Skip to main content

Advertisement

SpringerLink
Log in

Autumn fertilization with nitrogen improves nutritional status, cold hardiness and the oxidative stress response of Holm oak (Quercus ilex ssp. ballota [Desf.] Samp) nursery seedlings

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

Abstract

Holm oak (Quercus ilex ssp. ballota [Desf.] Samp) is one of the most important species in forest communities of the western Mediterranean Basin, but is very vulnerable to environmental stress during the first years of its life. In particular, summer drought and winter frosts limit the distribution, survival, and growth of Holm oak. These two stress factors can lead to plasmolysis and/or oxidative stress. We hypothesized that autumn fertilization with nitrogen (N) can improve plant tolerance to these abiotic stress factors and improve plant quality and therefore reforestation success. A 12-week autumn application of 30 or 60 mg N (plus 70 mg N applied to both treatments during the previous 28 weeks in the nursery, i.e. 100 and 130 mg N in total, respectively) improved overall growth, root growth capacity, frost tolerance, and nutritional status of plants relative to plants given 0.0 and 1.5 mg autumnal N, and had no negative effect on seedling response to water stress. A very small increment in N doses during the autumn (1.5 vs. 0.0 mg N) improved some morphological parameters, such as stem diameter (D) and shoot dry weight, and physiological parameters, such as total antioxidant activity. The highest autumnal N dose (60 mg) increased leaf nutrient content without decreasing the concentration, but had a tendency to reduce frost tolerance relative to seedlings given a lower autumnal N dose (30 mg).

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

  • Andivia E, Fernández M, Vázquez-Piqué J (2011) Autumn fertilization of Quercus ilex ssp. ballota (Desf.) Samp. nursery seedlings: effects on morpho-physiology and field performance. Ann For Sci 68:543–553

    Article  Google Scholar 

  • Aranda I, Castro L, Alía L, Pardos JA, Gil L (2005) Low temperature during winter elicits differential responses among populations of the Mediterranean evergreen cork oak (Quercus suber). Tree Physiol 25:1085–1090

    Article  PubMed  CAS  Google Scholar 

  • Birchler T, Rose RW, Royo A, Pardos M (1998) La planta ideal: revisión del concepto, parámetros definitorios e implementación práctica. Inv Agrar-Sist Rec F 7:109–121

    Google Scholar 

  • Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot Lond 91:179–194

    Article  CAS  Google Scholar 

  • Boivin JR, Miller BD, Timmer VR (2002) Late-season fertilization of Picea mariana seedlings under greenhouse culture: biomass and nutrient dynamics. Ann For Sci 59:255–264

    Article  Google Scholar 

  • Brand-Williams W, Cuvelier ME, Berset C (1995) Use of a free radical method to evaluate antioxidant activity. Food Sci Technol LEB 28:25–30

    CAS  Google Scholar 

  • Briat JF (2002) Metal ion-activated oxidative stress and its control. In: Inzé D, Montagu M (eds) Oxidative stress in plants. Taylor and Francis, London, pp 171–189

    Google Scholar 

  • Broncano MJ, Riba M, Retana J (1998) Seed germination and seedling performance of two Mediterranean tree species. Holm oak (Quercus ilex L.) and Aleppo pine (Pinus halepensis Mill.): a multifactor experimental approach. Plant Ecol 138:17–26

    Article  Google Scholar 

  • del Campo AD, Navarro-Cerillo RM, Ceacero CJ (2010) Seedling quality and field performance of commercial stocklots of containerized Holm oak (Quercus ilex) in Mediterranean Spain: an approach for establishing a quality standard. New For 39:19–37

    Article  Google Scholar 

  • Clijsters H, Cuypers A, Vangronsveld J (1999) Physiological responses to heavy metals in higher plants: defence against oxidative stress. Z Naturforsch C 54:730–734

