Skip to main content

Advertisement

SpringerLink
Log in

Sex-specific competition differently regulates ecophysiological responses and phytoremediation of Populus cathayana under Pb stress

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aims

Lead (Pb) contamination seriously threatens agroforestry production and safety. We aim to determine the interactive influence of Pb and sexual competition on the growth performance, photosynthetic and biochemical traits, ultrastructure and phytoremediation-related parameters of males and females.

Methods

In the present study, eco-physiological responses and phytoremediation traits of Populus cathayana females and males were evaluated under interactive treatments of Pb and competition.

Results

There were significant sex-specific competition effects on biomass partition, photosynthetic activities, carbohydrate contents, nitrogen and phosphorus use efficiencies, ultrastructure and phytoremediation under Pb stress. When competition within the same sex was compared, females were more sensitive to Pb stress, while males possessed greater Pb contents, and a higher bioconcentration factor and tolerance index. Under inter-sexual competition, males alleviated competition effects through greater Pb absorption, and lower photosynthetic rates, nutrient use efficiencies and biomass accumulation. Moreover, Pb stress altered competition intensities of both sexes.

Conclusions

Sex-specific competition and neighbor effects may regulate responses and phytoremediation under heavy metal stress in dioecious plants. In the future, more attention should be paid on the effects of inter- and intra-sexual competition on dioecious species in the process of forestation and restoration of contaminated soil.

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

Access this article

Log in via an institution

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
Fig. 5

Similar content being viewed by others

References

  • Ahmad-Ramli MF, Cornulier T, Johnson D (2013) Partitioning of soil phosphorus regulates competition between Vaccinium vitis-idaea and Deschampsia cespitosa. Ecol Evol 3:4243–4252

    Article  PubMed  PubMed Central  Google Scholar 

  • Baker AJM, McGrath SP, Sideli CMD, Reeves RD (1994) The possibility of in-situ heavy metal decontamination of polluted soils using crops of metal-accumulating plants - a feasibility study. Resour Conserv Recycl 11:41–49

    Article  Google Scholar 

  • Bertness MD, Callaway R (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193

    Article  CAS  PubMed  Google Scholar 

  • Bloor JMG, Leadley PW, Barthes L (2008) Responses of Fraxinus excelsior seedlings to grass-induced above- and below-ground competition. Plant Ecol 194:293–304

    Article  Google Scholar 

  • Callaway RM, Walker L (1997) Competition and facilitation: a synthetic approach to interactions in a plant community. Ecology 78:1958–1965

    Article  Google Scholar 

  • Chen LH, Zhang S, Zhao HX, Korpelainen H, Li CY (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 LH, Han Y, Jiang H, Korpelainen H, Li CY (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 

  • 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 

  • Deyn GB, Van der Putten WH (2005) Linking aboveground and belowground diversity. Trends Ecol Evol 20:625–633

    Article  PubMed  Google Scholar 

  • Donaldson JR, Kruger EL, Lindroth RL (2006) Competition and resource-mediated tradeoffs between growth and defensive chemistry in trembling aspen (Populus tremuloides). New Phytol 169:561–570

    Article  CAS  PubMed  Google Scholar 

  • Duan BL, Dong TF, Zhang XL, Zhang YB, Chen J (2014) Ecophysiological responses of two dominant subalpine tree species Betula albosinensis and Abies faxoniana to intra- and interspecific competition under elevated temperature. For Ecol Manag 323:20–27

    Article  Google Scholar 

  • Dudley LS (2006) Ecological correlates of secondary dimorphism in Salix glauca (Salicaceae). Am J Bot 93:1775–1783

    Article  PubMed  Google Scholar 

  • Dybzinski R, Tilman D (2007) Resource use patterns predict long-term outcomes of plant competition for nutrients and light. Am Nat 170:305–318

    PubMed  Google Scholar 

  • Eppley SM (2006) Females make tough neighbours: sex-specific competitive effects in seedlings of a dioecious grass. Oecologia 46:549–554

    Article  Google Scholar 

  • Ermakov VV, Petrunina NS, Tyutikov SF, Danilova VN, Khushvakhtova SD, Degtyarev AP, Krechetova EV (2015) Concentrating metals by plants of the genus Salix and their importance for identification of Cd anomalies. Geochem Int 53:951–963

