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The Role of Microbial Inoculants in Integrated Crop Management Systems

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Abstract

One of the major issues facing humankind is global food security. A changing climate, coupled with a heightened consumer awareness of how food is produced and legislative changes governing the usage of agrichemicals for improving plant health and yield, means that alternative, more integrated and sustainable approaches are needed for crop management practices. To this end, there is increasing recognition of the value of the role of microbial inoculants in agriculture. The focus of this review is to understand how plant-growth-promoting bacteria and arbuscular mycorrhizal fungi can play a part in improving crop yield by promoting the health status of the plant through the sequestration of various nutrients and in the control of plant diseases.

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References

  • Adesemoye AO, Kloepper JW (2009) Plant-microbes interactions in enhanced fertilizer-use efficiency. Appl Microbiol Biotechnol 85:1–12. doi:10.1007/s00253-009-2196-0

    CAS  PubMed  Google Scholar 

  • Anandham R, Gandhi PI, Sentil Kumar M, Sridar R, Nalayini P, Sa T-M (2011) Sulfur-oxidizing bacteria: a novel bioinoculant for sulfur nutrition and crop production. In: Maheshwari DK (ed) Bacteria in agrobiology: plant nutrient management. Springer, Berlin, pp 81–107

  • Arkhipova TN, Veselov SU, Melentiev AI, Martynenko EV, Kudoyarova GR (2005) Ability of bacterium Bacillus subtilis to produce cytokinins and to influence the growth and endogenous hormone content of lettuce plants. Plant Soil 272:201–209. doi:10.1007/s11104-004-5047-x

    CAS  Google Scholar 

  • Arkhipova TN, Prinsen E, Veselov SU, Martinenko EV, Melentiev AI, Kudoyarova GR (2007) Cytokinin producing bacteria enhance plant growth in drying soil. Plant Soil 292:305–315. doi:10.1007/s11104-007-9233-5

    CAS  Google Scholar 

  • Bakker PA, Pieterse CM, van Loon LC (2007) Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 97:239–243. doi:10.1094/phyto-97-2-0239

    PubMed  Google Scholar 

  • Bar T, Okon Y (1992) Induction of indole-3-acetic acid synthesis and possible toxicity of tryptophan in Azospirillum brasilense Sp7. Symbiosis 13:191–198

    CAS  Google Scholar 

  • Bashan Y, Kamnev A, de-Bashan L (2013a) A proposal for isolating and testing phosphate-solubilizing bacteria that enhance plant growth. Biol Fertil Soils 49:1–2. doi:10.1007/s00374-012-0756-4

    Google Scholar 

  • Bashan Y, Kamnev A, de-Bashan L (2013b) Tricalcium phosphate is inappropriate as a universal selection factor for isolating and testing phosphate-solubilizing bacteria that enhance plant growth: a proposal for an alternative procedure. Biol Fertil Soils 49:465–479. doi:10.1007/s00374-012-0737-7

    CAS  Google Scholar 

  • Bauer H et al. (2013) The stomatal response to reduced relative humidity requires guard cell-autonomous ABA synthesis. Curr Biol 23:53–57. doi:10.1016/j.cub.2012.11.022

    CAS  PubMed  Google Scholar 

  • Baz M et al. (2012) Control of potato soft rot caused by Pectobacterium carotovorum and Pectobacterium atrosepticum by Moroccan actinobacteria isolates. World J Microbiol Biotechnol 28:303–311. doi:10.1007/s11274-011-0820-5

    CAS  PubMed  Google Scholar 

  • Bender CL, Rangaswamy V, Loper J (1999) Polyketide production by plant-associated Pseudomonads. Annu Rev Phytopathol 37:175–196. doi:10.1146/annurev.phyto.37.1.175

    CAS  PubMed  Google Scholar 

  • Beneduzi A, Ambrosini A, Passaglia LM (2012) Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genet Mol Biol 35:1044–1051

    PubMed Central  CAS  PubMed  Google Scholar 

  • Boiero L, Perrig D, Masciarelli O, Penna C, Cassan F, Luna V (2007) Phytohormone production by three strains of Bradyrhizobium japonicum and possible physiological and technological implications. Appl Microbiol Biotechnol 74:874–880. doi:10.1007/s00253-006-0731-9

