[en] TaqMan-based quantitative PCR (qPCR) assays were developed to study the persistence of two well-characterized strains of plant growth-promoting rhizobacteria (PGPR), Pseudomonas fluorescens Pf153 and Pseudomonas sp. DSMZ 13134, in the root and rhizoplane of inoculated maize plants. This was performed in pot experiments with three contrasting field soils (Buus, Le Caron and DOK-M). Potential cross-reactivity of the qPCR assays was assessed with indigenous Pseudomonas and related bacterial species, which had been isolated from the rhizoplane of maize roots grown in the three soils and then characterized by Matrix-Assisted Laser Desorption Ionization (MALDI) Time-of-Flight (TOF) mass spectrometry (MS). Sensitivity of the qPCR expressed as detection limit of bacterial cells spiked into a rhizoplane matrix was 1.4 × 102 CFU and 1.3 × 104 CFU per gram root fresh weight for strain Pf153 and DSMZ 13134, respectively. Four weeks after planting and inoculation, both strains could readily be detected in root and rhizoplane, whereas only Pf153 could be detected after 8 weeks. The colonization rate of maize roots by strain Pf153 was significantly influenced by the soil type, with a higher colonization rate in the well fertile and organic soil of Buus. Inoculation with strain DSMZ 13134, which colonized roots and rhizoplane to the same degree, independently of the soil type, increased yield of maize, in terms of biomass accumulation, only in the acidic soil of Le Caron, whereas inoculation with strain Pf153 reduced yield in the soil Buus, despite of its high colonization rate and persistence. These results indicate that the colonization rate and persistence of inoculated Pseudomonas strains can be quantitatively assessed by the TaqMan-based qPCR technique, but that it cannot be taken for granted that inoculation with a well-colonizing and persistent Pseudomonas strain has a positive effect on yield of maize.
Mosimann, Carla; Department of Environmental Sciences, Botany, Zürich-Basel Plant Science Center, University of BaselBasel, Switzerland, Research Institute of Organic Agriculture (FIBL)Frick, Switzerland
Oberhänsli, Thomas; Research Institute of Organic Agriculture (FIBL) Frick, Switzerland
Ziegler, Dominik; Mabritec AG Riehen, Switzerland
Nassal, Dinah; Institute of Soil Science and Land Evaluation, University of Hohenheim Stuttgart, Germany
Kandeler, Ellen; Institute of Soil Science and Land Evaluation, University of Hohenheim Stuttgart, Germany
Boller, Thomas; Department of Environmental Sciences, Botany, Zürich-Basel Plant Science Center, University of Basel Basel, Switzerland
Mäder, Paul; Research Institute of Organic Agriculture (FIBL) Frick, Switzerland
Thonar, Cécile ; Université de Liège - ULiège > Département GxABT > Plant Sciences ; Research Institute of Organic Agriculture (FIBL) Frick, Switzerland
Language :
English
Title :
Tracing of Two Pseudomonas Strains in the Root and Rhizoplane of Maize, as Related to Their Plant Growth-Promoting Effect in Contrasting Soils.
FP7 - 312117 - BIOFECTOR - Resource Preservation by Application of BIOefFECTORs in European Crop Production
Funders :
EU - European Union [BE]
Funding text :
We thank following persons for the provision of bacterial strains: J. Fuchs (FiBL, Switzerland) for P. fluorescens Pf153, W. Vogt (Sourcon-Padena, Germany) for Pseudomonas sp. DSMZ 13134, K. Smalla (Julius K?hn Institute, Germany) for P. jessenii RU47 and M. Maurhofer (ETH Z?rich, Switzerland) for P. protegens CHA0, P. protegens Pf-5 as well as P. chlororaphis LMG 1245. We thank H.-M. Krause (FiBL, Switzerland) for provision of the plasmid for the internal standard as well as D. Gobbin (Tecan Group Ltd, Switzerland) for the sequence of the SCAR fragment. This study was funded by the BIOFECTOR project (Resource preservation by application of BIOefFECTORs in European crop production, grant agreement number 312117) under the 7th Framework Program (FP7), European Commission, Brussels, Belgium.
