The alleviation of reforestation challenges by beneficial soil microorganisms

  • Vera Karličić University of Belgrade, Faculty of Agriculture
  • Vesna Golubović Ćurguz University of Belgrade, Faculty of Forestry
  • Vera Raičević University of Belgrade, Faculty of Agriculture
Keywords: Post-mining Landscapes, Reforestation, Mycorrhizal Fungi, Plant Growth Promoting Rhizobacteria

Abstract

Surface mining causes major destruction of natural landscapes and ecosystems. The most fertile, surface soil layer is lost permanently, together with vegetation, wildlife, and micro flora. Post-mining areas are characterized with diverse edaphic, topographic, hydrographic conditions, which complicate land restoration. Successful establishment of forest ecosystems on such land depends mostly on selection of tree species. The chosen plants must be capable of tolerating a wide range of acidity, fertility, moisture, and have potential to ameliorate such substrates for more demanding species. But, reforestation of heavily damaged ecosystems, such as post-mining areas, demands a new approach in seedlings production. This new approach takes into account specific requirements of habitat and integrates them into “targeted production of planting materialâ€. A good strategy for successful reforestation of post-mining areas is the input of organic matter (compost, mulch). Also, current knowledge and experiences emphasize the potential of beneficial microorganisms such as, mycorrhizal fungi (MF) and plant growth promoting rhizobacteria (PGPR). The majority of studies that deal with beneficial interactions between trees and microorganisms are focused on the mycorrhiza, while plant growth promoting rhizobacteria are less present in silviculture. In this study, the focus is on the reforestation challenges of two mining basins, Majdanpek and Kolubara and suggests beneficial microorganisms as potential solution. The study presents results of several years’ researches on plant response to the presence of mycorrhizal fungi and PGPR. The substrates used for plant growth were Majdanpek and Kolubara mine deposals. Mycorrhizal seedlings were grown in Majdanpek mine deposal, and at the end of the experiment they had 30% higher biomass in comparison to control (seedlings without mycorrhiza). Seedlings linked with fungi had a higher survival rate. Deposals from Kolubara Mining Basin were used as a substrate for seedlings inoculated with PGPR. In the first experiment, Scots pine and Norway spruce were inoculated with Azotobacter chroococcum, Bacillus megaterium, B. circulans, B. licheniformis, B. pumilus, B. amyloliquefaciens. Inoculation resulted with higher biomass production (Scots pine 43%, Norway spruce 34%). Similar results were obtained in the second experiment where Scots pine and black locust were inoculated with Bacillus licheniformis, Aeromonas hydrophila, Pseudomonas putida and Burkholderia cepacia. Both species had higher biomass (around 20%) in comparison to un-inoculated control. The results confirmed the fact that early establishment and successful growth of vegetation on devastated areas depends on the presence and activity of soil microbes. Microorganisms as a “nature’s solution†pose the potential to alleviate reforestation challenges of anthropogenic devastated landscapes. Their presence and activity is crucial for ecosystem stability. In areas with compromised balance, their introduction is justified action for achieving the goal of long term ecosystem sustainability.

Downloads

Download data is not yet available.

References

Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: Current perspective. J King Saud Univ – Science 26:1–20. http://dx.doi.org/10.1016/j.jksus.2013.05.001

Ahemad M, Khan MS (2012) Productivity of greengram in tebuconazole-stressed soil, by using a tolerant and plant growth promoting Bradyrhizobium sp. MRM6 strain. Acta Physiol Plant 34:245–254. http://dx.doi.org/10.1007/s11738-011-0823-8

Anand R, Chanway CP (2013a) N2-fixation and growth promotion in cedar colonized by an endophytic strain of Paenibacillus polymyxa. Biol Fert Soil 49:235–239. http://dx.doi.org/10.1007/s00374-012-0735-9

Anand R, Grayston S, Chanway C (2013b) N2-Fixation and Seedling Growth Promotion of Lodgepole Pine by Endophytic Paenibacillus polymyxa. Microb Ecol 66:369–374. http://dx.doi.org/10.1007/s00248-013-0196-1

Atanasković I, JoviÄić Petrović J, BioÄanin M, KarliÄić V, RaiÄević V, Lalević B (2015) Stimulation of diesel degradation and biosurfactant production by aminoglycosides in a novel oil-degrading bacterium Pseudomonas luteola PRO23, Hem ind, OnLine-First 00: 20-20.

