Skip to main content

Advertisement

Log in

Microbiological process in agroforestry systems. A review

  • Review paper
  • Published:
Agronomy for Sustainable Development Aims and scope Submit manuscript

Abstract

Soils around the world are degraded due to inappropriate management practices. There is thus the necessity to find more conservationist agricultural systems. Agroforestry system is an alternative system that helps prevent land degradation while allowing continuing use of land to produce crops and livestock on a sustainable basis. Agroforestry system is a form of sustainable land use that combines trees and shrubs with crops and livestock in ways that increase and diversify farm and forest production while also conserving natural resources. This system enhances organic carbon accumulation in soils by the inclusion of cover crops and permanent vegetation, which is expected to increase the soil microbial biomass. The use of microorganisms aims at improving nutrient availability for plants. Currently, there is an emerging demand to decrease the dependence on chemical fertilizers and achieve sustainable agriculture and agroforestry. Arbuscular mycorrhizal fungi, plant growth-promoting rhizobacteria, and the association of rhizobia with leguminous plants are mutualistic symbioses of high economic importance for increasing agricultural production. The biological nitrogen fixation (BNF) process is an economically attractive and ecologically sound method to reduce external nitrogen input and improve the quality and quantity of internal resources. BNF by associative diazotrophic bacteria is a spontaneous process where soil nitrogen is limited and adequate carbon sources are available. However, the ability of these bacteria to contribute to increased crop yields is only partly a result of BNF. The successful use of legumes is dependent upon appropriate attention to the formation of effective symbioses with root nodule bacteria. An essential component for increasing the use of legumes is the integration of plant breeding and cultivar development, with appropriate research leading to the selection of elite strains of root nodule bacteria. An expansion of the utility of inoculants is also necessary to develop a broad conceptual framework and methodology that is supported by scientific arguments; it is destined to impact assessment of the use of new biological products in agriculture.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Aguilar OM, López MV, Riccillo PM (2001) The diversity of rhizobia nodulating beans in Northwest Argentina as a source of more efficient inoculant strains. J Biotech 91:181–188

    Article  CAS  Google Scholar 

  • Albareda M, Rodriguez-Navarro DN, Camacho M, Temprano FJ (2008) Alternatives to peat as a carrier for rhizobia inoculants: solid and liquid formulations. Soil Biol Biochem 40:2771–2779

    Article  CAS  Google Scholar 

  • Alberton O, Kaschuk G, Hungria M (2006) Sampling effects on the assessment of genetic diversity of rhizobia associated with soybean and common bean. Soil Biol Biochem 38:1298–1307

    Article  CAS  Google Scholar 

  • Albrecht A, Kandji ST (2003) Carbon sequestration in tropical agroforestry systems. Agric Ecosyst Environ 99:15–27

    Article  CAS  Google Scholar 

  • Alexandre A, Laranjo M, Oliveira S (2006) Natural populations of chickpea rhizobia evaluated by antibiotic resistance profiles and molecular methods. Microb Ecol 51:128–136

    Article  PubMed  CAS  Google Scholar 

  • Alexandre A., Brígido C., Laranjo M., Rodrigues S., Oliveira S. (2009) Survey of Chickpea Rhizobia Diversity in Portugal Reveals the Predominance of Species Distinct from Mesorhizobium ciceri and Mesorhizobium mediterraneum. Microb Ecol 1–12. doi:10.1007/s00248-009-9536-6.

  • Almeida EF, Polizel RPH, Gomes LC, Xavier FA, Mendonça ES (1997) Biomassa microbiana em sistemas agroflorestais na zona da mata mineira. Rev Bras Agroecol 2:739–742

    Google Scholar 

  • Andrade G, Mihara KL, Linderman RG, Bethlenfalvay GJ (1998) Soil aggregation status and rhizobacteria in the mycorrhizosphere. Plant Soil 202:89–96

    Article  CAS  Google Scholar 

  • Andronov EE, Roumyantseva ML, Sagoulenko VV, Simarov BV (1999) Effect of the host plant on the genetic diversity of a natural population of Sinorhizobium meliloti. Russian J Genet 35:1169–1176

    CAS  Google Scholar 

  • Anyango B, Wilson KJ, Beynon JL, Giller KE (1995) Diversity of rhizobia nodulating Phaseolus vulgaris L. in two Kenyan soils with contrasting pHs. App Env Microb 61:4016–4021

    CAS  Google Scholar 

  • Araújo ASF, Monteiro RTR (2006) Microbial biomass and activity in a Brazilian soil plus untreated and composted textile sludge. Chemosphere 64:1043–1046

    Article  PubMed  CAS  Google Scholar 

  • Araújo ASF, Monteiro RTR, Abarkeli RB (2003) Effect of glyphosate on the microbial activity of two Brazilian soils. Chemosphere 52:799–804

    Article  PubMed  CAS  Google Scholar 

  • Araújo FB, Hungria M (1999) Nodulação e rendimento de soja co-infectada com Bacillus subtilis e Bradyrhizobium japonicum/Bradyrhizobium elkanii. Pesq Agropec Bras 34:1633–1643

    Article  Google Scholar 

  • Aysan E, Demir S (2009) Using arbuscular mycorrhizal fungi and Rhizobium leguminosarum, Biovar Phaseoli Against Sclerotinia sclerotiorum (Lib.) de bary in the common bean Phaseolus vulgaris L. Plant Pathol J 8:74–78

    Article  Google Scholar 

  • Bai YM, Zhou XM, Smith DL (2003) Enhanced soybean plant growth resulting from coinoculation of Bacillus strains with Bradyrhizobium japonicum. Crop Sci 43:1774–1781

    Article  Google Scholar 

  • Bala A, Giller KE (2006) Relationships between rhizobial diversity and host legume nodulation and nitrogen fixation in tropical ecosystems. Nut Cycl Agroecosys 76:319–330