    Article  CAS  Google Scholar 

  • Fargione J, Brown CS, Tilman D (2003) Community assembly and invasion: an experimental test of neutral versus niche processes. Proc Natl Acad Sci U S A 100:8916–8920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grace JB (1995) On the measurement of plant competition intensity. Ecology 76(1):305–308

  • Guo QX, Li JY, Zhang YX, Zhang JX, Lu DL, Korpelainen H, Li CY (2016) Species-specific competition and N fertilization regulate non-structural carbohydrate contents in two Larix species. For Ecol Manag 364:60–69

  • Han Y, Wang L, Zhang XL, Korpelainen H, Li CY (2013) Sexual differences in photosynthetic activity, ultrastructure and phytoremediation potential of Populus cathayana exposed to lead and drought. Tree Physiol 33:1043–1060

    Article  CAS  PubMed  Google Scholar 

  • He J, Ma C, Ma Y, Li H, Kang J, Liu T, Polle A, Peng C, Luo ZB (2013) Cadmium tolerance in six poplar species. Environ Sci Pollut Res 20:163–174

    Article  CAS  Google Scholar 

  • Herrera CM (1988) Plant size, spacing patterns, and host-plant selection in Osyris quadripartita, a hemiparasitic dioecious shrub. J Ecol 76:995–1006

    Article  Google Scholar 

  • Hötscher M, Hay MJM (1997) Genotypic differences in physiological integration, morphological plasticity and utilization of phosphorus induced by variation in phosphate supply in Trifolium repens. J Ecol 85:341–350

    Article  Google Scholar 

  • Islam E, Liu D, Li T, Yang X, Jin X, Mahmood Q, Tian S, Li J (2008) Effect of Pb toxicity on leaf growth, physiology and ultrastructure in the two ecotypes of Elsholtzi aargyi. J Hazard Mater 154:914–926

    Article  CAS  PubMed  Google Scholar 

  • Jiang H, Korpelainen H, Li CY (2013) Populus yunnanensis males adopt more efficient protective strategies than females to cope with excess zinc and acid rain. Chemosphere 91:1213–1220

    Article  CAS  PubMed  Google Scholar 

  • Julkunen-Tiitto R (1985) Phenolic constituents in the leaves of northern willows-methods for the analysis of certain phenolics. J Agric Food Chem 33:213–217

    Article  CAS  Google Scholar 

  • Juvany M, Munné-Boch S (2015) Sex-related differences in stress tolerance in dioecious plants: a critical appraisal in a physiological context. J Exp Bot 66:6083–6092

    Article  CAS  PubMed  Google Scholar 

  • Kalaji HM, Loboda T (2007) Photosystem II of barley seedlings under cadmium and lead stress. Plant Soil and. Environment 53:511–516

    CAS  Google Scholar 

  • Kegge W, Pierik R (2010) Biogenic volatile organic compounds and plant competition. Trends Plant Sci 15:126–132

    Article  CAS  PubMed  Google Scholar 

  • Korpelainen H (1991) Sex ratio variation and spatial segregation of the sexes in populations of Rumex acetosa and R. acetosella (Polygonaceae). Plant Syst Evol 174:183–195

    Article  Google Scholar 

  • Li CY, Xu G, Zang RG, Korpelainen H, Berninger F (2007) Sex-related differences in leaf morphological and physiological responses of Hippophae rhamnoides along an altitudinal gradient. Tree Physiol 27:399–406

    Article  CAS  PubMed  Google Scholar 

  • Liancourt P, Callaway RM, Michalet R (2005) Stress tolerance and competitive response ability determine the outcome of biotic interactions. Ecology 86:1611–1618

    Article  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Liu X, Kozovits AR, Grams TEE, Blaschke H, Rennenberg H, Matyssek R (2004) Competition modifies effects of enhanced ozone/carbon dioxide concentrations on carbohydrate and biomass accumulation in juvenile Norway spruce and European beech. Tree Physiol 24:1045–1055