    CAS  Google Scholar 

  • Colombo SJ, Glerum C, Webb DP (2003) Daylength, temperature and fertilization effects on desiccation resistance, cold hardiness and root growth potential of Picea mariana seedlings. Ann For Sci 60:307–317

    Article  Google Scholar 

  • Corcuera L, Morales F, Abadia A, Gil-Pelegrin E (2005) Seasonal changes in photosynthesis and photoprotection in a Quercus ilex subsp. ballota woodland located in its upper altitudinal extreme in the Iberian Peninsula. Tree Physiol 25:599–608

    Article  PubMed  CAS  Google Scholar 

  • Cuesta B, Villar-Salvador P, Puértolas J, Jacobs DF, Rey Benayas JM (2010) Why do large, nitrogen rich seedlings better resist stressful transplanting conditions? A physiological analysis in two functionally contrasting Mediterranean forest species. For Ecol Manage 260:71–78

    Article  Google Scholar 

  • Fernández M (2008) Endurecimiento en vivero de especies leñosas mediterráneas destinadas a plantación forestal. Cuad Soc Esp Cienc For 28:13–24

    Google Scholar 

  • Fernández M, Alejano R, Domínguez L, Tapias R (2008) Temperature controls cold hardening more effectively than photoperiod in four Mediterranean broadleaf evergreen species. Tree For Sci Biotech 2:43–49

    Google Scholar 

  • Fernández M, Marcos C, Tapias R, Ruiz F, López G (2007) Nursery fertilisation affects the frost-tolerance and plant quality of Eucalyptus globulus Labill. cuttings. Ann For Sci 68:865–873

    Article  Google Scholar 

  • Fernández M, Novillo C, Pardos JA (2006) Effects of water and nutrient availability in Pinus pinaster Ait. open pollinated families at an early age: growth, gas exchange and water relations. New For 31:321–342

    Article  Google Scholar 

  • Foyer CH (1993) Ascorbic acid. In: Alscher EG, Hess JL (eds) Antioxidants in higher plants. CRC Press, Florida, pp 32–54

    Google Scholar 

  • Foyer CH, Lelandais M, Kunert KJ (1994) Photooxidative stress in plants. Physiol Plantarum 92:696–717

    Article  CAS  Google Scholar 

  • García-Plazaola JI, Artetxe U, Becerril JM (1999) Diurnal changes in antioxidant and carotenoid composition in the Mediterranean sclerophyll tree Quercus ilex (L.) during winter. Plant Sci 143:125–133

    Article  Google Scholar 

  • Gimeno TE, Pías B, Lemos-Filhos JP, Valladares F (2009) Plasticity and stress tolerance override local adaptation in the response of Mediterranean Holm oak seedlings to drought and cold. Tree Physiol 29:87–98

    Article  PubMed  Google Scholar 

  • Harvey HP, Van den Driessche (1999) Nitrogen and potassium effects on xylem cavitation and water-use efficiency in poplars. Tree Physiol 19:943–950

    PubMed  Google Scholar 

  • Heino P, Palva ET (2003) Signal transduction in plant cold acclimation. In: Hirt H, Shinozaki K (eds) Plant responses to abiotic stress. Top Curr Gen Vol 4. Springer, Berlin, pp 151–185

    Chapter  Google Scholar 

  • Hernández EI, Vilagrosa A, Luis VC, Llorca M, Chirino E, Vallejo VR (2009) Root hydraulic conductance, gas exchange and leaf water potential in seedling of Pistacea lentiscus L. and Quercus suber L. grown under different fertilization and light regimes. Environ Exp Bot 67:269–276

    Article  Google Scholar 

  • Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611

    Article  CAS  Google Scholar 

  • Jacobs DF, Salifu KF, Oliet JA (2009) Sobrecarga exponencial de nutrientes para la optimización de la fertilización en vivero de plantas de Quercus ilex L. In: Sociedad Española de Ciencias Forestales, Junta de Castilla y León (eds) Proceedings V Congreso Forestal Español, vol 1. Ávila, Spain, pp 11

