[9]  A. Salami,et al.  Elevated neuroinflammation contributes to the deleterious impact of iron overload on brain function in aging , 2021, NeuroImage.

[10]  A. Viktorínová,et al.  Mini-Review: Is iron-mediated cell death (ferroptosis) an identical factor contributing to the pathogenesis of some neurodegenerative diseases? , 2021, Neuroscience Letters.

[11]  Santosh B. Satbhai,et al.  Iron homeostasis in plants and its crosstalk with copper, zinc, and manganese , 2021 .

[12]  L. Reinert,et al.  Optimization of the phytoremediation conditions of wastewater in post-treatment by Eichhornia crassipes and Pistia stratiotes: kinetic model for pollutants removal , 2020, Environmental technology.

[13]  Md. Mominur Rahman,et al.  Morpho-physiological retardations due to iron toxicity involve redox imbalance rather than photosynthetic damages in tomato. , 2020, Plant physiology and biochemistry : PPB.

[14]  H. Masuda,et al.  How Does Rice Defend Against Excess Iron?: Physiological and Molecular Mechanisms , 2020, Frontiers in Plant Science.

[15]  H. Mohamed,et al.  Silicon Alleviates Copper Toxicity in Flax Plants by Up-Regulating Antioxidant Defense and Secondary Metabolites and Decreasing Oxidative Damage , 2020, Sustainability.

[16]  A. Nunes‐Nesi,et al.  Evaluation of morphological and metabolic responses to glyphosate exposure in two neotropical plant species , 2020 .

[17]  A. Nunes‐Nesi,et al.  Understanding photosynthetic and metabolic adjustments in iron hyperaccumulators grass , 2020, Theoretical and Experimental Plant Physiology.

[18]  Jingjing Ren,et al.  Melatonin alleviates iron stress by improving iron homeostasis, antioxidant defense and secondary metabolism in cucumber , 2020 .

[19]  S. Gill,et al.  Phytoremediation of contaminated waters: An eco-friendly technology based on aquatic macrophytes application , 2020 .

[20]  F. Thompson,et al.  Metal concentrations and biological effects from one of the largest mining disasters in the world (Brumadinho, Minas Gerais, Brazil) , 2020, Scientific Reports.

[21]  C. Curie,et al.  Paspalum urvillei and Setaria parviflora, two grasses naturally adapted to extreme iron-rich environments. , 2020, Plant physiology and biochemistry : PPB.

[22]  M. Rizwan,et al.  Application of Floating Aquatic Plants in Phytoremediation of Heavy Metals Polluted Water: A Review , 2020 .

[23]  C. S. Marinato,et al.  Evaluation of Metals in Soil and Tissues of Economic‐Interest Plants Grown in Sites Affected by the Fundão Dam Failure in Mariana, Brazil , 2020, Integrated environmental assessment and management.

[24]  Ke Chen,et al.  Lead-induced oxidative stress triggers root cell wall remodeling and increases lead absorption through esterification of cell wall polysaccharide. , 2019, Journal of hazardous materials.

[25]  J. Oliveira,et al.  Phytoremediation of arsenite-contaminated environments: is Pistia stratiotes L. a useful tool? , 2019, Ecological Indicators.

[26]  G. An,et al.  Nicotianamine Synthesis by OsNAS3 Is Important for Mitigating Iron Excess Stress in Rice , 2019, Front. Plant Sci..

[27]  A. Mahender,et al.  Tolerance of Iron-Deficient and -Toxic Soil Conditions in Rice , 2019, Plants.

[28]  Jonathan M. Banks Chlorophyll fluorescence as a tool to identify drought stress in Acer genotypes , 2018, Environmental and Experimental Botany.

[29]  Takanori Kobayashi,et al.  Rice HRZ ubiquitin ligases are crucial for response to excess iron. , 2018, Physiologia plantarum.

[30]  Mohammed A. Dakhil,et al.  Bioaccumulation and rhizofiltration potential of Pistia stratiotes L. for mitigating water pollution in the Egyptian wetlands , 2018, International journal of phytoremediation.

[31]  M. Udvardi,et al.  An Iron-Activated Citrate Transporter, MtMATE67, Is Required for Symbiotic Nitrogen Fixation1[OPEN] , 2017, Plant Physiology.

[32]  S. Khalid,et al.  A comparison of technologies for remediation of heavy metal contaminated soils , 2017 .