    Article  CAS  PubMed  Google Scholar 

  • Llugany M, Tolra R, Martin SR, Poschenrieder C, Barcelo J (2013) Cadmium-induced changes in glutathione and phenolics of Thlaspi and Noccaea species differing in Cd accumulation. J Plant Nutr Soil Sci 176:851–858

    Article  CAS  Google Scholar 

  • Long SP, Bernacchi CJ (2003) Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. J Exp Bot 54:2393–2401

    Article  CAS  PubMed  Google Scholar 

  • Maestre FT, Callaway RM, Valladares F, Lortie CJ (2009) Refining the stress-gradient hypothesis for competition and facilitation in plant communities. J Ecol 97:199–205

    Article  Google Scholar 

  • Mayor JR, Wright SJ, Turner BL (2014) Species-specific responses of foliar nutrients to long-term nitrogen and phosphorus additions in a lowland tropical forest. J Ecol 102:36–44

    Article  CAS  Google Scholar 

  • McKane RB, Johnson LC, Shaver GR, Nadelhoffer KJ, Rastetter EB, Fry B, Giblin AE, Kielland K, Kwiatkowski BL, Laundre JA, Murray G (2002) Resource-based niches provide a basis for plant species diversity and dominance in arctic tundra. Nature 415:68–71

    Article  CAS  PubMed  Google Scholar 

  • Millard P, Way DA (2011) Tree competition and defense against herbivores: currency matters when counting the cost. Tree Physiol 31:579–581

    Article  PubMed  Google Scholar 

  • Miller AE, Bowman WD, Suding KN (2007) Plant uptake of inorganic and organic nitrogen: neighbor identity matters. Ecology 88:1832–1840

    Article  PubMed  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 

  • Myers JA, Kitajima K (2007) Carbohydrate storage enhances seedling shade and stress tolerance in a neotropical forest. J Ecol 95:383–395

    Article  CAS  Google Scholar 

  • Nanami S, Kawaguchi H, Yamakura T (2005) Sex ratio and gender dependent neighboring effects in Podocarpus nagi, a dioecious tree. Plant Ecol 177:209–222

    Article  Google Scholar 

  • Nicotra AB (1999) Sexually dimorphic growth in the dioecious tropical shrub, Siparuna grandiflora. Funct Ecol 13:322–331

    Article  Google Scholar 

  • O’Brien MJ, Leuzinger S, Philipson CD, Tay J, Hector A (2014) Drought survival of tropical tree seedlings enhanced by non-structural carbohydrate levels. Nat Clim Chang 4:710–714

    Article  Google Scholar 

  • Olsson T, Leverenz JW (1994) Non-uniform stomatal closure and the apparent convexity of the photosynthetic photon flux density response curve. Plant Cell Environ 17:701–710

    Article  Google Scholar 

  • Onyekwelu SS, Harper JL (1979) Sex ratio and niche differentiation in spinach (Spinacia oleracea L). Nature 282:609–611

    Article  Google Scholar 

  • Paul-Victor C, Zust T, Rees M, Kliebenstein DJ, Turnbull LA (2010) A new method for measuring relative growth rate can uncover the costs of defensive compounds in Arabidopsis thaliana. New Phytol 187:1102–1111

    Article  PubMed  Google Scholar 

  • Prioul JL, Chartier P (1977) Partitioning of transfer and carboxylation components of intracellular resistance to photosynthetic CO2 fixation: a critical analysis of the methods used. Ann Bot 41:789–800

    Article  Google Scholar 

  • Qasim B, Motelica-Heino M, Bourgerie S, Gauthier A, Morabito D (2016) Rhizosphere effects of Populus euramericana Dorskamp on the mobility of Zn, Pb and Cd in contaminated technosols. J Soils Sediments 16:811–820

    Article  CAS  Google Scholar 

  • Renner SS, Ricklefs RE (1995) Dioecy and its correlates in the flowering plants. Am J Bot 82:596–606

    Article  Google Scholar 

  • Rogers SR, Eppley SM (2012) Testing the interaction between inter-sexual competition and phosphorus availability in a dioecious grass. Botany 90:704–710

    Article  CAS  Google Scholar 

  • Sánchez-Vilas J, Turner A, Pannell JR (2011) Sexual dimorphism in intra- and inter-specific competitive ability of the dioecious herb Mercurialis annua. Plant Biol 13:218–222

