Probiotics and Plant Health pp 21-40 | Cite as
Microbial Inoculants for Optimized Plant Nutrient Use in Integrated Pest and Input Management Systems
Abstract
The use of fertilizers and pesticides has greatly increased agricultural productivity over the past few decades. However, there is still an ongoing search for additional or alternate tools that can proffer agricultural sustainability and meet the needs of profitability and greater food production for the growing world population. This review examines the enhancement of plant nutrient use efficiency derived from interactions of the diverse microorganisms that live in and around plants such as plant growth-promoting rhizobacteria (PGPR) and mycorrhizal fungi. These microorganisms form the major bases of the biorational sector of the agriculture industry which has exploded in the last few years with the production of many new microbial inoculant products and the improvement of existing products. Microbial inoculants cannot replace chemical fertilizers now or in the immediate future; thus this review discusses the concept of integrated pest and input management (IPIM), compatibility of inoculants with existing chemicals, and efficacy issues associated with biologicals. Also discussed are inoculant products, the conditions that may affect their success, the untapped potentials for agriculture, and the possible impacts on greenhouse gas emissions and global warming.
References
- Adesemoye AO, Kloepper JW (2009) Plant–microbes interactions in enhanced fertilizer use efficiency. Appl Microbiol Biotechnol 85:1–12CrossRefPubMedGoogle Scholar
- Adesemoye AO, Obini M, Ugoji EO (2008a) Comparison of plant growth-promotion with Pseudomonas aeruginosa and Bacillus subtilis in three vegetables. Braz J Microbiol 39:423–426CrossRefPubMedPubMedCentralGoogle Scholar
- Adesemoye AO, Torbert HA, Kloepper JW (2008b) Enhanced plant nutrient use efficiency with PGPR and AMF in an integrated nutrient management system. Can J Microbiol 54:876–886CrossRefPubMedGoogle Scholar
- Adesemoye AO, Torbert HA, Kloepper JW (2009) Plant growth-promoting rhizobacteria allow reduced application rates of chemical fertilizers. Microb Ecol 58:921–929CrossRefPubMedGoogle Scholar
- Akiyama H, Yan X, Yagi K (2010) Evaluation of effectiveness of enhanced-efficiency fertilizers as mitigation options for N2O and NO emissions from agricultural soils: meta-analysis. Glob Chang Biol 16:1837–1846CrossRefGoogle Scholar
- Arshad M, Shaharoona B, Mahmood T (2008) Inoculation with Pseudomonas spp. containing ACC-deaminase partially eliminates the effects of drought stress on growth, yield, and ripening of pea (Pisum sativum L.) Pedosphere 18:611–620CrossRefGoogle Scholar
- Artursson V, Finlay RD, Jansson JK (2006) Interactions between arbuscular mycorrhizal fungi and bacteria and their potential for stimulating plant growth. Environ Microbiol 8(1):1–10CrossRefPubMedGoogle Scholar
- Barea JM, Azcón R, Azcón-Aguilar C (1993) Mycorrhiza and crops. In: Tommerup I (ed) Advances in plant pathology, vol 9: Mycorrhiza: a synthesis. Academic, London, pp 167–189. ISBN: 84-604-7996-XGoogle Scholar
- Barea JM, Azcon R, Azcon-Aguilar C (2002) Mycorrhizosphere interactions to improve plant fitness and soil quality. Antonie van Leeuwenkoek 81:343–351CrossRefGoogle Scholar
- Bashan Y (1999) Interactions of Azospirillum spp. in soils: a review. Biol Fertil Soils 29:246–256CrossRefGoogle Scholar
- Bashan Y, Holguin G (1998) Proposal for the division of plant growth-promoting rhizobacteria into two classifications: biocontrol-PGPB (plant growth-promoting bacteria) and PGPB. Soil Biol Biochem 30:1225–1228CrossRefGoogle Scholar
- Biswas JC, Ladha JK, Dazzo FB (2000) Rhizobia inoculation improves nutrient uptake and growth of lowland rice. Soil Sci Soc Am J 64:1644–1650CrossRefGoogle Scholar
