Skip to main content
SpringerLink
Log in

Sex-specific responses to Pb stress in Populus deltoides: root architecture and Pb translocation

  • Original Article
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Key message

Pb-induced negative effects on Populus deltoides root growth were sex-related and branch-order specific. Pb translocation from lower- to higher-order roots was correlated closely with the structural heterogeneity in fine-root architecture.

Abstract

Growing evidence has revealed sexual dimorphism in the aboveground processes of poplars under environmental stresses. However, the belowground performance of poplars has not been well studied to date. Moreover, both structure and function differ markedly among different fine-root orders. Nevertheless, little information is available concerning root branch-specific responses to environmental stresses. In this study, Populus deltoides was employed as a model species to detect sexual differences in root morphology, architecture and metal accumulation under Pb stress. Compared with plants in control conditions, Pb decreased total root length, total surface area, root diameter and biomass, but markedly increased the Pb concentration and accumulation in both sexes. In general, Pb-induced changes in the measured parameters were greater in females than these in males. In contrast to changes resulting from the Pb concentration, root Pb storage was lowest in middle-order roots. Compared to higher root orders, Pb often caused more significant effects on root length, surface area and Pb concentration in lower orders, except for root diameter. The results demonstrate that females are more sensitive to Pb stress than males. In conclusion, males of P. deltoides could concentrate Pb in the roots of lower orders, and suppress transportation of Pb to high order of root. Moreover, negative effects of Pb were generally branch-order specific and Pb translocation was correlated closely with structural heterogeneity in fine-root architecture.

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

Similar content being viewed by others

References

  • Ariani A, Francini A, Andreucci A, Sebastiani L (2016) Over-expression of AQUA1 in Populus alba Villafranca clone increases relative growth rate and water use efficiency, under Zn excess condition. Plant Cell Rep 35:289–301

    Article  CAS  PubMed  Google Scholar 

  • Baker A (1987) Metal tolerance. New Phytol 106:93–111

    Article  CAS  Google Scholar 

  • Baldantoni D, Cicatelli A, Bellino A, Castiglione S (2014) Different behaviours in phytoremediation capacity of two heavy metal tolerant poplar clones in relation to iron and other trace elements. J Environ Manag 146:94–99

    Article  CAS  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, Gao S, Zhu P, Liu Y, Hu T, Zhang J (2014) Comparative study of metal resistance and accumulation of lead and zinc in two poplars. Physiol Plant 151:390–405

    Article  CAS  PubMed  Google Scholar 

  • Davies M, Atkinson D (1991) Effect of toxic concentrations of metals on root growth and development. In: Atkinson D (ed) Plant root growth: an ecological perspective. Blackwell Sci Publ, Oxford, pp 211–227

    Google Scholar 

  • Duarte B, Caetano M, Almeida PR, Vale C, Caçador I (2010) Accumulation and biological cycling of heavy metal in four salt marsh species, from Tagus estuary (Portugal). Environ Pollut 158:1661–1668

    Article  CAS  PubMed  Google Scholar 

  • Eun S, Shik Youn H, Lee Y (2000) Lead disturbs microtubule organization in the root meristem of Zea mays. Physiol Plant 110:357–365

    Article  CAS  Google Scholar 

  • Fahr M, Laplaze L, Bendaou N, Hocher V, El Mzibri M, Bogusz D, Smouni A (2013) Effect of lead on root growth. Front Plant Sci 4:1–7

    Article  Google Scholar 

  • Fernàndez-Martínez J, Zacchini M, Fernández-Marín B, García-Plazaola JI, Fleck I (2014) Gas-exchange, photo-and antioxidant protection, and metal accumulation in I-214 and Eridano Populus sp. clones subjected to elevated zinc concentrations. Environ Exp Bot 107:144–153

    Article  CAS  Google Scholar 

  • Guo DL, Mitchell RJ, Hendricks JJ (2004) Fine root branch orders respond differentially to carbon source-sink manipulations in a longleaf pine forest. Oecologia 140:450–457