    Article  PubMed  Google Scholar 

  • Santiago LS, Wright SJ, Harms KE, Yavitt JB, Korine C, Garcia MN, Turner BL (2012) Tropical tree seedling growth responses to nitrogen, phosphorus and potassium addition. J Ecol 100:309–316

    Article  CAS  Google Scholar 

  • Secchi F, Zwieniecki MA (2011) Sensing embolism in xylem vessels: the role of sucrose as a trigger for refilling. Plant Cell Environ. 34:514–524

    Article  CAS  PubMed  Google Scholar 

  • Shahid M, Pinelli E, Pourrut B, Silvestre J, Dumat C (2011) Lead-induced genotoxicity to Vicia faba L. roots in relation with metal cell uptake and initial speciation. Ecotoxicol Environ Saf 74:78–84

    Article  CAS  PubMed  Google Scholar 

  • Stehlik I, Friedman J, Barrett SCH (2008) Environmental influence on primary sex ratio in a dioecious plant. Proc Natl Acad Sci U S A 105:10847–10852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princeton

    Google Scholar 

  • Tilman D (1982) Resource competition and community structure. Princeton University Press, Princeton

  • Trinder CJ, Brooker RW, Davidson H, Robinson D (2012) Dynamic trajectories of growth and nitrogen capture by competing plants. New Phytol 193:948–958

    Article  CAS  PubMed  Google Scholar 

  • Xu X, Yang F, Xiao XW, Zhang S, Korpelainen H, Li CY (2008) Sex-specific responses of Populus cathayana to drought and elevated temperatures. Plant Cell Environ 31:850–860

    Article  CAS  PubMed  Google Scholar 

  • Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508–514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zayed A, Gowthaman S, Terry N (1998) Phytoaccumulation of trace elements by wetland plants: I. Duckweed. J Environ Qual 27:715–721

    Article  CAS  Google Scholar 

  • Zhang CY, Zhao XH, Gao LS, Gadow K (2009) Gender, neighboring competition and habitat effects on the stem growth in dioecious Fraxinus mandshurica trees in a northern temperate forest. Ann For Sci 812:1–9

    Google Scholar 

  • Zhang S, Jiang H, Zhao HX, Korpelainen H, Li CY (2014) Sexually different physiological responses of Populus cathayana to nitrogen and phosphorus deficiencies. Tree Physiol 34:343–354

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the China Postdoctoral Science Foundation (2015M570797), the Talent Program of the Mianyang Normal University (QD2015A005) and the Talent Program of the Hangzhou Normal University (2016QDL020).

Author information

Authors and Affiliations

  1. Key Laboratory of Mountain Surface Processes and Ecological Regulation, Chinese Academy of Sciences, Institute of Mountain Hazards and Environment, Chengdu, 610041, China

    Juan Chen, Qingquan Han & Baoli Duan

  2. Sichuan Province Key Laboratory of Ecological Security and Protection, Mianyang Normal University, Mianyang, 621000, China

    Juan Chen

  3. College of Life and Environmental Sciences, Hangzhou Normal University, 310036, Hangzhou, China

    Chunyang Li

  4. Department of Agricultural Sciences, Viikki Plant Science Centre, University of Helsinki, P.O. Box 27, Helsinki, FI-00014, Finland

    Helena Korpelainen

Authors
  1. Juan Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qingquan Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Baoli Duan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Helena Korpelainen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chunyang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Juan Chen had the main responsibility for data collection, analysis and writing, Qingquan Han and Baoli Duan had a significant contribution to data collection and analysis, Helena Korpelainen had a significant contribution to the interpretation of data and manuscript preparation, and Chunyang Li (the corresponding author) had the overall responsibility for experimental design and project management.

Corresponding author

Correspondence to Chunyang Li.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Additional information

Responsible Editor: Henk Schat

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, J., Han, Q., Duan, B. et al. Sex-specific competition differently regulates ecophysiological responses and phytoremediation of Populus cathayana under Pb stress. Plant Soil 421, 203–218 (2017). https://doi.org/10.1007/s11104-017-3450-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-017-3450-3

Keywords

Search

Navigation