Skip to main content

Advertisement

Log in

Flooding alleviates copper stress on Salix: Evidence from stoichiometric patterns among plant tissues

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

Abstract

Background and aims

The increasing flooding occurrence associated with climate change, results in soil becoming more vulnerable to heavy metal contamination. However, the mechanisms underlying the combined effects of flooding and metals on the stoichiometry of fast-growing trees (potential for bioremediation) remains poorly understood. Such information is vital to understand how Salix integra Thunb ‘Yizhibi’ (S. integra) alters the nutrient stoichiometry to cope with a single or combined stress of copper (Cu) and flooding.

Methods

S. integra seedlings were cultivated in four soil Cu treatments (control, 50, 150 and 450 mg.kg−1) and examined after a 90-day flooding period. The stoichiometric patterns of C:N:P among different tissues were analyzed upon single or co-exposure to Cu and flooding. Redundancy analysis (RDA) and partial least squares-path modeling (PLS-PM) were used to elucidate the relationship between the C:N:P stoichiometry of soil and plants.

Results

Leaf C concentration negatively correlated with leaf P concentration upon exposure to Cu stress. Flooding significantly increased the leaf C:N and C:P ratios, and leaf N:P increased (3.7–46.3%) with increasing soil Cu dose. The stoichiometric patterns of C:N:P in aboveground tissues were generally affected by flooding, and the ratios of C:N or C:P were in the order of cutting > stem > leaf. The PLS-PM result implied that flooding or Cu had a significantly positive effect on the nutrient stoichiometry (C:N and C:P) of stems and leaves. Moreover, flooding exhibited a stronger effect on C, N and P stoichiometry, with standardized path coefficients of 0.83 and 0.34 in stems and leaves, respectively.

Conclusions

Flooding is a primary factor that alters the C:N:P stoichiometry in tissues of S. integra under Cu induced stress. Flooding is likely to alleviate Cu induced stress via alterations in C:N:P stoichiometry patterns in Salix tissues. Thus, plants can regulate nutrient stoichiometric patterns to cope with single or combined stress, which might be used as an indicator of stress tolerance or ecological adaptation.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adrees M, Ali S, Rizwan M, Ibrahim M, Abbas F, Farid M, Zia-ur-Rehman M, Irshad MK, Bharwana SA (2015) The effect of excess copper on growth and physiology of important food crops: a review. Environ Sci Pollut Res 22:8148–8162

    Article  CAS  Google Scholar 

  • Aerts R (1996) Nutrient resorption from senescing leaves of perennials: are there 447 general patterns? J Ecol 84:597–608

    Article  Google Scholar 

  • Bai YF, Wu JG, Clark CM, Pan QM, Zhang LX, Chen SQ, Wang QB, Han XG (2012) Grazing alters ecosystem functioning and C: N: P stoichiometry of grasslands along a regional precipitation gradient. J Appl Ecol 49:1204–1215

    Article  CAS  Google Scholar 

  • Berman-Frank I, Dubinsky Z (1999) Balanced growth in aquatic plants: myth or reality? Bioscience 49:29–37

    Article  Google Scholar 

  • Borjas-Ventura R, Alves LR, de Oliveira R, Martínez CA, Gratão PL (2019) Impacts of warming and water deficit on antioxidant responses in Panicum maximum Jacq. Physiol Plant 165:413–426

    CAS  PubMed  Google Scholar 

  • Bouazizi H, Jouili H, Geitmann A, El Ferjani E (2010) Copper toxicity in expanding leaves of Phaseolus vulgaris L.: antioxidant enzyme response and nutrient element uptake. Ecotoxicol Environ Saf 73:1304–1308

    Article  CAS  PubMed  Google Scholar 

  • Cao YN, Ma CX, Chen GC, Zhang JF, Xing BS (2017) Physiological and biochemical responses of Salix integra Thunb. under copper stress as affected by soil flooding. Environ Pollut 225:644–665

    Article  CAS  PubMed  Google Scholar 

  • Cao YN, Ma CX, Zhang JF, Wang SF, White JC, Chen GC, Xing BS (2019) Accumulation and spatial distribution of copper and nutrients in willow as affected by soil flooding: A synchrotron-based X-ray fluorescence study. Environ Pollut 246:980–989

    Article  CAS  PubMed  Google Scholar 

  • Chen YS, Stagg CL, Cai YJ, L u XT, Wang XL, Shen RC, Lan ZC, (2020) Scaling responses of leaf nutrient stoichiometry to the lakeshore flooding duration gradient across different organizational levels. Sci Total Environ 740:139740