[33]  A. Fernie,et al.  Photosynthetic and metabolic acclimation to repeated drought events play key roles in drought tolerance in coffee , 2017, Journal of experimental botany.

[34]  P. E. Menezes-Silva,et al.  The Involvement of Nitric Oxide in Integration of Plant Physiological and Ultrastructural Adjustments in Response to Arsenic , 2017, Front. Plant Sci..

[35]  S. Rezania,et al.  Comprehensive review on phytotechnology: Heavy metals removal by diverse aquatic plants species from wastewater. , 2016, Journal of hazardous materials.

[36]  S. Datta,et al.  Analysis of high iron rice lines reveals new miRNAs that target iron transporters in roots , 2016, Journal of experimental botany.

[37]  Chaobo Tong,et al.  Vacuolar Iron Transporter BnMEB2 Is Involved in Enhancing Iron Tolerance of Brassica napus , 2016, Front. Plant Sci..

[38]  A. Ismail,et al.  Understanding the regulation of iron nutrition: can it contribute to improving iron toxicity tolerance in rice? , 2016, Functional Plant Biology.

[39]  A. Haque,et al.  Genetic variation in Fe toxicity tolerance is associated with the regulation of translocation and chelation of iron along with antioxidant defence in shoots of rice. , 2016, Functional plant biology : FPB.

[40]  M. Oliva,et al.  Oxidative damage and photosynthetic impairment in tropical rice cultivars upon exposure to excess iron , 2016 .

[41]  A. Nunes‐Nesi,et al.  Arsenic hyperaccumulation induces metabolic reprogramming in Pityrogramma calomelanos to reduce oxidative stress. , 2016, Physiologia plantarum.

[42]  X. Lin,et al.  Elevation of NO production increases Fe immobilization in the Fe-deficiency roots apoplast by decreasing pectin methylation of cell wall , 2015, Scientific Reports.

[43]  G. R. Rout,et al.  ROLE OF IRON IN PLANT GROWTH AND METABOLISM , 2015 .

[44]  K. Kuki,et al.  Morphoanatomical responses induced by excess iron in roots of two tolerant grass species , 2015, Environmental Science and Pollution Research.

[45]  F. S. Farnese,et al.  Evaluation of the potential of Pistia stratiotes L. (water lettuce) for bioindication and phytoremediation of aquatic environments contaminated with arsenic. , 2014, Brazilian journal of biology = Revista brasleira de biologia.

[46]  J. Fett,et al.  Iron toxicity in field-cultivated rice: contrasting tolerance mechanisms in distinct cultivars , 2014, Theoretical and Experimental Plant Physiology.

[47]  S. Teixeira,et al.  Bioremediation of an Iron-Rich Mine Effluent by Lemna minor , 2014, International journal of phytoremediation.

[48]  Paulo E. M. Silva,et al.  Effects of Adding Nitroprusside on Arsenic Stressed Response of Pistia stratiotes L. Under Hydroponic Conditions , 2014, International journal of phytoremediation.

[49]  W. Schmidt,et al.  Iron in seeds – loading pathways and subcellular localization , 2014, Front. Plant Sci..

[50]  K. Kuki,et al.  Leaf morphoanatomy of species tolerant to excess iron and evaluation of their phytoextraction potential , 2014, Environmental Science and Pollution Research.

[51]  Laise Rosado-Souza,et al.  Iron excess affects rice photosynthesis through stomatal and non-stomatal limitations. , 2013, Plant science : an international journal of experimental plant biology.

[52]  G. Noctor,et al.  Plant catalases: peroxisomal redox guardians. , 2012, Archives of biochemistry and biophysics.

[53]  P. Tlustoš,et al.  The Use of Water Lettuce (Pistia Stratiotes L.) for Rhizofiltration of a Highly Polluted Solution by Cadmium and Lead , 2011, International journal of phytoremediation.

[54]  S. Shigeoka,et al.  Understanding Oxidative Stress and Antioxidant Functions to Enhance Photosynthesis1 , 2010, Plant Physiology.

[55]  G. Brewer,et al.  Risks of copper and iron toxicity during aging in humans. , 2010, Chemical research in toxicology.

[56]  T. Sun,et al.  Iron-Deficiency Induces Cadmium Uptake and Accumulation in Solanum nigrum L. , 2009, Bulletin of environmental contamination and toxicology.

[57]  H. Sallanon,et al.  Microplate quantification of enzymes of the plant ascorbate-glutathione cycle. , 2008, Analytical biochemistry.

