High NaCl tolerance potential of Bruguiera cylindrica (L.) Blume compromised by mild CuSO4 concentration as evidenced by unique physiochemical features
Introduction
Copper (Cu) is a fundamental micronutrient essential for the plant growth in low concentration, due to its involvement in many metabolic processes (Sharma and Agrawal, 2005). Excess Cu cause toxicity in plants through chromatin structure alteration, chlorophyll and protein synthesis, antioxidant mechanisms, photosynthesis and respiration, water content and plant biomass (Connolly and Guerinot, 2002; Burzynski and Klobus, 2004). Plants are forced to take up excess Cu when soils contain prominent levels of this metal due to widespread use of pesticide, application of sewage sludge in agriculture and also by mining and smelting actions (Li and Zhang, 2010). Cu catalyses the formation of reactive oxygen species (ROS), produced in living cells as a by-product of metabolism under oxidative stress (Blokhina and Fagerstedt, 2010). ROS such as superoxide (O2• -), hydrogen peroxide (H2O2) are damaging to essential cellular components such as DNA, proteins and lipids and therefore induction of ROS production can lead to oxidative stress, affecting plant growth (Sharma et al., 2010).
In a natural wetland ecosystem, mangrove species are growing in an environment of high NaCl concentrations and these areas are also accumulation sites of industrial and urban effluents, mostly polluted by heavy metals (Carvalho et al., 2006). Hence, these salt marshes are considered as efficient sinks of Cu deposition by means of anthropogenic activities (Reboreda and Caçador, 2007). Halophytes have the ability to phytoremediate heavy metal pollution in vastly contaminated coastal saline areas. Generally mangroves are highly tolerant to heavy metal pollution and useful for the removal of such hazardous pollutants (Macfarlane and Burchett, 2000). Phytoremediation is an aesthetic solution for the remediation of metal contaminated sites, also cost-effective and long-lasting technique by plants (Arthur et al., 2005). The major technique adopted by plants to take care of up taken metal is by phytostabilization, i.e. roots accommodate the large part of the metal absorbed and are thus acting as a barrier for transport of metals to the shoots (Cambrollé et al., 2008). Peters et al. (1997) reported that, many mangrove species like Kandelia candel, Rhizophora species and Avicennia species have proven to be the major source for heavy metal exclusion from the contaminated soils. Hence in the coastal saline areas highly contaminated with heavy metal pollution may possibly be remediate by using plant species which are able to grow in extremely saline conditions. It would, therefore be appropriate to investigate the heavy metal tolerance potential by various halotolerant species and also analyze their mechanism of metal detoxification. Such reports on the simultaneous performance of plant system encountering high salinity and heavy metal toxicity in the soil are few.
B. cylindrica is a facultative mangrove, can grow normally in non-saline condition and is a predominant non-secretor tree mangrove that is highly tolerant to higher NaCl concentrations (600 mM), which grows along the Indian seacoast (Palliyath and Jos, 2018). Unlike some other mangroves, propagation is only with propagules and it takes two to three months to become healthy seedlings with 2–3 pairs of leaves. Generally mangroves growing under the influence of high salinity with heavy metal absorption potential seem to be promising candidates for phytoremediation in coastal wetlands. Hence the present investigation aims at determining the impact of individual (CuSO4) and combined (CuSO4 + NaCl) stress on B. cylindrica response towards heavy metal (Cu) absorption, in terms of photosynthetic efficiency, oxidative damage caused and histological variations. The outcome of the study will explore the suitability of B. cylindrica as a strong candidate for phytoremediation of heavy metals in estuaries.
Section snippets
Plant material
The mature propagules of B. cylindrica (reddish brown in colour) were collected from the mangrove ecosystem of Murikkumpadam, Puthuvyppu, Kochi, Kerala. The mangrove area selected for the collection of propagules has been located between latitudes 90 59’ North and longitude 760 14′ East and is located at Murikkumpadam in Vypeen island, Kerala, India. The collection of mature propagules was done during June to October; it was normally the seasonal time for propagule formation.
Experimental setup
These propagules
Results
In the preliminary screening to identify stress imparting concentration of CuSO4 + 400 mM NaCl in healthy plantlets of B. cylindrica, various parameters such as total chlorophyll, carotenoid and MDA content were analysed. The plantlets exposed to different CuSO4 concentrations along with NaCl imparted significant negative effects on the physiochemical characteristics such as significant reduction of total chlorophyll and carotenoid content as well as significant enhancement in MDA content, and
Discussion
Salt marshes are considered as an important sink for heavy metal pollutants, and at the same time these are major productive system of the earth (Vinagre et al., 2008). Plants growing in these regions have to encounter the heavy metals in the presence of salinity which can compromise their salinity as well as heavy metal tolerance potential. In the current study, combined stress of CuSO4 (0.15 mM) and NaCl (400 mM) imparts negative effect on the physiochemical mechanisms and metabolism of the
Conclusion
The combined stress of CuSO4 + NaCl negatively affects the photosynthetic efficiency of B. cylindrica plantlets and leads to structural and functional alterations in photosynthetic apparatus. Also the combined stress leads to the toxicity to the plants by generating oxidative stress mediated by reactive oxygen species (superoxide and hydrogen peroxide contents), there by disrupting membrane stability, which leads to electrolytic leakage of cells. The SEM EDXMA analysis revealed the accumulation
CRediT authorship contribution statement
Palliyath Sruthi:Investigation, Formal analysis, Writing - original draft.Jos T. Puthur:Conceptualization, Methodology, Writing - review & editing.
