Skip to main content
Springer Nature Link
Log in

Sex-related differences in physiological and ultrastructural responses of Populus cathayana to Ni toxicity

  • Original Paper
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

We used Populus cathayana, a native species with an extensive distribution in northern, central, and southwestern China, as a model species to detect the sex-specific differences in photosynthetic capacity, ultrastructure, nitrogen (N) metabolism, and nickel (Ni) accumulation and distribution in response to Ni stress. Exposure to 100 μM Ni2+ in a hydroponic system for 1 month significantly decreased the pigment content and the photosynthetic rate, caused visible impairment in cellular organelle structure, and induced obvious disturbance and imbalance in the N content of female plants, while male plants suffered a lower negative influence on all the above measured parameters. However, males accumulated a higher Ni concentration in both leaves and roots than females, while the transportation ratio of Ni from roots to shoots in males was slightly lower than that in females. Our results, therefore, suggest that males have a better tolerance capacity and a greater ability to remediate Ni-polluted soil than females. This greater tolerance capacity in males might be highly correlated with the better maintenance of N balance and more effective physiological detoxification responses (such as the response to proline) under Ni stress. The differences between the sexes in tolerance capacity to heavy metals should be verified after performing a field investigation using adult trees as materials in the future study.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

Chl a:

Chlorophyll a

Chl b:

Chlorophyll b

Gs:

Grana

Lcp:

Light compensation point

NR:

Nitrate reductase

P max :

Light-saturated photosynthetic rate

P n :

Net photosynthetic rate

PPFD:

Photosynthetic photon flux density

Q :

Apparent quantum efficiency

R d :

Dark respiration rate

ROS:

Reactive oxygen species

TC:

Total chlorophyll content

TEM:

Transmission electron microscopy

References

  • Ahmad MSA, Ashraf M, Hussain M (2011) Phytotoxic effects of nickel on yield and concentration of macro- and micro-nutrients in sunflower (Helianthus annuus L.) achenes. J Hazard Mater 185:1295–1303

    Article  CAS  PubMed  Google Scholar 

  • Borghi M, Tognetti R, Monteforti G, Sebastiani L (2008) Responses of two poplar species (Populus alba and Populus × canadensis) to high copper concentrations. Environ Exp Bot 62:290–299

    Article  CAS  Google Scholar 

  • Borišev M, Pajević S, Nikolić N, Pilipović A, Krstić B, Orlović S (2009) Phytoextraction of Cd, Ni, and Pb using four willow clones (Salix spp.). Pol J Environ Stud 18:553–561

    Google Scholar 

  • Borišev M, Pajević S, Nikolić N, Krstić B, Pilipović A (2010) Influence of Cd and Ni on content of N, P, K, nitrates and activity of nitrate reductase in clones of Salix spp. Biotechnol Biotec Eq 24:228–235

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Brooks RR, Chambers MF, Nicks LJ, Robinson BH (1998) Phytomining. Trends Plant Sci 3:359–362

    Article  Google Scholar 

  • Chen L, Zhang S, Zhao H, Korpelainen H, Li C (2010) Sex-related adaptive responses to interaction of drought and salinity in Populus yunnanensis. Plant Cell Environ 33:1767–1778

    Article  CAS  PubMed  Google Scholar 

  • Chen L, Han Y, Jiang H, Korpelainen H, Li C (2011) Nitrogen nutrient status induces sexual differences in responses to cadmium in Populus yunnanensis. J Exp Bot 62:5037–5050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen L, Wang L, Chen F, Korpelainen H, Li C (2013) The effects of exogenous putrescine on sex-specific responses of Populus cathayana to copper stress. Ecotoxicol Environ Safe 97:94–102

    Article  CAS  Google Scholar 

  • Comino E, Whiting SN, Neumann PM, Baker AJM (2005) Salt (NaCl) tolerance in the Ni hyperaccumulator Alyssum murale and the Zn hyperaccumulator Thlaspi caerulescens. Plant Soil 270:91–99

    Article  CAS  Google Scholar 

  • Correia I, Nunes A, Duarte IF, Barros A, Delgadillo I (2005) Sorghum fermentation followed by spectroscopic techniques. Food Chem 90:853–859

    Article  CAS  Google Scholar 

  • Dahiya DJ, Singh JP, Kumar V (1994) Nitrogen uptake in wheat as influenced by the presence of nickel. Arid Soil Res Rehab 8:51–58

    CAS  Google Scholar 

  • Dawson TE, Ehleringer JR (1993) Gender-specific physiology, carbon isotope discrimination, and habitat distribution in boxelder, Acer Negundo. Ecology 74:798–815

    Article  Google Scholar 

  • Dixon NE, Gazzola C, Blakeley RL, Zerner B (1975) Jack bean urease (EC 3.5. 1.5). metalloenzyme. Simple biological role for nickel. J Am Chem Soc 97:4131–4133