    Article  Google Scholar 

  • Bala A, Murphy P, Giller KE (2002) Occurrence and genetic diversity of rhizobia nodulating Sesbania sesban in African soils. Soil Biol Biochem 34:1759–1768

    Article  CAS  Google Scholar 

  • Bala A, Murphy P, Giller KE (2003a) Distribution and diversity of rhizobia nodulating agroforestry legumes in soils from three continents in the tropics. Mol Ecol 12:917–929

    Article  PubMed  CAS  Google Scholar 

  • Bala A, Murphy PJ, Osunde AO, Giller KE (2003b) Nodulation of tree legumes and the ecology of their native rhizobial populations in tropical soils. App Soil Ecol 22:211–223

    Article  Google Scholar 

  • Balachandar D, Raja P, Kumar K, Sundaram SP (2007) Non-rhizobial nodulation in legumes. Biotech Mol Biol Rev 2:49–57

    Google Scholar 

  • Barea JM, Azcon R, Azcon-Aguilar C (1992) Vesicular–arbuscular mycorrhizal fungi in nitrogen-fixing systems. In: Norris JR, Read DJ, Varma AK (eds) Methods in microbiology. Academic, London, pp 391–416

    Google Scholar 

  • Barea JM, Azcon R, Azcon-Aguilar C (2002) Mycorrhizosphere interactions to improve plant fitness and soil quality. Antonie van Leeuwenhoek Inter J Gen Mol Microbiol 81:343–351

    Article  CAS  Google Scholar 

  • Barea JM, Azcon R, Azcon-Aguilar C (2004) Mycorrhizal fungi and plant growth promoting rhizobacteria. In: Varma A, Abbott L, Werner D, Hampp R (eds) Plant surface microbiology. Springer, Heidelberg, pp 351–371

    Google Scholar 

  • Barea JM, Werner D, Azcon-Aguilar C, Azcon R (2005) Interactions of arbuscular mycorrhiza and nitrogen fixing simbiosis in sustainable agriculture. In: Werner D, Newton WE (eds) Agriculture, forestry, ecology and the environment. Kluwer, The Netherlands

    Google Scholar 

  • Barreto PAB, Gama-Rodrigues EF, Gama-Rodrigues AC, Fontes AG, Polidoro JC, Moço MKS, Machado RCR, Baligar VC (2010) Distribution of oxidizable organic C fractions in soils under cacao agroforestry systems in Southern Bahia, Brazil. Agrofor Sys doi:10.1007/s10457-010-9300-4

  • Barrett CF, Parke MA (2005) Prevalence of Burkholderia sp. nodule symbionts on four mimosoid legumes from Barro Colorado Island. Panama Syst App Microbiol 28:57–65

    Article  CAS  Google Scholar 

  • Barrett CF, Parke MA (2006) Coexistence of Burkholderia, Cupriavidus, and Rhizobium sp. nodule bacteria on two Mimosa spp. in Costa Rica. Appl Environ Microbiol 72:1198–1206

    Article  PubMed  CAS  Google Scholar 

  • Bashan Y, Salazar B, Puente ME (2009) Responses of native legume desert trees used for reforestation in the Sonoran Desert to plant growth-promoting microorganisms in screen house. Biol Fert Soils 45:655–662

    Article  Google Scholar 

  • Belsky AJ, Amundson RG, Duxbury JM (1989) The effects of trees on their physical, chemical and biological environments in a semi-arid savanna in Kenya. J App Ecol 26:1005–1024

    Article  Google Scholar 

  • Ben RF, Prévost D, Yezza A, Tyagi RD (2007) Agro-industrial waste materials and wastewater sludge for rhizobium inoculant production: a review. Biores Tech 98:3535–3546

    Article  CAS  Google Scholar 

  • Benata H, Mohammed O, Noureddine B, Abdelbasset B, Abdelmoumen H, Muresu R, Squartini A, Idrissi MME (2008) Diversity of bacteria that nodulate Prosopis juliflora in the eastern area of Morocco. Syst App Microbiol 31:378–386

    Article  CAS  Google Scholar 

  • Benhizia Y, Benhizia H, Benguedouar A, Muresu R, Giacomini A, Squartir A (2004) Gamma proteobacteria can nodulate legumes of the genus Hedysarum. Syst Appl Microbiol 27:462–468

    Article  PubMed  CAS  Google Scholar 

  • Bontemps C, Elliott GN, Simon MF, Reis Júnior FB, Gross E, Lawton RC, Elias NN, Loureiro MF, De Faria SM, Sprent JI, James EK, Young JPW (2009) Burkholderia species are ancient symbionts of legumes. Mol Ecol 19:44–52

    Article  PubMed  CAS  Google Scholar 

  • Bowen GD, Rovira AD (1991) The rhizosphere. The hidden half of the hidden half. In: Waisel Y, Eshel A, Kafkafi U (eds) Plant roots: the hidden half. Marcel Dekker, New York, pp 641–669

    Google Scholar 

  • Bressiani JA (2001). Seleção sequencial em cana-de-açúcar Agronomy—Plant Breed. Genet. USP, Piracicaba, pp 159

  • Brockman FJ, Bezdicek DF (1989) Diversity within serogroups of Rhizobium leguminosarum biovar viceae in the Palouse region of eastern Washington as indicated by plasmid profiles, intrinsic antibiotic resistance, and topography. App Env Microb 55:109–115

    CAS  Google Scholar 

  • Brookes PC (2001) The soil microbial biomass: concept, measurement and applications in soil ecosystem research. Microbes Environ 16:131–140

    Article  Google Scholar 

  • Browaldh M (1997) Change in soil mineral nitrogen and respiration following tree harvesting from an agrisilvicultural system in Sweden. Agrofor Sys 35:131–138

    Article  Google Scholar 

  • Caballero-Mellado J, Martinez-Romero E (1999) Soil fertilization limits the genetic diversity of Rhizobium in bean nodules. Symbiosis 26:111–121

