Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Seed Priming of Trifolium repens L. Improved Germination and Early Seedling Growth on Heavy Metal-Contaminated Soil

Abstract

Seed priming effects on Trifolium repens were analysed both in Petri dishes and in two soils (one unpolluted soil and a soil polluted with Cd and Zn). Priming treatments were performed with gibberellic acid 0.1 mM at 22 °C during 12 h or with polyethylene glycol (−6.7 MPa) at 10 °C during 72 h. Both priming treatments increased the germination speed and the final germination percentages in the presence of 100 μM CdCl2 or 1 mM ZnSO4. Flow cytometry analysis demonstrated that the positive effect of priming was not related with any advancement of the cell cycle in embryos. Seed imbibition occurred faster for primed seeds than for control seeds. X-ray and electronic microscopy analysis suggested that circular depressions on the seed coat, in addition to tissue detachments inside the seed, could be linked to the higher rate of imbibition. Priming treatments had no significant impact on the behaviour of seedlings cultivated on non-polluted soil while they improved seedling emergence and growth on polluted soil. The two priming treatments reduced Zn accumulation. Priming with gibberellic acid increased Cd accumulation by young seedlings while priming with polyethylene glycol reduced it. Priming improved the light phase of photosynthesis and strengthened the antioxidant system of stressed seedlings. Optimal priming treatment may thus be recommended as efficient tools to facilitate revegetation of former mining area.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Abbreviations

PEG:

Polyethylene glycol

d:

Day

h:

Hour

GA3 :

Gibberellic acid

References

  1. Ajouri, A., Asgedom, H., & Becker, M. (2004). Seed priming enhances germination and seedling growth of barley under conditions of P and Zn deficiency. Journal of Plant Nutrition and Soil Science, 167, 630–636.

  2. Ashraf, M., & Bray, C. M. (1993). DNA synthesis in osmoprimed leek (Allium porrum L.) seeds and evidence for repair and replication. Seed Science Research, 3, 15–23.

  3. Bernal, M. P., Clemente, R., & Walker, D. J. (2007). The role of organic amendments in the bioremediation of heavy metal-polluted soils. In R. B. Gore (Ed.), Environmental research at the leading edge (pp. 1–57). New York: Nova Publishers.

  4. Bidar, G., Garcon, G., Pruvot, C., Dewaele, D., Cazier, F., Douay, F., & Shirali, P. (2007). Behavior of Trifolium repens and Lolium perenne growing in a heavy metal contaminated field: Plant metal concentration and phytotoxicity. Environmental Pollution, 147, 546–553.

  5. Bino, R. J., Devries, J. N., Kraak, H. L., & Van Pijlen, J. G. (1992). Flow cytometric determination of nuclear replication stages in tomato seeds during priming and germination. Annals of Botany, 69, 231–236.

  6. Bradford, K. J. (1986). Manipulation of seed water relations via osmotic priming to improve germination under stress conditions. Hortscience, 21, 1105–1112.

  7. Bush, D. S. (1996). Effects of gibberellic acid and environmental factors on cytosolic calcium in wheat aleurone cells. Planta, 199, 89–99.

  8. Cayuela, E., Pérez-Alfocea, F., Caro, M., & Bolarin, M. C. (1996). Priming of seeds with NaCl induces physiological changes in tomato plants grown under salt stress. Physiologia Plantarum, 96, 231–236.

  9. Chen, K., & Arora, R. (2011). Dynamics of the antioxidant system during seed osmopriming, post-priming germination, and seedling establishment in Spinach (Spinacea oleracea). Plant Science, 180, 212–220.

  10. Chen, K., Fessehaie, A., & Arora, R. (2013). Aquaporin expression during seed osmopriming and post-priming germination in spinach. Biologia Plantarum, 57, 193–198.

  11. Claassen, V. P., & Hogan, M. P. (2002). Soil nitrogen pools associated with revegetation of disturbed sites in the Lake Tahoe area. Restoration Ecology, 10, 195–203.