    Article  CAS  PubMed  Google Scholar 

  • Djebali W, Zarrouk M, Brouquisse R, El Kahoui S, Limam F, Ghorbel MH, Chaïbi W (2005) Ultrastructure and lipid alterations induced by cadmium in tomato (Lycopersicon esculentum) chloroplast membranes. Plant Biol 7:358–368

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Eränen JK (2008) Rapid evolution towards heavy metal resistance by mountain birch around two subarctic copper-nickel smelters. J Evol Biol 21:492–501

    Article  PubMed  Google Scholar 

  • Gajewska E, Wielanek M, Bergier K, Skłodowska M (2009) Nickel-induced depression of nitrogen assimilation in wheat roots. Acta Physiol Plant 31:1291–1300

    Article  CAS  Google Scholar 

  • Gheibi MN, Malakouti MJ, Kholdebarin B, Ghanati F, Teimouri S, Sayadi R (2009) Significance of nickel supply for growth and chlorophyll content of wheat supplied with urea or ammonium nitrate. J Plant Nutr 32:1440–1450

    Article  CAS  Google Scholar 

  • Hall JL (2002) Cellular mechanisms for heavy metal detoxification and tolerance. J Exp Bot 53:1–11

    Article  CAS  PubMed  Google Scholar 

  • Hirose T, Werger MJA (1987) Nitrogen use efficiency in instantaneous and daily photosynthesis of leaves in the canopy of a Solidago altissima stand. Physiol Plant 70:215–222

    Article  CAS  Google Scholar 

  • Kevresan S, Petrovic N, Popovic M, Kandrac J (2001) Nitrogen and protein metabolism in young pea plants as affected by different concentrations of nickel, cadmium, lead, and molybdenum. J Plant Nutr 24:1633–1644

    Article  CAS  Google Scholar 

  • Kozlov MV (2005) Pollution resistance of mountain birch, Betula pubescens subsp. czerepanovii, near the copper-nickel smelter: natural selection or phenotypic acclimation? Chemosphere 59:189–197

    Article  CAS  PubMed  Google Scholar 

  • Kumar PBAN, Dushenkov V, Motto H, Raskin I (1995) Phytoextraction: the use of plants to remove heavy metals from soils. Environ Sci Technol 29:1232–1238

    Article  CAS  PubMed  Google Scholar 

  • Kutman BY, Kutman UB, Cakmak I (2013) Nickel-enriched seed and externally supplied nickel improve growth and alleviate foliar urea damage in soybean. Plant Soil 363:61–75

    Article  CAS  Google Scholar 

  • Lei Y, Chen K, Tian X, Korpelainen H, Li C (2007a) Effect of Mn toxicity on morphological and physiological changes in two Populus cathayana populations originating from different habitats. Trees Struct Funct 21:569–580

    Article  CAS  Google Scholar 

  • Lei Y, Korpelainen H, Li C (2007b) Physiological and biochemical responses to high Mn concentrations in two contrasting Populus cathayana populations. Chemosphere 68:686–694

    Article  CAS  PubMed  Google Scholar 

  • Li W, Chen T, Huang Z, Lei M, Liao X (2006) Effect of arsenic on chloroplast ultrastructure and calcium distribution in arsenic hyperaccumulator Pteris vittata L. Chemosphere 62:803–809

    Article  CAS  PubMed  Google Scholar 

  • Llamas A, Sanz A (2008) Organ-distinctive changes in respiration rates of rice plants under nickel stress. Plant Growth Regul 54:63–69

    Article  CAS  Google Scholar 

  • Llamas A, Ullrich CI, Sanz A (2000) Cd2+ effects on transmembrane electrical potential difference, respiration and membrane permeability of rice (Oryza sativa L.) roots. Plant Soil 219:21–28

    Article  CAS  Google Scholar 

  • Mihucz VG, Csog Á, Fodor F, Tatár E, Szoboszlai N, Silaghi-Dumitrescu L, Záray G (2012) Impact of two iron (III) chelators on the iron, cadmium, lead and nickel accumulation in poplar grown under heavy metal stress in hydroponics. J Plant Physiol 169:561–566

    Article  CAS  PubMed  Google Scholar 

  • Minocha R, Minocha SC (2005) Effects of soil pH and aluminum on plant respiration. In: Lambers H, Ribas-Carbo M (eds) Plant respiration: from cell to ecosystem advances in photosynthesis and respiration. Springer, Dordrecht, pp 159–176

    Chapter  Google Scholar 

  • Mishra P, Dubey RS (2011) Nickel and Al-excess inhibit nitrate reductase but upregulate activities of aminating glutamate dehydrogenase and aminotransferases in growing rice seedlings. Plant Growth Regul 64:251–261

    Article  CAS  Google Scholar 

  • Mitchell AK (1998) Acclimation of Pacific yew (Taxus brevifolia) foliage to sun and shade. Tree Physiol 18:749–757

