iForest - Biogeosciences and Forestry


Controlled-release fertilizers combined with Pseudomonas fluorescens rhizobacteria inoculum improve growth in Pinus halepensis seedlings

Jose Alfonso Dominguez-Nuñez (1)   , Daniel Delgado-Alvez (1), Marta Berrocal-Lobo (1), Analía Anriquez (2), Ada Albanesi (2)

iForest - Biogeosciences and Forestry, Volume 8, Issue 1, Pages 12-18 (2015)
doi: https://doi.org/10.3832/ifor1110-007
Published: May 12, 2014 - Copyright © 2015 SISEF

Research Articles

Pinus halepensis seedlings are currently used to regenerate arid Mediterranean regions. Optimized methods for seedling fertilization in nurseries improve plant growth and are essential for successful reforestation. Previously, we showed that inoculation of P. halepensis seedlings with Pseudomonas fluorescens CECT 844 rhizobacteria improved plant growth and N uptake. The aim of this study was to determine the physiological and morphological response of P. halepensis seedlings to a combined treatment including controlled-release fertilization and inoculation with the rhizobacterium P. fluorescens. P. halepensis seedlings were grown in a nursery under well-watered conditions and were fertilized (F), inoculated with P. fluorescens (Ps) or fertilized and inoculated (F x Ps). Growth and water parameters (osmotic potential at both full and zero turgor and modulus of elasticity) were measured in seedlings under each treatment. The total N, P, K, Ca, Mg and Fe contents and concentrations in seedling roots and shoots were also measured. Finally, root growth potential was estimated. F x Ps increased both seedling growth and nutrient uptake compared with the independent treatments. Interestingly, amendment with rhizobacteria had a slight negative effect on osmotic potential and P uptake, which was lessened by combining Ps with F. The present work shows that F x Ps is highly efficient for improving the quality of forest seedlings in nurseries. As such, F x Ps represents a potential alternative treatment that could reduce contaminant emissions and increase microbiota soil regeneration in degraded soils.


Controlled-release Fertilization, Rhizobacteria, Pinus halepensis, Water Parameters, Mineral Nutrition, Nursery, Root Growth Potential, Osmotic Potential

Authors’ address

Jose Alfonso Dominguez-Nuñez
Daniel Delgado-Alvez
Marta Berrocal-Lobo
E.T.S.I Montes & E.U.I.T Forestal, Polytechnic University of Madrid, Av/da Ciudad Universitaria s/n, E-28040 Madrid (Spain)
Analía Anriquez
Ada Albanesi
Faculty of Agronomy & Agroindustries, National University of Santiago del Estero, Av/da Belgrano (S) 1912, 4200 Santiago del Estero (Argentina)

Corresponding author

Jose Alfonso Dominguez-Nuñez


Dominguez-Nuñez JA, Delgado-Alvez D, Berrocal-Lobo M, Anriquez A, Albanesi A (2015). Controlled-release fertilizers combined with Pseudomonas fluorescens rhizobacteria inoculum improve growth in Pinus halepensis seedlings. iForest 8: 12-18. - doi: 10.3832/ifor1110-007

Academic Editor

Roberto Tognetti

Paper history

Received: Aug 20, 2013
Accepted: Dec 26, 2013

First online: May 12, 2014
Publication Date: Feb 02, 2015
Publication Time: 4.57 months

Breakdown by View Type

(Waiting for server response...)

Article Usage

Total Article Views: 45926
(from publication date up to now)

Breakdown by View Type
HTML Page Views: 39003
Abstract Page Views: 2335
PDF Downloads: 3492
Citation/Reference Downloads: 18
XML Downloads: 1078

Web Metrics
Days since publication: 3687
Overall contacts: 45926
Avg. contacts per week: 87.19

Article Citations

Article citations are based on data periodically collected from the Clarivate Web of Science web site
(last update: Feb 2023)

Total number of cites (since 2015): 3
Average cites per year: 0.33


Publication Metrics

by Dimensions ©

Articles citing this article

List of the papers citing this article based on CrossRef Cited-by.

