Skip to main content
SpringerLink
Log in

Seed Priming of Handroanthus heptaphyllus for the Restoration of the Mining Fields

  • Published:
Water, Air, & Soil Pollution Aims and scope Submit manuscript

Abstract

Seed priming is a low-cost pre-sowing treatment used to improve germination and seedling establishment performance under adverse environmental conditions. The priming using signaling molecules, such as nitric oxide and hydrogen peroxide, act on plant growth and development alleviating the negative influence of abiotic stress by heavy metals. Thus, this work aimed to investigate the influence of priming with NO, H2O2, or their combination of Handroanthus heptaphyllus (Vell.) Mattos seeds on the germination and establishment of seedlings cultivated in iron mining tailings. The priming treatments were as follows: H2O, SNP (NO donor), H2O2 as well as SNP + H2O2. These primed seeds were cultivated in iron ore tailings or in a reference red oxisoil. The molecules used for the priming technique promoted distinct responses during seedlings’ establishment. Seedlings from NO-primed seeds exhibited higher Fe and Mn absorption in the tailing, with increased activities of the antioxidant system. The priming with H2O2 led to an avoidance strategy, with lower absorption of these elements by the seedlings. It can be concluded that NO and H2O2 induced different resistance mechanisms to Fe and Mn in H. heptaphyllus seedlings.

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
Fig. 6
Fig. 7

Similar content being viewed by others

Data Availability

The authors declare that all other data supporting the findings of this study are available within the article.

References

  • Anderson, M. D., Prasad, T. K., & Stewart, C. R. (1995). Changes in isozyme profiles of catalase, peroxidase, and glutathione reductase during acclimation to chilling in mesocotyls of maize seedlings. Plant Physiology, 109(4), 1247–1257.

    Article  CAS  Google Scholar 

  • Andresen, E., Peiter, E., & Küpper, H. (2018). Trace metal metabolism in plants. Journal Of Experimental Botany, [S.L.], 69(5), 909–954. 13 fev.

    Article  CAS  Google Scholar 

  • Aniceto, A. F. B., Ikeda-Castrillon, S. K., Fernandez, J. R. C., Martins, B. A. A., Duarte, Í. S., & Morais, F. F. (2021). Evaluation of no-tillage and litter transposition techniques for the emergence and establishment of Manduvi (Sterculiaapetala (jacq). Karts.) in ecological restoration work in an area of degraded springs in the PantanalMato-grossense. Research, Society And Development, [S.L.], 10(2), 1–16. 3 fev.

    Google Scholar 

  • Armada, C. A. S. (2020). The environmental disasters of Mariana and Brumadinho in the face of the Brazilian socio-environmental state. Territorium, 28, 13–22.

    Article  Google Scholar 

  • Bailly, C., El-Maarouf-Bouteau, H., & Corbineau, F. (2008). From intracellular signaling networks to cell death: The dual role of reactive oxygen species in seed physiology. ComptesRendusBiologies, [s.l.], 331(10), 806–814, out.

    CAS  Google Scholar 

  • Baker, N. R. (2008). Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annual review of plant biology, 59, 89.

  • Baker, N. R., & Rosenqvist, E. (2004). Applications of chlorophyll fluorescence can improve crop production strategies: An examination of future possibilities. Journal ofExperimental Botany, 55(403), 1607–1621.

    Article  CAS  Google Scholar 

  • Beckers, G. J. M., & Conrath, U. (2007). Priming for stress resistance: From the lab to the field. Current Opinion in Plant Biology, 10, 1–7. https://doi.org/10.1016/j.pbi.2007.06.002

    Article  Google Scholar 

  • Bilger, W., & Björkman, O. (1990). Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. Photosynthesis research, 25(3), 173–185.

  • Borges, A. A., Jiménez-Arias, D., Expósito-Rodríguez, M., Sandalio, L. M., & Pérez, J. A. (2014). Priming crops against biotic and abiotic stresses: MSB as a tool for studying mechanisms. Frontiers in Plant Science, 5, 642. https://doi.org/10.3389/fpls.2014.00642

    Article  Google Scholar 

  • Cargnelutti, D., Tabaldi, L. A., Spanevello, R. M., Jucoski, G. O., Battisti, V., Redin, M., Linares, C. E. B., Dressler, V. L., Flores, E. M. M., Nicoloso, F. T., Morsch, V. M., & Schetinger, M. R. C. (2006). Mercury toxicity induces oxidative stress in growing cucumber seedlings. Chemosphere, 65, 999–1006.

    Article  CAS  Google Scholar 

  • Carillo, P., & Gibbon, Y. (2011). Protocol: Extraction and determination of proline. Protocols in ecological &environmental plant physiology.

