Skip to main content
Log in

Natural and commercial Salix clones differ in their ecophysiological response to Zn stress

  • Original Papers
  • Published:
Photosynthetica

Abstract

This study was carried out to determine the effect of different zinc concentrations on the ecophysiological response of Salix clones: four commercial clones (“1962”, “1968”, “Drago”, and “Levante”) selected for short rotation coppice, and one natural clone, “Sacco”, obtained from a contaminated area. Gas exchanges, chlorophyll a fluorescence (JIP-test), relative chlorophyll content, and biometric parameters were measured in plants grown for fifteen days in soil containing Zn concentrations of 0, 300, 750, and 1,500 mg(ZnCl2) kg−1. Ecophysiological response to metal stress differed in dependence on the Zn concentration and clone. At the low Zn concentration (300 mg kg−1), the absence of any significant reductions in parameters investigated indicated an efficient plant homeostasis to maintain the metal content within phytotoxic limits. Stomatal limitation, observed at 750 and 1,500 mg kg−1, which was found in all clones after three days of the treatment, might be caused by indirect effects of metal on guard cells. Among commercial clones, “Drago” was more sensitive to Zn stress, showing inhibition of growth, while “1962” clone showed a downregulation of PSII photochemistry following the slowdown in the Calvin-Benson cycle. On the contrary, the natural Salix clone (“Sacco”) performed better compared to the other clones due to activation of a photosynthetic compensatory mechanism.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

C i :

substomatal CO2 concentration

DAT:

days after treatment

DM:

dry mass

F0 :

minimal fluorescence yield of the dark-adapted state

Fm :

maximal fluorescence yield of the dark-adapted state

FM:

fresh mass

g s :

stomatal conductance

LA:

leaf area

PIabs :

performance index (potential) for energy conservation from photons absorbed by PSII to the reduction of intersystem electron acceptors

PItotal :

performance index (potential) for energy conservation from photons absorbed by PSII to the reduction of PSI end acceptors

P N :

net assimilation rate

RC/CS0 :

number proportional to the active RCs to the cross-section of the measured sample

RH:

relative air humidity

RuBP:

ribulose-1,5-bisphosphate

SLA:

specific leaf area

SRC:

short rotation coppice

ΔVI-P :

amplitude of the I-P phase of the OJIP fluorescence transient

φP0 :

maximal quantum yield of PSII photochemistry

Ψ0 :

probability that a photon trapped by the PSII RC enters the electron transport chain

References

  • Adamski J.M., Peters J.A., Danieloski R., Bacarin M.A.: Excess iron-induced changes in the photosynthetic characteristics of sweet potato. — J. Plant Physiol. 168: 2056–2062, 2011.

    Article  PubMed  CAS  Google Scholar 

  • Agarwal A., Sharma I., Tripathi B.N. et al.: Metal toxicity and photosynthesis. — In: Itoh S., Mohanty P., Guruprasad K.N. (ed.): Photosynthesis: Overviews on Recent Progress & Future Perspective. Pp. 229–236. I.K. International Publ., New Delhi 2012.

    Google Scholar 

  • Ayeni O.O., Ndakidemi P.A., Snyman R.G., Odendaal J.P.: Chemical, biological and physiological indicators of metal pollution in wetlands. — Sci. Res. Essays 5: 1938–1949, 2010.

    Google Scholar 

  • Babu N.G., Sarma P.A., Attitalla I.H., Murthy S.D.S.: Effect of selected heavy metal ions on the photosynthetic electron transport and energy transfer in the thylakoid membrane of the Cyanobacterium, Spirulina platensis. — Acad. J. Plant Sci. 3: 46–49, 2010.

    Google Scholar 

  • Battisti S., Caminiti A., Ciotoli G. et al.: A spatial, statistical approach to map the risk of milk contamination by β-hexachlorocyclohexane in dairy farms. — Geospat. Health 8: 77–86, 2013.

    Article  PubMed  Google Scholar 

  • Belatik A., Hotchandani S., Carpentier R.: Inhibition of the water oxidizing complex of photosystem II and the reoxidation of the quinone acceptor QA by Pb2+. — PLoS One 8: e68142, 2013.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Chugh L.K., Sawhney S.K.: Photosynthetic activities of Pisum sativum seedlings grown in presence of cadmium. — Plant Physiol. Bioch. 37: 297–303, 1999.