  • Kaminska-Rozek E, Pukacki PM (2005) Effect of freezing desiccation on cold hardiness, ROS, membrane lipid levels antioxidant status in spruce seedling. Acta Soc Bot Pol 3:219–228

    Google Scholar 

  • Knörzer OC, Durner J, Boger P (1996) Alterations in the antioxidative system of suspension cultured soybean cells (Glycine max) induced by oxidative stress. Physiol Plantarum 97:388–396

    Article  Google Scholar 

  • Lambers H, Cambridge ML, Konings H, Pons TL (1990) Causes and consequences of variation in growth rate and productivity of higher plant. SPB Academic Publishing, Amsterdam, p 363

    Google Scholar 

  • Larcher W (2000) Temperature stress and survival ability of Mediterranean sclerophyllous plants. Plant Biosyst 134:279–295

    Article  Google Scholar 

  • Leong LP, Shui G (2002) An investigation of antioxidant capacity of fruits in Singapore markets. Food Chem 76:69–75

    Article  CAS  Google Scholar 

  • Lloret F, Casanovas C, Peñuelas J (1999) Seedlings survival of Mediterranean shrubland species in relation to root: shoot ratio, seed size and water and nitrogen use. Funct Ecol 13:210–216

    Article  Google Scholar 

  • MAPA (2006) Forestación de tierras agrícolas. Ministerio de Agricultura y Pesca, Madrid, p 373

    Google Scholar 

  • Márquez-García B, Córdoba F (2010) Antioxidative system in wild populations of Erica andevalensis. Environ Exp Bot 68:58–65

    Article  Google Scholar 

  • Márquez-García B, Fernández MA, Córdoba F (2009) Phenolics composition in Erica sp. differentially exponed to metal pollution in the Iberian Southwestern Pyritic Belt. Bioresour Technol 100:446–451

    Article  PubMed  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants. Academic Press, London, p 889

    Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  PubMed  CAS  Google Scholar 

  • Mollá S, Villar-Salvador P, García-Fayos P, Peñuelas-Rubira JL (2006) Physiological and transplanting performance of Quercus ilex L. (holm oak) seedlings grown in nurseries with different winter conditions. For Ecol Manage 237:218–226

    Article  Google Scholar 

  • Morin X, Ameglio T, Ahas R, Kurz-Besson C, Lanta V, Lebourgeois F, Miglietta F, Chuine I (2007) Variation in cold hardiness and carbohydrates concentration from dormancy induction to bud burst among provenances of three European oak species. Tree Physiol 27:817–825

    Article  PubMed  CAS  Google Scholar 

  • Navarro-Cerillo RM, Pemán J, del Campo A, Moreno J, Lara MA, Díaz JL, Pousa F, Piñón FM (2009) Manual de especies para la forestación de tierras agrarias en Andalucía. Junta de Andalucía, Consejería de Agricultura y Pesca, Sevilla, p 395

    Google Scholar 

  • Oliet JA, Tejada M, Salifu KF, Collazos A, Jacobs DF (2009) Performance and nutrient dynamics of Holm oak (Quercus ilex L.) seedlings in relation to nursery nutrient loading and post-transplant fertility. Eur J Forest Res 128:253–263

    Article  Google Scholar 

  • Oliet JA, Salazar JM, Villar R, Robredo E, Valladares F (2011) Fall fertilization of Holm oak affects N and P dynamics, root growth potential, and post-planting phenology and growth. Ann For Sci 68:647–656

    Article  Google Scholar 

  • Palacio S, Milla R, Albuixech J, Pérez-Rontomé C, Camarero JJ, Maestro M, Montserrat-Martí G (2008) Seasonal variability of dry matter content and its relationship with shoot growth and non-structural carbohydrates. New Phytol 180:133–142