  • Cava, M. G. B., Isernhagen, I., Mendonça, A. H., & Durigan, G. (2016). Comparison of techniques for restoration of woody Cerrado vegetation in abandoned pastures. Hoehnea, 43(2), 301–315. https://doi.org/10.1590/2236-8906-18.2016

    Article  Google Scholar 

  • Ci, D., Jiang, D., Dai, T., Jing, Q., & Cao, W. (2010). Variation in cadmium tolerance and accumulation and their relationship in wheat recombinant inbred lines at seedling stage. Biological Trace Element Research, 142(3), 807–818.

    Article  Google Scholar 

  • Clark, L.J., Whalley, W. R., Barraclough, P.B. (2003). How do roots penetrate strong soil? In: Abe, J. (Ed.), Roots: The dynamic interface between plants and the earth. Developments in Plant and Soil Sciences. Springer, Dordrecht, pp. 93–104

  • Corpas, F. J., Gupta, D. K., & Palma, J. M. (2005). Production sites of reactive oxygen species (ROS) in organelles from plant cells. In D. K. Gupta, J. M. Palma, & F. J. Corpas (Eds.), Reactive oxygen species and oxidative damage in plants under stress (pp. 1–22). Springer.

    Google Scholar 

  • Corpas, F. J., Barroso, J. B., Palma, J. M., & Rodríguez-Ruiz, M. (2017). Plantperoxisomes: A nitro-oxidativecocktail. Redox Biology, 11, 535–542.

    Article  CAS  Google Scholar 

  • Cruz, F. V., Da S., Gomes, M. P., Bicalho, E. M., Della Torre, F., & Garcia, Q. S. (2020). Does Samarco’s spilled mud impair the growth of native trees of the Atlantic Rainforest? Ecotoxicology and Environmental Safety, 189

  • Ederli, L., Reale, L., Madeo, L., Ferranti, F., Gehring, C., Fornaciari, M., & Pasqualini, S. (2009). NO release by nitric oxide donors in vitro and in planta. Plant Physiology and Biochemistry, 47(1), 42–48. https://doi.org/10.1016/j.plaphy.2008.09.008

    Article  CAS  Google Scholar 

  • Egbichi, I., Keyster, M., & Ludidi, N. (2014). Effect of exogenous application of nitric oxide on salt stress responses of soybean. South African Journal of Botany, 90, 131–136. https://doi.org/10.1016/j.sajb.2013.11.002

    Article  CAS  Google Scholar 

  • Farooq, M., et al. (2005). Thermal hardening: A new seed vigor enhancement tool in rice. Journal of Integrative Plant Biology, 47(2), 187–193.

    Article  Google Scholar 

  • Fernandes, R., Barrón, V., Torrent, J., & Fontes, M. (2004). Quantificationof iron oxides in Brazilian Oxi soils by diffuse reflectance. Revista Brasileira De Ciência Do Solo, 28, 245–257.

    Article  CAS  Google Scholar 

  • Fontaine, O., Huault, C., Pavis, N., & Billard, J. P. (1994). Dormancy breakage of Hordeumvulgare seeds: Effect of hydrogen peroxide and stratification on glutathione level and glutathione reductase activity. Plant Physiology and Biochemistry, 32, 677–683.

    CAS  Google Scholar 

  • Gai, A. P. C., Dos Santos, D. S., & Vieira, E. A. (2017). Effects of zinc excess on antioxidant metabolism, mineral content and initial growth of Handroanthus impetiginosus (Mart. ex DC.) Mattos and Tabebuiaroseoalba (Ridl.) Sandwith. Environmental and Experimental Botany, 144, 88–99.

    Article  CAS  Google Scholar 

  • Gavassi, M. A., Gaion, L. A., Monteiro, C. C., Santos, J. C., & Carvalho, R. F. (2019). Seed priming with sodium nitroprusside attenuates the effects of water deficit on soybean seedlings. Comunicata Scientiae, 10(1), 176–184.

    Article  Google Scholar 

  • Giannopolitis, C. N., & Ries, S. K. (1977). Superoxide dismutases: I. Occurrence in higher plants. Plant physiology, 59(2), 309–314.

    Article  CAS  Google Scholar 

  • Gomes, M. P., & Garcia, Q. S. (2014). Reactive oxygen species and seed germination. Biologia (poland), 68(3), 351–357.

    Article  Google Scholar 

  • Graziano, M., & Lamattina, L. (2005). Nitric oxide and iron in plants: An emerging and converging story. Trends in Plant Science, 10(1), 4–8.