    Article  PubMed  Google Scholar 

  • Pietrini F, Zacchini M, Iori V, Pietrosanti L, Ferretti M, Massacci A (2010) Spatial distribution of cadmium in leaves and its impact on photosynthesis: examples of different strategies in willow and poplar clones. Plant Biol 12:355–363

    Article  CAS  PubMed  Google Scholar 

  • Pollard AJ, Powell KD, Harper FA, Smith JAC (2002) The genetic basis of metal hyperaccumulation in plants. Crit Rev Plant Sci 21:539–566

    Article  CAS  Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. Biochim Biophys Acta 975:384–394

    Article  CAS  Google Scholar 

  • Pulford ID, Watson C (2003) Phytoremediation of heavy metal-contaminated land by trees-a review. Environ Int 29:529–540

    Article  CAS  PubMed  Google Scholar 

  • Rafati M, Khorasani N, Moattar F, Shirvany A, Moraghebi F, Hosseinzadeh S (2011) Phytoremediation potential of Populus alba and Morus alba for cadmium, chromium and nickel absorption from polluted soil. Int J Environ Res 5:961–970

    CAS  Google Scholar 

  • Romero-Puertas MC, Palma JM, Gómez M, Del Río LA, Sandalio LM (2002) Cadmium causes the oxidative modification of proteins in pea plants. Plant Cell Environ 25:677–686

    Article  CAS  Google Scholar 

  • Rosales EP, Iannone MF, Groppa MD, Benavides MP (2012) Polyamines modulate nitrate reductase activity in wheat leaves: involvement of nitric oxide. Amino Acids 42:857–865

    Article  CAS  PubMed  Google Scholar 

  • Schaumlöffel D, Ouerdane L, Bouyssiere B, Łobinski R (2003) Speciation analysis of nickel in the latex of a hyperaccumulating tree Sebertia acuminata by HPLC and CZE with ICP MS and electrospray MS-MS detection. J Anal At Spectrom 18:120–127

    Article  Google Scholar 

  • Sreekanth TVM, Nagajyothi PC, Lee KD, Prasad TNVKV (2013) Occurrence, physiological responses and toxicity of nickel in plants. Int J Environ Sci Technol 10:1129–1140

    Article  CAS  Google Scholar 

  • Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97

    Article  CAS  PubMed  Google Scholar 

  • Tabatabaei SJ (2009) Supplements of nickel affect yield, quality, and nitrogen metabolism when urea or nitrate is the sole nitrogen source for cucumber. J Plant Nutr 32:713–724

    Article  CAS  Google Scholar 

  • Troll W, Lindsley J (1955) A photometric method for the determination of proline. J Biol Chem 215:655–660

    CAS  PubMed  Google Scholar 

  • Velikova V, Tsonev T, Loreto F, Centritto M (2011) Changes in photosynthesis, mesophyll conductance to CO2, and isoprenoid emissions in Populus nigra plants exposed to excess nickel. Environ Pollut 159:1058–1066

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Feng L, Jiang H, Ma W, Korpelainen H, Li C (2012) Biochemical and proteomic analyses reveal that Populus cathayana males and females have different metabolic activities under chilling stress. J Proteome Res 11:5815–5826

    CAS  PubMed  Google Scholar 

  • Zornoza P, Robles S, Martin N (1999) Alleviation of nickel toxicity by ammonium supply to sunflower plants. Plant Soil 208:221–226

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the National Natural Science Foundation of China (No. 31300513), the Project funded by China Postdoctoral Science Foundation (No. 2012M521707), the Application Foundation Project in Sichuan Province (2013JY0083), and the National Key Technologies R & D Program of China (No. 2011BAC09B05).

Author information

Authors and Affiliations

  1. Institute of Ecological Forestry, Sichuan Agricultural University, Chengdu, 611130, China

    Lianghua Chen, Li Zhang, Zhenfeng Xu, Jian Zhang & Shun Gao

  2. College of Forestry, Sichuan Agricultural University, Ya’an, 625014, China

    Lihua Tu

Authors
  1. Lianghua Chen
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Li Zhang
    View author publications

    You can also search for this author inPubMed Google Scholar

  3. Lihua Tu
    View author publications

    You can also search for this author inPubMed Google Scholar

  4. Zhenfeng Xu
    View author publications

    You can also search for this author inPubMed Google Scholar

  5. Jian Zhang
    View author publications

    You can also search for this author inPubMed Google Scholar

  6. Shun Gao
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Shun Gao.

Additional information

Communicated by L. Bavaresco.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, L., Zhang, L., Tu, L. et al. Sex-related differences in physiological and ultrastructural responses of Populus cathayana to Ni toxicity. Acta Physiol Plant 36, 1937–1946 (2014). https://doi.org/10.1007/s11738-014-1570-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-014-1570-4

Keywords