    Article  CAS  PubMed  Google Scholar 

  • Chrysargyris A, Papakyriakou E, Petropoulos SA, Tzortzakis N (2019) The combined and single effect of salinity and copper stress on growth and quality of Mentha spicata plants. J Hazard Mater 368:584–593

    Article  CAS  PubMed  Google Scholar 

  • Demars BO, Edwards A (2007) Tissue nutrient concentrations in freshwater aquatic macrophytes: high inter-taxon differences and low phenotypic response to nutrient supply. Freshw Biol 52:2073–2086

    Article  CAS  Google Scholar 

  • Elser JJ, Fagan WF, Denno RF, Dobberfuhl DR, Folarin A, Huberty A, Interlandi S, Kilham SS, McCauley E, Schulz KL, Siemann EH, Sterner RW (2000) Nutritional constraints in terrestrial and freshwater food webs. Nature 408:578–580

    Article  CAS  PubMed  Google Scholar 

  • Fan H, Wu J, Liu W, Yuan Y, Hu L, Cai Q (2015) Linkages of plant and soil C: N: P stoichiometry and their relationships to forest growth in subtropical plantations. Plant Soil 392:127–138

    Article  CAS  Google Scholar 

  • Fisher KA, Meisinger JJ, James BR (2016) Urea hydrolysis rate in soil toposequences as influenced by pH, carbon, nitrogen, and soluble metals. J Environ Qual 45:349–359

    Article  CAS  PubMed  Google Scholar 

  • Godwin CM, Whitaker EA, Cotner JB (2017) Growth rate and resource imbalance interactively control biomass stoichiometry and elemental quotas of aquatic bacteria. Ecology 98:820

    Article  PubMed  Google Scholar 

  • Güleryüz G, Erdemir US, Arslan H, Akpinar A, Çiçek A, Güçer S (2015) Variation in trace element mobility and nitrogen metabolism of Verbascum olympicum Boiss. under copper stress. Chem Ecol 31:494–509

    Article  Google Scholar 

  • Hao Z, Kuang Y, Kang M (2015) Untangling the influence of phylogeny, soil and climate on leaf element concentrations in a biodiversity hotspot. Funct Ecol 29:165–176

    Article  Google Scholar 

  • Hu MJ, Peñuelas J, Sardans J, Sun ZG, Wilson BJ, Huang JF, Zhu QL, Tong C (2018) Stoichiometry patterns of plant organ N and P in coastal herbaceous wetlands along the East China Sea: implications for biogeochemical niche. Plant Soil 431:273–288

    Article  CAS  Google Scholar 

  • Huang D, Wang DM, Ren Y (2019) Using leaf nutrient stoichiometry as an indicator of flood tolerance and eutrophication in the riparian zone of the Lijang River. Ecol Indic 98:821–829

    Article  CAS  Google Scholar 

  • Izydorczyk G, Mikul K, Skrzypczak D, Moustakas K, Witek-Krowiak A, Chojnacka K (2021) Potential environmental pollution from copper metallurgy and methods of management. Environ Res 197:111050

    Article  CAS  PubMed  Google Scholar 

  • Kirwan ML, Guntenspergen GR (2012) Feedbacks between inundation, root production, and shoot growth in a rapidly submerging brackish marsh. J Ecol 100:764–770

    Article  Google Scholar 

  • Knecht MF, Goransson A (2004) Terrestrial plants require nutrients in similar proportions. Tree Physiol 24:447–460

    Article  CAS  PubMed  Google Scholar 

  • Kováčik J, Klejdus B, Hedbavny J, Štork F, Grúz J (2012) Modulation of copper uptake and toxicity by abiotic stresses in Matricaria chamomilla plants. J Agric Food Chem 60:6755–6763

    Article  PubMed  Google Scholar 

  • Lavres J, Rabêlo FHS, Capaldi FR, dos Reisc AR, Rosssi ML, Franco MR, Azevedo RA, Abreu-Junior CH, Nogueira NDL (2019) Investigation into the relationship among Cd bioaccumulation, nutrient composition, ultrastructural changes and antioxidative metabolism in lettuce genotypes under Cd stress. Ecotoxicol Environ Saf 170:578–589

    Article  CAS  PubMed  Google Scholar 

  • Lei Y, Zhou J, Xiao H, Duan B, Wu Y, Korpelainen H, Li C (2015) Soil nematode assemblages as bioindicators of primary succession along a 120-year-old chronosequence on the Hailuogou Glacier forefield, SW China. Soil Biol Biochem 88:362–371