    Article  CAS  Google Scholar 

  • Gupta, D. K., Palma, J. M., Corpas, F. J. (Eds.). (2019). Nitric oxide and hydrogen peroxide signaling in higher plants. https://doi.org/10.1007/978-3-030-11129-8

  • Hemalatha, G., Renugadevi, J., & Eevera, T. (2017). Studies on seed priming with hydrogen peroxide for mitigating salt stress in rice. International Journal Of Current Microbiology And Applied Sciences, [S.L.], 6(6), 691–695.

    Article  CAS  Google Scholar 

  • Hossain, M. A., & Fujita, M. (2013). Hydrogen peroxide priming stimulates drought tolerance in mustard (Brassica juncea L.). Plant Gene Trait., 4, 109–123.

    Google Scholar 

  • Hossain, M. A., Bhattacharjee, S., Armin, S. M., Qian, P., Xin, W., Li, H. Y., ... & Tran, L. S. P. (2015). Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: insights from ROS detoxification and scavenging. Frontiers in plant science, 6, 420.

  • Jorge, R. A. B., Abreu, C. A., Andrade, C. A., & Camargo, O. A. (2010). Filter cake and peat as amendments of contaminated soil with residue of scrap rich in boron. Bragantia, 69, 467–476.

    Article  CAS  Google Scholar 

  • Korshunova, Y. O., Eide, D., Clark, W. G., Guerinot, M. L., & Pakrasi, H. B. (1999). The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Molecular Biology, 40, 37–44.

    Article  CAS  Google Scholar 

  • Kumari, A., Sheokand, S., & Swaraj, K. (2010). Nitric oxide induced alleviation of toxic effects of short term and long term Cd stress on growth, oxidative metabolism and Cd accumulation in Chickpea. Brazilian Journal Of Plant Physiology, 22(4), 271–284.

    Article  Google Scholar 

  • Küpper, H. (2017). Lead toxicity in plants. In: Sigel A, Sigel H, Sigel RKO, eds. Lead: Its effects on environment and health. Berlin: Walter de Gruyter, GmbH, 491–500

  • Lechowska, K., Kubala, S., Wojtyla, Ł., Nowaczyk, G., Quinet, M., Lutts, S., & Garnczarska, M. (2019). New insight on water status in germinating Brassica napus seeds in relation to priming-improved germination. International Journal of Molecular Sciences, 20(3), 540.

  • Leung, D. W. M. (2019). Participation of hydrogen peroxide and nitric oxide in improvement of seed germination performance under unfavourable conditions. Nitric Oxide and Hydrogen Peroxide Signaling in Higher Plants, 145–156. https://doi.org/10.1007/978-3-030-11129-8_7

  • Li, B., Sun, L., Huang, J., Göschl, C., Shi, W., Chory, J., et al. (2019). GSNOR provides plant tolerance to Fe toxicity via preventing iron-dependent nitrosative and oxidative cytotoxicity. Nature Communications, 10(1), 1–13.

    Google Scholar 

  • Lichtenthaler, H. K., & Buschmann, C. (2001). Chlorophylls and carotenoids: Measurement and characterization by UV-VIS spectroscopy. Current Protocols in Food Analytical Chemistry, 1(1), F4.3.1-F4.3.8. https://doi.org/10.1002/0471142913.faf0403s01

    Article  Google Scholar 

  • Lubben, S., & Sauerbeck, D. (1991). The uptake and distribution of heavy metals by spring wheat. Water, Air and Soil Pollution, 57–58, 239–247.

    Article  Google Scholar 

  • Maguire, J. D. (1962). Speed of germination aid in selection and evaluation for seedling emergence and vigor. Crop Science, Madison, 2(2), 176–177.

    Article  Google Scholar 

  • Marschner, H. (2012). Marschner’s mineral nutrition of higher plants (p. 2173). Academic Press.

    Google Scholar 

  • Mehraban, P., Zadeh, A. A., & Sadeghipour, H. R. (2008). Iron toxicity in rice (Oryza sativa L.), under different potassium nutrition. Asian Jounal of Plant Science, 7(3), 251–259.

  • Myers, N., Mittermeier, R. A., Mittermeier, C. G., Da Fonseca, G. A. B., & Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature, 403(6772), 853–858. https://doi.org/10.1038/35002501

    Article  CAS  Google Scholar 

  • Nakano, Y., & Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology, 22(5), 867–880.

    CAS  Google Scholar 

  • Nicolás, J., Chiari, M., Crespo, J., Orellana, I. G., Lucarelli, F., & Nava, S. (2008). Quantification of Saharan and local dust impact in an arid Mediterranean area by the positive matrix factorization (PMF) technique. Atmospheric Environment, 42(39), 8872–8882.