    Google Scholar 

  • Cacho O (2001) An analysis of externalities in agroforestry systems in the presence of land degradation. Ecol Econ 39:131–143

    Article  Google Scholar 

  • Cardoso MI, Kuyper TW (2006) Mycorrhizas and tropical soil fertility. Agric Ecosys Environ 116:72–84

    Article  Google Scholar 

  • Catroux G, Hartmann A, Revellin C (2001) Trends in rhizobial inoculant production and use. Plant Soil 230:21–30

    Article  CAS  Google Scholar 

  • Ceccon E (2008) Production of bioenergy on small farms: a two-year agroforestry experiment using Eucalyptus urophylla intercropped with rice and beans in Minas Gerais, Brazil. New For 35:285–298

    Article  Google Scholar 

  • Chander K, Goyal S, Nandal DP, Kapoor KK (1998) Soil organic matter, microbial biomass and enzyme activities in a tropical agroforestry system. Biol Fertil Soils 27:168–172

    Article  CAS  Google Scholar 

  • Chebotar VK, Asis CA, Akao S (2001) Production of growthpromoting substances and high colonization ability of rhizobacteria enhance the nitrogen fixation of soybean when inoculated with Bradyrhizobium japonicum. Biol Fert Soils 34:427–432

    CAS  Google Scholar 

  • Chen W, De Faria SM, Straliotto R, Pitard RM, Simões-Araújo JL, Chou J, Chou Y, Barrios E, Prescott AR, Elliott GN, Sprent JI, Young PW, James EK (2005) Proof that Burkholderia strains form effective symbioses with legumes: a study of novel mimosa-nodulating strains from South America. App Environ Microbiol 71:7461–7471

    Article  CAS  Google Scholar 

  • Chen W-M, Laevens S, Lee TM, Coenye T, de Vos P, Mergeay M, Vandamme P (2001) Ralstonia taiwanensis sp. nov., isolated from root nodules of Mimosa species and sputum of a cystic fibrosis patient. Int J Syst Evol Microbiol 51:1729–1735

    Article  PubMed  CAS  Google Scholar 

  • Chen WM, Moulin L, Bontemps C, Vandamme P, Béna G, Boivin-Masson C (2003) Legume symbiotic nitrogen fixation by β-Proteobacteria is widespread in nature. J Bacteriol 185:7266–7272

    Article  PubMed  CAS  Google Scholar 

  • Chen WM, Faria SM, Chou JH, James EK, Elliott GN, Sprent JI, Bontemps C, Young JPW, Vandamme P (2008) Burkholderia sabiae sp nov., isolated from root nodules of Mimosa caesalpiniifolia. Int J Syst Evol Microbiol 58:2174–2179

    Article  PubMed  CAS  Google Scholar 

  • Chesney P (2008) Nitrogen and fine root length dynamics in a tropical agroforestry system with periodically pruned Erythrina poeppigiana. Agrofor Sys 72:149–159

    Article  Google Scholar 

  • Chikowo R, Mapfumo P, Leffelaar PA, Giller KE (2006) Integrating legumes to improve N cycling on smallholder farms in sub-humid Zimbabwe: resource quality, biophysical and environmental limitations. Nut Cycl Agroecosys 76:219–231

    Article  Google Scholar 

  • Collins MT, Thies JE, Abbott LK (2002) Diversity and symbiotic effectiveness of Rhizobium leguminosarum bv. trifolii isolates from pasture soils in south-western Australia. Austr J Soil Res 40:1319–1329

    Article  Google Scholar 

  • Daba S, Haile M (2000) Effects of rhizobial inoculant and nitrogen fertilizer on yield and nodulation of common bean. J Pl Nut 23:581–591

    Article  CAS  Google Scholar 

  • Dashti N, Zhang F, Hynes R, Smith DL (1998) Plant growth promoting rhizobacteria accelerate nodulation and increase nitrogen fixation activity by field grown soybean [Glycine max (L.) Merr.] under short season conditions. Plant Soil 2:205–213

    Article  Google Scholar 

  • Date RA (1997) The contribution of R&D on root-nodule bacteria to future cultivars of tropical forage legumes. Trop Grass 31:350–354

    Google Scholar 

  • Date RA (2000) Inoculated legumes in cropping systems of the tropics. Field Crops Res 65:123–136

    Article  Google Scholar 

  • Daudin D, Sierra J (2008) Spatial and temporal variation of below-ground N transfer from a leguminous tree to an associated grass in an agroforestry system. Agric Ecosys Environ 126:275–280

    Article  CAS  Google Scholar 

  • De Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795–811

    Article  PubMed  CAS  Google Scholar 

  • Deaker R, Roughley RJ, Kennedy IR (2004) Legume seed inoculation technology—a review. Soil Biol Biochem 36:1275–1288

    Article  CAS  Google Scholar 

  • Demir S, Akkopru A (2007) Using of arbuscular mycorrhizal fungi (AMF) for biocontrol of soil-borne fungal plant pathogens. In: Chincholkar SB, Mukerji KG (eds) Biological control of plant diseases. Haworth Press, USA, pp 17–37

    Google Scholar 

  • Diabate M, Munive A, Faria SM, Ba A, Dreyfus B, Galiana A (2005) Occurrence of nodulation in unexplored leguminous trees native to the West African tropical rainforest and inoculation response of native species useful in reforestation. New Phytol 166:231–239

    Article  PubMed  Google Scholar 

  • Dick RP (1997) Soil enzymes activities as integrative indicator of soil health. In: Pankhurst C, Doube BM, Gupta VVSR (eds) Biological indicators of soil health. CAB International, Cambridge, pp 121–156

    Google Scholar 

  • Diouf D, Samba-Mbaye R, Lesueur D, Ba AT, Dreyfus B, De Lajudie P, Neyra M (2007) Genetic diversity of Acacia seyal Del. rhizobial populations indigenous to senegalese soils in relation to salinity and pH of the sampling sites. Micro Ecol 54:553–566