  12. Clemente, A. S., Werner, C., Maguas, C., Cabral, M. S., Martins-Loucao, M. A., & Correia, O. (2004). Restoration of a limestone quarry: Effect of soil amendments on the establishment of native Mediterranean sclerophyllous shrubs. Restoration Ecology, 12, 20–28.

  13. Communities C o t E (1986). Council directive of 12 June 1986 on the protection of the environment, and in particular of the soil, when sewage sludge is used in agriculture. Official Journal of European Communities no. L181, 6–12.

  14. Danneberger, T. K., McDonald, M. B., Geron, C. A., & Kumari, P. (1992). Rate of germination and seedling growth of perennial ryegrass seed following osmoconditioning. HortScience, 27, 28–30.

  15. Davison, P. A., & Bray, C. M. (1991). Protein synthesis during osmopriming of leek (Allium porrum L.) seeds. Seed Science Research, 1, 29–35.

  16. de Castro, R. D., van Lammeren, A. A. M., Groot, S. P. C., Bino, R. J., & Hilhorst, H. W. M. (2000). Cell division and subsequent radicle protrusion in tomato seeds are inhibited by osmotic stress but DNA synthesis and formation of microtubular cytoskeleton are not. Plant Physiology, 122, 327–335.

  17. de Lespinay A. (2009). Study of seed priming mechanisms of three plant species used in revegetation of industrial sites. Ph.D. thesis, Université catholique de Louvain, Louvain-la-Neuve, Belgium, 257 p.

  18. de Lespinay, A., Lequeux, H., Lambillotte, B., & Lutts, S. (2010). Protein synthesis is differentially required for germination in Poa pratensis and Trifolium repens in the absence or in the presence of cadmium. Plant Growth Regulation, 61, 205–214.

  19. Farooq, M., Basra, S. M. A., Khalid, M., Tabassum, R., & Mahmood, T. (2006). Nutrient homeostasis, metabolism of reserves, and seedling vigor as affected by seed priming in coarse rice. Canadian Journal of Botany, 84, 1196–1202.

  20. Frett, J. J., & Pill, W. G. (1995). Improved seed performance of four fescue species with priming. Journal of Turfgrass Management, 1, 13–31.

  21. Gallardo, K., Job, C., Groot, S. P. C., Puype, M., Demol, H., Vandekerckhove, J., & Job, D. (2001). Proteomic analysis of Arabidopsis seed germination and priming. Plant Physiology, 126, 835–848.

  22. Garnczarska, M., Zalewski, T., & Kempka, M. (2007). Water uptake and distribution in germinating lupine seeds studied by magnetic resonance imaging and NMR spectroscopy. Physiologia Plantarum, 130, 23–32.

  23. Gendreau, E., Romaniello, S., Barad, S., Leymarie, J., Benech-Arnold, R., & Corbineau, F. (2008). Regulation of cell cycle activity in the embryo of barley seeds during germination as related to grain hydration. Journal of Experimental Botany, 59, 203–212.

  24. Gurusinghe, S. H., Cheng, Z. Y., & Bradford, K. J. (1999). Cell cycle activity during seed priming is not essential for germination advancement in tomato. Journal of Experimental Botany, 50, 101–106.

  25. Haigh, A. M., Barlow, E. W. R., Milthorpe, F. L., & Sinclair, P. J. (1986). Field emergence of tomato, carrot, and onion seeds primed in an aerated salt solution. Journal of the American Society for Horticultural Science, 111, 660–665.

  26. Harris, D., Joshi, A., Khan, P. A., Gothkar, P., & Sodhi, P. S. (1999). On-farm seed priming in semi-arid agriculture: Development and evaluation in maize, rice and chickpea in India using participatory methods. Experimental Agriculture, 35, 15–29.

  27. Heath, R. L., & Packer, L. (1968). Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics, 125, 185–188.

  28. ISTA (2008). International rules for seed testing. Bassersdorf: ISTA.

  29. Jeliazkova, E., Craker, L. E., & Xing, B. S. (2003). Seed germination of anise, caraway, and fennel in heavy metal contaminated solutions. Journal of Herbs, Spices & Medicinal Plants, 10, 83–93.