    CAS  PubMed  Google Scholar 

  • Borriss R (2011) Use of plant-associated Bacillus strains as biofertilizers and biocontrol agents in agriculture. In: Maheshwari DK (ed) Bacteria in agrobiology: plant growth responses. Springer, Berlin, pp 41–76

    Google Scholar 

  • Bottini R, Cassan F, Piccoli P (2004) Gibberellin production by bacteria and its involvement in plant growth-promotion and yield increase. Appl Microbiol Biotechnol 65:497–503. doi:10.1007/s00253-004-1696-1

    CAS  PubMed  Google Scholar 

  • Brencic A, Winans SC (2005) Detection of and response to signals involved in host-microbe interactions by plant-associated bacteria. Microbiol Mol Biol Rev 69:155–194. doi:10.1128/mmbr.69.1.155-194.2005

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838. doi:10.1146/annurev-arplant-050312-120106

    CAS  PubMed  Google Scholar 

  • Cassán F, Perrig D, Sgroy V, Masciarelli O, Penna C, Luna V (2009) Azospirillum brasilense Az39 and Bradyrhizobium japonicum E109, inoculated singly or in combination, promote seed germination and early seedling growth in corn (Zea mays L.) and soybean (Glycine max L.). Eur J Soil Biol 45:28–35. doi:10.1016/j.ejsobi.2008.08.005

    Google Scholar 

  • Cheng X, Ruyter-Spira C, Bouwmeester H (2013) The interaction between strigolactones and other plant hormones in the regulation of plant development. Front Plant Sci 4:199. doi:10.3389/fpls.2013.00199

    PubMed Central  PubMed  Google Scholar 

  • Chin AWTF, Bloemberg GV, Mulders IH, Dekkers LC, Lugtenberg BJ (2000) Root colonization by phenazine-1-carboxamide-producing bacterium Pseudomonas chlororaphis PCL1391 is essential for biocontrol of tomato foot and root rot. Mol Plant Microbe Interact 13:1340–1345. doi:10.1094/mpmi.2000.13.12.1340

    Google Scholar 

  • Chin-A-Woeng TFC, Bloemberg GV, Lugtenberg BJJ (2003) Phenazines and their role in biocontrol by Pseudomonas bacteria. New Phytol 157:503–523. doi:10.1046/j.1469-8137.2003.00686.x

    CAS  Google Scholar 

  • Choi HK, Song GC, Yi HS, Ryu CM (2014) Field evaluation of the bacterial volatile derivative 3-pentanol in priming for induced resistance in pepper. J Chem Ecol 40:882–892. doi:10.1007/s10886-014-0488-z

    CAS  PubMed  Google Scholar 

  • Cohen A, Bottini R, Piccoli P (2008) Azospirillum brasilense Sp 245 produces ABA in chemically-defined culture medium and increases ABA content in Arabidopsis plants. Plant Growth Regul 54:97–103. doi:10.1007/s10725-007-9232-9

    CAS  Google Scholar 

  • Cohen AC, Travaglia CN, Bottini R, Piccoli PN (2009) Participation of abscisic acid and gibberellins produced by endophytic Azospirillum in the alleviation of drought effects in maize. Botany 87:455–462. doi:10.1139/B09-023

    CAS  Google Scholar 

  • Compant S, Duffy B, Nowak J, Clément C, Barka EA (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959. doi:10.1128/aem.71.9.4951-4959.2005

    PubMed Central  CAS  PubMed  Google Scholar 

  • Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678. doi:10.1016/j.soilbio.2009.11.024

    CAS  Google Scholar 

  • Conrath U et al (2006) Priming: getting ready for battle. Mol Plant Microbe Interact 19:1062–1071. doi:10.1094/mpmi-19-1062

    CAS  PubMed  Google Scholar 

  • Crowley D (2006) Microbial siderophores in the plant rhizosphere. In: Barton L, Abadia J (eds) Iron nutrition in plants and rhizospheric microorganisms. Springer, Netherlands, pp 169–198. doi:10.1007/1-4020-4743-6_8

    Google Scholar 

  • Dandurishvili N et al. (2011) Broad-range antagonistic rhizobacteria Pseudomonas fluorescens and Serratia plymuthica suppress Agrobacterium crown gall tumours on tomato plants. J Appl Microbiol 110:341–352. doi:10.1111/j.1365-2672.2010.04891.x