Avera BN (2014) Development of Ecosystem Structure and Function on Reforested Surface-Mined Lands. Master of Science In Forestry, Virginia Polytechnic Institute and State University.

Barriuso J, Solano RB, Santamaría C, Daza A, Gutiérrez Ma-ero FJ (2008) Effect of inoculation with putative plant growth-promoting rhizobacteria isolated from Pinus spp. on Pinus pinea growth, mycorrhization and rhizosphere microbial communities. J Appl Microbiol 105: 1298-309. http://dx.doi.org/10.1111/j.1365-2672.2008.03862.x

Baslam M, Esteban R, García-Plazaola JI, Goicoechea N (2013) Effectiveness of arbuscular mycorrhizal fungi (AMF) for inducing the accumulation of major carotenoids, chlorophylls and tocopherol in green and red leaf lettuces. Appl Microbiol Biotechnol 97:3119–3128. http://dx.doi.org/10.1007/s00253-012-4526-x

Baum C, Hrynkiewicz K, Leinweber P, Meibner R (2006) Heavy-metal mobilization and uptake by mycorrhizal and nonmycorrhizal willows (Salix x dasyclados). J Plant Nutr Soil Sci 169׃ 516-522. http://dx.doi.org/10.1002/jpln.200521925

Caravaca F, Bareab JM, Palenzuelab J, Figueroa D, Alguacila MM, Roldána A, (2003) Establishment of shrub species in a degraded semiarid site after inoculation with native or allochthonous arbuscular mycorrhizal fungi. Appl Soil Ecol 22:103–111. http://dx.doi.org/10.1016/S0929-1393(02)00136-1

Castellano MA, Molina R (1989) Mycorrhizae. In: Landis TD, Tinus RW, McDonald SE, Barnett JP (eds.) The container tree nursery manual, Agricu handbk 674. USDA Forest Service, Washington DC, pp 101-167.

Chanway CP, Holl FB (1991) Biomass increase and associative nitrogen fixation of mycorrhizal Pinus contorta seedlings inoculated with a plant growth promoting Bacillus strain. Can J Bot 69: 507-511. http://dx.doi.org/10.1139/b91-069

Chanway CP (1997) Inoculation of tree roots with plant growth promoting soil bacteria: an emerging technology for reforestation. For Sci 43: 99-112.

Chanway CP, Shishido M, Nairna J, Jungwirth S, Markham J, Xiao G, Holl FB (2000) Endophytic colonization and field responses of hybrid spruce seedlings after inoculation with plant growth-promoting rhizobacteria. For Ecol Manage 133: 81-88. http://dx.doi.org/10.1016/S0378-1127(99)00300-X

Chodak M, Pietrzykowski M, Niklinska M (2009) Development of microbial properties in a chronosequence of sandy mine soils. Appl Soil Ecol 41: 259-268. http://dx.doi.org/10.1016/j.apsoil.2008.11.009

Colpaert JV, Van Tichelen KK, Van Assche JA, Van Laere A (1999) Short-term phosphorus uptake rates in mycorrhizal and non-mycorrhizal roots of intact Pinus sylvestris seedlings. New phytol 143: 589-597. http://dx.doi.org/10.1046/j.1469-8137.1999.00471.x

Dahm H (2005) Role of Mycorrhizae in Forestry. In: Rai MK (ed) Handbook of microbial biofertilizers. Food product press, New York, pp 241-270.