  30. Jisha, K. C., Vijayakumari, K., & Puthur, J. T. (2013). Seed priming for abiotic stress tolerance: An overview. Acta Physiologiae Plantarum, 35, 1381–1396.

  31. Kibinza, S., Bazin, J., Bailly, C., Farrant, J. M., Corbineau, F., & El-Maarouf-Bouteau, H. (2011). Catalase is a key enzyme in seed recovery from ageing during priming. Plant Science, 181, 309–315.

  32. Lambrechts, T., Gustot, Q., Couder, E., Houben, D., Iserentant, A., & Lutts, S. (2011a). Comparison of EDTA-enhanced phytoextraction and phytostabilisation strategies with Lolium perenne on a heavy metal contaminated soil. Chemosphere, 85, 1290–1298.

  33. Lambrechts, T., Couder, E., Bernal, P., Faz, A., Iserentant, A., & Lutts, S. (2011b). Assessment of heavy metal bioavailability in contaminated soils from a former mining area (La Union, Spain) using a rhizospheric test. Water, Air, and Soil Pollution, 217, 333–346.

  34. Lanteri, S., Portis, E., Bergervoet, H. M., & Groot, S. P. C. (2000). Molecular markers for the priming of pepper seeds (Capsicum annuum L.). Journal of Horticultural Science and Biotechnology, 75, 607–611.

  35. Lefèvre, I., Corréal, E., & Lutts, S. (2009). Evolution of plant response to heavy metals during vegetative growth in Dorycnium pentaphyllum. Plant Growth Regulation, 59, 1–11.

  36. Liu, Z., Ma, Z., Guo, X., Shao, H., Cui, Q., & Song, W. (2010). Changes of cytosolic Ca2+ fluorescence intensity and plasma membrane calcium channels of maize root tip cells under osmotic stress. Plant Physiology and Biochemistry, 48, 860–865.

  37. Lopareva-Pohu, A., Verdin, A., Garon, G., Louns-Hadj, S., Pourrut, B., Debiane, D., Waterlot, C., Laruelle, F., Bidar, G., Douay, F., & Shirali, P. (2011). Influence of fly ash aided phytostabilisation of Pb, Cd and Zn highly contaminated soils on Lolium perenne and Trifolium repens metal transfer and physiological stress. Environmental Pollution, 159, 1721–1729.

  38. Ma, F., Cholewa, E., Tasneem, M., Peterson, C. A., & Gijzen, M. (2004). Cracks in the palisade cuticle of soybean seed coats correlate with their permeability to water. Annals of Botany, 94, 213–228.

  39. Martens, H., Jakobsen, H. B., & Lyshede, O. B. (1995). Development of the strophiole in seeds of white clover (Trifolium repens L.). Seed Science Research, 5, 171–176.

  40. Masubelele, N. H., Dewitte, W., Menges, M., Maughan, S., Collins, C., Huntley, R., Nieuwland, J., Scofield, S., & Murray, J. A. H. (2005). D-type cyclins activate division in root apex to promote germination in Arabidopsis. Proceedings of the National Academy of Sciences, USA, 102, 15694–15699.

  41. Maxwell, K., & Johnson, G. N. (2000). Chlorophyll fluorescence—a practical guide. Journal of Experimental Botany, 51, 659–668.

  42. Meng, L., Qiao, M., & Arp, H. P. H. (2011). Phytoremediation efficiency of a PAH-contaminated industrial soil using ryegrass, white clover, and celery as mono- and mixed cultures. Journal of Soils and Sediments, 11, 482–490.

  43. Mihoub, A., Chaoui, A., & El Ferjani, E. (2005). Biochemical changes associated with cadmium and copper stress in germinating pea seeds (Pisum sativum L.). Comptes Rendus Biologie, 328, 33–41.

  44. Murungu, F. S., Nyamugafata, P., Chiduza, C., Clark, L. J., & Whalley, W. R. (2003). Effects of seed priming, aggregate size and soil matric potential on emergence of cotton (Gossypium hirsutum L.) and maize (Zea mays L.). Soil Tillage Research, 74, 161–168.