Adesina, M. F., Lembke, A., Costa, R., Speksnijder, A., and Smalla, K. (2007). Screening of bacterial isolates from various European soils for in vitro antagonistic activity towards Rhizoctonia solani and Fusarium oxysporum: site-dependent composition and diversity revealed. Soil Biol. Biochem. 39, 2818-2828. doi: 10.1016/j.soilbio.2007.06.004
Alstrom, S., and Burns, R. G. (1989). Cyanide production by rhizobacteria as a possible mechanism of plant-growth inhibition. Biol. Fertil. Soils 7, 232-238. doi: 10.1007/BF00709654
Barea, J. M., Andrade, G., Bianciotto, V. V., Dowling, D., Lohrke, S., Bonfante, P., et al. (1998). Impact on arbuscular mycorrhiza formation of Pseudomonas strains used as inoculants for biocontrol of soil-borne fungal plant pathogens. Appl. Environ. Microbiol. 64, 2304-2307.
Bashan, Y., and de-Bashan, L. E. (2010). How the plant growth-promoting Bacterium Azospirillum promotes plant growth-a critical assessment. Adv. Agron. 108, 77-136. doi: 10.1016/s0065-2113(10)08002-8
Bashan, Y., Puente, M. E., Rodriguez-Mendoza, M. N., Toledo, G., Holguin, G., Ferrera-Cerrato, R., et al. (1995). Survival of Azospirillum brasilense in the bulk soil and rhizosphere of 23 soil types. Appl. Environ. Microbiol. 61, 1938-1945.
Brundrett, M. (1991). Mycorrhizas in natural ecosystems. Adv. Ecol. Res. 21, 171-313. doi: 10.1016/S0065-2504(08)60099-9
Brundrett, M. C., Piché, Y., and Peterson, R. L. (1984). A new method for observing the morphology of vesicular-arbuscular mycorrhizae. Can. J. Bot. 62, 2128-2134. doi: 10.1139/b84-290
Buddrus-Schiemann, K., Schmid, M., Schreiner, K., Welzl, G., and Hartmann, A. (2010). Root colonization by Pseudomonas sp. DSMZ 13134 and impact on the indigenous rhizosphere bacterial community of barley. Microb. Ecol. 60, 381-393. doi: 10.1007/s00248-010-9720-8
Bull, C., Weller, D., and Thomashow, L. (1991). Relationship between root colonization and suppression of Gaeumannomyces graminis var. triciti by Pseudomonas strain 2-79. Phytopathology 81, 954-959. doi: 10.1094/Phyto-81-954
Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., et al. (2009). The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55, 611-622. doi: 10.1373/clinchem.2008.112797
Chin-A-Woeng, T. F., Bloemberg, G. V., Mulders, I. H., Dekkers, L. C., and Lugtenberg, B. J. J. (2000). Root colonization by phenazine-1-carboxamide-producing bacterium Pseudomonas chlororaphis PCL1391 is essential for biocontrol of tomato foot and root rot. MPMI 13, 1340-1345. doi: 10.1094/MPMI.2000.13.12.1340
Compant, S., Clément, C., and 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
Demeter International, e.V. (2012). Production Standards for the Use of Demeter, Biodynamic and Related Trademarks. Demeter International production standards: The standards committee.