    Article  CAS  Google Scholar 

  • Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149

    Article  CAS  Google Scholar 

  • Doignon-Bourcier F, Sy A, Willems A, Torck U, Dreyfus B, Gillis M, De Lajudie P (1999) Diversity of Bradyrhizobia from 27 tropical Leguminosae species native of Senegal. Syst App Microbiol 22:647–661

    Article  Google Scholar 

  • Doyle JJ, Doyle J (1998) Phylogenetic perspectives on nodulation: evolving views of plants and symbiotic bacteria. Trends Plant Sci 3:473–478

    Article  Google Scholar 

  • Duodu S, Nsiah EK, Bhuvaneswari TV, Svenning MM (2006) Genetic diversity of a natural population of Rhizobium leguminosarum biovar trifolii analysed from field nodules and by a plant infection technique. Soil Biol Biochem 38:1162–1165

    Article  CAS  Google Scholar 

  • Duodu S, Carlsson G, Huss-Danell K, Svenning MM (2007) Large genotypic variation but small variation in N2 fixation among rhizobia nodulating red clover in soils of northern Scandinavia. J App Microbiol 102:1625–1635

    Article  CAS  Google Scholar 

  • Elliott GN, Chou J-H, Chen W-M, Bloemberg GV, Bontemps C, Martinez-Romero E, Velazquez E, Young JPW, Sprent JI, James EK (2009) Burkholderia spp. are the most competitive symbionts of Mimosa, particularly under N-limited conditions. Environ Microbiol 11:762–778

    Article  PubMed  Google Scholar 

  • Fagerli IL, Svenning MM (2005) Arctic and subarctic soil populations of Rhizobium leguminosarum biovar trifolii nodulating three different clover species: characterisation by diversity at chromosomal and symbiosis loci. Pl Soil 275:371–381

    Article  CAS  Google Scholar 

  • FAO (2005) The importance of soil organic matter. Key to drought-resistant soil and sustained food and production. Rome, p 78

  • Faria S.M. (1997) Obtenção de Estirpes de Rizóbio Eficientes na Fixação Biológica de Nitrogênio para Espécies Florestais. (Aproximação 1997). Embrapa Agrobiologia, Serop‚dica, p 4

  • Faria SM (2000) Obtenção de estirpes de rizóbio eficientes na fixação de nitrogênio para espécies florestais (aproximação 2000). Embrapa Agrobiologia, Seropédica, p 10

    Google Scholar 

  • Faria SM (2002) Obtenção de estirpes de rizóbio eficientes na fixação de nitrogênio para espécies florestais (aproximação 2001). Embrapa Agrobiologia, Seropédica, p 16

    Google Scholar 

  • Faria SM, Lima HC (1998) Additional studies of the nodulation status of legume species in Brazil. Plant Soil 200:185–192

    Article  Google Scholar 

  • Faria SM, Franco AA (2002) Identificação de bactérias eficientes na fixação biológica de nitrogênio para espécies leguminosas arbóreas. EMBRAPA-Agrobiologia, Seropédica, p 16

    Google Scholar 

  • Faria SM, Moreira VCG, Franco AA (1984) Seleção de estirpes de Rhizobium para espécies leguminosas florestais. Pesq Agropec Bras 19:175–179

    Google Scholar 

  • Faria, S.M. Ocurrence and rhizobial selection for legume trees adapted to acid soils (1995). In: Evans DO, Szott T (eds) Nitrogen fixing trees for acid soil. Nitrogen Fixing Tree Association. Morrilton, USA, pp 295–300

  • Ferguson BJ, Mathesius U (2003) Signaling interactions during nodule development. J Plant Growth Regul 22:47–72

    Article  CAS  Google Scholar 

  • Fernandes Júnior PI, Rohr TG, Oliveira PJ, Xavier GR, Rumjanek NG (2009) Polymers as carriers for rhizobial inoculant formulations. Pesq Agropec Bras 44:184–1190

    Article  Google Scholar 

  • Figueiredo MVB, Martinez CR, Burity HA, Chanway CP (2008) Plant growth-promoting rhizobacteria for improving nodulation and nitrogen fixation in the common bean (Phaseolus vulgaris L.). World J. Microbiol Biotechnol 24:1187–1193

    Article  CAS  Google Scholar 

  • Fisher RF (1995) Amelioration of degraded rain forest soils by plantations of native trees. Soil Sci Soc Am J 59:544–549

    Article  CAS  Google Scholar 

  • Fontes SJ, Barrios E, Six J (2010) Earthworms, soil fertility and aggregate-associated soil organic matter dynamics in the Quesungual agroforestry system. Geoderma 155:320–328

    Article  CAS  Google Scholar 

  • Freitas ADS, Sampaio EVSB, Santos CERS, Fernandes AR (2010) Biological nitrogen fixation in tree legumes of the Brazilian semi-arid caatinga. J Arid Environ 74:344–349

    Article  Google Scholar 

  • Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36

    Article  PubMed  CAS  Google Scholar 

  • Galli-Terasawa LV, Glienke-Blanco C, Hungria M (2003) Diversity of a soybean rhizobial population adapted to a Cerrados soil. World J Microb Biotech 19:933–939

    Article  CAS  Google Scholar 

  • Garbaye J (1994) Helper bacteria: a new dimension to the mycorrhizal symbiosis. New Phytol 128:197–210

    Article  Google Scholar 

  • García-Fraile P, Velázquez E, Mateos PF, Martínez-Molina E, Rivas R (2008) Cohnella phaseoli sp. nov., isolated from root nodules of Phaseolus coccineus in Spain, and emended description of the genus Cohnella. Int J Syst Evol Microbiol 58:1855–1859

    Article  PubMed  CAS  Google Scholar 

  • Gomez E, Bisaro V, Conti M (2000) Potential C-source utilization patterns of bacterial communities as influenced by clearing and land use in a vertic soil of Argentina. Appl Soil Ecol 15:273–281