    Article  PubMed  CAS  Google Scholar 

  • Palacios G, Navarro-Cerrillo RM, del Campo A, Toral M (2009) Site preparation, stock quality and planning date effect on early establishment of Holm oak (Quercus ilex L.) seedlings. Ecol Eng 35:38–46

    Article  Google Scholar 

  • Pardos M, Royo A, Pardos JA (2005) Growth, nutrient, water relations, and gas exchange in Holm oak plantation in response to irrigation and fertilization. New For 30:75–94

    Article  Google Scholar 

  • Pausas JG, Blade C, Valdecantos A, Seva JP, Fuentes D, Alloza JA, Milagrosa A, Bautista S, Cortina J, Vallejo R (2004) Pines and oaks in the restoration of Mediterranean landscapes of Spain: new perspectives for an old practice—a review. Plant Ecol 171:209–220

    Article  Google Scholar 

  • Puttonen P (1997) Looking for the “silver-bullet”—can one test do it? New For 13:9–27

    Article  Google Scholar 

  • Rose R, Rose CL, Omi SK, Forry KR, Durral DM, Bigg WL (1991) Starch determination by perchloric acid vs enzymes: evaluating the accuracy and precision of six colorimetric methods. J Agric Food Chem 39:2–11

    Article  CAS  Google Scholar 

  • Ruiz de la Torre J (2006) Flora mayor. Ministerio de Medio Ambiente. Organismo Autónomo Parques Nacionales, Madrid

  • Sanz-Pérez V, Castro-Díez P, Valladares F (2007) Growth versus storage: response of Mediterranean oak seedlings to changes in nutrient and water availabilities. Ann For Sci 64:201–210

    Article  Google Scholar 

  • Shaw BP, Sahu SK, Mishra RK (2004) Heavy metal induced oxidative damage in terrestrial plants. In: Prassad MNV (ed) Heavy metal stress in plants: from biomolecules to ecosystem. Springer, Berlín, pp 84–126

    Google Scholar 

  • Simpson DG, Ritchie GA (1996) Does RGP predict field performance? A debate. New For 13:249–273

    Google Scholar 

  • Smirnoff N (1998) Plant resistance to environmental stress. Curr Opin Biotech 9:214–219

    Article  PubMed  CAS  Google Scholar 

  • Smirnoff N (2000) Ascorbic acid: metabolism and functions of a multi-facceted molecule. Curr Opin Plant Biol 3:229–235

    CAS  Google Scholar 

  • Spiro RG (1966) Analysis of sugars found in glycoproteins. In: Neufeld EF, Ginsburg V (eds) Methods in ezymology. Vol. VIII, Complex carbohydrates. Academic Press, New York, pp 3–26

    Chapter  Google Scholar 

  • Strand M, Öquist G (1985) Inhibition of photosynthesis by freezing temperatures and high light levels in cold-acclimated seedlings of Scots pine (Pinus sylvestris). I. Effects on the light-limited and light-saturated rates of CO2 assimilation. Physiol Plant 64:425–530

    Article  CAS  Google Scholar 

  • Trubat R, Cortina J, Vilagrosa A (2010) Nursery fertilization affects seedling traits but not field performance in Quercus suber L. J Arid Environ 74:491–497

    Article  Google Scholar 

  • Trubat R, Cortina J, Vilagrosa A (2011) Nutrient deprivation improves field performance of woody seedlings in a degraded semi-arid shrubland. Ecol Eng 37:1164–1173

    Article  Google Scholar 

  • Valdecantos A, Cortina J, Vallejo VR (2006) Nutrient status and field performance of tree seedlings planted in Mediterranean degraded areas. Ann For Sci 63:249–256

    Article  CAS  Google Scholar 

  • Vilagrosa A, Villar-Salvador P, Puértolas J (2006) El endurecimiento en vivero de especies forestales mediterráneas. In: Cortina J, Peñuelas JL, Puértolas J, Savé R, Vilagrosa A (eds) Calidad de planta forestal para la restauración en ambientes mediterráneos: estado actual de conocimientos. MMA, Organismo Autónomo de Parques Nacionales, Madrid, pp 119–140