    CAS  PubMed  Google Scholar 

  • de Souza JT, Arnould C, Deulvot C, Lemanceau P, Gianinazzi-Pearson V, Raaijmakers JM (2003) Effect of 2,4-diacetylphloroglucinol on Pythium: cellular responses and variation in sensitivity among propagules and species. Phytopathology 93:966–975. doi:10.1094/phyto.2003.93.8.966

    PubMed  Google Scholar 

  • Diaz RJ, Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321:926–929. doi:10.1126/science.1156401

    CAS  PubMed  Google Scholar 

  • Duijff B, Meijer J, Bakker PHM, Schippers B (1993) Siderophore-mediated competition for iron and induced resistance in the suppression of Fusarium wilt of carnation by fluorescent Pseudomonas spp. Neth J Plant Pathol 99:277–289. doi:10.1007/BF01974309

    CAS  Google Scholar 

  • Dunne C, Moenne-Loccoz Y, de Bruijn FJ, O'Gara F (2000) Overproduction of an inducible extracellular serine protease improves biological control of Pythium ultimum by Stenotrophomonas maltophilia strain W81. Microbiology 146:2069–2078

    CAS  PubMed  Google Scholar 

  • Effmert U, Kalderás J, Warnke R, Piechulla B (2012) Volatile mediated interactions between bacteria and fungi in the soil. J Chem Ecol 38:665–703. doi:10.1007/s10886-012-0135-5

    CAS  PubMed  Google Scholar 

  • El-Tarabily KA, Sykes ML, Kurtböke ID, Hardy GESJ, Barbosa AM, Dekker RFH (1996) Synergistic effects of a cellulase-producing Micromonospora carbonacea and an antibiotic-producing Streptomyces violascens on the suppression of Phytophthora cinnamomi root rot of Banksia grandis. Can J Bot 74:618–624. doi:10.1139/b96-078

    Google Scholar 

  • Fernando WGD, Ramarathnam R, Krishnamoorthy AS, Savchuk SC (2005) Identification and use of potential bacterial organic antifungal volatiles in biocontrol. Soil Biol Biochem 37:955–964. doi:10.1016/j.soilbio.2004.10.021

    CAS  Google Scholar 

  • Fernando WGD, Nakkeeran S, Zhang Y (2006) Biosynthesis of antibiotics by PGPR and its relation in biocontrol of plant diseases. In: Siddiqui Z (ed) PGPR: biocontrol and biofertilization. Springer, Netherlands, pp 67–109. doi:10.1007/1-4020-4152-7_3

    Google Scholar 

  • Fogliano V, Ballio A, Gallo M, Woo S, Scala F, Lorito M (2002) Pseudomonas lipodepsipeptides and fungal cell wall-degrading enzymes act synergistically in biological control. Mol Plant Microbe Interact 15:323–333. doi:10.1094/mpmi.2002.15.4.323

    CAS  PubMed  Google Scholar 

  • Franche C, Lindström K, Elmerich C (2009) Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil 321:35–59. doi:10.1007/s11104-008-9833-8

    CAS  Google Scholar 

  • Fulchieri M, Lucangeli C, Bottini R (1993) Inoculation with Azospirillum lipoferum affects growth and gibberellin status of corn seedling roots. Plant Cell Physiol 34:1305–1309

    CAS  Google Scholar 

  • Gamalero E, Glick B (2011) Mechanisms used by plant growth-promoting bacteria. In: Maheshwari DK (ed) Bacteria in agrobiology: plant nutrient management. Springer, Berlin, pp 17–46

    Google Scholar 

  • Garcia de Salamone IE, Hynes RK, Nelson LM (2001) Cytokinin production by plant growth-promoting rhizobacteria and selected mutants. Can J Microbiol 47:404–411

    CAS  PubMed  Google Scholar 

  • Garcia de Salamone IE, Hynes RK, Nelson LM (2006) Role of cytokinins in plant growth promotion by rhizosphere bacteria. In: Siddiqui Z (ed) PGPR: biocontrol and biofertilization. Springer, Netherlands, pp 173–195

    Google Scholar 

  • Ghyselinck J (2013) Understanding the composition and role of the prokaryotic diversity in the potato rhizopshere for crop improvement in the Andes. PhD Thesis, Ghent University, Ghent

    Google Scholar 

  • Ghyselinck J et al. (2013) Bioprospecting in potato fields in the Central Andean Highlands: screening of rhizobacteria for plant growth-promoting properties. Syst Appl Microbiol 36:116–127. doi:10.1016/j.syapm.2012.11.007