    Article  PubMed  Google Scholar 

  • Guo D, Li H, Mitchell RJ, Han W, Hendricks JJ, Fahey TJ, Hendrick RL (2008a) Fine root heterogeneity by branch order: exploring the discrepancy in root turnover estimates between minirhizotron and carbon isotopic methods. New Phytol 177:443–456

    Article  CAS  PubMed  Google Scholar 

  • Guo D, Xia M, Wei X, Chang W, Liu Y, Wang Z (2008b) Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species. New Phytol 180:673–683

    Article  PubMed  Google Scholar 

  • Guo YY, Wang JJ, Kong DL, Wang W, Guo DL, Wang YB, Xie QL, Liu YS, Zeng H (2013) Fine root branch orders contribute differentially to uptake, allocation, and return of potentially toxic metals. Environ Sci Technol 47:11465–11472

    Article  CAS  PubMed  Google Scholar 

  • Gupta D, Huang H, Yang X, Razafindrabe B, Inouhe M (2010) The detoxification of lead in Sedum alfredii H. is not related to phytochelatins but the glutathione. J Hazard Mater 177:437–444

    Article  CAS  PubMed  Google Scholar 

  • Han Z, Bi X, Li Z, Yang W, Wang L, Yang H, Li F, Ma Z (2012) Occurrence, speciation and bioaccessibility of lead in Chinese rural household dust and the associated health risk to children. Atmos Environ 46:65–70

    Article  CAS  Google Scholar 

  • He J, Li H, Luo J, Ma C, Li S, Qu L, Gai Y, Jiang X, Janz D, Polle A, Tyree M, Luo Z-B (2013a) A transcriptomic network underlies microstructural and physiological responses to cadmium in Populus × canescens. Plant Physiol 162:424–439

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  Google Scholar 

  • He J, Li H, Ma C, Zhang Y, Polle A, Rennenberg H, Cheng X, Luo Z-B (2015) Overexpression of bacterial γ-glutamylcysteine synthetase mediates changes in cadmium influx, allocation and detoxification in poplar. New Phytol 205:240–254

    Article  CAS  PubMed  Google Scholar 

  • Islam E, Yang X, Li T, Liu D, Jin X, Meng F (2007) Effect of Pb toxicity on root morphology, physiology and ultrastructure in the two ecotypes of Elsholtzia argyi. J Hazard Mater 147:806–816

    Article  CAS  PubMed  Google Scholar 

  • Jia S, Wang Z, Li X, Sun Y, Zhang X, Liang A (2010) N fertilization affects on soil respiration, microbial biomass and root respiration in Larix gmelinii and Fraxinus mandshurica plantations in China. Plant Soil 333:325–336

    Article  CAS  Google Scholar 

  • Joslin J, Gaudinski JB, Torn MS, Riley W, Hanson PJ (2006) Fine-root turnover patterns and their relationship to root diameter and soil depth in a 14C-labeled hardwood forest. New Phytol 172:523–535

    Article  CAS  PubMed  Google Scholar 

  • Kaur G, Singh HP, Batish DR, Kohli RK (2013) Lead (Pb)-induced biochemical and ultrastructural changes in wheat (Triticum aestivum) roots. Protoplasma 250:53–62

    Article  CAS  PubMed  Google Scholar 

  • King JS, Albaugh TJ, Allen HL, Buford M, Strain BR, Dougherty P (2002) Below-ground carbon input to soil is controlled by nutrient availability and fine root dynamics in loblolly pine. New Phytol 154:389–398

    Article  Google Scholar 

  • Kovačević B, Miladinović D, Orlović S, Katanić M, Kebert M, Kovinčić J (2013) Lead tolerance and accumulation in white poplar cultivated in vitro. South East Eur For 4:3–12

    Article  Google Scholar 

  • Leigh A, Nicotra AB (2003) Sexual dimorphism in reproductive allocation and water use efficiency in Maireana pyramidata (Chenopodiaceae), a dioecious, semi-arid shrub. Aust J Bot 51:509–514