    Article  Google Scholar 

  • Pawar, V. A., & Laware, S. L. (2018). Seed priming a critical review. International Journal Of Scientific Research In Biological Sciences, 5(5), 94–101. 31 out.

    Article  Google Scholar 

  • Pedas, P., Ytting, C. K., Fuglsang, A. T., Jahn, T. P., Schjoerring, J. K., & Husted, S. (2008). Manganese efficiency in barley: identification and characterization of the metal ion transporter HvIRT1. Plant physiology, 148(1), 455–466.

  • Pedrini, S., Gibson‐Roy, P., Trivedi, C., Gálvez‐Ramírez, C., Hardwick, K., Shaw, N., & Dixon, K. (2020). Collection and production of native seeds for ecological restoration. Restoration Ecology, 28, S228–S238.

  • Peña-Olmos, J. E., & Casierra-Posada, F. (2013). Photochemical efficiency of photosystem II (PSII) in broccoli plants (Brassica oleracea varItalica) affected by excess iron. Orinoquia, 17(1), 15–22.

    Article  Google Scholar 

  • Pinto, S. D. S., Souza, A. E. D., Oliva, M. A., & Pereira, E. G. (2016). Oxidative damage and photosynthetic impairment in tropical rice cultivars upon exposure to excess iron. Scientia Agricola, 73(3), 217–226.

    Article  Google Scholar 

  • Rahman, M. M., Azirun, S. M., & Boyce, A. N. (2013). Enhanced accumulation of copper and lead in amaranth (Amaranthuspaniculatus), Indian mustard (Brassica juncea) and sunflower (Helianthus annuus). PLOS ONE, 8, e62941.

    Article  CAS  Google Scholar 

  • Ramirez, L., Zabaleta, E. J., Lamattina, L. (2010). Nitric oxide and frataxin: two players contributing to maintain cellular iron homeostasis. Ann Bot

  • Raupp, P. P., Ferreira, M. C., Alves, M., Campos-Filho, E. M., Sartorelli, P. A. R., Consolaro, H. N., & Vieira, D. L. M. (2020). Direct seeding reduces the costs of tree planting for forest and savana restoration. Ecological Engineering, 148, 105788.

    Article  Google Scholar 

  • Reitz, R., Klein, R. M., & Reis, A. (1983). Rio Grande do Sul wood project. Sellowia, Itajaí, 34(e35), 1–525.

    Google Scholar 

  • Rodrigues, R. R., Lima, R. A. F., Gandolfi, S., & Nave, A. G. (2009). On the restoration of high diversity forests: 30 years of experience in the Brazilian Atlantic Forest. Biological Conservation, 142, 1242–1251.

    Article  Google Scholar 

  • Rodrigues, A. B. M., Giuliatti, N. M., & Júnior, A. P. (2020). Application of methodologies for the recovery of degraded areas in Brazilian biomes. Brazilian Applied Science Review, 4(1), 333–369.

    Article  Google Scholar 

  • Sathiyaraj, G., Srinivasan, S., Kim, Y. J., Lee, O. R., Balusamy, S. D. R., & Khorolaragchaa, A. (2014). Acclimation of hydrogen peroxide enhances salt tolerance by activating defense-related proteins in Panax ginseng CA Meyer. Molecular Biology Reports, 41, 3761–3771. https://doi.org/10.1007/s11033-014-3241-3

    Article  CAS  Google Scholar 

  • Seneviratne, M., Rajakaruna, N., Rizwan, M., Madawala, H. M. S. P., Ok, Y. S., & Vithanage, M. (2017). Heavy metal-induced oxidative stress on seed germination and seedling development: A critical review. Environmental Geochemistry and Health. https://doi.org/10.1007/s10653-017-0005-8

    Article  Google Scholar 

  • Singh, O. P. (2005). Problems and remedies. In O. P. Singh (Ed.), Mining Environment (pp. 278–279). Regency Publications.

    Google Scholar 

  • Singh, N., & Bhatla, S. C. (2018). Nitric oxide regulates lateral root formation through modulation of ACC oxidase activity in sunflower seedlings under salt stress. Plant Signaling & Behavior, 25, 1–7.

    Google Scholar 

  • Sullivan, Y., & Ross, M. (1979). Selecting for drought and heat resistance in grain sorghum. In: Mussell H. & Staples R., C. (Eds.). Stress physiology in crop plants. Wiley, New York, pp 263–281.