    CAS  PubMed  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227. doi:10.1146/annurev.phyto.43.040204.135923

    CAS  PubMed  Google Scholar 

  • Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012:15. doi:10.6064/2012/963401

    Google Scholar 

  • Glick B, Cheng Z, Czarny J, Duan J (2007a) Promotion of plant growth by ACC deaminase-producing soil bacteria. Eur J Plant Pathol 119:329–339. doi:10.1007/s10658-007-9162-4

    CAS  Google Scholar 

  • Glick BR, Todorovic B, Czarny J, Cheng Z, Duan J, McConkey B (2007b) Promotion of plant growth by bacterial ACC deaminase. Crit Rev Plant Sci 26:227–242. doi:10.1080/07352680701572966

    CAS  Google Scholar 

  • Goltapeh EM, Danesh YR, Prasad R, Varma A (2008) Mycorrhizal fungi: what we know and what should we know? In: Varma A (ed) Mycorrhiza. Springer, Berlin, pp 3–27

    Google Scholar 

  • Gutiérrez-Mañero FJ, Ramos-Solano B, Probanza AN, Mehouachi J, Tadeo FR, Talon M (2001) The plant growth-promoting rhizobacteria Bacillus pumilus and Bacillus licheniformis produce high amounts of physiologically active gibberellins. Physiol Plant 111:206–211. doi:10.1034/j.1399-3054.2001.1110211.x

    Google Scholar 

  • Han H, Lee K (2005) Phosphate and potassium solubilizing bacteria effect on mineral uptake, soil availability and growth of eggplant. Res J Agric Biol Sci 1:176–180

    Google Scholar 

  • Hartmann A, Rothballer M, Schmid M (2008) Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant Soil 312:7–14. doi:10.1007/s11104-007-9514-z

    CAS  Google Scholar 

  • Hernández-Montiel LG, Rueda-Puente EO, Cordoba-Matson MV, Holguín-Peña JR, Zulueta-Rodríguez R (2013) Mutualistic interaction of rhizobacteria with arbuscular mycorrhizal fungi and its antagonistic effect on Fusarium oxysporum in Carica papaya seedlings. Crop Prot 47:61–66. doi:10.1016/j.cropro.2013.01.008

    Google Scholar 

  • Huang C-J, Tsay J-F, Chang S-Y, Yang H-P, Wu W-S, Chen C-Y (2012) Dimethyl disulfide is an induced systemic resistance elicitor produced by Bacillus cereus C1L. Pest Manag Sci 68:1306–1310. doi:10.1002/ps.3301

    CAS  PubMed  Google Scholar 

  • Hussain A, Hasnain S (2009) Cytokinin production by some bacteria: its impact on cell division in cucumber cotyledons. Afr J Microbiol Res 3:704–712

    CAS  Google Scholar 

  • Idris EE, Iglesias DJ, Talon M, Borriss R (2007) Tryptophan-dependent production of indole-3-acetic acid (IAA) affects level of plant growth promotion by Bacillus amyloliquefaciens FZB42. Mol Plant Microbe Interact 20:619–626. doi:10.1094/mpmi-20-6-0619

    CAS  PubMed  Google Scholar 

  • Jones DL, Nguyen C, Finlay RD (2009) Carbon flow in the rhizosphere: carbon trading at the soil–root interface. Plant Soil 321:5–33. doi:10.1007/s11104-009-9925-0

    CAS  Google Scholar 

  • Jung WJ, An KN, Jin YL, Park RD, Lim KT, Kim KY, Kim TH (2003) Biological control of damping-off caused by Rhizoctonia solani using chitinase-producing Paenibacillus illinoisensis KJA-424. Soil Biol Biochem 35:1261–1264. doi:10.1016/S0038-0717(03)00187-1

    CAS  Google Scholar 

  • Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38:651–664. doi:10.1007/s10886-012-0134-6

    CAS  PubMed  Google Scholar 

  • Kai M, Effmert U, Berg G, Piechulla B (2007) Volatiles of bacterial antagonists inhibit mycelial growth of the plant pathogen Rhizoctonia solani. Arch Microbiol 187:351–360. doi:10.1007/s00203-006-0199-0