    Article  Google Scholar 

  • Letts MG, Phelan CA, Johnson DR, Rood SB (2008) Seasonal photosynthetic gas exchange and leaf reflectance characteristics of male and female cottonwoods in a riparian woodland. Tree Physiol 28:1037–1048

    Article  CAS  PubMed  Google Scholar 

  • Li TQ, Yang XE, Jin XF, He ZL, Stoffella PJ, Hu QH (2005) Root responses and metal accumulation in two contrasting ecotypes of Sedum alfredii Hance under lead and zinc toxic stress. J Environ Sci Health 40:1081–1096

    Article  CAS  Google Scholar 

  • Mao Q, Huang G, Ma K, Sun Z (2014) Variations of soil lead in different land uses along the urbanization gradient in the Beijing metropolitan area. Int J Environ Res Public Health 11:3199–3214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marmiroli M, Pietrini F, Maestri E, Zacchini M, Marmiroli N, Massacci A (2011) Growth, physiological and molecular traits in Salicaceae trees investigated for phytoremediation of heavy metals and organics. Tree Physiol 31:1319–1334

    Article  CAS  PubMed  Google Scholar 

  • Matamala R, Gonzalez-Meler MA, Jastrow JD, Norby RJ, Schlesinger WH (2003) Impacts of fine root turnover on forest NPP and soil C sequestration potential. Science 302:1385–1387

    Article  CAS  PubMed  Google Scholar 

  • McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo D, Helmisaari H, Hobbie EA, Iversen CM, Jackson RB, Leppälammi-Kujansuu J, Norby RJ, Phillips RP, Pregitzer KS, Pritchard SG, Rewald B, Zadworny M (2015) Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes. New Phytol 207:505–518

    Article  PubMed  Google Scholar 

  • Mishra S, Srivastava S, Tripathi R, Kumar R, Seth C, Gupta D (2006) Lead detoxification by coontail (Ceratophyllum demersum L.) involves induction of phytochelatins and antioxidant system in response to its accumulation. Chemosphere 65:1027–1039

    Article  CAS  PubMed  Google Scholar 

  • Nishizono H, Ichikawa H, Suziki S, Ishii F (1987) The role of the root cell wall in the heavy metal tolerance of Athyrium yokoscense. Plant Soil 101:15–20

    Article  CAS  Google Scholar 

  • Piechalak A, Tomaszewska B, Baralkiewicz D, Malecka A (2002) Accumulation and detoxification of lead ions in legumes. Phytochemistry 60:153–162

    Article  CAS  PubMed  Google Scholar 

  • Pourrut B, Shahid M, Dumat C, Winterton P, Pinelli E (2011) Lead uptake, toxicity, and detoxification in plants. Rev Environ Contam Toxicol 213:113–136

    CAS  PubMed  Google Scholar 

  • Pregitzer KS, DeForest JL, Burton AJ, Allen MF, Ruess RW, Hendrick RL (2002) Fine root architecture of nine North American trees. Ecol Monogr 72:293–309

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Rewald B, Ephrath JE, Rachmilevitch S (2011) A root is a root is a root? Water uptake rates of Citrus root orders. Plant Cell Environ 34:33–42

    Article  PubMed  Google Scholar 

  • Robinson D, Hodge A, Fitter A (2003) Constraints on the form and function of root systems. In: Kroon HD (ed) Root eco1ogy. Springer, Heidelberg, pp 1–26

    Chapter  Google Scholar 

  • Romeo S, Trupiano D, Ariani A, Renzone G, Scippa GS, Scaloni A, Sebastiani L (2014) Proteomic analysis of Populus × euramericana (clone I-214) roots to identify key factors involved in zinc stress response. J Plant Physiol 171:1054–1063

    Article  CAS  PubMed  Google Scholar 

  • Samardakiewicz S, Woźny A (2005) Cell division in Lemna minor roots treated with lead. Aquat Bot 83:289–295