    Article  CAS  Google Scholar 

  • Li MJ, Xiong ZT, Dai LP, Huang Y (2007) Effects of copper on nitrogen assimilation in copper-tolerant and non-tolerant populations of Elsholtzia haichowensis S. Water Air Soil Pollut 184:323–333

    Article  CAS  Google Scholar 

  • Li W, Cao T, Ni LY, Zhang XL, Zhu GR, Xie P (2013) Effects of water depth on carbon, nitrogen and phosphorus stoichiometry of five submersed macrophytes in an in situ experiment. Ecol Eng 61:358–365

    Article  Google Scholar 

  • Lin YM, Chen AM, Yan SW, Rafay L, Du K, Wang DJ, Ge YG, Li J (2019) Availvable soil nutrients and water content affect leaf nutrient concentrations and stoichiometry at different ages of Leucaenaleucocephala forests in dry-hot valley. J Soil Sediment 19:511–521

    Article  CAS  Google Scholar 

  • Liu FD, Zheng Y, Liu YH, Dong YF, Li DS, Wang MH (2019a) Stoichiometric nutrient balance of Suaeda salsa wetlands in different supratidal habitats of Tianjin, China. Hydrobiologia 827:3–19

    Article  CAS  Google Scholar 

  • Liu JZ, Sun PF, Sun R, Wang SC, Gao B, Tang J, Wu YH, Dolfing J (2019b) Carbon-nutrient stoichiometry drives phosphorus immobilization in phototrophic biofilms at the soil-water interface in paddy fields. Water Res 167:115129

    Article  CAS  PubMed  Google Scholar 

  • Llorens N, Arola L, Bladé C, Mas A (2000) Effects of copper exposure upon nitrogen metabolism in tissue cultured Vitis vinifera. Plant Sci 160:159–163

    Article  CAS  PubMed  Google Scholar 

  • Lu RK (2000) Methods of Soil and Agrochemical Analysis. China Agricultural Science and Technology Press, Beijing, pp 127–332

    Google Scholar 

  • Luo YQ, Sherry R, Zhou XH, Wan SQ (2009) Terrestrial carbon-cycle feedback to climate warming: experimental evidence on plant regulation and impacts of biofuel feedstock harvest. GCB Bioenergy 1:62–74

    Article  CAS  Google Scholar 

  • Luo FL, Nagel KA, Scharr H, Zeng B, Schurr U, Matsubara S (2010) Recovery dynamics of growth, photosynthesis and carbohydrate accumulation after de-submergence: a comparison between two wetland plants showing escape and quiescence strategies. Ann Bot 107:49–63

    Article  PubMed  PubMed Central  Google Scholar 

  • Mao R, Chen HM, Zhang XH, Shi FX, Song CC (2016) Effects of P addition on plant C: N: P stoichiometry in an N-limited temperate wetland of Northeast China. Sci Total Environ 559:1–6

    Article  CAS  PubMed  Google Scholar 

  • Martins LL, Mourato MP (2006) Effects of copper on tomato plants: growth parameters, enzyme activities, chlorophyll and mineral content. J Plant Nutr 29:2179–2198

    Article  CAS  Google Scholar 

  • Matías L, Castro J, Zamora R (2011) Soil-nutrient availability under a global-change scenario in a Mediterranean mountain ecosystem. Glob Chang Biol 17:1646–1657

    Article  Google Scholar 

  • McGroddy ME, Daufresne T, Hedin LO (2004) Scaling of C: N: P stoichiometry in forests worldwide: implications of terrestrial red field-type ratios. Ecology 85:2390–2401

    Article  Google Scholar 

  • Minden V, Kleyer M (2014) Internal and external regulation of plant organ stoichiometry. Plant Biol 16:897–907

    Article  CAS  PubMed  Google Scholar 

  • Ministry of Environmental Protection, China (1995) Environmental quality standard for soils, GB 15618–1995. China Environmental Science Press, Beijing

    Google Scholar 

  • Niu D, Zhang C, Ma P, Fu H, Elser JJ (2019) Responses of leaf C: N: P stoichiometry to water supply in the desert shrub Zygophyllum xanthoxylum. Plant Biol 21:82–88

    Article  CAS  PubMed  Google Scholar 

  • Panda D, Sharma SG, Sarkar RK (2008) Chlorophyll fluorescence parameters, CO2 photosynthetic rate and regeneration capacity as a result of complete submergence and subsequent re-emergence in rice (Oryza sativa L.). Aquat Bot 88:127–133