  • Tanou, G., Filippou, P., Belghazi, M., Diamantidis, G., Fotopoulos, V., & Molassiotis, A. (2012). Oxidative and nitrosative-based signaling and associated post-translational modifications orchestrate the acclimation of citrus plants to salinity stress. The Plant Journal, 72, 585–599. https://doi.org/10.1111/j.1365-313X.2012.05100.x

    Article  CAS  Google Scholar 

  • Taylor, G. T., & Crowder, A. A. (1983). Uptake and accumulation of copper, nickel and iron by Thyphalatifolia grown in solution culture. Canadian Journal of Botany, 61, 1825–1830.

    Article  CAS  Google Scholar 

  • Teng, K., Li, J., Liu, L., Han, Y., Dum, Y., & Zhang, J. (2014). Exogenous ABA induces drought tolerance in upland rice: The role of chloroplast and ABA biosynthesis-related gene expression on photosystem II during PEG stress. Acta Physiologiae Plantarum, 36, 2219–2227. https://doi.org/10.1007/s11738-014-1599-4

    Article  CAS  Google Scholar 

  • Tewari, R. K., Hadacek, F., Sassmann, S., & Lang, I. (2013). Iron deprivationinduced reactive oxygen species generation leads to non-autolytic PCD in Brassica napus leaves. Environmental and Experimental Botany, 91, 74–83.

    Article  CAS  Google Scholar 

  • Velikova, V., Yordanov, I., & Edreva, A. (2000). Oxidative stress and some antioxidant systems in acid rain-treated bean plants: Protective role of exogenous polyamines. Plantscience, 151(1), 59–66.

    CAS  Google Scholar 

  • Veloso, L. L. De S. A., Capitulino, J. D., Soares De Lima, G., Vieira De Azevedo, C. A., Rodrigues Da Silva, A. A., &Gheyi, H. R. (2020). Methods of applying hydrogen peroxide to soursop seedlings irrigated with saline water. Comunicata Scientiae, 12

  • Verbruggen, N., & Hermans, C. (2008). Proline accumulation in plants: A review. Amino Acids, 35, 753–759.

    Article  CAS  Google Scholar 

  • Verma, S. R., Chaudhari, P. R., & Satyanaranyan, S. (2012). Impact ofleaching fromironore mines on terrestrial and aquatic environment. International Journal of Environmental Sciences, 2, 2378–2386.

    CAS  Google Scholar 

  • Xue, S. G., Wang, J., Wu, C., Li, S., Hartley, W., Wu, H., Zhu, F., & Cui, M. Q. (2018). Physiological response of Polygonumperfoliatum L. following exposure to elevated manganese concentrations. Environmental Science and Pollution Research, 25, 132–140.

    Article  CAS  Google Scholar 

  • Yemm E. W., & Cocking F., C. (1955). The determination of amino acids with ninhydrin. Analyst, 80, 208–213.

  • Zanandrea, I., Alves, J. D., Deuner, S., de FP Goulart, P., Henrique, P. D. C., & Silveira, N. M. (2010). Tolerance of Sesbania virgata plants to flooding. Australian Journal of Botany, 57(8), 661–669.

  • Zheng, Y., Shen, L., Yu, M., Fan, B., Zhao, D., Liu, L., & Sheng, J. (2011). Nitric oxide synthase as a postharvest response in pathogen resistance of tomato fruit. Post Harvest Biology and Technology, 60, 38–46.

    Article  CAS  Google Scholar 

Download references

Funding

This work received financial support and research grants from the Minas Gerais State Research Support Foundation (FAPEMIG) and Coordination of Superior Level Staff Improvement (CAPES). EMB and EGP received a research productivity grant from National Council for Scientific and Technological Development (CNPq).

Author information

Authors and Affiliations

  1. Universidade Federal de Lavras, Lavras, MG, Brazil

    Victor Navarro Silva, Mateus Moreira Bernardes, Aline Aparecida Silva Pereira, Rafael Agostinho Ferreira & Elisa Monteze Bicalho

  2. Universidade Federal de Viçosa - Campus Florestal, Florestal, MG, Brazil

    Eduardo Gusmão Pereira

Authors
  1. Victor Navarro Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mateus Moreira Bernardes
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aline Aparecida Silva Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Rafael Agostinho Ferreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Eduardo Gusmão Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Elisa Monteze Bicalho
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elisa Monteze Bicalho.

Ethics declarations

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Silva, V.N., Bernardes, M.M., Pereira, A.A.S. et al. Seed Priming of Handroanthus heptaphyllus for the Restoration of the Mining Fields. Water Air Soil Pollut 234, 31 (2023). https://doi.org/10.1007/s11270-022-06032-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11270-022-06032-7

Keywords

Search

Navigation