    Article  CAS  Google Scholar 

  • Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17:35–52

    Article  CAS  Google Scholar 

  • Shi W-G, Li H, Liu T-X, Polle A, Peng C-H, Luo Z-B (2014) Exogenous abscisic acid alleviates zinc uptake and accumulation in Populus × canescens exposed to excess zinc. Plant Cell Environ 38:207–223

    Article  CAS  PubMed  Google Scholar 

  • Stoláriková-Vaculíková M, Romeo S, Minnocci A, Luxová M, Vaculík M, Lux A, Sebastiani L (2015) Anatomical, biochemical and morphological responses of poplar Populus deltoides clone Lux to Zn excess. Environ Exp Bot 109:235–243

    Article  CAS  Google Scholar 

  • Strand AE, Pritchard SG, McCormack ML, Davis MA, Oren R (2008) Irreconcilable differences: fine-root life spans and soil carbon persistence. Science 319:456–458

    Article  CAS  PubMed  Google Scholar 

  • Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604

    Article  CAS  PubMed  Google Scholar 

  • Utmazian MNDS, 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  CAS  Google Scholar 

  • Wang Z, Guo D, Wang X, Gu J, Mei L (2006) Fine root architecture, morphology, and biomass of different branch orders of two Chinese temperate tree species. Plant Soil 288:155–171

    Article  CAS  Google Scholar 

  • Wang JJ, Guo YY, Guo DL, Yin SL, Kong DL, Liu YS, Zeng H (2012) Fine root mercury heterogeneity: metabolism of lower-order roots as an effective route for mercury removal. Environ Sci Technol 46:769–777

    Article  CAS  PubMed  Google Scholar 

  • Wells CE, Glenn DM, Eissenstat DM (2002) Changes in the risk of fine-root mortality with age: a case study in peach, Prunus persica (Rosaceae). Am J Bot 89:79–87

    Article  PubMed  Google Scholar 

  • Wierzbicka M (1998) Lead in the apoplast of Allium cepa L. root tips-ultrastructural studies. Plant Sci 133:105–119

    Article  CAS  Google Scholar 

  • Xu X, Zhao H, Zhang X, Hānninen H, Korpelainen H, Li C (2010) Different growth sensitivity to enhanced UV-B radiation between male and female Populus cathayana. Tree Physiol 30:1489–1498

    Article  CAS  PubMed  Google Scholar 

  • Xu Z, Yin H, Xiong P, Wan C, Liu Q (2012) Short-term responses of Picea asperata seedlings of different ages grown in two contrasting forest ecosystems to experimental warming. Environ Exp Bot 77:1–11

    Article  Google Scholar 

  • Zhivotovsky OP, Kuzovkina JA, Schulthess CP, Morris T, Pettinelli D, Ge M (2011) Hydroponic screening of willows (Salix L.) for lead tolerance and accumulation. Int J Phytoremediation 13:75–94

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Xiangwei Hu and Mingjin Zhang for help in setting up the experimental facilities, and Yong Peng for help in root measurements. This study was supported financially by the National Natural Science Foundation of China (31300513, 31570601) and Eco-environment Monitoring Station of Rainy-Zone of West China.

Author information

Authors and Affiliations

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

    Zhenfeng Xu, Lianghua Chen, Shishan Tang, Liyan Zhuang, Wanqin Yang, Lihua Tu, Bo Tan & Li Zhang

Authors
  1. Zhenfeng Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lianghua Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shishan Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Liyan Zhuang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wanqin Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lihua Tu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bo Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Li Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Zhenfeng Xu or Lianghua Chen.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by K. Noguchi.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, Z., Chen, L., Tang, S. et al. Sex-specific responses to Pb stress in Populus deltoides: root architecture and Pb translocation. Trees 30, 2019–2027 (2016). https://doi.org/10.1007/s00468-016-1429-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-016-1429-y

Keywords

Search

Navigation