    Article  CAS  Google Scholar 

  • Peñuelas J, Sardans J, Llusia J, Owen SM, Carnicer J, Giambelluca TW, Rezende EL, Waite M, Niinemets Ü (2010) Faster returns on leaf economics and different biogeochemical niche in invasive compared with native plant species. Glob Chang Biol 16:2171–2185

    Article  Google Scholar 

  • Qiu XC, Wang HB, Peng DL, Liu X, Yang F, Li Z, Cheng S (2020) Thinning drives C: N: P stoichiometry and nutrient resorption in Larix principis-rupprechtii plantations in North China. Forest Ecol Manag 462:117984

    Article  Google Scholar 

  • Ryan BM, Kirby JK, Degryse F, Harris H, McLaughlin MJ, Scheiderich K (2013) Copper speciation and isotopic fractionation in plants: uptake and translocation mechanisms. New Phytol 199:367–378

    Article  CAS  PubMed  Google Scholar 

  • Sánchez-Rodríguez AR, Hill PW, Chadwick DR, Jones DL (2019) Typology of extreme flood event leads to differential impacts on soil functioning. Soil Biol Biochem 129:153–168

    Article  Google Scholar 

  • Sardans J, Peñuelas J, Estiarte M (2008) Changes in soil enzymes related to C and N cycle and in soil C and N content under prolonged warming and drought in a Mediterranean shrubland. Appl Soil Ecol 39:223–235

    Article  Google Scholar 

  • Shen RC, Lan ZC, Huang XY, Chen YS, Hu QW, Fang CM, Jin BS, Chen JK (2020) Soil and plant characteristics during two hydrologically contrasting years at the lakeshore wetland of Poyang Lake, China. J Soil Sediment 20:3368–3379

    Article  CAS  Google Scholar 

  • Tessier JT, Raynal DJ (2003) Use of nitrogen to phosphorus ratios in plant tissue as an indicator of nutrient limitation and nitrogen saturation. J Appl Ecol 40:523–534

    Article  CAS  Google Scholar 

  • Tripathi AM, Klem K, Fischer M, Orság M, Trnka M (2018) Water availability influences accumulation and allocation of nutrients and metals in short-rotation poplar plantation. Biomass Bioenerg 116:151–160

    Article  CAS  Google Scholar 

  • Viciedo DO, Prado RDM, Martínez CA, Habermann E, Piccolo MDC (2019) Short-term warming and water stress affect Panicum maximum Jacq. stoichiometric homeostasis and biomass production. Sci Total Environ 681:267–274

    Article  Google Scholar 

  • Wang A, Wang X, Tognetti R, Lei JP, Pan HL, Liu XL, Jiang Y, Wang XY, He P, Yu FH, Li MH (2018a) Elevation alters carbon and nutrient concentrations and stoichiometry in Quercus aquifolioides in southwestern China. Sci Total Environ 622–623:1463–1475

    PubMed  Google Scholar 

  • Wang WQ, Sardans J, Wang C, Zeng CS, Tong C, Bartrons M, Asensio D, Peñuelas J (2018b) Shifts in plant and soil C, N and P accumulation and C: N: P stoichiometry associated with flooding intensity in subtropical estuarine wetlands in China. Estuar Coast Shelf S 215:172–184

    Article  CAS  Google Scholar 

  • Wang J, Liu X, Zhang X, Li L, Lam SK, Pan G (2019) Changes in plant C, N and P ratios under elevated [CO2] and canopy warming in a rice-winter wheat rotation system. Sci Rep 9:5424

    Article  PubMed  PubMed Central  Google Scholar 

  • Warton DI, Duursma RA, Falster DS, Taskinen S (2012) SMATR 3–an R package for estimation and inference about allometric lines. Methods Ecol Evol 3:257–259

    Article  Google Scholar 

  • Xiong ZT, Liu C, Geng B (2006) Phytotoxic effects of copper on nitrogen metabolism and plant growth in Brassica pekinensis Rupr. Ecotoxicol Environ Saf 64:273–280

    Article  CAS  PubMed  Google Scholar 

  • Yan T, Lü XT, Zhu JJ, Yang K, Yu LZ, Gao T (2017) Changes in nitrogen and phosphorus cycling suggest a transition to phosphorus limitation with the stand development of larch plantations. Plant Soil 422:385–396