Di, H. J., and Cameron, K. C. (2002). Nitrate leaching in temperate agroecosystems: sources, factors and mitigating strategies. Nutr. Cycling Agroecosyst. 64, 237-256. doi: 10.1023/A:1021471531188
Egamberdiyeva, D. (2007). The effect of plant growth promoting bacteria on growth and nutrient uptake of maize in two different soils. Appl. Soil Ecol. 36, 184-189. doi: 10.1016/j.apsoil.2007.02.005
El Zemrany, H., Czarnes, S., Hallett, P. D., Alamercery, S., Bally, R., and Monrozier, L. J. (2007). Early changes in root characteristics of maize (Zea mays) following seed inoculation with the PGPR Azospirillum lipoferum CRT1. Plant Soil 291, 109-118. doi: 10.1007/s11104-006-9178-0
FAOSTAT (2012). Available online at: http://faostat3.fao.org/home/E
Fliessbach, A., Winkler, M., Lutz, M. P., Oberholzer, H. R., and Mäder, P. (2009). Soil amendment with Pseudomonas fluorescens CHA0: lasting effects on soil biological properties in soils low in microbial biomass and activity. Microb. Ecol. 57, 611-623. doi: 10.1007/s00248-009-9489-9
Flisch, R., Sinaj, S., Charles, R., and Richner, W. (2009). Grundlagen für die Düngung im Acker-und Futterbau (GRUDAF). Agrarforschung Schweiz. 16, 6-31. Available online at: http://www.agrarforschungschweiz.ch/archiv_11en.php?id_artikel=1449
Fröhlich, A., Buddrus-Schiemann, K., Durner, J., Hartmann, A., and von Rad, U. (2012). Response of barley to root colonization by Pseudomonas sp. DSMZ 13134 under laboratory, greenhouse, and field conditions. J. Plant Interact. 7, 1-9. doi: 10.1080/17429145.2011.597002
Fuchs, J.-G. (1993). Paramètres Influençant la Lutte Biologique Contre la Fusariose Vasculaire de la Tomate et la Pourriture Noire des Racines de Concombre. Dissertation Techn. Wiss. ETH Zürich, MS Wolfe; Korref: G. Défago.
Fuchs, J.-G., Moënne-Loccoz, Y., and Defago, G. (2000). The laboratory medium used to grow biocontrol Pseudomonas sp. Pf153 infuences its subsequent ability to protect cucumber from black root rot. Soil Biol. Biochem. 32, 421-425. doi: 10.1016/S0038-0717(99)00169-8
Gholami, A., Shahsavani, S., and Nezarat, S. (2009). The effect of Plant Growth Promoting Rhizobacteria (PGPR) on germination, seedling growth and yield of maize. Int. J. Biol. Life Science 5, 35-40.
Gobbin, D., Rezzonico, F., and Gessler, C. (2007). Quantification of the biocontrol agent Pseudomonas fluorescens Pf153 in soil using a quantitative competitive PCR assay unaffected by variability in cell lysis-and DNA-extraction efficiency. Soil Biol. Biochem. 39, 1609-1619. doi: 10.1016/j.soilbio.2007.01.015
Green, M. J., Thompson, D. A., and MacKenzie, D. J. (1999). Easy and Efficient DNA extraction from woody plants for the detection of Phytoplasmas by polymerase chain reaction. Plant Dis 83, 482-485. doi: 10.1094/PDIS.1999.83.5.482
Gyaneshwar, P., Kumar, G. N., Parekh, L. J., and Poole, P. S. (2002). Role of soil microorganisms in improving P nutrition of plants. Plant Soil 245, 83-93. doi: 10.1023/A:1020663916259
Gyaneshwar, P., Naresh Kumar, G., and Parekh, L. J. (1998). Effect of buffering on the phosphate-solubilizing ability of microorganisms. World J. Microb. Biot. 14, 669-673. doi: 10.1023/A:1008852718733
Hartel, P. G., Fuhrmann, J. J., Johnson, W. F., Wolf, D. C., Lawrence, E. G., Staley, T. E., et al. (1994). Survival of a lacZY-containing Pseudomonas putida strain under stressful abiotic soil conditions. Soil Sci. Soc. Am. J. 58, 770-776. doi: 10.2136/sssaj1994.03615995005800030019x
Höppener-Ogawa, S., Leveau, J. H., Smant, W., van Veen, J. A., and de Boer, W. (2007). Specific detection and real-time PCR quantification of potentially mycophagous bacteria belonging to the genus Collimonas in different soil ecosystems. Appl. Environ. Microbiol. 73, 4191-4197. doi: 10.1128/AEM.00387-07
Howell, C. R., and Stipanovic, R. D. (1980). Suppression of Phytium ultimum-Induced Damping-Off of Cotton seedlings by Pseudomonas fluorescens and its antibiotic, pyoluteorin. Phytopathology 70, 712-715. doi: 10.1094/Phyto-70-712
Ibekwe, A. M., and Grieve, C. M. (2003). Detection and quantification of Escherichia coli O157: H7 in environmental samples by real-time PCR. J. Appl. Microbiol. 94, 421-431. doi: 10.1046/j.1365-2672.2003.01848.x
IFOAM (ed.). (2006). The IFOAM Norms for Organic Production and Processing. Bonn: Die Deutsche Bibliothek.