- Bremner JM (1997) Sources of nitrous oxide in soils. Nutr Cycl Agroecosyst 49:7–16CrossRefGoogle Scholar
- Buensanteai N, Yuen GY, Prathuangwong S (2008) The biocontrol bacterium Bacillus amyloliquefaciens KPS46 produces auxin, surfactin and extracellular proteins for enhanced growth of soybean plant. Thai J Agric Sci 41:101–116Google Scholar
- Calvo P, Watts DB, Ames RN, Kloepper JW, Torbert HA (2013) Microbial-based inoculants impact nitrous oxide emissions from an incubated soil medium containing urea fertilizers. J Environ Qual 42:704–712CrossRefPubMedGoogle Scholar
- Calvo P, Nelson L, Kloepper JW (2014) Agricultural uses of plant biostimulants. Plant Soil 383:3–41CrossRefGoogle Scholar
- Calvo P, Watts DB Kloepper JW, Torbert HA (2016a) Application of microbial-based inoculants for reducing N2O emissions from soil under two difference ammonium nitrate-based fertilizers. Soil Science. 181:427–434Google Scholar
- Calvo P, Watts DB, Kloepper JW, Torbert HA (2016b) Microbial-based inoculants influence on N2O emissions from soil planted to corn (Zea mays L.) under greenhouse conditions with different nitrogen fertilizer regimens. Can J Microbiol 62:1041–1056Google Scholar
- Canbolat M, Bilen S, Çakmak R, Şahin F, Aydın A (2006) Effect of plant growth-promoting bacteria and soil compaction on barley seedling growth, nutrient uptake, soil properties and rhizosphere microflora. Biol Fert Soils 42:350–357CrossRefGoogle Scholar
- Chabot R, Antoun H, Cescas M (1996) Growth promotion of maize and lettuce by phosphate-solubilizing Rhizobium leguminosarum biovar phaseoli. Plant Soil 184:311–321CrossRefGoogle 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 prospect. Appl Environ Microbiol 71:4951–4959CrossRefPubMedPubMedCentralGoogle Scholar
- Cook RJ (2002) Advances in plant health management in the twentieth century. Ann Rev Phytopathol 38:95–116CrossRefGoogle Scholar
- de Freitas JR, Banerjee MR, Germida JJ (1997) Phosphatesolubilizing rhizobacteria enhance the growth and yield but not phosphorus uptake of canola (Brassica napus). Biol Fertil Soils 36:842–855Google Scholar
- Del Grosso SJ, Mosier AR, Parton WJ, Ojima DS (2005) DAYCENT model analysis of past and contemporary soil N2O and net greenhouse gas flux for major crops in the USA. Soil Tillage Res 83:9–24CrossRefGoogle Scholar
- Dell CJ, Han K, Bryant RB, Schmidt JP (2014) Nitrous oxide emissions with enhanced efficiency nitrogen fertilizers in a rainfed system. Agron J 106:723–731CrossRefGoogle Scholar
- Egamberdieva D (2007) The effect of plant growth promoting bacteria on growth and nutrient uptake of maize in two different soils. Appl Soil Ecol 36:184–189CrossRefGoogle Scholar
- Egamberdieva D, Adesemoye AO (2016) Improvement of crop protection and yield in hostile agroecological conditions with PGPR-based biopesticide and biofertilizer formulations. In: Arora NK, Mehnaz S, Balestrini R (eds) Bioformulations for sustainable agriculture. Springer, pp 199–211. doi: 10.1007/978-81-322-2779-3_11
- Figueiredo M, Seldin L, Araujo F, Mariano R (2010) Plant growth promoting rhizobacteria: fundamentals and applications. In: Maheshwari DK (ed) Plant growth and health promoting bacteria. Springer, Berlin, pp 21–43Google Scholar
- Firestone MK, Davidson EA (1989) Microbial basis of NO and N2O production and consumption in soil. In: Andreae MO, Schimel DS (eds) Exchange of trace gases between terrestrial ecosystems and the atmosphere. Wiley, New York, pp 7–21Google Scholar
- Fravel DR (2005) Commercialization and implementation of biocontrol. Annu Rev Phytopathol 43:337–359CrossRefPubMedGoogle Scholar
- Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117CrossRefGoogle Scholar
- Glick BR, Bashan Y (1997) Genetic manipulation of plant growth-promoting bacteria to enhance biocontrol of phytopathogens. Biotechnol Adv 15:353–378CrossRefPubMedGoogle Scholar