  45. Nagarajan, S., Pandita, V. K., Joshi, D. K., Sinha, J. P., & Modi, B. S. (2005). Characterization of water status in primed seeds of tomato (Lycopersicon esculentum Mill.) by sorption properties and NMR relaxation times. Seed Science Research, 15, 99–111.

  46. Özbingöl, N., Corbineau, F., Groot, S. P. C., Bino, R. J., & Côme, D. (1999). Activation of the cell cycle in tomato (Lycopersicon esculentum Mill.) seeds during osmoconditioning as related to temperature and oxygen. Annals of Botany, 84, 245–251.

  47. Pace, R., Benincasa, P., Ghanem, M. E., Quinet, M., & Lutts, S. (2012). Germination of untreated and primed seeds in rapeseed (Brassica napus var. oleifera del.) under salinity and low matric potential. Experimental Agriculture, 48, 238–251.

  48. Page, A. L., Miller, R. H., & Keeney, D. R. (1982). Methods of soil analysis. Part 2—chemical and microbiological properties (2nd ed.). Madison: American Society of Agronomy.

  49. Parera, C. A., & Cantliffe, D. J. (1994). Presowing seed priming. Horticultural Reviews, 16, 109–141.

  50. Pietrzak, L. N., Fregeau-Reid, J., Chatson, B., & Blackwell, B. (2002). Observations on water distribution in soybean seed during hydration processes using nuclear magnetic resonance imaging. Canadian Journal of Plant Science, 82, 513–519.

  51. Redfearn, M., & Osborne, D. J. (1997). Effects of advancement on nucleic acids in sugarbeet (Beta vulgaris) seeds. Seed Science Research, 7, 261–267.

  52. Smith, M. J., Flowers, T. H., Duncan, H. J., & Alder, J. (2006). Effects of polycyclic aromatic hydrocarbons on germination and subsequent growth of grasses and legumes in freshly contaminated soil and soil with aged PAHs residues. Environmental Pollution, 141, 519–525.

  53. Varier, A., Vari, A. K., & Dadlani, M. (2010). The subcellular basis of seed priming. Current Science, 99, 450–456.

  54. Windauer, L., Altuna, A., & Benech-Arnold, R. (2007). Hydrotime analysis of Lesquerella fendleri seed germination responses to priming treatments. Industrial Crops and Products, 25, 70–74.

  55. Yacoubi, R., Job, C., Belghazi, M., Chaibi, W., & Job, D. (2011). Toward characterizing seed vigor in alfalfa through proteomic analysis of germination and priming. Journal of Proteome Research, 10, 3891–3903.

  56. Ye, Z. H., Wong, J. W. C., & Wong, M. H. (2000). Vegetation response to lime and manure compost amendments on acid lead/zinc mine tailings: A greenhouse study. Restoration Ecology, 8, 289–295.

  57. Zhang, Z. Q., Shu, W. S., Lan, C. Y., & Wong, M. H. (2001). Soil seed bank as an input of seed source in revegetation of lead/zinc mine tailings. Restoration Ecology, 9, 378–385.

Download references

Acknowledgments

This work was supported by the European Union and by the Région Wallonne of Belgium (Division générale de la Recherche et de la Coopération scientifique) through the Convention First-Europe Objectif 1 No. EP1A320501R051F/415734 (2004–2008). The authors thank Dr S. Rios Ruiz, University of Alicante, for support with the electron microscopy and Dr. T. Lambrechts for precious help in soil analysis.

Author information

Correspondence to Stanley Lutts.

Additional information

Laurence Galhaut and Alexis de Lespinay contributed equally to this work.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Galhaut, L., de Lespinay, A., Walker, D.J. et al. Seed Priming of Trifolium repens L. Improved Germination and Early Seedling Growth on Heavy Metal-Contaminated Soil. Water Air Soil Pollut 225, 1905 (2014). https://doi.org/10.1007/s11270-014-1905-1

Download citation

Keywords

  • Polluted soils
  • Germination
  • Revegetation
  • Seed priming
  • White clover (Trifolium repens)