    Article  CAS  Google Scholar 

  • Clemens S.: Molecular mechanisms of plant metal tolerance and homeostasis. — Planta 212: 475–486, 2001.

    Article  PubMed  CAS  Google Scholar 

  • de Silva N.D., Cholewa E., Ryser P.: Effects of combined drought and heavy metal stresses on xylem structure and hydraulic conductivity in red maple (Acer rubrum L.). — J. Exp. Bot. 63: 5957–5966, 2012.

    Article  PubMed  CAS  Google Scholar 

  • Desotgiu R., Pollastrini M., Cascio C. et al.: Responses to ozone on Populus “Oxford” clone in an open top chamber experiment assessed before sunrise and in full sunlight. — Photosynthetica 51: 267–280, 2013.

    Article  CAS  Google Scholar 

  • Dhir B., Sharmila P., Pardha Saradhi P.: Photosynthetic performance of Salvinia natans exposed to chromium and zinc rich wastewater. — Braz. J. Plant Physiol. 20: 61–70, 2008.

    Article  CAS  Google Scholar 

  • Di Baccio D., Tognetti R., Minnocci A., Sebastiani L.: Responses of the Populus × euramericana clone I-214 to excess zinc: carbon assimilation, structural modifications, metal distribution and cellular localization. — Environ. Exp. Bot. 67: 153–163, 2009.

    Article  CAS  Google Scholar 

  • Di Baccio D., Tognetti R., Sebastiani L., Vitagliano C.: Responses of Populus deltoides × Populus nigra (Populus × euramericana) clone I-214 to high zinc concentrations. — New Phytol. 159: 443–452, 2003.

    Article  CAS  Google Scholar 

  • Dos Santos Utmazian M.N., Wieshammer G., Vega R., Wenzel W.: Hydroponic screening for metal resistance and accumulation of cadmium and zinc in twenty clones of willows and poplars. — Environ. Pollut. 148: 155–165, 2007.

    Article  PubMed  CAS  Google Scholar 

  • Durand T.C., Baillif P., Albéric P. et al.: Cadmium and zinc are differentially distributed in Populus tremula × P. alba exposed to metal excess. — Plant Biosyst. 145: 397–405, 2011.

    Article  Google Scholar 

  • Ernst W.H.O., Peterson P.J.: The role of biomarkers in environmental assessment (4). Terrestrial plants. — Ecotoxicol. 3: 180–192, 1994.

    Article  CAS  Google Scholar 

  • Hermle S., Günthardt-Goerg M.S., Schulin R.: Effects of metalcontaminated soil on the performance of young trees growing in model ecosystems under field conditions. — Environ. Pollut. 144: 703–714, 2006.

    Article  PubMed  CAS  Google Scholar 

  • Kalaji H.M., Schansker G., Ladle R.J.et al.: Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. — Photosynth. Res. 122: 121–158, 2014

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Khan N.A., Samiullah, Singh S., Nazar R.: Activities of antioxidative enzymes, sulphur assimilation, photosynthetic activity and growth of wheat (Triticum aestivum) cultivars differing in yield potential under cadmium stress. — J. Agro. Crop Sci. 193: 435–444, 2007.

    Article  CAS  Google Scholar 

  • Kim C.S., Jung J.: The susceptibility of mung bean chloroplasts to photoinhibition is increased by an excess supply of iron to plants: a photobiological aspect of iron toxicity in plant leaves. — Photochem. Photobiol. 58: 120–126, 1993.

    Article  CAS  Google Scholar 

  • Konlechner C., Türktas M., Langer I. et al.: Expression of zinc and cadmium responsive genes in leaves of willow (Salix caprea L.) genotypes with different accumulation characteristics. — Environ. Pollut. 178: 121–127, 2013.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Küpper H., Küpper F., Spiller M.: In situ detection of heavy metal substituted chlorophylls in water plants. — Photosynth. Res. 58: 123–133, 1998.