Jansa, J., Mozafar, A., Anken, T., Ruh, R., Sanders, I. R., and Frossard, E. (2002). Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza 12, 225-234. doi: 10.1007/s00572-002-0163-z
Jones, D. L. (1998). Organic acids in the rhizosphere-a critical review. Plant Soil 205, 25-44. doi: 10.1023/A:1004356007312
Kawasaki, E. S. (1990). "Sample preparation from blood, cells, and other fluids, " in PCR Protocols-A Guide to Methods and Applications, eds M. A. Innis, D. H. Gelfand, J. J. Sninsky, and T. J. White (New York, NY: Academic Press), 146-152.
Khan, M. S., Zaidi, A., and Wani, P. A. (2007). Role of phosphate-solubilizing microorganisms in sustainable agriculture-A review. Agron. Sustain. Dev. 27, 29-43. doi: 10.1051/agro:2006011
King, E. O., Ward, M. K., and Raney, D. E. (1954). Two simple media for the demonstration of pyocyanin and fluorescin. J. Lab. Clin. Med. 44, 301-307.
Kremer, R. J., and Li, J. M. (2003). Developing weed-suppressive soils through improved soil quality management. Soil Tillage Res. 72, 193-202. doi: 10.1016/S0167-1987(03)00088-6
Kremer, R. J., and Souissi, T. (2001). Cyanide production by rhizobacteria and potential for suppression of weed seedling growth. Curr. Microbiol. 43, 182-186. doi: 10.1007/s002840010284
Llop, P., Caruso, P., Cubero, J., Morente, C., and López, M. M. (1999). A simple extraction procedure for efficient routine detection of pathogenic bacteria in plant material by polymerase chain reaction. J. Microbiol. Methods 37, 23-31. doi: 10.1016/S0167-7012(99)00033-0
Lucy, M., Reed, E., and Glick, B. R. (2004). Applications of free living plant growth-promoting rhizobacteria. Antonie Van Leeuwenhoek 86, 1-25. doi: 10.1023/B:ANTO.0000024903.10757.6e
Mäder, P., Edenhofer, S., Boller, T., Wiemken, A., and Niggli, U. (2000). Arbuscular mycorrhizae in a long-term field trial comparing low-input (organic, biological) and high-input (conventional) farming systems in a crop rotation. Biol. Fertil. Soils 31, 150-156. doi: 10.1007/s003740050638
Mäder, P., Fliessbach, A., Dubois, D., Gunst, L., Fried, P., and Niggli, U. (2002). Soil fertility and biodiversity in organic farming. Science 296, 1694-1697. doi: 10.1126/science.1071148
Mäder, P., Kaiser, F., Adholeya, A., Singh, R., Uppal, H. S., Sharma, A. K., et al. (2011). Inoculation of root microorganisms for sustainable wheat-rice and wheat-black gram rotations in India. Soil Biol. Biochem. 43, 609-619. doi: 10.1016/j.soilbio.2010.11.031
Martinez-Viveros, O., Jorquera, M. A., Crowley, D. E., Gajardo, G., and Mora, M. L. (2010). Mechanisms and practical considerations involved in plant growth promotion by rhizobacteria. J. Soil Sci. Plant Nutr. 10, 293-319. doi: 10.4067/S0718-95162010000100006
Mayo, K., Davis, R. E., and Motta, J. (1986). Stimulation of germination of spores of Glomus versiforme by spore-associated bacteria. Mycologia 78, 426-431. doi: 10.2307/3793046
Meyer, J. B., Frapolli, M., Keel, C., and Maurhofer, M. (2011). Pyrroloquinoline quinone biosynthesis gene pqqC, a novel molecular marker for studying the phylogeny and diversity of phosphate-solubilizing pseudomonads. Appl. Environ. Microbiol. 77, 7345-7354. doi: 10.1128/AEM.05434-11
Meyer, J. R., and Linderman, R. G. (1986). Response of subterranean clover to dual inoculation with vesicular-arbuscular mycorrhizal fungi and a plant growth-promoting bacterium, Pseudomonas putida. Soil Biol. Biochem. 18, 185-190. doi: 10.1016/0038-0717(86)90025-8