Davis AS, Jacobs DF (2005) Quantifying root system quality of nursery seedlings and relationship to outplanting performance. New Forest 30: 295–311. http://dx.doi.org/10.1007/s11056-005-7480-y

Dražić D (2002) Multifunkcionalna valorizacija predela i ekosistema stvorenih rekultivacijom odlagališta površinskih kopova Kolubarskog basena. Savezni sekretarijat za rad, zdravstvo i socijalno staranje, Sektor za životnu sredinu, Beograd.

Dominguez-Nu-ez JA, Medina M, Berrocal-Lobo M, Anriquez A, Albanesi A (2015) The combined effects of Pseudomonas fluorescens CECT 844 and the black truffle co-inoculation on Pinus nigra seedlings. iForest 8: 624-630. http://dx.doi.org/10.3832/ifor1334-007

Dominguez-Nu-ez JA, Delgado-Alvez D, Berrocal-Lobo M, Anriquez A, Albanesi A (2014) Controlled-release fertilizers combined with Pseudomonas fluorescens rhizobacteria inoculum improve growth in Pinus halepensis seedlings. iForest 8: 12-18. http://dx.doi.org/10.3832/ifor1110-007

Danilović M, Stojnić D, Vasiljević V, GaÄić D (2013) Biomass from Short Rotation Energy Plantations of Black Locust on Tailing Dump of »Field B« Open Pit in »Kolubara« Mining Basin. Nova meh Å¡umar 34: 11-19.

Egamberdiyeva E (2007) The effect of plant growth promoting bacteria on growth and nutrient uptake of maize in two different soils. Appl Soil Ecol 36: 184-189. http://dx.doi.org/10.1016/j.apsoil.2007.02.005

Fatemeh A, Masoud T, Pejman A, Aidin H (2014) Effect of plant growth promoting rhizobacteria (PGPRs) and stratification on germination traits of Crataegus pseudoheterophylla Pojark. Seeds. Sci Hortic 172: 61-67. http://dx.doi.org/10.1016/j.scienta.2014.03.049

Figueiredo MVB, Seldin L, Araujo FF, Mariano RLR (2010) Plant Growth Promoting Rhizobacteria: Fundamentals and Applications. In: Maheshwari DK (ed) Plant Growth and Health Promoting Bacteria, Microbiology Monographs 18, Springer-Verlag Berlin Heidelberg. pp 21-43. http://dx.doi.org/10.1007/978-3-642-13612-2_2

Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36. http://dx.doi.org/10.1111/j.1469-8137.2007.02191.x

Gamalero E, Berta G, Massa N, Glick B, Lingua G (2010) Interactions between Pseudomonas putida UW4 and Gigaspora rosea BEG9 and their consequences for the growth of cucumber under salt-stress conditions. J Appl Microbiol 108:236-245. http://dx.doi.org/10.1111/j.1365-2672.2009.04414.x

Golubović Ćurguz V, RaiÄević V, Veselinović M, Tabakovic-ToÅ¡ić M, Vilotić D (2012) Influence of Heavy Metals on Seed Germination and Growth of Picea abies L. Karst. Pol J Environ Stud 21Ë 353-359.

Golubović-ÄŒurguz V, Tabaković ToÅ¡ić M, Veselinović M, RaiÄević V, Dražić D, Jovanović Lj, Kiković D (2010a) The influence of heavy metals on the growth of ectomycorrhizal fungi. Minerva Biotechnol 22: 17-22.

Golubović Ćurguz V, RaiÄević V, Tabaković ToÅ¡ić M, Veselinović M, Jovanović Lj (2010b) Same physiological characteristics of the three ectomycorrhizal fungi from Suillus genus, Minerva Biotecnol, 22Ë 1-7.

