High NaCl tolerance potential of Bruguiera cylindrica (L.) Blume compromised by mild CuSO4 concentration as evidenced by unique physiochemical features

https://doi.org/10.1016/j.marpolbul.2020.111260Get rights and content

Highlights

  • Differential responses of B. cylindrica towards combined (NaCl + CuSO4) stress was evaluated for the first time.

  • 400 mM NaCl and 0.15 mM CuSO4 treatments beneficial when applied individually, for the plant growth and stress tolerance.

  • The combination of Cu along with CaOx crystals is an effective internal tolerance mechanism in B. cylindrica.

  • NaCl tolerance potential of B. cylindrica is highly compromised in the presence of mild CuSO4 concentration.

Abstract

Differential response of Bruguiera cylindrica to individual (CuSO4) and combined (CuSO4 NaCl) effect was evaluated. The plantlets were treated with control, 0.15 mM CuSO4, 400 mM NaCl and 0.15 mM CuSO4 + 400 mM NaCl. Under combined stress, higher accumulation of Cu in the roots indicate that the roots are the primary site of Cu accumulation and thus the plant perform as an excluder and photosynthetic efficiency reduced drastically and significant enhancement in the superoxide and hydroxyl free radicals which increase membrane lipid peroxidation, leading to cellular damage and destruction. As evidenced from SEM-EDXMA, increase in Cu and Na+ levels in xylem and pith regions of leaf and stem and the presence of deeply stained structures, denoting the probable formation of complex containing the metal. Increased CaOx crystal forming cells (crystal idioblasts) reveals the regulation of bioaccumulated Cu and Na+ by complexing with CaOx. Thus the study suggested that, 400 mM NaCl and 0.15 mM CuSO4 treatments does not have negative impact on plant growth, the NaCl tolerance potential compromised in the presence of mild CuSO4 concentration during combined stress.

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)

  • D. Jauregui-Zuniga et al.

    Crystallochemical characterization of calcium oxalate crystals isolated from seed coats of Phaseolus vulgaris and leaves of Vitis vinifera

    J. Plant Physiol.

    (2003)
  • H.M. Kalaji et al.

    Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces

    Environ. Exp. Bot.

    (2011)
  • H.M. Kalaji et al.

    Fluorescence parameters as early indicators of light stress in barley

    J. Photoch. Photobio. B.

    (2012)
  • S.Y. Li et al.

    Risk assessment and seasonal variations of dissolved trace elements and heavy metals in the upper Han River, China

    J. Hazard. Mater.

    (2010)
  • S. Lutts et al.

    NaCl-induced senescence in leaves of rice (Oriza sativa L.) cultivars differing in salinity resistance

    Ann. Bot.

    (1996)
  • S. Lutts et al.

    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.

    (2004)
  • G.R. MacFarlane et al.

    Cellular distribution of Cu, Pb and Zn in the Grey Mangrove Avicennia marina (Forsk.)

    Veirh.Aquat. Bot.

    (2000)
  • N. Mallick et al.

    Use of chlorophyll fluorescence in metal-stress research: a case study with the green microalga Scenedesmus

    Ecotoxicol. Environ. Saf.

    (2003)
  • E. Mateos-Naranjo et al.

    Assessing the effect of copper on growth, copper accumulation and physiological responses of grazing species Atriplex halimus: Ecotoxicological implications

    Ecotoxicol. Environ. Safety.

    (2013)
  • B. Molano-Flores

    Herbivory and calcium concentrations affect calcium oxalate crystal formation in leaves of Sida (Malvaceae)

    Ann. Bot.

    (2001)
  • G. Ouzounidou et al.

    Photoacoustic measurements of photosynthetic activities in intact leaves under copper stress

    Plant Sci.

    (1993)
  • C. Pagliano et al.

    Evidence for PSII donor-side damage and photoinhibition induced by cadmium treatment on rice (Oryza sativa L.)

    J. Photochem. Photobio. B.

    (2006)
  • C. Peng et al.

    Translocation and biotransformation of CuO nanoparticles in rice (Oryza sativa L.) plants

    Environ. Pollut.

    (2015)
  • W.E. Pereira et al.