    Google Scholar 

  • Villar-Salvador P, Planelles R, Enriquez E, Peñuelas-Rubira JL (2004a) a Nursery cultivation regimes, plant functional attributes, and field performance relationships in the Mediterranean oak Quercus ilex L. For Ecol Manag 196:257–266

    Article  Google Scholar 

  • Villar-Salvador P, Planelles R, Oliet JA, Peñuelas-Rubira JL, Jacobs DF, González M (2004b) b Drought tolerance and transplanting performance of Holm oak (Quercus ilex L.) seedlings after drought hardening in the nursery. Tree Physiol 24:1147–1155

    Article  PubMed  Google Scholar 

  • Villar-Salvador P, Puértolas J, Peñuelas JL, Planelles R (2005) Effect of nitrogen fertilization in the nursery on the drought and frost resistance of Mediterranean forest species. Invest Agrar Sist Recur For 14:408–418

    Google Scholar 

  • Walker MA, McKersie BD (1993) Role of the ascorbate–glutathione antioxidant system in chilling resistance of tomato. J Plant Physiol 141:234–239

    Article  CAS  Google Scholar 

  • Wise RR, Naylor AW (1987) Chilling-enhanced photooxidation: evidence for the role of singlet oxygen and superoxide in the breakdown of pigment and endogenous antioxidants. Plant Physiol 83:278–282

    Google Scholar 

  • Wolfinger RD (1996) Heterogeneous variance-covariance structures for repeated measures. J Agric Biol Environ Stat 1:205–230

    Article  Google Scholar 

  • Wong SP, Leong LP, Koh JHW (2006) Antioxidant activities of aqueous extracts of selected plants. Food Chem 99:775–783

    Article  CAS  Google Scholar 

  • Zwiazek J, Renault S, Croser C, Hansen J, Beck E (2001) Biochemical and biophysical changes in relation to cold hardiness. In: Bigras FJ, Colombo SJ (eds) Conifer cold hardiness. Kluwer Academic Publishers, Dordrecht, pp 165–186

    Google Scholar 

Download references

Acknowledgments

This work has been financed by MEC of Spain (ref. AGL2006-12609-C02-01/FOR). In addition, the work was partially supported by University of Huelva and Andalucía Research Programs to promote research groups activity. First author is benefiting from a doctoral grant from the Ministry of Education of Spain. We gratefully acknowledge the support of the laboratory of research and Agrifood control (LICAH) of the University of Huelva for carrying out chemical analysis.

Author information

Authors and Affiliations

  1. Departamento de Ciencias Agroforestales, Universidad de Huelva, Escuela Técnica Superior de Ingeniería, Campus Universitario de La Rábida, Carretera de Palos de la Frontera, S/N, 21819, Palos de la Frontera, Huelva, Spain

    Enrique Andivia, Javier Vázquez-Piqué & Manuel Fernández

  2. Departamento de Biología Ambiental y Salud Pública, Universidad de Huelva, Facultad de Ciencias Experimentales, Campus Universitario de El Carmen, Avda de las Fuerzas Armadas, S/N, 21071, Huelva, Spain

    Belén Márquez-García & Francisco Córdoba

Authors
  1. Enrique Andivia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Belén Márquez-García
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Javier Vázquez-Piqué
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Francisco Córdoba
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Manuel Fernández
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Manuel Fernández.

Additional information

Communicated by R. Hampp.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Andivia, E., Márquez-García, B., Vázquez-Piqué, J. et al. Autumn fertilization with nitrogen improves nutritional status, cold hardiness and the oxidative stress response of Holm oak (Quercus ilex ssp. ballota [Desf.] Samp) nursery seedlings. Trees 26, 311–320 (2012). https://doi.org/10.1007/s00468-011-0593-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-011-0593-3

Keywords

Search

Navigation