Graf F, Frei M (2013) Soil aggregate stability related to soil density, root length, and mycorrhiza using site-specific Alnus incana and Melanogaster variegatus s.l. Ecol Eng 57: 314-323. http://dx.doi.org/10.1016/j.ecoleng.2013.04.037

Grobelak A, Napora A, Kacprzak M (2015) Using plant growth-promoting rhizobacteria (PGPR) to improve plant growth. Ecol Eng 84:22–28. http://dx.doi.org/10.1016/j.ecoleng.2015.07.019

GujaniÄić V, Golubović-Ćurguz V, RaiÄević V, Lalević B, Spasojević I, Kiković D (2012) Effects of biofertilization on spruce (Picea abies L.Karst) and pine seedlings (Pinus sylvestris L.) growth in deposol. In: Rakonjac Lj (ed) Proceedings of the International Scientific Conference Forests in future-sustainable use, risks and challenges. Belgrade (Serbia), 4-5 October 2012. Klik tim doo, Belgrade, pp 461-467.

Hao X, Xie P, Johnstone L, Miller SJ, Rensing C, Weia G (2012) Genome Sequence and Mutational Analysis of Plant-Growth-Promoting Bacterium Agrobacterium tumefaciens CCNWGS0286Isolated from a Zinc-Lead Mine Tailing. Appl Environ Microbiol 78: 5384-5394. http://dx.doi.org/10.1128/AEM.01200-12

Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60:579-598. http://dx.doi.org/10.1007/s13213-010-0117-1

Huang Y, Chen Y, Tao S (2000) Effect of rhizospheric environment of VA-mycorrhizal plants on forms of Cu, Zn, Pb and Cd in polluted soil. Ying Yong Sheng Tai Xue Bao 11: 431-434.

Inglis GD, Kawchuk L M (2002) Comparative degradation of oomycete, ascomycete, and basidiomycete cell walls by mycoparasitic and biocontrol fungi. Can J Microbiol 48: 60-70. http://dx.doi.org/10.1139/w01-130

Isajev V, Ivetić V, Vukin M (2006) Namenska proizvodnja sadnog materijala za pošumljavanja u zaštitnim šumama kitnjaka, sladuna i cera. Šumarstvo 3: 141-148.

Isajev V, Mataruga M, Rakonjac Lj, IvetićV (2010) Specific-purpose production and the development of technological process of tree and shrub planting stock production. In: Rakonjac Lj (ed) Plenary Lectures of the International Scientific Conference Forest Ecosystem and Climate Changes, Belgrade (Serbia), 9-10 March 2010. Institute of Forestry, Belgrade pp. 47-55.

Izumi H, Anderson IC, Alexander IJ, Killham K, Moore ER (2006) Endobacteria in some ectomycorrhiza of Scots pine (Pinus sylvestris). FEMS Microbiol Ecol 56:34–43. http://dx.doi.org/10.1111/j.1574-6941.2005.00048.x

Jacob C, Courbot M, Brun A, Steinman HM, Jacquot JP, Botton B, Chalot M (2001) Molecular cloning characterization and regulation by cadmium of a superoxide dismutase from the ectomycorrhizal fungus Paxillus involutus. Eur J Biochem 268: 3223-32. http://dx.doi.org/10.1046/j.1432-1327.2001.02216.x

Jafari TH, Jarak M, Äurić S, Stamenov D, Orlović S (2014) The effects of microbial inocula on the growth of black locust, Siberian elm and silver maple seedlings. Matica Srpska J Nat Sci 127:15-22. http://dx.doi.org/10.2298/ZMSPN1427015H

Jakovljević M, Lilić N, Kolonja B, Knežević D, Petrić M, Tadić V, Nedić M (2015) Biomass production as renewable energy resource at reclaimed Serbian lignite open-cast mines. Term Sci 19: 823-835. http://dx.doi.org/10.2298/tsci140626014j

Ji X, Lu G, Gai Y, Gao H, Lu B, Kong L, Mu Z (2010) Colonization of Morus alba L. by the plantgrowth-promoting and antagonistic bacterium Burkholderia cepacia strain Lu10-1. BMC Microbiology 10:243. http://dx.doi.org/10.1186/1471-2180-10-243

Jing Y, He Z, Yang X (2007) Role of soil Rhizobacteria in phytoremediation of heavy metal contaminated soils. J Zhejiang Univ Sci B 8: 192-207. http://dx.doi.org/10.1631/jzus.2007.B0192

JoviÄić Petrović J, Danilović G, ĆurÄić N, Milinković M, StoÅ¡ić N, Panković D, RaiÄević V (2014) Copper tolerance of Trichoderma species. Arch Biol Sci 66: 137-142. http://dx.doi.org/10.2298/ABS1401137J

Karen O (1997) Effects of Air Pollution and Forest Regeneration Methods on the Community Structure of Ectomycorrhizal Fungi. Dissertation, Swedish University of Agricultural Sciences.