    CAS  PubMed  Google Scholar 

  • Kamilova F, Kravchenko LV, Shaposhnikov AI, Azarova T, Makarova N, Lugtenberg B (2006) Organic acids, sugars, and L-tryptophane in exudates of vegetables growing on stonewool and their effects on activities of rhizosphere bacteria. Mol Plant Microbe Interact 19:250–256. doi:10.1094/mpmi-19-0250

    CAS  PubMed  Google Scholar 

  • Kang SM et al. (2009) Gibberellin production and phosphate solubilization by newly isolated strain of Acinetobacter calcoaceticus and its effect on plant growth. Biotechnol Lett 31:277–281. doi:10.1007/s10529-008-9867-2

    CAS  PubMed  Google Scholar 

  • Khalid A, Tahir S, Arshad M, Zahir ZA (2004) Relative efficiency of rhizobacteria for auxin biosynthesis in rhizosphere and non-rhizosphere soils. Soil Res 42:921–926. doi:10.1071/SR04019

    CAS  Google Scholar 

  • Kloepper JW, Leong J, Teintze M, Schroth MN (1980) Enhanced plant growth by siderophores produced by plant growth-promoting rhizobacteria. Nature 286:885–886

    CAS  Google Scholar 

  • Kloepper JW, Ryu CM, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259–1266. doi:10.1094/phyto.2004.94.11.1259

    CAS  PubMed  Google Scholar 

  • Kuiper I, Bloemberg GV, Lugtenberg BJ (2001) Selection of a plant-bacterium pair as a novel tool for rhizostimulation of polycyclic aromatic hydrocarbon-degrading bacteria. Mol Plant Microbe Interact 14:1197–1205. doi:10.1094/mpmi.2001.14.10.1197

    CAS  PubMed  Google Scholar 

  • Lakshmanan V, Kitto SL, Caplan JL, Hsueh YH, Kearns DB, Wu YS, Bais HP (2012) Microbe-associated molecular patterns-triggered root responses mediate beneficial rhizobacterial recruitment in Arabidopsis. Plant Physiol 160:1642–1661. doi:10.1104/pp.112.200386

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lee B, Farag MA, Park HB, Kloepper JW, Lee SH, Ryu C-M (2012) Induced resistance by a long-chain bacterial volatile: elicitation of plant systemic defense by a C13 volatile produced by Paenibacillus polymyxa. PLoS ONE 7:e48744. doi:10.1371/journal.pone.0048744

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ligon JM, Hill DS, Hammer PE, Torkewitz NR, Hofmann D, Kempf H-J, K-Hv P (2000) Natural products with antifungal activity from Pseudomonas biocontrol bacteria. Pest Manag Sci 56:688–695. doi:10.1002/1526-4998(200008)56:8<688::AID-PS186>3.0.CO;2-V

    CAS  Google Scholar 

  • Liu F, Xing S, Ma H, Du Z, Ma B (2013) Cytokinin-producing, plant growth-promoting rhizobacteria that confer resistance to drought stress in Platycladus orientalis container seedlings. Appl Microbiol Biotechnol 97:9155–9164. doi:10.1007/s00253-013-5193-2

    CAS  PubMed  Google Scholar 

  • Lugtenberg B, Kamilova F (2009) Plant growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556. doi:10.1146/annurev.micro.62.081307.162918

    CAS  PubMed  Google Scholar 

  • MacMillan J (2001) Occurrence of gibberellins in vascular plants, fungi, and bacteria. J Plant Growth Regul 20:387–442. doi:10.1007/s003440010038

    CAS  PubMed  Google Scholar 

  • Mitter B, Brader G, Afzal M, Compant S, Naveed M, Trognitz F, Sessitsch A (2013) Advances in elucidating beneficial interactions between plants, soil, and bacteria. In: Donald LS (ed) Advances in Agronomy, vol 121. Academic Press, pp 381–445

  • Mohamed AA, Eweda WEE, Heggo AM, Hassan EA (2014) Effect of dual inoculation with arbuscular mycorrhizal fungi and sulphur-oxidising bacteria on onion (Allium cepa L.) and maize (Zea mays L.) grown in sandy soil under green house conditions. Ann Agric Sci 59:109–118. doi:10.1016/j.aoas.2014.06.015

    Google Scholar 

  • Morgan JA, Bending GD, White PJ (2005) Biological costs and benefits to plant-microbe interactions in the rhizosphere. J Exp Bot 56:1729–1739. doi:10.1093/jxb/eri205

    CAS  PubMed  Google Scholar 

  • Muller B, Sheen J (2007) Advances in cytokinin signaling. Science 318:68–69. doi:10.1126/science.1145461