    Article  Google Scholar 

  • Landberg T., Greger M.: Differences in uptake and tolerance to heavy metals in Salix from unpolluted and polluted areas. — Appl. Geochem. 11: 175–180, 1996.

    Article  CAS  Google Scholar 

  • Lin Y-F., Aarts M.G.M.: The molecular mechanism of zinc and cadmium stress response in plants. — Cell. Mol. Life Sci. 69: 3187–3206, 2012.

    Article  PubMed  CAS  Google Scholar 

  • Lingua G., Franchin C., Todeschini V. et al.: Arbuscular mycorrhizal fungi differentially affect the response to high zinc concentrations of two registered poplar clones. — Environ. Pollut. 153: 137–147, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Lunáčkova L., Masarovičová E., Král’ová K., Streško V.: Response of fast growing woody plants from family Salicaceae to cadmium treatment. — Bull. Environ. Contam. Toxicol. 70: 576–585, 2003.

    Article  PubMed  CAS  Google Scholar 

  • Marmiroli M., Pietrini F., Maestri E. et al.: Growth, physiological and molecular traits in Salicaceae trees investigated for phytoremediation of heavy metals and organics. — Tree Physiol. 31: 1319–1334, 2011.

    Article  PubMed  CAS  Google Scholar 

  • Marshner H.: Mineral Nutrition of Higher Plants. Pp. 347–365. Academic Press, London 1997.

    Google Scholar 

  • Mereu S., Gerosa G., Marzuoli R. et al.: Gas exchange and JIPtest parameters of two Mediterranean maquis species are affected by sea spray and ozone interaction. — Environ. Exp. Bot. 73: 80–88, 2011.

    Article  CAS  Google Scholar 

  • Migeon A., Richaud P., Guinet F. et al.: Metal accumulation by woody species on contaminated sites in the North of France. — Water Air Soil Pollut. 204: 89–101, 2009.

    Article  CAS  Google Scholar 

  • Mittler R., Vanderauwera S., Gollery M., Van Breusegem F.: Reactive oxygen gene network of plants. — Trends Plant Sci. 9: 490–498, 2004.

    Article  PubMed  CAS  Google Scholar 

  • Mleczek M., Rissmann I., Rutkowski P. et al.: Accumulation of selected heavy metals by different genotypes of Salix. — Environ. Exp. Bot. 66: 289–296, 2009.

    Article  CAS  Google Scholar 

  • Morgan A.J., Evans M., Winters C. et al.: Assaying the effects of chemical ameliorants with earthworms and plants exposed to a heavily polluted metalliferous soil. — Eur. J. Soil Biol. 38: 323–327, 2002.

    Article  CAS  Google Scholar 

  • Nagajyoti P.C., Lee K.D., Sreekanth T.V.M.: Heavy metals, occurrence and toxicity for plants: a review. — Environ. Chem. Lett. 8: 199–216, 2010.

    Article  CAS  Google Scholar 

  • Nikiforou C., Manetas Y.: Inherent nitrogen deficiency in Pistacia lentiscus preferentially affects photosystem I: a seasonal field study. — Funct. Plant Biol. 38: 848–855, 2011.

    Article  CAS  Google Scholar 

  • Oukarroum A., Schansker G., Strasser R.J.: Drought stress effects on photosystem I content and photosystem II thermotolerance analyzed using Chl a fluorescence kinetics in barley varieties differing in their drought tolerance. — Physiol. Plantarum 137: 188–199, 2009.

    Article  CAS  Google Scholar 

  • Panagos P., van Liedekerke M., Yigini Y., Montanarella L.: Contaminated sites in Europe: review of the current situation based on data collected through a European Network. — J. Environ. Public Health. 2013: 158764, 2013.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Papazoglou E.G., Serelis K.G., Bouranis D.L.: Impact of high cadmium and nickel soil concentration on selected physiological parameters of Arundo donax L.. — Eur. J. Soil Biol. 43, 207–215, 2007.

    Article  CAS  Google Scholar 

  • Pollastrini M., Desotgiu R., Camin F. et al.: Severe drought events increase the sensitivity to ozone on poplar clones. — Environ. Exp. Bot. 100: 94–104, 2014.