Ahamadou B, Huang Q, Chen W, Wen S, Zhang J, Mohamed I, Cai P, Liang W (2009)
Microcalorimetric assessment of microbial activity in long-term fertilization experimental soils of Southern China. FEMS Microbiology Ecology 70: 186-195.
CrossRef | Gscholar
Benlloch-González M, Arquero O, Fournier JM, Barranco D, Benlloch M (2008)
K+ starvation inhibits water-stress-induced stomatal closure. Journal of Plant Physiology 165: 623-630.
CrossRef | Gscholar
Bolton HJ, Fredickson JK, Elliott LF (1993)
Microbial ecology of the rhizosphere. In: “Soil Microbial Ecology” (Metting FBJ ed). Marcel Dekker, New York, USA, pp. 27-63.
Bowman WD, Roberts SW (1985)
Seasonal changes in tissue elasticity in chaparral shrubs. Physiologia Plantarum 65: 233-236.
CrossRef | Gscholar
Caravaca F, Alguacil MM, Azcón R, Parladé J, Torres P, Roldán A (2005)
Establishment of two ectomycorrhizal shrub species in a semiarid site after in situ amendment with sugar beet, rock phosphate, and Aspergillus níger. Microbial Ecology 49: 73-82.
CrossRef | Gscholar
Cañellas I, Finat L, Bachiller A, Montero G (1999)
Comportamiento de planta de Pinus pinea en vivero y campo: ensayos de técnicas de cultivo de planta, fertilización y aplicación de herbicidas [Behaviour of Pinus pinea plants in nursery and field: Trials of plant production, fertilisation and herbicides]. Investigacion Agraria: Produccion y Proteccion Vegetal 8: 335-359. [in Spanish]
Chanway CP (1997)
Inoculation of tree roots with plant growth promoting soil bacteria: an emerging technology for reforestation. Forest Science 43: 99-112.
Online | Gscholar
Cheung YNS, Tyree MT, Dainty J (1975)
Water relations parameters on single leaves obtained in a pressure bomb and some ecological interpretations. Canadian Journal of Botany 53: 1342-1346.
CrossRef | Gscholar
Dominguez JA, Martin A, Anriquez A, Albanesi A (2012)
The combined effects of Pseudomonas fluorescens and Tuber melanosporum on the quality of Pinus halepensis seedlings. Mycorrhiza 22 (6): 429-436.
CrossRef | Gscholar
Domínguez-Núñez JA, Muñóz D, De la Cruz A, Saiz de Omeñaca JA (2013)
Effects of Pseudomonas fluorescens on the water parameters of mycorrhizal and non-mycorrhizal seedlings of Pinus halepensis. Agronomy 3: 571-582.
CrossRef | Gscholar
He JZ, Zheng Y, Chen CR, He YQ, Zhang LM (2008)
Microbial composition and diversity of an upland red soil under long-term fertilization treatments as revealed by culture-dependent and culture-independent approaches. Journal of Soils and Sediments 8:349-358
CrossRef | Gscholar
Jones MM, Turner NC (1980)
Osmotic adjustment in expanding and fully expanded leves of sunlower in response to water deficits. Australian Journal of Plant Physiology 7: 181-192.
CrossRef | Gscholar
Karabaghli C, Frey-Klett P, Sotta B, Bonnet M, Le Tacon F (1998)
In vitro effects of Laccaria bicolor S238 N and Pseudomonas fluorescens strain BBc6 on rooting of derooted shoot hypocotyls of Norway spruce. Tree Physiology 18: 103-111.
CrossRef | Gscholar
Lehto T, Zwiazek J (2011)
Ectomycorrhizas and water relations of trees: a review. Mycorrhiza 21 (2): 71-90.
CrossRef | Gscholar
Lucas-García JA, Domenech J, Santamaría C, Camacho M, Daza A, Gutiérrez Mañero FJ (2004)
Growth of forest plants (pine and holm-oak) inoculated with rhizobacteria: relationship with microbial community structure and biological activity of its rhizosphere. Environmental and Experimental Botany 52 (3): 239-251.
CrossRef | Gscholar
Maestre FT, Cortina J (2004)
Are Pinus halepensis plantations useful as a restauration tool in semiarid Mediterranean areas? Forest Ecology and Management 198: 303-317.
CrossRef | Gscholar
Matthijs S, Tehrani KA, Laus G, Jackson RW, Cooper RM, Cornelis P (2007)
Thioquinolobactin, a Pseudomonas siderophore with antifungal and anti-Pythium activity. Environmental Microbiology 9 (2): 425-434.
CrossRef | Gscholar
Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006)
Plant stomata function in innate immunity against bacterial invasion. Cell 126: 969-980.
CrossRef | Gscholar
Oliet J, Segura ML, Martin- Domínguez F, Blanco E, Serrada R, Lopez Arias M, Artero F (1999)
Los fertilizantes de liberación controlada lenta aplicados a la producción de planta forestal de vivero. Efecto de dosis y formulaciones sobre la calidad de Pinus halepensis Mill. [Slow-controlled release fertilizers used in nursery geedling productions. Doses and formulations effects on Pinus halepensis Mill. seedling quality]. Investigacion Agraria: Sistemas y Recursos Forestales 8 (1): 207-228. [in Spanish]
Oliet J, Planelles R, Artero F, Montes ME, Linarejos AL, Alejano R, Arias LM (2003)