    PubMed  Google Scholar 

  • Naveed M, Qureshi MA, Zahir Z, Hussain MB, Sessitsch A, Mitter B (2014) L-Tryptophan-dependent biosynthesis of indole-3-acetic acid (IAA) improves plant growth and colonization of maize by Burkholderia phytofirmans PsJN. Ann Microbiol:1–9 doi:10.1007/s13213-014-0976-y

  • Niu DD, Liu HX, Jiang CH, Wang YP, Wang QY, Jin HL, Guo JH (2011) The plant growth-promoting rhizobacterium Bacillus cereus AR156 induces systemic resistance in Arabidopsis thaliana by simultaneously activating salicylate- and jasmonate/ethylene-dependent signaling pathways. Mol Plant Microbe Interact 24:533–542. doi:10.1094/mpmi-09-10-0213

    CAS  PubMed  Google Scholar 

  • Nordström A, Tarkowski P, Tarkowska D, Norbaek R, Åstot C, Dolezal K, Sandberg G (2004) Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: a factor of potential importance for auxin–cytokinin-regulated development. Proc Natl Acad Sci U S A 101:8039–8044. doi:10.1073/pnas.0402504101

    PubMed Central  PubMed  Google Scholar 

  • Palumbo JD, Yuen GY, Jochum CC, Tatum K, Kobayashi DY (2005) Mutagenesis of beta-1,3-glucanase genes in Lysobacter enzymogenes strain C3 results in reduced biological control activity toward Bipolaris leaf spot of tall fescue and Pythium damping-off of sugar beet. Phytopathology 95:701–707. doi:10.1094/phyto-95-0701

    CAS  PubMed  Google Scholar 

  • Park KH, Lee CY, Son HJ (2009) Mechanism of insoluble phosphate solubilization by Pseudomonas fluorescens RAF15 isolated from ginseng rhizosphere and its plant growth-promoting activities. Lett Appl Microbiol 49:222–228. doi:10.1111/j.1472-765X.2009.02642.x

    PubMed  Google Scholar 

  • Park HB, Lee B, Kloepper JW, Ryu CM (2013) One shot-two pathogens blocked: exposure of Arabidopsis to hexadecane, a long chain volatile organic compound, confers induced resistance against both Pectobacterium carotovorum and Pseudomonas syringae. Plant Signal Behav 8:e24619. doi:10.4161/psb.24619

    PubMed  Google Scholar 

  • Parmar P, Sindhu S (2013) Potassium solubilization by rhizosphere bacteria: influence of nutritional and environmental conditions. J Microbiol Res 3:25–31

    Google Scholar 

  • Patten CL, Glick BR (1996) Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol 42:207–220

    CAS  PubMed  Google Scholar 

  • Peix A, Velázquez E, Silva L, Mateos P (2010) Key molecules involved in beneficial infection process in Rhizobia–legume symbiosis. In: Khan M, Musarrat J, Zaidi A (eds) Microbes for legume improvement. Springer, Vienna, pp 55–80. doi:10.1007/978-3-211-99753-6_3

    Google Scholar 

  • Perrig D, Boiero ML, Masciarelli OA, Penna C, Ruiz OA, Cassan FD, Luna MV (2007) Plant growth-promoting compounds produced by two agronomically important strains of Azospirillum brasilense, and implications for inoculant formulation. Appl Microbiol Biotechnol 75:1143–1150. doi:10.1007/s00253-007-0909-9

    CAS  PubMed  Google Scholar 

  • Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SCM (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316

    CAS  PubMed  Google Scholar 

  • Pliego C, Kamilova F, Lugtenberg B (2011) Plant growth-promoting bacteria: fundamentals and exploitation. In: Maheshwari DK (ed) Bacteria in agrobiology: crop ecosystems. Springer, Berlin, pp 295–343

    Google Scholar 

  • Powelson ML, Rowe RC (2008) Managing diseases caused by seedborne and soilborne fungi and fungus-like pathogens. In: Johnson DA (ed) Potato health management. APS Press, Minnesota, pp 183–195

    Google Scholar 

  • Pozo MJ, Verhage A, García-Andrade J, García JM, Azcón-Aguilar C (2009) Priming plant defence against pathogens by arbuscular mycorrhizal fungi. In: Azcón-Aguilar C, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (eds) Mycorrhizas - functional processes and ecological impact. Springer, Berlin, pp 123–135