    Article  Google Scholar 

  • Grange L, Hungria M (2004) Genetic diversity of indigenous common bean (Phaseolus vulgaris) rhizobia in two Brazilian ecosystems. Soil Biol Biochem 36:1389–1398

    Article  CAS  Google Scholar 

  • Handley BA, Hedges AJ, Beringer JE (1998) Importance of host plants for detecting the population diversity of Rhizobium leguminosarum biovar Viciae in soil. Soil Biol Biochem 30:241–249

    Article  CAS  Google Scholar 

  • Haney RL, Senseman SA, Krutz LJ, Hons FM (2003) Soil carbon and nitrogen mineralization as affected by atrazine and glyphosate. Biol Fert Soils 35:35–40

    Google Scholar 

  • Heuvelop J, Fassbender HW, Alpizar L, Enriquez G, Falster H (1988) Modelling agroforestry systems of cacao (Theobroma cacao) in Costa Rica. II. Cacao and wood production, litter production and decomposition. Agrofor Syst 6:37–48

    Google Scholar 

  • Hirsch AM, Lum MR, Downie JA (2001) What makes the rhizobia-legume symbiosis so special? Plant Physiol 127:1484–1492

    Article  PubMed  CAS  Google Scholar 

  • Howieson J, Ballard R (2004) Optimising the legume symbiosis in stressful and competitive environments within southern Australia—some contemporary thoughts. Soil Biol Biochem 36:1261–1273

    Article  CAS  Google Scholar 

  • Hubbell DH, Kidder G (2003) Biological nitrogen fixation. SL-16, soil and water science department, Florida cooperative extension service, institute of food and agricultural sciences. University of Florida, USA, pp 1–4

    Google Scholar 

  • Hungria M, Vargas MAT (2000) Environmental factors affecting N2 fixation in grain legumes in the tropics, with an emphasis on Brazil. Field Crops Res 65:151–164

    Article  Google Scholar 

  • Jaftha JB, Strijdom BW, Steyn PL (2002) Characterization of pigmented methylotrophic bacteria which nodulate Lotononis bainesii. Syst Appl Microbiol 25:440–449

    Article  PubMed  CAS  Google Scholar 

  • Jalonen R, Nygren P, Sierra J (2009) Transfer of nitrogen from a tropical legume tree to an associated fodder grass via root exudation and common mycelial networks. Plant Cell Environ 32:1366–1376

    Article  PubMed  CAS  Google Scholar 

  • Jenkinson DS, Ladd JN (1981) Microbial biomass in soil: measurement and turnover. In: Paul EA, Ladd JN (eds) Soil biochemistry. Dekker, New York, pp 415–471

    Google Scholar 

  • Jesus EC, Moreira FMS, Florentino LA, Rodrigues MID, Oliveira MS (2005) Diversidade de bactérias que nodulam siratro em três sistemas de uso da terra da Amazônia Ocidental. Pesq Agropec Bras 40:769–776

    Article  Google Scholar 

  • Kaur B, Gupta SR, Singh G (2000) Soil carbon, microbial activity and nitrogen availability in agroforestry systems on moderately alkaline soils in northern India. App Soil Ecol 15:283–294

    Article  Google Scholar 

  • Kirby KR, Potvin C (2007) Variation in carbon storage among tree species: implications for the management of a small-scale carbon sink project. For Ecol Manage 246:208–221

    Article  Google Scholar 

  • Kuklinsky-Sobral J, Araujo WL, Mendes R, Geraldi IO, Pizzirani-Kleiner AA, Azevedo JL (2004) Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ Microbiol 6:1244–1251

    Article  PubMed  CAS  Google Scholar 

  • Langer H, Nandasena KG, Howieson JG, Jorquera M, Borie F (2008) Genetic diversity of Sinorhizobium meliloti associated with alfalfa in Chilean volcanic soils and their symbiotic effectiveness under acidic conditions. World J Microb Biot 24:301–308

    Article  Google Scholar 

  • Law IJ, Botha WF, Majaule UC, Phalane FL (2007) Symbiotic and genomic diversity of ‘cowpea’ bradyrhizobia from soils in Botswana and South Africa. Biol Fert Soils 43:653–663

    Article  Google Scholar 

  • Lesueur D, Ingleby K, Odee D, Chamberlain J, Wilson J, Manga TT, Sarrailh JM, Pottinger A (2001) Improvement of forage production in Calliandra calothyrsus: methodology for the identification of an effective inoculum containing Rhizobium strains and arbuscular mycorrhizal isolates. J Biotech 91:269–282

    Article  CAS  Google Scholar 

  • Loveall ST, Sullivan WC (2006) Environmental benefits of conservation buffers in the United States: evidence, promise, and open questions. Agric Ecosyst Environ 112:249–260

    Article  Google Scholar 

  • Lowrance R, Dabney S, Schultz R (2002) Improving water and soil quality with conservation buffers. J Soil Water Conserv 57:36–43

    Google Scholar 

  • Lucas-Garcia JA, Probanza A, Ramos B, Colon-Flores JJ, Gutierrez-Mañero FJ (2004) Effects of plant growth promoting rhizobateria (PGPRs) on the biological nitrogen fixation, nodulation and growth of Lupinus albus I. cv. Multolupa. Eng Life Sci 4:71–77

    Article  CAS  Google Scholar 

  • Ma W, Penrose DM, Glick BR (2002) Strategies used by rhizobia to lower plant ethylene levels and increase nodulation. Can J Microbiol 48:947–954

    Article  PubMed  CAS  Google Scholar 

  • Macdicken KG, Vergara NT (1990) Agroforestry: classification and management. Wiley, New York, p 382

    Google Scholar 

  • Makatiani ET, Odee DW (2007) Response of Sesbania sesban (L.) Merr. to rhizobial inoculation in an N-deficient soil containing low numbers of effective indigenous rhizobia. Agrofor Sys 70:211–216