- Glick BR, Todorovic B, Czarny J, Cheng Z, Duan J, McConkey B (2007) Promotion of plant growth by bacterial ACC deaminase. Crit Rev Plant Sci 26:227–242CrossRefGoogle Scholar
- Gruhn P, Golletti F, Yudelman M (2000) Integrated nutrient management, soil fertility, and sustainable agriculture: current issues and future challenges. A 2020 vision for food, agriculture, and the environment, discussion paper 32. International Food Policy Research Institute, Washington, pp 15–16Google Scholar
- Haas D, Defago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3:307–319CrossRefPubMedGoogle Scholar
- Halvorson AD, Del Grosso SJ, Alluvione F (2010) Nitrogen source effects on nitrous oxide emissions from irrigated no-till corn. J Environ Qual 39:1554–1562CrossRefPubMedGoogle Scholar
- Halvorson AD, Snyder CS, Blaylock AD, Del Grosso SJ (2014) Enhanced-efficiency nitrogen fertilizers: potential role in nitrous oxide emission mitigation. Agron J 106:715–722CrossRefGoogle Scholar
- Hansen J, Ruedy R, Sato M, Lo K (2010) Global surface temperature change. Rev Geophys 48:4. doi: 10.1029/2010RG000345
- Hussain A, Arshad M, Hussain E (1987) Response of maize (Zea mays) to Azotobacter inoculation under fertilized and unfertilized conditions. Biol Fert Soils 4:73–77Google Scholar
- Idriss EE, Makarewicz O, Farouk A, Rosner K, Greiner R, Bochow H, Richter T, Borriss R (2002) Extracellular phytase activity of Bacillus amyloliquefaciens FZB45 contributes to its plant-growth-promoting effect. Microbiology 148:2097–2109CrossRefPubMedGoogle Scholar
- Joo G-J, Kim Y-M, Lee IJ, Song KS, Rhee IK (2004) Growth promotion of red pepper plug seedlings and the production of gibberellins by Bacillus cereus, Bacillus macroides, and Bacillus pumilus. Biotechnol Lett 26:487–491CrossRefPubMedGoogle Scholar
- Kloepper JW, Lifshitz R, Zablotowicz RM (1989) Free living bacterial inocula for enhancing crop productivity. Trends Biotechnol 7:39–44CrossRefGoogle Scholar
- Kloepper JW, Zablotowick RM, Tipping EM, Lifshitz R (1991) Plant growth promotion mediated by bacterial rhizosphere colonizers. In: Keister DL, Cregan PB (eds) The rhizosphere and plant growth. Kluwer Academic Press, DordrechtGoogle Scholar
- Kohler J, Hernandez JA, Caravaca F, Roldan A (2008) Plant growth-promoting rhizobacteria and arbuscular mycorrhizal fungi modify alleviation biochemical mechanisms in waterstressed plants. Funct Plant Biol 35:141–151CrossRefGoogle Scholar
- Kumar KVK, Reddy MS, Kloepper JW, Lawrence KS, Yellareddygari SKR, Zhou XG, Sudini H, Surrendranatha Reddy EC, Groth DE, Miller ME (2011) Screening and selection of elite plant growth promoting rhizobacteria (PGPR) for suppression of Rhizoctonia solani and enhancement of rice seedling vigor. J Pure Appl Microbiol 5(2):641–651Google Scholar
- Lim J-H, Kim S-D (2013) Induction of drought stress resistance by multi-functional PGPR Bacillus licheniformis K11 in pepper. Plant Pathol J 29:201–208CrossRefPubMedPubMedCentralGoogle Scholar
- Mandic-Mulec I, Prosser JI (2011) Diversity of endospore-forming bacteria in soil: characterization and driving mechanisms. In: Logan NA, Vos PD (eds) Endospore-forming soil bacteria. Springer, LondonGoogle Scholar
- Millar N, Robertson G, Grace P, Gehl R, Hoben J (2010) Nitrogen fertilizer management for nitrous oxide (N2O) mitigation in intensive corn (Maize) production: an emissions reduction protocol for US Midwest agriculture. Mitig Adapt Strateg Global Change 15:185–204CrossRefGoogle Scholar
- Mosier AR, Delgado JA, Keller M (1998) Methane and nitrous oxide fluxes in an acid Oxisol in western Puerto Rico: effects of tillage, liming and fertilization. Soil Biol Biochem 30:2087–2098CrossRefGoogle Scholar