El potencial de crecimiento radical en planta de vivero de Pinus halepensis Mill. Influencia de la fertilización [Root growth potential in nursery of Pinus halepensis Mill seedlings. Fertilization effect]. Investigacion Agraria: Sistemas y Recursos Forestales 12 (1): 51-60. [in Spanish]
Oliet J, Planelles R, Artero F, Valverde R, Douglas FJ, Segura M (2009)
Field performance of Pinus halepensis planted in Mediterranean arid conditions: relative influence of seedling morphology and mineral nutrition. New Forests 37: 313-331
CrossRef | Gscholar
Ouahmane L, Revel JC, Hafidi M, Thioulouse J, Prin Y, Galiana A, Dreyfus B, Duponnois R (2009)
Responses of Pinus halepensis growth, soil microbial catabolic functions and phosphate-solubilizing bacteria after rock phosphate amendment and ectomycorrhizal inoculation. Plant and Soil 320: 169-179.
CrossRef | Gscholar
Patakas A, Nikolaou N, Zioziou K, Radoglou K, Noitsakis B (2002)
The role of organic solute and ion accumulation in osmotic adjustment in drought-stressed grapevines. Plant Science 163: 361-367
CrossRef | Gscholar
Probanza A, Mateos JL, Lucas GJA, Ramos B, De Felipe MR, Gutierrez MFJ (2001)
Effects of inoculation with PGPR bacillus and Pisolithus tinctorius on Pinus pinea L. growth, bacterial rhizosphere colonization, and mycorrhizal infection. Microbial Ecology 41: 140-148.
CrossRef | Gscholar
Puértolas J, Gil L, Pardos JA (2003)
Effects of nutritional status and seedling size on field performance of Pinus halepensis planted on former arable land in the Mediterranean basin. Forestry 76 (2): 159-168.
CrossRef | Gscholar
Rincón A, Valladares F, Gimeno TE, Pueyo JJ (2008)
Water stress responses of two Mediterranean tree species influenced by native soil microorganisms and inoculation with a plant growth promoting rhizobacterium. Tree Physiology 28: 1693-1701.
CrossRef | Gscholar
Robichaux RH (1984)
Variation in the tissue water relations of two sympatric Hawaiian Dubautia species and their natural hybrid. Oecologia 65: 75-81.
CrossRef | Gscholar
Sardans J, Rodá F, Peñuelas J (2006)
Effects of a nutrient pulse supply on nutrient status of the Mediterranean trees Quercus ilex subsp. ballota and Pinus halepensis on different soils and under different competitive pressure. Trees 20: 619-632.
CrossRef | Gscholar
Scholander PF, Hammel HT, Bradstreet ED, Hemmingsen EA (1965)
Sap pressure in vascular plants. Science 148: 339-346.
CrossRef | Gscholar
Silby MW, Cerdeño-Tárraga AM, Vernikos GS, Giddens SR, Jackson RW, Preston GM, Zhang XX, Moon CD, Gehrig SM, Godfrey SA, Knight CG, Malone JG, Robinson Z, Spiers AJ, Harris S, Challis GL, Yaxley AM, Harris D, Seeger K, Murphy L, Rutter S, Squares R, Quail MA, Saunders E, Mavromatis K, Brettin TS, Bentley SD, Hothersall J, Stephens E, Thomas CM, Parkhill J, Levy SB, Rainey PB, Thomson NR (2009)
Genomic and genetic analyses of diversity and plant interactions of Pseudomonas fluorescens. Genome Biology 10 (5): R51.
CrossRef | Gscholar
Simpson DG, Ritchie GA (1997)
Does RGP predict field performance? A debate. New Forests 13 (1-3): 253-277.
CrossRef | Gscholar
Somerville C, Bauer S, Brininstool G, Facette M, Hamann T, Milne J, Osborne E, Paredez A, Persson S, Raab T, Vorwerk S, Youngs H (2004)
Toward a systems approach to understanding plant cell walls. Science 306 (5705): 2206-2211.
CrossRef | Gscholar
Tinus RW, Burr KE, Atzmon N, Riov J (2000)
Relationships between carbohydrate concentration and root growth potential in coniferous seedlings from three climates during cold hardening and dehardening. Tree Physiology 20: 1097-1104.
CrossRef | Gscholar
Tyree M, Hammel HT (1972)
The measurement of the turgor pressure and the water relations of plants by the pressure technique. Journal of Experimental Botany 23: 267-282.
CrossRef | Gscholar
Tyree M, Jarvis PG (1982)
Water in tissues and cells. In: “Encyclopedia of Plant Physiology” (Lange OL, Nobel PS, Osmond CB, Ziegler H eds). New Series, Vol. 12B, Physiological Plant Ecology II, Springer-Verlag, Berlin, Germany, pp. 36-77.
Villar-Salvador P, Ocaña L, Peñuelas JL, Carrasco I (1999)
Effects of water stress conditioning on the water relations, root growth capacity, and the nitrogen an non-structural carbohydrate concentration of Pinus halepensis Mill. (Aleppo pine) seedlings. Annals of Forest Science 56: 459-465.
CrossRef | Gscholar
Vorwerk S, Somerville S, Somerville C (2004)
The role of plant cell wall polysaccharide composition in disease resistance. Trends in Plant Science 9(4): 203-9.
CrossRef | Gscholar
Yuan C-L, Mou C-X, Wu W-L, Guo Y-B (2011)
Effect of different fertilization treatments on indole-3-acetic acid producing bacteria in soil. Journal of Soils and Sediments 11: 322-329.
CrossRef | Gscholar

This website uses cookies to ensure you get the best experience on our website. More info