    Article  CAS  Google Scholar 

  • Prasad M.N.V.: Heavy Metal Stress in Plants: from Biomolecules to Ecosystems. Pp. 146–181. Springer, Berlin 2004.

    Book  Google Scholar 

  • Pulford I.D., Watson C.: Phytoremediation of heavy metalcontaminated land by trees: a review. — Environ. Int. 29: 529–540, 2003.

    Article  PubMed  CAS  Google Scholar 

  • [Report Department of Epidemiology of the Regional Health Service, Lazio Region.] — In: Porta D., Narduzzi S., Blasetti et al. (ed.): [Sanitary and Epidemiological Surveillance of the Population Lives in the Sacco River.] Pp. 24–26. Rome 2013. [in Italian]

  • [Report Institute for the Protection and Environmental Research.] — In: Pirani G., Vecchio A. (ed.): [Determination of Natural Background Values for some Metals-Metals in the Soils of the National Site of Sacco Valley.] Pp. 13–48. Rome 2009. [in Italian]

  • Rosselli W., Keller C., Boschi K.: Phytoextraction capacity of trees growing on a metal contaminated soil. — Plant Soil 256: 265–272, 2003.

    Article  CAS  Google Scholar 

  • Sagardoy R., Morales F., López-Millán A.F. et al.: Effects of zinc toxicity on sugar beet (Beta vulgaris L.) plants grown in hydroponics. — Plant Biol. 11: 339–350, 2009.

    Article  PubMed  CAS  Google Scholar 

  • Sala M., Caminiti A., Rombolà P. et al.: [Betahexachlorocyclohexane contamination in dairy farms of the Sacco River Valley, Latium, Italy. A Retrospective study.] — Epidemiol. Prev. 36: 34–43, 2012. [in Italian]

    PubMed  Google Scholar 

  • Salvatori E., Fusaro L., Mereu S. et al.: Different O3 response of sensitive and resistant snap bean genotypes (Phaseolus vulgaris L.): The key role of growth stage, stomatal conductance, and PSI activity. — Environ. Exp. Bot. 87: 79–91, 2013.

    Article  CAS  Google Scholar 

  • Salvatori E., Fusaro L., Gottardini E. et al.: Plant stress analysis: Application of prompt, delayed chlorophyll fluorescence and 820 nm modulated reflectance. Insights from independent experiments. — Plant Physiol. Bioch. 85: 105–113, 2014.

    Article  CAS  Google Scholar 

  • Santos D., Duarte B., Caçador I.: Unveiling Zn hyperaccumulation in Juncus acutus: Implications on the electronic energy fluxes and on oxidative stress with emphasis on nonfunctional Zn-chlorophylls. — J. Photoch. Photobio. 140: 228–239, 2014.

    Article  CAS  Google Scholar 

  • Shah F.R., Ahmad N., Masood K.R. et al.: Heavy metal toxicity in plants. — In: Ashraf M., Ozturk M., Ahmad M.S.A. (ed.): Plant Adaptation and Phytoremediation. Pp 71–97. Springer Sci. Business Media, London 2010.

    Chapter  Google Scholar 

  • Shi G.R., Cai Q.S.: Photosynthetic and anatomic responses of peanut leaves to zinc stress. — Biol. Plantarum 53: 391–394, 2009.

    Article  CAS  Google Scholar 

  • Siegel S., Castellan N.J.: Nonparametric Statistics for The Behavioral Sciences. Pp. 16–32. McGraw-Hill, New York 1988.

    Google Scholar 

  • Solanki R., Dhankhar R.: Biochemical changes and adaptive strategies of plants under heavy metal stress. — Biologia 66: 195–204, 2011.

    Article  CAS  Google Scholar 

  • Strasser R.J., Tsimilli-Michael M., Qiang S., Goltsev V.: Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. — Biochim. Biophys. Acta 1797: 1313–1326, 2010.

    Article  PubMed  CAS  Google Scholar 

  • Strasser R.J., Tsimilli-Michael M., Srivastava A.: Analysis of the fluorescence transient. — In: Papageorgiou GC, Govindjee (ed.): Chlorophyll a Fluorescence: A Signature of Photosynthesis. Pp. 321–362. Springer, Dordrecht 2004.