    Google Scholar 

  • Raaijmakers JM, de Bruijn I, de Kock MJ (2006) Cyclic lipopeptide production by plant-associated Pseudomonas spp.: diversity, activity, biosynthesis, and regulation. Mol Plant Microbe Interact 19:699–710. doi:10.1094/mpmi-19-0699

    CAS  PubMed  Google Scholar 

  • Raaijmakers J, Paulitz T, Steinberg C, Alabouvette C, Moënne-Loccoz Y (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321:341–361. doi:10.1007/s11104-008-9568-6

    CAS  Google Scholar 

  • Raaijmakers JM, De Bruijn I, Nybroe O, Ongena M (2010) Natural functions of lipopeptides from Bacillus and Pseudomonas: more than surfactants and antibiotics. FEMS Microbiol Rev 34:1037–1062. doi:10.1111/j.1574-6976.2010.00221.x

    CAS  PubMed  Google Scholar 

  • Rodríguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth-promotion. Biotechnol Adv 17:319–339. doi:10.1016/S0734-9750(99)00014-2

    PubMed  Google Scholar 

  • Rodríguez 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. doi:10.1007/s11104-006-9056-9

    Google Scholar 

  • Rowe RC, Powelson ML (2008) Potato health management: a holistic approach. In: Johnson DA (ed) Potato health management. APS Press, Minnesota, pp 1–5

    Google Scholar 

  • Ryu C-M, Farag MA, Hu C-H, Reddy MS, Wei H-X, Paré PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci 100:4927–4932. doi:10.1073/pnas.0730845100

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ryu C-M, Farag MA, Hu C-H, Reddy MS, Kloepper JW, Paré PW (2004) Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol 134:1017–1026. doi:10.1104/pp.103.026583

    PubMed Central  CAS  PubMed  Google Scholar 

  • Schüβler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421. doi:10.1017/S0953756201005196

    Google Scholar 

  • Senés-Guerrero C, Torres-Cortés G, Pfeiffer S, Rojas M, Schüßler A (2014) Potato-associated arbuscular mycorrhizal fungal communities in the Peruvian Andes. Mycorrhiza 24:405–417. doi:10.1007/s00572-013-0549-0

    PubMed  Google Scholar 

  • Sharma A, Johri BN, Sharma AK, Glick BR (2003) Plant growth-promoting bacterium Pseudomonas sp. strain GRP3 influences iron acquisition in mung bean (Vigna radiata L. Wilzeck). Soil Biol Biochem 35:887–894. doi:10.1016/S0038-0717(03)00119-6

    CAS  Google Scholar 

  • Sharma A, Shankhdhar D, Shankhdhar S (2013) Enhancing grain iron content of rice by the application of plant growth-promoting rhizobacteria. Plant Soil Environ 59:89–94

    CAS  Google Scholar 

  • Sheng XF, He LY (2006) Solubilization of potassium-bearing minerals by a wild-type strain of Bacillus edaphicus and its mutants and increased potassium uptake by wheat. Can J Microbiol 52:66–72. doi:10.1139/w05-117

    CAS  PubMed  Google Scholar 

  • Siddiqui IA, Shaukat SS, Sheikh I, Khan A (2006) Role of cyanide production by Pseudomonas fluorescens CHA0 in the suppression of root-knot nematode, Meloidogyne javanica in tomato. World J Microbiol Biotechnol 22:641–650. doi:10.1007/s11274-005-9084-2

    CAS  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic press, Cambridge

    Google Scholar 

  • Smyth EM, McCarthy J, Nevin R, Khan MR, Dow JM, O'Gara F, Doohan FM (2011) In vitro analyses are not reliable predictors of the plant growth promotion capability of bacteria; a Pseudomonas fluorescens strain that promotes the growth and yield of wheat. J Appl Microbiol 111:683–692. doi:10.1111/j.1365-2672.2011.05079.x

    CAS  PubMed  Google Scholar 

  • Song G, Ryu C-M (2013) Two volatile organic compounds trigger plant self-defense against a bacterial pathogen and a sucking insect in cucumber under open field conditions. Int J Mol Sci 14:9803–9819

    PubMed Central  PubMed  Google Scholar 

  • Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448. doi:10.1111/j.1574-6976.2007.00072.x