    Article  Google Scholar 

  • Manassila M, Nuntagij A, Kotepong S, Boonkerd N, Teaumroong N (2007) Characterization and monitoring of selected rhizobial strains isolated from tree legumes in Thailand. African J Biotech 6:1393–1402

    CAS  Google Scholar 

  • Manley R, Feller C, Swift MJ (2007) Historical evolution of soil organic matter concepts and their relationships with the fertility and sustainability of cropping systems. Agric Ecosys Environ 119:217–233

    Article  Google Scholar 

  • Martinez-Romero E, Segovia L, Mercante FM, Franco AA, Graham P, Pardo MA (1991) Rhizobium tropici, a novel species nodulating Phaseolus vulgaris L. beans and Leucaena sp. trees. Int J Sys Bacteriol 41:417–426

    Article  CAS  Google Scholar 

  • Martins LMV, Xavier GR, Rangel FW, Ribeiro JRA, Neves MCP, Morgado LB, Rumjanek NG (2003) Contribution of biological nitrogen fixation to cowpea: a strategy for improving grain yield in the semi-arid region of Brazil. Biol Fert Soils 38:333–339

    Article  Google Scholar 

  • Masson-Boivin C, Giraud E, Perret X, Batut J (2009) Establishing nitrogen-fixing symbiosis with legumes: how many Rhizobium recipes? Trends Microbiol 17:458–466

    Article  PubMed  CAS  Google Scholar 

  • Mayak S, Tirosh T, Glick BR (1999) Effect of wild type and mutant plant growth promoting rhizobacteriaon the rooting of mung bean cuttings. J Plant Growth Regul 18:49–53

    Article  PubMed  CAS  Google Scholar 

  • Mendonça ES, Leite LFC, Ferreira Neto PS (2001) Cultivo do café em sistema agroflorestal: uma opção para recuperação de solos degradados. Rev Arvore 25:375–383

    Google Scholar 

  • Miralles I, Ortega R, Alemandros G, SancheZ-Maranon M, Soriano M (2009) Soil quality and organic carbon ratios in mountain agroecosystems of South-east Spain. Geoderma 150:32–40

    Article  CAS  Google Scholar 

  • Mnasri B, Mrabet M, Laguerre G, Aouani ME, Mhamdi R (2007) Salt-tolerant rhizobia isolated from a Tunisian oasis that are highly effective for symbiotic N 2 -fixation with Phaseolus vulgaris constitute a novel biovar (bv. mediterranense) of Sinorhizobium meliloti. Arch Microbiol 187:79–85

    Article  PubMed  CAS  Google Scholar 

  • Moonen AC, Bàrberi P (2008) Functional biodiversity: an agroecosystem approach. Agric Ecosys Environ 127:7–21

    Article  Google Scholar 

  • Mostasso L, Mostasso FL, Dias BG, Vargas MAT, Hungria M (2002) Selection of bean (Phaseolus vulgaris L.) rhizobial strains for the Brazilian Cerrados. Field Crops Res 73:121–132

    Article  Google Scholar 

  • Moulin L, Munive A, Dreyfus B, Boivin-Masson C (2001) Nodulation of legumes by members of the β-subclass of Proteobacteria. Nature 411:948–950

    Article  PubMed  CAS  Google Scholar 

  • Moulin L, Chen W-M, Béna G, Dreyfus B, Boivin-Masson C (2002) Rhizobia: the family is expanding. In: Finan T, O’Brian M, Layzell D, Vessey K, Newton W (eds) Nitrogen fixation: global perspectives. CAB International, Wallingford, pp 61–65

    Google Scholar 

  • Mungai NW, Motavalli PP, Kremer RJ, Nelson KA (2005) Spatial variation of soil enzyme activities and microbial functional diversity in temperate alley cropping systems. Biol Fertil Soils 42:129–136

    Article  Google Scholar 

  • Muresu R, Polone E, Sulas L, Baldan B, Tondello A, Delogu G, Cappuccinelli P, Alberghini S, Benhizia Y, Benhizia H, Benguedouar A, Mori B, Calamassi R, Dazzo FB, Squartini A (2008) Coexistence of predominantly nonculturable rhizobia with diverse, endophytic bacterial taxa within nodules of wild legumes. FEMS Microbiol Ecol 63:383–400

    Article  PubMed  CAS  Google Scholar 

  • Myers RT, Zak DR, White DC, Peacock A (2001) Landscape-level patterns of microbial community composition and substrate use in upland forest ecosystems. Soil Sci Soc Am J 65:359–367

    Article  CAS  Google Scholar 

  • Nair PKR, Gordone AM, Mosquera-Losadac, MR (2008) Agroforestry. Elsevier, Netherland, pp. 101–110

  • Nair PKR, Kumar BM, Nair VD (2009) Agroforestry as a strategy for carbon sequestration. J Pl Nutrit Soil Sci 172:10–23

    Article  CAS  Google Scholar 

  • Nygren P, Leblanc HA (2009) Natural abundance of 15N in two cacao plantations with legume and non-legume shade trees. Agrofor Sys 76:303–315

    Article  Google Scholar 

  • Odee DW, Haukka K, McInroy SG, Sprent JI, Sutherland JM, Young JPW (2002) Genetic and symbiotic characterization of rhizobia isolated from tree and herbaceous legumes grown in soils from ecologically diverse sites in Kenya. Soil Biol Biochem 34:801–811

    Article  CAS  Google Scholar 

  • Okasaki S, Sugawara M, Yuhashi KI, Minamisawa K (2007) Rhizobitoxine-induced chlorosis occurs in coincidence with methionine deficiency in soybeans. Ann Botany 100:55–59

    Article  CAS  Google Scholar 

  • Palma JHN, Graves AR, Bunce RGH, Burgess PJ, Filippi R, Keesman K, van Keulen H, Liagre F, Mayus M, Moreno G, Reisner Y, Herzog F (2007) Modeling environmental benefits of silvoarable agroforestry in Europe. Agric Ecosyst Environ 119:320–334