    Chapter  Google Scholar 

  • SWS Society of Wetlands Scientists: Pollution and environmental restoration: characterization of the riparian species Salix alba L. in contaminated site. — In: Borin M., Malagoli M., Salvato M., Tanis B. (ed.): European Chapter Meeting International Conference, Wetland Systems: Ecology, Functioning and Management. Pp. 105–106. P.A.N. s.r.l., Padua 2013.

  • Todeschini V., Lingua G., D’Agostino G. et al.: Effects of high zinc concentration on poplar leaves: A morphological and biochemical study. — Environ. Exp. Bot. 71: 50–56, 2011.

    Article  CAS  Google Scholar 

  • Tsala Ndzono N.G., Omokolo Ndoumou D., Tita Awah M.: Effect of Fe2+, Mn2+, Zn2+ and Pb2+ on H+/K+ fluxes in excised Pistia stratiotes roots. — Biol. Plantarum 36: 591–597, 1994.

    Article  Google Scholar 

  • Tsonev T., Cebola Lidon F. J.: Zinc in plants — An overview. — Emir. J. Food Agric. 24: 322–333, 2012.

    Google Scholar 

  • Ugolini F., Massetti L., Pedrazzoli F. et al.: Ecophysiological responses and vulnerability to other pathologies in European chestnut coppices, heavily infested by the Asian chestnut gall wasp. — Forest Ecol. Manag. 314: 38–49, 2014.

    Article  Google Scholar 

  • Vaillant N., Monnet F., Hitmi A. et al.: Comparative study of responses in four Datura species to a zinc stress. — Chemosphere 59: 1005–1013, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Wang C., Zhang S.H., Wang P.F. et al.: The effect of excess Zn on mineral nutrition and antioxidative response in rapeseed seedlings. — Chemosphere 75:1468–1476, 2009.

    Article  PubMed  CAS  Google Scholar 

  • Wang S., Zhang D., Pan X.: Effects of arsenic on growth and photosystem II (PSII) activity of Microcystis aeruginosa. — Ecotoxicol. Environ. Saf. 84: 104–111, 2012.

    Article  PubMed  CAS  Google Scholar 

  • Wodala B., Eitel G., Gyula T.N. et al.: Monitoring moderate Cu and Cd toxicity by chlorophyll fluorescence and P700 absorbance in pea leaves. — Photosynthetica 50: 380–386, 2012.

    Article  CAS  Google Scholar 

  • Xue Z.C., Gao H.Y., Zhang L.T.: Effects of cadmium on growth, photosynthetic rate, and chlorophyll content in leaves of soybean seedlings. — Biol. Plantarum 57: 587–590, 2013.

    Article  CAS  Google Scholar 

  • Yang H.M., Zhang X.Y., Wang G.X.: Effects of heavy metals on stomatal movements in broad bean leaves. — Russ. J. Plant Physl+ 51: 464–468, 2004.

    Article  CAS  Google Scholar 

  • Zacchini M., Pietrini F., Scarascia Mugnozza G. et al.: Metal tolerance, accumulation and translocation in poplar and willow clones treated with cadmium in hydroponics. — Water Air Soil Pollut. 197: 23–34, 2009.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. Bernardini.

Additional information

Acknowledgements: This research was supported by project Joint Lab Environment (2008), “Integrated project for monitoring, requalification and environmental restoration of the Sacco River Valley, Site of National Interest” (Lazio Region, Italy), and by Sapienza Ateneo Research Project “Study of the phytoremediation processes in simulated laboratory experiments through ecophysiological analysis in the context of the recovery of contaminated sites from heavy metals” (2013, prot. C26N13B3ER). We thank to the Istituto Sperimentale for the Pioppicoltura (Casale Monferrato, Italy) for providing woody cuttings of Salix alba (1962 and 1968 clones) and Salix matsudana ×? (Drago and Levante clones).

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bernardini, A., Salvatori, E., Di Re, S. et al. Natural and commercial Salix clones differ in their ecophysiological response to Zn stress. Photosynthetica 54, 56–64 (2016). https://doi.org/10.1007/s11099-015-0155-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11099-015-0155-9

Additional key words

Navigation