Miller, S. H., Browne, P., Prigent-Combaret, C., Combes-Meynet, E., Morrissey, J. P., and O'Gara, F. (2010). Biochemical and genomic comparison of inorganic phosphate solubilization in Pseudomonas species. Environ. Microbiol. Rep. 2, 403-411. doi: 10.1111/j.1758-2229.2009.00105.x
Mulet, M., Gomila, M., Scotta, C., Sánchez, D., Lalucat, J., and García-Valdés, E. (2012). Concordance between whole-cell matrix-assisted laser-desorption/ionization time-of-flight mass spectrometry and multilocus sequence analysis approaches in species discrimination within the genus Pseudomonas. Syst. Appl. Microbiol. 35, 455-464. doi: 10.1016/j.syapm.2012.08.007
Muyzer, G., de Waal, E. C., and Uitterlinden, A. G. (1993). Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl. Environ. Microbiol. 59, 695-700.
Nkebiwe, N. P., Weinmann, M., and Müller, T. (2016). Improving fertilizer-depot exploitation and maize growth by inoculation with plant growth-promoting bacteria: from lab to field. Chem. Biol. Technol. Agric. 3:15. doi: 10.1186/s40538-016-0065-5
Oehl, F., Sieverding, E., Mäder, P., Dubois, D., Ineichen, K., Boller, T., et al. (2004). Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia 138, 574-583. doi: 10.1007/s00442-003-1458-2
Omirou, M., Fasoula, D. A., and Ioannides, I. M. (2016). Bradyrhizobium inoculation alters indigenous AMF community assemblages and interacts positively with AMF inoculum to improve cowpea performance. Appl. Soil Ecol. 108, 381-389. doi: 10.1016/j.apsoil.2016.09.018
Philippot, L., Tscherko, D., Bru, D., and Kandeler, E. (2011). Distribution of high bacterial taxa across the chronosequence of two alpine glacier forelands. Environ. Microbiol. 61, 303-312. doi: 10.1007/s00248-010-9754-y
Phillips, J. M., and Hayman, D. S. (1970). Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc. 55, 158. doi: 10.1016/S0007-1536(70)80110-3
Postma, J. A., and Lynch, J. P. (2011). Theoretical evidence for the functional benefit of root cortical aerenchyma in soils with low phosphorus availability. Ann. Bot. 107, 829-841. doi: 10.1093/aob/mcq199
Ramette, A., Frapolli, M., Fischer-Le Saux, M., Gruffaz, C., Meyer, J.-M., Défago, G., et al. (2011). Pseudomonas protegens sp. nov., widespread plant-protecting bacteria producing the biocontrol compounds 2, 4-diacetylphloroglucinol and pyoluteorin. Syst. Appl. Microbiol. 34, 180-188. doi: 10.1016/j.syapm.2010.10.005
Rodríguez, H., and 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
Rosas, S. B., Avanzini, G., Carlier, E., Pasluosta, C., Pastor, N., and Rovera, M. (2009). Root colonization and growth promotion of wheat and maize by Pseudomonas aurantiaca SR1. Soil Biol. Biochem. 41, 1802-1806. doi: 10.1016/j.soilbio.2008.10.009
Sauer, S., and Kliem, M. (2010). Mass spectrometry tools for the classification and identification of bacteria. Nat. Rev. Microbiol. 8, 74-82. doi: 10.1038/nrmicro2243
Savazzini, F., Longa, C. M., Pertot, I., and Gessler, C. (2008). Real-time PCR for detection and quantification of the biocontrol agent Trichoderma atroviride strain SC1 in soil. J. Microbiol. Methods 73, 185-194. doi: 10.1016/j.mimet.2008.02.004
Schinner, F., öhlinger, R., Kandeler, E., and Margesin, R. (1993). Bodenbiologische Arbeitsmethoden. Heidelberg: Springer-Verlag.