    Article  Google Scholar 

  • Yang C, Qiu WW, Chen ZX, Chen WY, Li YF, Zhu JL, Rahman SU, Han ZX, Jiang Y, Yang GJ, Tian J, Ma Q, Zhang Y (2020) Phosphorus influence Cd phytoextraction in Populus stems via modulating xylem development, cell wall Cd storage and antioxidant defense. Chemosphere 242:125154

    Article  CAS  PubMed  Google Scholar 

  • Yu Q, Chen Q, Elser JJ, He N, Wu H, Zhang G, Wu J, Bai Y, Han X (2010) Linking stoichiometric homoeostasis with ecosystem structure, functioning and stability. Ecol Lett 13:1390–1399

    Article  PubMed  Google Scholar 

  • Yu Q, Elser JJ, He N, Wu HH, Chen QS, Zhang GM, Han XG (2011) Stoichiometric homeostasis of vascular plants in the Inner Mongolia grassland. Oecologia 166:1–10

    Article  PubMed  Google Scholar 

  • Yu Q, Wilcox K, La PK, Knapp AK, Han X, Smith MD (2015) Stoichiometric homeostasis predicts plant species dominance, temporal stability, and responses to global change. Ecology 96:2328–2335

    Article  PubMed  Google Scholar 

  • Yuan ZY, Chen HYH (2015) Decoupling of nitrogen and phosphorus in terrestrial plants associated with global changes. Nat Clim Chang 5:465–469

    Article  CAS  Google Scholar 

  • Yuan ZY, Chen HYH, Reich PB (2011) Global-scale latitudinal patterns of plant fine-root nitrogen and phosphorus. Nat Commun 2:344

    Article  CAS  PubMed  Google Scholar 

  • Zhang ZS, Song XL, Lu XG, Xue ZS (2013) Ecological stoichiometry of carbon, nitrogen, and phosphorus in estuarine wetland soils: influences of vegetation coverage, plant communities, geomorphology, and seawalls. J Soil Sediment 13:1043–1051

    Article  CAS  Google Scholar 

  • Zhang JH, Zhao N, Liu CC, Yang H, Li ML, Yu GR, Wilcox K, Yu Q, He NP (2018) C: N: P stoichiometry in China’s forests: From organs to ecosystems. Funct Ecol 32:50–60

    Article  Google Scholar 

  • Zhang W, Liu W, Xu M, Deng J, Han X, Yang G, Feng Y, Ren G (2019) Response of forest growth to C:N: P stoichiometry in plants and soils during Robinia pseudoacacia afforestation on the Loess Plateau, China. Geoderma 337:280–289

    Article  CAS  Google Scholar 

  • Zhang JH, He NP, Liu CC, Xu L, Chen Z, Li Y, Wang RM, Yu GR, Sun W, Xiao CW, Chen HYH, Reich PB (2020) Variation and evolution of C: N ratio among different organs enable plants to adapt to N-limited environments. Glob Change Biol 26:2534–2543

    Article  Google Scholar 

  • Zhao N, Yu GR, Wang QF, Wang RL, Zhang JH, Liu CC, He NP (2019) Conservative allocation strategy of multiple nutrients among major plant organs: From species to community. J Ecol 108:267–278

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the Fundament Research Funds of CAF (Grant No. CAFYBB2019SZ001), the National Natural Science Foundation of China (31470619 & 31770653), and the Program for Guangdong Introducing Innovative and Entrepreneurial Teams (2019ZT08L213). The authors would like to express the sincere gratitude to editor & Dr. Gustavo Gabriel Striker and three anonymous reviewers for their valuable comments, which have greatly improved this paper.

Author information

Authors and Affiliations

Authors

Contributions

Yini Cao: Conceptualization, Investigation, Data analysis, Writing the paper. Chuanxin Ma: Formal analysis, Writing-review and editing. Ran Tong: Methodology, Formal analysis, Manuscript revision. Jie Chen, Xiaogang Li: Sample preparation, Data curation. Guangcai Chen: Conceptualization, Methodology, Manuscript revision, Funding acquisition and Project administration.

Corresponding author

Correspondence to Guangcai Chen.

Ethics declarations

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Additional information

Responsible Editor: Gustavo Gabriel Striker.

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 125 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cao, Y., Ma, C., Tong, R. et al. Flooding alleviates copper stress on Salix: Evidence from stoichiometric patterns among plant tissues. Plant Soil 478, 545–558 (2022). https://doi.org/10.1007/s11104-022-05489-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-022-05489-z

Keywords

Navigation