- Myhre G, Shindell D, Bréon F-M, Collins W, Fuglestvedt J, Huang J, Koch D, Lamarque J-F, Lee D, Mendoza B, Nakajima T, Robock A, Stephens G, Takemura T, Zhang H (2013) Anthropogenic and natural radiative forcing. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Climate change 2013: the physical science basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, CambridgeGoogle Scholar
- Nelson LM (2004) Plant growth promoting rhizobacteria (PGPR): prospects for new inoculants. Online Crop Manag. doi: 10.1094/CM-2004-0301-05-RV
- Okon Y, Kapulnik Y (1986) Development and function of Azospirillum-inoculated roots. Plant Soil 90:3–16CrossRefGoogle Scholar
- Omar MNA, Mahrous NM, Hamouda AM (1996) Evaluating the efficiency of inoculating some diazotrophs on yield and protein content of 3 wheat cultivars under graded levels of nitrogen fertilization. Ann Agric Sci 41:579–590Google Scholar
- Parkin TB (1987) Soil microsites as a source of denitrification variability. Soil Sci Soc Am J 51:1194–1199CrossRefGoogle Scholar
- Parkin TB, Kaspar TC (2006) Nitrous oxide emissions from corn-soybean systems in the Midwest. J Environ Qual 35:1496–1506CrossRefPubMedGoogle Scholar
- Parr JF, Papendick RI, Hornick SB, Meyer RE (1992) Soil quality: attributes and relationship to alternative and sustainable agriculture. Am J Altern Agric 7:5–11CrossRefGoogle Scholar
- Piccini D, Azcon R (1987) Effect of phosphate-solubilizing bacteria and vesicular-arbuscular mycorrhizal fungi on the utilization of Bayovar rock phosphate by alfalfa plants using a sand-vermiculite medium. Plant Soil 101:45–50CrossRefGoogle Scholar
- Probanza A, Lucas JA, Acero N, Gutierrez Mañero FJ (1996) The influence of native rhizobacteria on european alder (Alnus glutinosa (L.) Gaertn.) growth. Part I. Characterization of growth promoting and inhibiting bacterial strains. Plant Soil 182:59–66CrossRefGoogle Scholar
- Reid A, Greene SE (2012) How microbes can help feed the world. Report of an American Academy of Microbiology Colloquium, p 3Google Scholar
- Requena N, Jimenez I, Toro M, Barea JM (1997) Interactions between plant-growth-promoting rhizobacteria (PGPR), arbuscular mycorrhizal fungi and Rhizobium spp. in the rhizosphere of Anthyllis cytisoides, a model legume for revegetation in mediterranean semi-arid ecosystems. New Phytol 136:667–677CrossRefGoogle Scholar
- Rodriguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339CrossRefPubMedGoogle Scholar
- Schenck NC (1981) Can mycorrhizae control root diseases? Plant Dis 65:230–234CrossRefGoogle Scholar
- Sharma A, Shankhdar D, Shankhdhar SC (2013) Enhancing grain iron content of rice by the application of plant growth promoting rhizobacteria. Plant Soil Environ 59:89–94Google Scholar
- Shen J, Li C, Mi G, Li L, Yuan L, Jiang R, Fuso F (2012) Maximizing root/rhizosphere efficiency to improve crop productivity and nutrient use efficiency in intensive agriculture of China. J Exp Bot 64:1181–1192CrossRefPubMedGoogle 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 52:66–72CrossRefPubMedGoogle Scholar
- Singh SN, Verma A (2007) Environmental review: the potential of nitrification inhibitors to manage the pollution effect of nitrogen fertilizers in agricultural and other soils: a review. Environ Pract 9:266–279CrossRefGoogle Scholar
- Sistani KR, Jn-Baptiste M, Lovanh N, Cook KL (2011) Atmospheric emissions of nitrous oxide, methane, and carbon dioxide from different nitrogen fertilizers. J Environ Qual 40:1797–1805CrossRefPubMedGoogle Scholar
- Snyder CS, Bruulsema TW, Jensen TL, Fixen PE (2009) Review of greenhouse gas emissions from crop production systems and fertilizer management effects. Agric Ecosyst Environ 133:247–266CrossRefGoogle Scholar
- Someya N, Akutsu K (2006) Biocontrol of plant diseases by genetically modified microorganisms: current status and future prospects. In: Siddiqui Z (ed) PGPR: biocontrol and biofertilization. Springer, Dordrecht, pp 297–312Google Scholar