    Gas exchange and chlorophyll fluorescence in four citrus rootstocks under aluminium stress

    J. Plant Physiol.

    (2000)
  • R. Reboreda et al.

    Copper, zinc and lead speciation in salt marsh sediments colonized by Halimione portulacoides and Spartina maritima

    Chemosphere

    (2007)
  • L. Sanita di Toppi et al.

    Response to cadmium in higher plants

    Environ. Exp. Bot.

    (1999)
  • S. Shu et al.

    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.

    (2016)
  • W. Surosz et al.

    Ultra structural changes induced by selected Cd and Cu concentrations in the cyanobacterium Phormidium: interaction with salinity

    J. Plant Physiol.

    (2000)
  • C. Vinagre et al.

    Influence of halophytes and metal contamination on salt marsh macro-benthic communities

    Estuar. Coast. Shelf S.

    (2008)
  • M. Wali et al.

    Cadmium hampers salt tolerance of Sesuvium portulacastrum

    Plant Physiol. Biochem.

    (2017)
  • F.Q. Zhang et al.

    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

    (2007)
  • J.E. Allan

    The preparation of agricultural samples for analysis by atomic absorption spectrometry

  • N.A. Anjum et al.

    Salt marsh halophyte services to metal-metalloid remediation: assessment of the processes and underlying mechanisms

    Crit. Rev. Environ. Sci. Technol.

    (2014)
  • E.L. Arthur et al.

    Phytoremediation - an overview

    Crit. Rev. Plant Sci.

    (2005)
  • A. Baryla et al.

    Leaf chlorosis in oilseed rape plants (Brassica napus) grown on cadmium-polluted soil: causes and consequences for photosynthesis and growth

    Planta

    (2001)
  • P. Berthomieu et al.

    Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance

    EMBO J

    (2003)
  • O. Blokhina et al.

    Reactive oxygen species and nitric oxide in plant mitochondria: origin and redundant regulatory systems

    Physiol. Plantarum.

    (2010)
  • C. Bowler et al.

    Superoxide dismutase and stress tolerance

    Annu. Rev. Plant Physiol. Plant Mol. Biol.

    (1992)
  • M. Burzynski et al.

    Changes of photosynthetic parameters in cucumber leaves under Cu, Cd, and Pb stress

    Photosynthetica

    (2004)
  • Connolly, E.L., Guerinot, M., 2002. Iron stress in plants. Genome Biol. 3: Reviews...
  • L.A. Del Río et al.

    Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes

    J. Exp. Bot.

    (2002)
  • M. Drazkiewicz et al.

    Copper-induced oxidative stress and antioxidant defence in Arabidopsis thaliana

    Biometals

    (2004)
  • E. Epstein

    Mineral Nutrition of Plants: Principles and Perspectives

    (1972)
  • Cited by (7)

    • Phytostabilization of arsenic and associated physio-anatomical changes in Acanthus ilicifolius L

      2022, Environmental Pollution
      Citation Excerpt :

      The maximum quantum yield of PSII (Fv/Fm) in As treated plantlets decreased and were maximally reduced at 90 μM. The plantlets subjected to severe As stress only showed drastic changes in Fv/Fm because quantum yield measurements are normally the least responsive in plants subjected to heavy metal treatments (Sruthi and Puthur, 2020). The higher content of metalloids in the tissues can inhibit photosynthesis, resulting in reduced biomass production.

    • Functional aspects of plant secondary metabolites in metal stress tolerance and their importance in pharmacology

      2021, Plant Stress
      Citation Excerpt :

      Increased thickness of cell walls protects the plants from the damaging effects of metal toxicity (Krzesłowska, 2011). Scanning electron microscope analysis and energy dispersive X-ray microanalysis in Bruguiera cylindrica subjected to CuSO4 along with NaCl stress treatments revealed the thickening of the xylem vessels by the accumulation of Na+and Cu2+ ions (Sruthi and Puthur, 2020). Metal stress can stimulate the synthesis pathway of phenolic secondary metabolites and increase lignin content in the secondary cell wall.

    • Phycoremediation and phytoremediation: Promising tools of green remediation

      2021, Sustainable Environmental Clean-up: Green Remediation
    View all citing articles on Scopus
    View full text