KarliÄić V, Radić D, JoviÄić Petrović J, Golubović-Ćurguz V, Kiković D, RaiÄević V (2015) Inoculation of Robinia pseudoacacia L. and Pinus sylvestris L. seedlings with plant growth promoting bacteria causes increased growth in coal mine overburden. In: Ivetić V, Stanković D (ed) Proceedings of the International conference Reforestation Challenges. Belgrade (Serbia), 03-06 June 2015. Reforesta, Belgrade, pp 42-49.

Karlidag H, Esitken A, Turan M, Sahin F (2007) Effects of root inoculation of plant growth promoting rhizobacteria (PGPR) on yield, growth and nutrient element contents of leaves of apple. Sci Hortic 114:16-20. http://dx.doi.org/10.1016/j.scienta.2007.04.013

Kavamura VN, Esposito E (2008) Biotechnological strategies applied to the decontamination of soils polluted with heavy metals. Biotechnol Adv 28: 61-69. http://dx.doi.org/10.1016/j.biotechadv.2009.09.002

Kieliszewska Rokicka B, Kurczynska EU, Leski T (2000) Physiological activity of ectomycorrhiyas in a moderately polluted forest (Ratanica catchment, southern Poland). Dendrobiology 45: 47-59.

Kirk JL, Beaudette LA, Hart M, Moutoglis P, Klironomos JN, Lee H, Trevors JT (2004) Methods of studying soil microbial diversity. J Microbiol Methods 58: 169-188. http://dx.doi.org/10.1016/j.mimet.2004.04.006

Kurth K, Zeitler K, Feldhahn L, Neu TR, Weber T, Krištůfek V, Wubet T, Herrmann S, Buscot F, Tarkka MT(2013) Detection and quantification of a mycorrhization helper bacterium and a mycorrhizal fungus in plant-soil microcosms at different levels of complexity. BMC Microbiology 13: 205. http://dx.doi.org/10.1186/1471-2180-13-205

Lalević B, RaiÄević V, Kiković D, Jovanović Lj, Å urlan-Momirović G, Jović J, Talaie AR, Morina F (2012) Biodegradation of MTBE by Bacteria Isolated from oil Hydrocarbons-Contaminated Environments. Int J Environ Res 6: 81-86.

Landis TD (2011) The target plant concept. A history and brief overview. USDA Forest Service, Rocky Mountain Research Station, Fort Collins, CO.

Lingua G, Bona E, Manassero P, Marsano F, Todeschini V, Cantamessa S, Copetta A, D'Agostino G, Gamalero E, Berta G (2013) Arbuscular Mycorrhizal Fungi and Plant Growth-Promoting Pseudomonads Increases Anthocyanin Concentration in Strawberry Fruits (Fragaria x ananassa var. Selva) in Conditions of Reduced Fertilization. Int J Mol Sci 14: 16207-16225. http://dx.doi.org/10.3390/ijms140816207

Lucy M, Reed E, Glick BR (2004) Applications of free living plant growth-promoting rhizobacteria. Antonie van Leeuwenhoek 86: 1–25. http://dx.doi.org/10.1023/B:ANTO.0000024903.10757.6e

Lugtenberg BJJ, Dekkers LC (1999) What makes Pseudomonas bacteria rhizosphere competent. Environ Microbiol 1:9-13. http://dx.doi.org/10.1046/j.1462-2920.1999.00005.x

Lux HB, Cumming JR (2001) Mycorrhizae confer aluminium resistance to tulip-poplar seedlings. Can J For Res. 31: 694-702. http://dx.doi.org/10.1139/cjfr-31-4-694