    Article  Google Scholar 

  • Porcel R, Barea JM, Ruiz-Lozano JM (2003) Antioxidant activities in mycorrhizal soybean plants under drought stress and their possible relationship to the process of nodule senescence. New Phytol 157:135–143

    Article  CAS  Google Scholar 

  • Powlson DS, Brookes PC, Christensen BT (1987) Measurement of soil microbial biomass provides an early indication of changes in total organic matter due to straw incorporation. Soil Biol Biochem 19:159–164

    Article  CAS  Google Scholar 

  • Pueppke SG, Broughton WJ (1999) Rhizobium sp. strain NGR234 and R. fredii USDA257 share exceptionally broad, nested host ranges. Mol Plant-Microbe Interact 12:293–318

    Article  PubMed  CAS  Google Scholar 

  • Rao DLN, Pathak H (1996) Ameliorative influence of organic matter on biological activity of salt affected soils. Arid Soil Res Rehab 10:311–319

    Article  CAS  Google Scholar 

  • Remans R, Croonenborghs A, Gutierrez RT, Michiels J, Vanderleyden J (2007) Effects of plant growth-promoting rhizobacteria on nodulation of Phaseolus vulgaris [L.] are dependent on plant P nutrition. Euro J Plant Pathol 119:341–351

    Article  CAS  Google Scholar 

  • Rhamani HA, Saleh-Rastin N, Khavazi K, Asgharzadeh A, Fewer D, Kiani S, Lindstrm K (2009) Selection of thermotolerant bradyrhizobial strains for nodulation of soybean (Glycine max L.) in semi-arid regions of Iran. World J Microb Biotech 25:591–600

    Article  Google Scholar 

  • Rivas R, Velázquez E, Willems A, Vizcaíno N, Subba-Rao NS, Mateos PF, Gillis M, Dazzo FB, Martínez-Molina E (2002) A new species of Devosia that forms a unique nitrogen-fixing rootnodule symbiosis with the aquatic legume Neptunia natans. Appl Environ Microbiol 68:5217–5222

    Article  PubMed  CAS  Google Scholar 

  • Roshetko JM, Lasco RD, Delos Angeles MD (2007) Smallholder agroforestry systems for carbon storage. Mitigation Adapt Strategies Global Change 12:219–242

    Article  Google Scholar 

  • Ruiz-Díez B, Fajardo S, Puertas-Mejía MA, De Felipe MDR, Fernández-Pascual M (2009) Stress tolerance, genetic analysis and symbiotic properties of root-nodulating bacteria isolated from Mediterranean leguminous shrubs in Central Spain. Arch Microbiol 191:35–46

    Article  PubMed  CAS  Google Scholar 

  • Ruiz-Lozano JM, Collados C, Barea JM, Azcon R (2001) Arbuscular mycorrhizal symbiosis can alleviate droughtinduced nodule senescence in soybean plants. New Phytol 151:493–502

    Article  CAS  Google Scholar 

  • Salati E, Santos AA, Klabin I (2006) Relevant environmental issues. Estudos Avançados 20:107–127

    Article  Google Scholar 

  • Saravana-Kumar D, Samiyappan R (2007) ACC deaminase from Pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J Appl Microbial 102:1283–1292

    Article  CAS  Google Scholar 

  • Scheublin TR, Van der Heijden MGA (2006) Arbuscular mycorrhizal fungi colonize nonfixing root nodules of several legume species. New Phytol 172:732–738

    Article  PubMed  Google Scholar 

  • Serraj R (2004) Symbiotic nitrogen fixation: prospects for enhanced application in tropical agriculture. IBH, New Delhi, p 367

    Google Scholar 

  • Sharrow SH, Ismail S (2004) Carbon and nitrogen storage in agroforests, tree plantations, and pastures in western Oregon, USA. Agroforest Syst 60:123–130

    Article  Google Scholar 

  • Silva MF, Oliveira PJ, Xavier GR, Rumjanek NG, Reis VM (2009) Inoculantes formulados com polímeros e bactérias endofíticas para a cultura da cana-de-açúcar. Pesq Agropec Bras 44:1437–1443

    Article  Google Scholar 

  • Silva VN, Silva LESF, Figueiredo MVB (2006) Atuação de rizóbios com rizobactérias promotora de crescimento em plantas na cultura do caupi (Vigna unguiculata L. Walp). Acta Sci Agron 28:407–412

    Google Scholar 

  • Silva VN, Silva LESF, Figueiredo MVB, Carvalho FG, Silva MLRB, Silva AJN (2007) Caracterização e seleção de populações nativas de rizóbios de solo da região semi-árida de Pernambuco. Pesq Agropec Trop 37:16–21

    Google Scholar 

  • Sørensen J, Sessitsch A (2007) Plant-associated bacterial-lifestyle and molecular interactions. In: Van Elsas JD, Jansson JK, Trevors JT (eds) Modern soil microbiology. CRC, New York, pp 221–236

    Google Scholar 

  • Sprent JI (2001) Nodulation in legumes. Royal Botanic Gardens, Kew, London

    Google Scholar 

  • Steenhoudt O, Vanderleyden J (2000) Azospirillum, a free-living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects. FEMS Microbiol Rev 24:487–506

    Article  PubMed  CAS  Google Scholar 

  • Sun Y, Cheng Z, Glick BR (2009) The presence of a 1-aminocyclopropane-1-carboxylate (ACC) deaminase deletion mutation alters the physiology of the endophytic plant growth-promoting bacterium Burkholderia phytofirmans PsJN. FEMS Microbiol Let 296:131–136

    Article  CAS  Google Scholar 

  • Sy A, Giraud E, Jourand P, Garcia N, Willems A, de Lajudie P, Prin Y, Neyra M, Gillis M, Boivin-Masson C, Dreyfus B (2001) Methylotrophic Methylobacterium bacteria nodulate and fix nitrogen in symbiosis with legumes. J Bacteriol 183:214–220