Declaration of competing interest
The authors declare that they have no conflict of interest.
Acknowledgements
SP greatly acknowledges the financial assistance provided by Department of Science and Technology, New Delhi; through INSPIRE fellowship (IF131045) for the research work. JTP acknowledges KSCSTE for funding through research grant from KSCSTE (KSCSTE/5179/2017-SRSLS).
References (86)
- et al.
Assessing of tolerance to metallic and saline stresses in the halophyte Suaeda fruticosa: the indicator role of antioxidative enzymes
Ecol. Indic.
(2016) - et al.
Comparison of the role of two Spartina species in terms of phytostabilization and bioaccumulation of metals in the estuarine sediment
Mar. Pollut. Bull.
(2008) - et al.
Distinct ubiquitin-ligase complexes define convergent pathways for the degradation of ER proteins
Cell
(2006) Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components
Physiol. Plant Pathol.
(1983)- et al.
Trace metal behaviour in estuarine and riverine floodplain soils and sediments: a review
Sci. Total Environ.
(2009) - et al.
Cadmium effects on growth and mineral nutrition of two halophytes: Sesuvium portulacastrum and Mesembryanthemum crystallinum
J. Plant Physiol.
(2005) - et al.
Comparative analysis of salt stress, duration and intensity, on the chloroplast ultrastructure and photosynthetic apparatus in Thellungiella salsuginea
J Photoch.Photobio. B
(2018) - et al.
Physiology is pivotal for interactions between salinity and acute copper toxicity to fish and invertebrates
Aquat.Toxicol.
(2007) - et al.
Cell-free formation of RNA granules: bound RNAs identify features and components of cellular assemblies
Cell
(2012) - et al.
Photoperoxidation in isolated chloroplast. I. Kinetics and stoichiometry of fatty acid peroxidation
Arch. Biochem. Biophys.
(1968)
Crystallochemical characterization of calcium oxalate crystals isolated from seed coats of Phaseolus vulgaris and leaves of Vitis vinifera
J. Plant Physiol.
Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces
Environ. Exp. Bot.
Fluorescence parameters as early indicators of light stress in barley
J. Photoch. Photobio. B.
Risk assessment and seasonal variations of dissolved trace elements and heavy metals in the upper Han River, China
J. Hazard. Mater.
NaCl-induced senescence in leaves of rice (Oriza sativa L.) cultivars differing in salinity resistance
Ann. Bot.
Salinity and water stress have contrasting effects on the relationship between growth and cell viability during and after stress exposure in durum wheat callus
Plant Sci.
Cellular distribution of Cu, Pb and Zn in the Grey Mangrove Avicennia marina (Forsk.)
Veirh.Aquat. Bot.
Use of chlorophyll fluorescence in metal-stress research: a case study with the green microalga Scenedesmus
Ecotoxicol. Environ. Saf.
Assessing the effect of copper on growth, copper accumulation and physiological responses of grazing species Atriplex halimus: Ecotoxicological implications
Ecotoxicol. Environ. Safety.
Herbivory and calcium concentrations affect calcium oxalate crystal formation in leaves of Sida (Malvaceae)
Ann. Bot.
Photoacoustic measurements of photosynthetic activities in intact leaves under copper stress
Plant Sci.
Evidence for PSII donor-side damage and photoinhibition induced by cadmium treatment on rice (Oryza sativa L.)
J. Photochem. Photobio. B.
Translocation and biotransformation of CuO nanoparticles in rice (Oryza sativa L.) plants
Environ. Pollut.
Gas exchange and chlorophyll fluorescence in four citrus rootstocks under aluminium stress
J. Plant Physiol.
Copper, zinc and lead speciation in salt marsh sediments colonized by Halimione portulacoides and Spartina maritima
Chemosphere
Response to cadmium in higher plants
Environ. Exp. Bot.
The role of 24-epibrassinolide in the regulation of photosynthetic characteristics and nitrogen metabolism of tomato seedlings under a combined low temperature and weak light stress
Plant Physiol. Biochem.
Ultra structural changes induced by selected Cd and Cu concentrations in the cyanobacterium Phormidium: interaction with salinity
J. Plant Physiol.
Influence of halophytes and metal contamination on salt marsh macro-benthic communities
Estuar. Coast. Shelf S.
Cadmium hampers salt tolerance of Sesuvium portulacastrum
Plant Physiol. Biochem.
Effect of heavy metal stress on antioxidative enzymes and lipid peroxidation in leaves and roots of two mangrove plant seedlings (Kandelia candel and Bruguiera gymnorrhiza)
Chemosphere
The preparation of agricultural samples for analysis by atomic absorption spectrometry
Salt marsh halophyte services to metal-metalloid remediation: assessment of the processes and underlying mechanisms
Crit. Rev. Environ. Sci. Technol.
Phytoremediation - an overview
Crit. Rev. Plant Sci.
Leaf chlorosis in oilseed rape plants (Brassica napus) grown on cadmium-polluted soil: causes and consequences for photosynthesis and growth
Planta
Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance
EMBO J
Reactive oxygen species and nitric oxide in plant mitochondria: origin and redundant regulatory systems
Physiol. Plantarum.
Superoxide dismutase and stress tolerance
Annu. Rev. Plant Physiol. Plant Mol. Biol.
Changes of photosynthetic parameters in cucumber leaves under Cu, Cd, and Pb stress
Photosynthetica
Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes
J. Exp. Bot.
Copper-induced oxidative stress and antioxidant defence in Arabidopsis thaliana
Biometals
Mineral Nutrition of Plants: Principles and Perspectives
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