Mafia RG, Alfenas AC, Ferreira EM, Binoti DHB, Machado G, Mafia V, Mounteer AH (2009) Root colonization and interaction among growth promoting rhizobacteria isolates and Eucalyptus species. Rev Ãrvore 33:1-9. http://dx.doi.org/10.1590/S0100-67622009000100001

Maiti SK (2007) Bioreclamation of coalmine overburden dumps-with special empasis on micronutrients and heavy metals accumulation in tree species. Environ Monit Assess 125: 111-122. http://dx.doi.org/10.1007/s10661-006-9244-3

Marx DH, Marrs LF, Cordell CE (2002) Practical use of the mycorrhizal fungal technology in forestry, reclamation, arboriculture and horticulture. Dendrobiology 47: 27-40.

Marx DH, Ruehle J L, Cordell CE (1991) Methods for studying nursery and field response of trees to specific ectomycorrhiza. In: Norris JR, Read DJ, Varma AK (eds.) Methods in microbiology. Academic Press, London, pp 383-411. http://dx.doi.org/10.1016/s0580-9517(08)70187-9

Mehta P, Walia A, Kulshrestha S, Chauhan A, Shirkot CK (2015) Efficiency of plant growth-promoting P-solubilizing Bacillus circulans CB7 for enhancement of tomato growth under net house conditions. J Basic Microbiol 55: 33-44. http://dx.doi.org/10.1002/jobm.201300562

Mirić M, Popović Z (2003) An improved method laboratorial investigation of interaction and or antagonism of fungi at the same nutritive substrate. Proceedings of the International scientific conference "50 years of the Faculty of Forestry" Sofia (Bulgaria), 1-5 October 2003 Faculty of Forestry, Sofia, pp 181-185.

Münzenberger B, Golldack J, Ullrich A, Schmincke B, Hüttl R F (2004) Abundance, diversity, and vitality of mycorrhizae of Scots pine (Pinus sylvestris L.) in lignite recultivation sites. Mycorrhiza 14׃193-202. http://dx.doi.org/10.1007/s00572-003-0257-2

Nadeem SM, Ahmad M, Zahir ZA, Javaid A, Ashraf M (2014) The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnol Adv 32:429–448. http://dx.doi.org/10.1016/j.biotechadv.2013.12.005

Ortas I (2003) Effect of Selected Mycorrhizal Inoculation on Phosphorus Sustainability in Sterile and Nonsterile Soils in the Harran Plain in South Anatolia. J Plant Nutr 26׃ 1-17. http://dx.doi.org/10.1081/PLN-120016494

ParladÄ— J, Pera J, Luque J (2004) Evaluation of mycelial inocula of edible Lactarius species for the production of Pinus pinaster and P. sylvestris mycorrhizal seedlings under greenhouse conditions. Mycorrhiza 14: 171-176. http://dx.doi.org/10.1007/s00572-003-0252-7

Pereira SIA, Castro PML (2014) Phosphate-solubilizing rhizobacteria enhance Zea mays growth in agricultural P-deficient soils. Ecol Eng 73: 526 535. http://dx.doi.org/10.1016/j.ecoleng.2014.09.060

Perry DA, Amaranthus MP, Borchers SL, Brainerd R (1989) Bootstrapping in ecosystem. Bioscience 39: 230-37. http://dx.doi.org/10.2307/1311159

PetriÄević J, GujaniÄić V, Radić D, Božić M, Rudić Ž, RaiÄević V, Lalević B (2012) The possibility of using macrophytes in Palic Lake sediment remediation. Arch of biol sci 64: 1481-1486. http://dx.doi.org/10.2298/ABS1204481P

Plamboeck AH, Dawson TE, Egerton Warburton LM, North M, Bruns TD, Querejeta JI (2007) Water transfer via ectomycorrhizal fungal hyphae to conifer seedlings. Mycorrhiza 17׃ 439-447. http://dx.doi.org/10.1007/s00572-007-0119-4

Priha O (1999) Microbial activities in soils under Scots pine, Norway spruce and silver birch. Dissertation, University of Helsinki.