- Stephens JHG, Rask HM (2000) Inoculant production and formulation. Field Crop Res 65:249–258CrossRefGoogle Scholar
- The Office of Technology (1979) Pest management strategies, vols 1 and 2. U.S. Government Printing Office, WashingtonGoogle Scholar
- Tien TM, Gaskins MH, Hubbell DH (1979) Plant growth substances produced by Azospirillum brasilense and their effect on the growth of pearl millet (Pennisetum americanum L.) Appl Environ Microbiol 37:1016–1024PubMedPubMedCentralGoogle Scholar
- US Environmental Protection Agency (2012) Inventory of U.S. greenhouse gas emissions and sinks: 1990–2010. EPA 430-R-12-001. U.S. Environmental Protection Agency, Washington. http://www.epa.gov/climatechange/ghgemissions/usinventoryreport.html
- USDA Economic Research Service (2012) Fertilizer use and markets: 1960–2011. USDA Economic Research Service, Washington. http://www.ers.usda.gov/topics/farm-practices-management/chemical-inputs/fertilizer-use-markets.aspx
- Vardharajula S, Ali SZ, Grover M, Reddy G, Bandi V (2011) Drought-tolerant plant growth promoting Bacillus spp.: effect on growth, osmolytes, and antioxidant status of maize under drought stress. J Plant Interact 6:1–14CrossRefGoogle Scholar
- Vassileva M, Serrano M, Bravo V, Jurado E, Nikolaeva I, Martos V, Vassilev N, (2010) Multifunctional properties of phosphate-solubilizing microorganisms grown on agro-industrial wastes in fermentation and soil conditions. Applied Microbiology and Biotechnology 85(5):1287–1299Google Scholar
- Venterea RT, Dolan MS, Ochsner TE (2010) Urea decreases nitrous oxide emissions compared with anhydrous ammonia in a Minnesota corn cropping systems. Soil Sci Soc Am J 74:407–418CrossRefGoogle Scholar
- Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586CrossRefGoogle Scholar
- Volpin H, Phillips DA (1998) Respiratory elicitors from Rhizobium meliloti affect intact alfalfa roots. Plant Physiol 116:777–783CrossRefPubMedPubMedCentralGoogle Scholar
- Watts DB, Torbert HA, Prior SA, Huluka G (2010) Long-term tillage and poultry litter impacts soil carbon and nitrogen mineralization and fertility. Soil Sci Soc Am J 74:1239–1247CrossRefGoogle Scholar
- Watts DB, Runion GB, Smith Nannenga KW, Torbert HA (2015) Impact of enhanced efficiency nitrogen fertilizer on greenhouse gas emissions in a coastal plain soil under cotton. J Environ Qual 44(6):1699–1710CrossRefPubMedGoogle Scholar
- Wu SC, Caob ZH, Lib ZG, Cheunga KC, Wonga MH (2005) Effects of biofertilizer containing N-fixer, P and K solubilizers and AM fungi on maize growth: a greenhouse trial. Geoderma 125:155–166CrossRefGoogle Scholar
- Yanni YG, Rizk RY, Corich V, Squartini A, Ninke K, Philip-Hollingsworth S, Orgambide F, de Bruijn F, Stoltzfus J, Buckley D, Schmidt TM, Mateos PF, Ladha JK, Dazzo FB (1997) Natural endophytic association between Rhizobium leguminosarum bv. trifolii and rice roots and assessment of its potential to promote rice growth. Plant Soil 194:99–114CrossRefGoogle Scholar
- Yildirim E, Taylor AG, Spittler TD (2006) Ameliorative effects of biological treatments on growth of squash plants under salt stress. Sci Hortic 111:1–6CrossRefGoogle Scholar
- Zehnder GW, Murphy JF, Sikora EJ, Kloepper JW (2001) Application of rhizobacteria for induced resistance. Eur J Plant Pathol 107:39–50CrossRefGoogle Scholar
- Zhang S, White KL, Martinez MC, McInroy JA, Kloepper JW, Klassen W (2010) Evaluation of plant growth-promoting rhizobacteria for control of Phytophthora blight on squash under greenhouse conditions. Biol Control 53:129–135CrossRefGoogle Scholar
- Zhou L, Yuen G, Wang Y, Wei L, Ji G (2016) Evaluation of bacterial biological control agents for control of rootknot nematode disease on tomato. Crop Prot 84:8–13CrossRefGoogle Scholar