    CAS  PubMed  Google Scholar 

  • Teixeira DA, Alfenas AC, Mafia RG, Ferreira EM, Siqueira LD, Maffia LA, Mounteer AH (2007) Rhizobacterial promotion of eucalypt rooting and growth. Braz J Microbiol 38:118–123

    Google Scholar 

  • Tester M, Langridge P (2010) Breeding technologies to increase crop production in a changing world. Science 327:818–822. doi:10.1126/science.1183700

    CAS  PubMed  Google Scholar 

  • Tjamos SE, Flemetakis E, Paplomatas EJ, Katinakis P (2005) Induction of resistance to Verticillium dahliae in Arabidopsis thaliana by the biocontrol agent K-165 and pathogenesis-related proteins gene expression. Mol Plant Microbe Interact 18:555–561. doi:10.1094/mpmi-18-0555

    CAS  PubMed  Google Scholar 

  • Toklikishvili N et al. (2010) Inhibitory effect of ACC deaminase-producing bacteria on crown gall formation in tomato plants infected by Agrobacterium tumefaciens or A. vitis. Plant Pathol 59:1023–1030. doi:10.1111/j.1365-3059.2010.02326.x

    Google Scholar 

  • Tsror L (2010) Biology, epidemiology and management of Rhizoctonia solani on potato. J Phytopathol 158:649–658. doi:10.1111/j.1439-0434.2010.01671.x

    Google Scholar 

  • Van de Mortel JE et al. (2012) Metabolic and transcriptomic changes induced in Arabidopsis by the rhizobacterium Pseudomonas fluorescens SS101. Plant Physiol 160:2173–2188. doi:10.1104/pp.112.207324

    PubMed Central  PubMed  Google Scholar 

  • Van der Ent S, Van Wees SCM, Pieterse CMJ (2009) Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry 70:1581–1588. doi:10.1016/j.phytochem.2009.06.009

    PubMed  Google Scholar 

  • Van Loon LC (2007) Plant responses to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119:243–254. doi:10.1007/s10658-007-9165-1

    Google Scholar 

  • Van Loon LC, Bakker PA, Pieterse CM (1998) Systemic resistance induced by rhizosphere bacteria. Annu Rev Phytopathol 36:453–483. doi:10.1146/annurev.phyto.36.1.453

    PubMed  Google Scholar 

  • Velivelli SLS, De Vos P, Kromann P, Declerck S, Prestwich BD (2014a) Biological control agents: from field to market, problems, and challenges. Trends Biotechnol 32:493–496. doi:10.1016/j.tibtech.2014.07.002

    CAS  PubMed  Google Scholar 

  • Velivelli SLS, Kromann P, Lojan P, Rojas M, Franco J, Suarez J, Prestwich B (2014b) Identification of mVOCs from Andean rhizobacteria and field evaluation of bacterial and mycorrhizal inoculants on growth of potato in its center of origin. Microb Ecol:1–16 doi:10.1007/s00248-014-0514-2

  • Vespermann A, Kai M, Piechulla B (2007) Rhizobacterial volatiles affect the growth of fungi and Arabidopsis thaliana. Appl Environ Microbiol 73:5639–5641. doi:10.1128/aem.01078-07

    PubMed Central  CAS  PubMed  Google Scholar 

  • Vessey JK (2003) Plant growth-promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586. doi:10.1023/A:1026037216893

    CAS  Google Scholar 

  • Walter RS, William WK, Zahi KA (2008) Managing foliar diseases: early blight, late blight and white mold. In: Johnson DA (ed) Potato health management. APS Press, Minnesota, pp 209–222

    Google Scholar 

  • Yuan J, Raza W, Shen Q, Huang Q (2012) Antifungal activity of Bacillus amyloliquefaciens NJN-6 volatile compounds against Fusarium oxysporum f. sp. cubense. Appl Environ Microbiol 78:5942–5944. doi:10.1128/aem.01357-12

    PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

The research project “VALORAM—Valorizing Andean microbial diversity through sustainable intensification of potato-based farming systems” was supported by European Commission’s Seventh Framework Program FP7/2007-2013 under grant agreement No 227522, 01/02/2009-31/01/2014.

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Velivelli, S.L.S., Sessitsch, A. & Prestwich, B.D. The Role of Microbial Inoculants in Integrated Crop Management Systems. Potato Res. 57, 291–309 (2014). https://doi.org/10.1007/s11540-014-9278-9

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