Probanza A, Lucas Garc´ıa JA, Ruiz Palomino M, Ramos B, Gutiérrez Ma-ero FJ (2002) Pinus pinea L. seedling growth and bacterial rhizosphere structure after inoculation with PGPR Bacillus (B. licheniformis CECT 5106 and B. pumilus CECT 5105). Appl Soil Ecol 20:75–84. http://dx.doi.org/10.1016/S0929-1393(02)00007-0

Puhe J (2003) Growth and development of the root system of Norway spruce (Picea abies) in forest stands-a rewiew. For Ecol Manage 175: 253-73. http://dx.doi.org/10.1016/S0378-1127(02)00134-2

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. Microb Ecol 41: 140-148. http://dx.doi.org/10.1007/s002480000081

Puente ML, Garcia JE, Pathauer P, Perticari A (2010) Inoculation with Azospirillum brasilience is a Useful Tool in Eucalyptus globules Management. Am Eurasian J Agric Environ Sci 8:124-130.

Qurashi AW, Sabri AN (2012) Bacterial exopolysaccharide and biofilm formation stimulate chickpea growth and soil aggregation under salt stress. Braz J Microbiol 1183-1191. http://dx.doi.org/10.1590/S1517-83822012000300046

Radić D, GujaniÄić V, PetriÄević J, RaiÄević V, Lalević B, Rudić Ž, Božić M (2013) Macrophytes as remediation technology in improving Ludas lake sediment. Fresenius Environmental Bulletin 22: 1787-1791.

Rakić A, Filipović V, Rakić I, Racić Z, Vasiljević V, Obradović D (2011). Rekultivacija odlagaliÅ¡ta pepela i Å¡ljake PD RB Kolubara i TE Veliki Crljeni – IzvoÄ‘enje radova na terenu. In: Ignjatović MR (ed) Proceedings of the II International Symposium MINING 2011- Mining present state and future prospects and sustainable developement. VrnjaÄka Banja (Serbia), 10-13 May 2011. Privredna komora Srbije, Beograd, Srbija, pp 552-555.

RaiÄević V, Antić Mladenović S, Lalević B, Golić Z, Jovanović Lj, Kiković D (2006) MikrobioloÅ¡ka aktivnost nerekultivisanih povrÅ¡ina povrÅ¡inskih kopova Kolubara. Energija 1-2: 94-96.

RaiÄević V, Lalević B, Kljujev I, Petrović J (2010) EkoloÅ¡ka mikrobiologija. Poljoprivredni fakultet, Beograd

Rigamonte TA, Pylro VS, Duarte GF (2010) The role of mycorrhization helper bacteria in the establishment and action of ectomycorrhizae associations. Braz J Microbiol 41: 832-840. http://dx.doi.org/10.1590/S1517-83822010000400002

Rincon 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 Physiol. 28: 1693-1701. http://dx.doi.org/10.1093/treephys/28.11.1693

Rodrigez H, Fraga R, Gonzalez T, Bashan Y (2006) Genetics of phosphate solubilization and its potential applications for improving plant growth-promoting bacteria. Plant Soil 287: 15-21. http://dx.doi.org/10.1007/s11104-006-9056-9

Rose R, Campbell SJ, Landis TD (1990) Target seedling concept. In: Rose R, Campbell SJ, Landis TD (eds) Proceedings of the Target seedling symposium. Rosenburg (Oregon), 13-17 August 1990. USDA Forest Service General Technical Report RM-200, pp 1-8.

Rudawska M, Kieliszewska Rokicka B, Leski T (2000) Effect of aluminium on Pinus sylvestris seedlings mycorrhizal with aluminium-tolerant and aluminium-sensitive strains of Suillus luteus. Dendrobiology 45: 89-96.

Shilev S, López AF, Prieto MS, Puebla EDS (2007). Induced protein profile changes in arsenate tolerant and sensitive Pseudomonas fluorescens strains. J Environ Eng Land Manag 15: 221-226.