    Article  PubMed  CAS  Google Scholar 

  • Sziderics AH, Rasche F, Trognitz F, Sessitsch A, Wilhelm E (2007) Bacterial endophytes contribute to abiotic stress adaptation in pepper plants (Capsicum annuum L.). Can J Microbiol 53:1195–1202

    Article  PubMed  CAS  Google Scholar 

  • Tangjang S, Arunachalam K, Arunachalam A, Shukla AK (2009) Microbial population dynamics of soil under traditional agroforestry systems in Northeast India. Res J Soil Biol 1:1–7

    Google Scholar 

  • Tilak KVBR, Rauganayaki N, Manoharachari C (2006) Synergistic effects of plant-growth promoting rhizobacteria and Rhizobium on nodulation and nitrogen fixation by pigeonpea (Cajanus cajan). Europ J Soil Sci 57:67–71

    Article  CAS  Google Scholar 

  • Tornquist CG, Hons FM, Feagley SE, Haggar J (1999) Agroforestry system effects on soil characteristics of the Sarapiquí region of Costa Rica. Agric Ecosys Environ 73:19–28

    Article  Google Scholar 

  • Udawatta RP, Kremer RJ, Adamson BW, Anderson SH (2008) Variations in soil aggregate stability and enzyme activities in a temperate agroforestry practice. App Soil Ecol 39:153–160

    Article  Google Scholar 

  • Van Berkum P, Eardly BD (2002) The aquatic budding bacterium Blastobacter denitrificans is a nitrogen-fixing symbiont of Aeschynomene indica. In: Finan TM, O’Brian MR, Layzell DB, Vessey JK, Newton WE (eds) Nitrogen fixation: global perspectives. CAB International, New York, p 520

    Google Scholar 

  • Vandamme P, Goris J, Chen WM, Vos P, Willems A (2002) Burkholderia tuberum sp. nov. and Burkholderia phymatum sp. nov., nodulate the roots of tropical legumes. Syst App Microbiol 25:507–512

    Article  Google Scholar 

  • Vessey JK, Buss TJ (2002) Bacillus cereus UW85 inoculation effects on growth, nodulation, and N accumulation in grain legumes. Controlled-environment studies. Can J Plant Sci 82:282–290

    Article  Google Scholar 

  • Vivas A, Marulanda A, Ruiz-Lozano JM, Barea JM, Azcon R (2003a) Influence of a Bacillus sp. on physiological activities of two arbuscular mycorrhizal fungi and on plant responses to PEG-induced drought stress. Mycorrhiza 13:249–256

    Article  PubMed  Google Scholar 

  • Vivas A, Azcon R, Biro B, Barea JM, Ruiz-Lozano JM (2003b) Influence of bacterial strains isolated from lead-polluted soil and their interactions with arbuscular mycorrhizae on the growth of Trifolium pretense L. under lead toxicity. Can J Microbiol 49:577–588

    Article  PubMed  CAS  Google Scholar 

  • Watanabe K, Hamamura N (2003) Molecular and physiological approaches to understanding the ecology of pollutant degradation. App Soil Ecol 31:120–135

    Google Scholar 

  • Willems A (2006) The taxonomy of rhizobia: an overview. Plant Soil 287:3–14

    Article  CAS  Google Scholar 

  • Wolde-Meskel E, Terefework Z, Lindström K, Frostegard A (2004) Rhizobia nodulating African Acacia spp. and Sesbania sesban trees in southern Ethiopian soils are metabolically and genomically diverse. Soil Biol Biochem 36:2013–2025

    Article  CAS  Google Scholar 

  • Xavier GR, Correia MEF, Aquino AM, Zilli JÉ, Rumjanek NG (2010) The structural and functional biodiversity of soil: an interdisciplinary vision for conservation agriculture in Brazil. In: Dion P (ed) Soil biol agric trop. Springer, Heidelberg, pp 65–80

    Chapter  Google Scholar 

  • Yadav RS, Yadav BL, Chhipa BR, Dhyani SK, Ram M (2010) Soil biological properties under different tree based traditional agroforestry systems in a semi-arid region of Rajasthan, India. Agroforest Syst 81:195–202

    Google Scholar 

  • Yan F, McBratney AB, Copeland L (2000) Functional substrate biodiversity of cultivated and uncultivated a horizons of vertisols in NW New South Wales. Geoderma 96:321–343

    Google Scholar 

  • Yates RJ, Howieson JG, Real D, Reeve WG, Vivas-Marfisi A, O’Hara GW (2005a) Evidence of selection for effective nodulation in the Trifolium spp. symbiosis with Rhizobium leguminosarum biovar trifolii. Aust J Experim Agric 45:189–198

    Article  Google Scholar 

  • Yates RJ, Howieson JG, Nandasena KG, O’Hara GW (2005b) Root-nodule bacteria from indigenous legumes in the north-west of Western Australia and their interaction with exotic legumes. Soil Biol Biochem 36:1319–1329

    Article  CAS  Google Scholar 

  • Zafar-ul-Hye M (2008) Improving nodulation in lentil through co-inoculation with rhizobia and ACC-deaminase containing plant growth promoting rhizobacteria, PhD Thesis, University of Agriculture, Faisalabad, Pakistan, p 198

  • Zhang F, Dashti N, Hynes RK, Smith DL (1996) Plant-growth promoting rhizobacteria and soybean (Glycine max [L.] Merr.) nodulation and nitrogen fixation at suboptimal root zone temperatures. Ann Botany 77:453–459

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ademir Sérgio Ferreira Araujo.

About this article

Cite this article

Araujo, A.S.F., Leite, L.F.C., Iwata, B.F. et al. Microbiological process in agroforestry systems. A review. Agron. Sustain. Dev. 32, 215–226 (2012). https://doi.org/10.1007/s13593-011-0026-0

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13593-011-0026-0

Keywords

Navigation