[58]  J. Bai,et al.  Photoprotective function of photorespiration in Reaumuria soongorica during different levels of drought stress in natural high irradiance , 2008, Photosynthetica.

[59]  Jagath C. Kasturiarachchi,et al.  Contribution of water hyacinth (Eichhornia crassipes (Mart.) Solms) grown under different nutrient conditions to Fe-removal mechanisms in constructed wetlands. , 2008, Journal of environmental management.

[60]  N. Wright,et al.  Mercury uptake and accumulation by four species of aquatic plants. , 2007, Environmental pollution.

[61]  M. Oliva,et al.  Responses of restinga plant species to pollution from an iron pelletization factory , 2006 .

[62]  A. Michalak Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress , 2006 .

[63]  Neetu,et al.  Signs of oxidative stress in the chlorotic leaves of iron starved plants , 2005 .

[64]  S. Zhao,et al.  Photoprotective Function of Photorespiration in Several Grapevine Cultivars Under Drought Stress , 2004, Photosynthetica.

[65]  D. Leister,et al.  The metal ion transporter IRT1 is necessary for iron homeostasis and efficient photosynthesis in Arabidopsis thaliana. , 2002, The Plant journal : for cell and molecular biology.

[66]  C. Werner,et al.  Characteristic patterns of chronic and dynamic photoinhibition of different functional groups in a Mediterranean ecosystem. , 2002, Functional plant biology : FPB.

[67]  Hendrik Poorter,et al.  Avoiding bias in calculations of relative growth rate. , 2002, Annals of botany.

[68]  Ji-Yeun Lee,et al.  Photodynamic Effect of Iron Excess on Photosystem II Function in Pea Plants¶ , 2002 .

[69]  P. Schopfer,et al.  Hydroxyl radical-induced cell-wall loosening in vitro and in vivo: implications for the control of elongation growth. , 2002, The Plant journal : for cell and molecular biology.

[70]  C Garbisu,et al.  Phytoextraction: a cost-effective plant-based technology for the removal of metals from the environment. , 2001, Bioresource technology.

[71]  J. Gebicki,et al.  A critical evaluation of the effect of sorbitol on the ferric-xylenol orange hydroperoxide assay. , 2000, Analytical biochemistry.

[72]  C. Forney,et al.  Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds , 1999, Planta.

[73]  P. R. Mosquim,et al.  Aluminum effects on lipid peroxidation and on the activities of enzymes of oxidative metabolism in sorghum. , 1999 .

[74]  E. Weinberg The Lactobacillus Anomaly: Total Iron Abstinence , 2015, Perspectives in biology and medicine.

[75]  Jang Ryol Liu,et al.  Enhancement of peroxidase activity by stress-related chemicals in sweet potato , 1996 .

[76]  D. Eide,et al.  A novel iron-regulated metal transporter from plants identified by functional expression in yeast. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[77]  D. Richardson,et al.  Identification of a mechanism of iron uptake by cells which is stimulated by hydroxyl radicals generated via the iron-catalysed Haber-Weiss reaction. , 1995, Biochimica et biophysica acta.

[78]  T. Winder,et al.  Early Iron Deficiency Stress Response in Leaves of Sugar Beet , 1995, Plant physiology.

[79]  A. Wellburn The Spectral Determination of Chlorophylls a and b, as well as Total Carotenoids, Using Various Solvents with Spectrophotometers of Different Resolution* , 1994 .

[80]  J. Briantais,et al.  The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence , 1989 .

[81]  E. Havir,et al.  Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. , 1987, Plant physiology.

[82]  J. Abadía,et al.  Function of iron in chloroplasts , 1986 .

[83]  A. P. Schwab,et al.  The chemistry of iron in soils and its availability to plants , 2016 .

[84]  B. Halliwell,et al.  Superoxide-dependent formation of hydroxyl radicals in the presence of iron salts. Detection of 'free' iron in biological systems by using bleomycin-dependent degradation of DNA. , 1981, The Biochemical journal.

[85]  K. Asada,et al.  Hydrogen Peroxide is Scavenged by Ascorbate-specific Peroxidase in Spinach Chloroplasts , 1981 .

[86]  C. N. Giannopolitis,et al.  Superoxide dismutases: I. Occurrence in higher plants. , 1977, Plant physiology.

[87]  M. M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.

[88]  R. Clárk Characterization of phosphatase of intact maize roots. , 1975, Journal of agricultural and food chemistry.

[89]  M. Karnovsky,et al.  A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron-microscopy , 1965 .