Smith S, Read D (2008) Mycorrhizal Symbiosis, 3rd edn. Academic Press, San Diego.

Sousa NR, Franco AR, Ramos MA, Oliveira RS, Castro PML (2015) The response of Betula pubescens to inoculation with an ectomycorrhizal fungus and a plant growth promoting bacterium is substrate-dependent. Ecol Eng 81: 439-443. http://dx.doi.org/10.1016/j.ecoleng.2015.04.024

Spaepen S, Vanderleyden J, Okon Y (2009) Plant Growth-promoting actions of rhizobacteria. In: Kader JC, Delseny M (eds) Advances in Botanical Research. Academic Press, pp 283-320.

Tilak KVBR, Ranganayaki N, Pal KK, De R, Saxena AK, Shekhar Nautiyal C, Mittal S, Tripathi AK, Johri BN (2005) Diversity of plant growth and soil health supporting bacteria. Curr Sci 89: 136-150.

Tischew S, Kirmer A, Lorenz A (2008) Alternative restoration strategies in former lignite mining areas of eastern Germany. In: Barthlott W, Linsenmair KE, Porembski S (eds) Biodiversity: Structure and Function, Eolss Publishers, Paris, pp 1-10.

Totola MR, Borges AC (2000) Growth and nutritional status of brazilian wood species Cedrella fissilis and Anadenanthera peregrina in bauxite spoil in response to arbuscular mycorrhizal inoculation and substrate amendment. Braz J Mycrob 31׃ 257-265. http://dx.doi.org/10.1590/s1517-83822000000400004

Tredici P (2008) Disturbance ecology and symbiosis in mine-reclamation design. In: Berger A (ed) Designing the reclaimed landscape. Taylor & Francis, UK, pp 13-25.

Veselinović M, Dražić D, Golubović Ćurguz V, Čule N, Mitrović S, Nikolić B, Rakonjac Lj (2010) Planting material production for biological recultivation of deposols. In: Dražić, G. (ed) Proceedings of International Conference: Degraded areas & ecoremediation, Belgrade (Serbia), 21- 22 May 2010. Faculty of applied ecology Futura, Belgrade pp 283-295.

Veselinović M, Golubović-Ćurguz V (2001) Recultivation by afforestation of deposols. Zemljište i biljka 50: 201-210.

Vessey KJ (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255: 571-586. http://dx.doi.org/10.1023/A:1026037216893

Vieira FCS, Nahas E (2005) Comparison of microbial numbers in soils by using various culture media and temperatures. Microbiol Res 160: 197-202. http://dx.doi.org/10.1016/j.micres.2005.01.004

VrbniÄanin S, Jovanović, L, Božić D, RaiÄević V, Pavlović D (2008) Germination of Iva xanthifolia, Amaranthus retroflexus and Sorghum halepense under media with microorganisms. Journal of Plant Deseases and Protection, XXI, 297-302.

Whipps JM (2001) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487-511. http://dx.doi.org/10.1093/jexbot/52.suppl_1.487

Živanović Miljković J, Džunić G (2013) Land Use in Large Mining Basins in Post-Exploitation Period: The Example of Serbia. In: Efe R, Atalay I, Cürebal I (eds) Proceedings of the 3rd International Geography Symposium – GEOMED. Kemer (Turkey), 10-13 June 2013. Kemer, pp 292-299.

Zuberer DA, Wollum AG (2004) Introduction and Historical Perspective. In: Sylvia DM, Fuhrmann JJ, Hartel PG, Zuberer DA (eds) Principles and applications of soil microbiology, 2nd edition, Prentice Hall, New Jersey, pp 3-25.

Published
2016-06-05
How to Cite
Karličić, V., Golubović Ćurguz, V., & Raičević, V. (2016). The alleviation of reforestation challenges by beneficial soil microorganisms. REFORESTA, 1(1), 238-260. https://doi.org/10.21750/REFOR.1.12.12