Schlaeppi, K., Bender, S. F., Mascher, F., Russo, G., Patrignani, A., Camenzind, T., et al. (2016). High-resolution community profiling of arbuscular mycorrhizal fungi. New Phytol. 212, 780-791. doi: 10.1111/nph.14070
Shaharoona, B., Arshad, M., Zahir, Z. A., and Khalid, A. (2006). Performance of Pseudomonas spp. containing ACC-deaminase for improving growth and yield of maize (Zea mays L.) in the presence of nitrogenous fertilizer. Soil Biol. Biochem. 38, 2971-2975. doi: 10.1016/j.soilbio.2006.03.024
Skalar Analytical, B. V. (1995). The SAN-Plus Segmented Flow Analyzer, Soil and Plant Analysis. De Breda: Skalar Analytical B. V.
Slawiak, M., Beckhoven, J. R. C. M., Speksnijder, A. G. C. L., Czajkowski, R., Grabe, G., and Wolf, J. M. (2009). Biochemical and genetical analysis reveal a new clade of biovar 3 Dickeya spp. strains isolated from potato in Europe. Eur. J. Plant Pathol. 125, 245-261. doi: 10.1007/s10658-009-9479-2
Smith, S., and Read, D. (2008). Mycorrhizal Symbiosis, 3rd edn. London: Academic Press.
Strigul, N. S., and Kravchenko, L. V. (2006). Mathematical modeling of PGPR inoculation into the rhizosphere. Environ. Model. Softw. 21, 1158-1171. doi: 10.1016/j.envsoft.2005.06.003
Stutz, E. W., Défago, G., and Kern, H. (1986). Naturally occuring fluorescent pseudomonads involved in suppression of black root rot of tobacco. Phytopathology 76, 181-185.
Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24, 1596-1599. doi: 10.1093/molbev/msm092
Thonar, C., Erb, A., and Jansa, J. (2012). Real-time PCR to quantify composition of arbuscular mycorrhizal fungal communities-marker design, verification, calibration and field validation. Mol. Ecol. Resour. 12, 219-232. doi: 10.1111/j.1755-0998.2011.03086.x
Vacheron, J., Desbrosses, G., Bouffaud, M. L., Touraine, B., Moënne-Loccoz, Y., Muller, D., et al. (2013). Plant growth-promoting rhizobacteria and root system functioning. Front. Plant Sci. 4:356. doi: 10.3389/fpls.2013.00356
Vance, E. D., Brookes, P. C., and Jenkinson, D. S. (1987). An extraction method for measuring soil microbial biomass C. Soil Biol. Biochem. 19, 703-707. doi: 10.1016/0038-0717(87)90052-6
VDLUFA (1991). VDLUFA-Methodenbuch. Band. I, Die Untersuchung von Böden. Darmstadt: VDLUFA-Verlag.
Vitousek, P. M., Aber, J. D., Howarth, R. W., Likens, G. E., Matson, P. A., Schindler, D. W., et al. (1997). Human alteration of the global nitrogen cycle: sources and consequences. Ecol. Appl. 7, 737-750. doi: 10.1890/1051-0761(1997)007[0737:haotgn.0.co;2]10.1890/1051-0761(1997)007[0737:haotgn]2.0.co;2
Von Felten, A., Défago, G., and Maurhofer, M. (2010). Quantification of Pseudomonas fluorescens strains F113, CHA0 and Pf153 in the rhizosphere of maize by strain-specific real-time PCR unaffected by the variability of DNA extraction efficiency. J. Microbiol. Methods 81, 108-115. doi: 10.1016/j.mimet.2010.02.003
Walker, V., Bertrand, C., Bellvert, F., Moënne-Loccoz, Y., Bally, R., and Comte, G. (2011). Host plant secondary metabolite profiling shows a complex, strain-dependent response of maize to plant growth-promoting rhizobacteria of the genus Azospirillum. New Phytol. 189, 494-506. doi: 10.1111/j.1469-8137.2010.03484.x
White, T. J., Bruns, T., Lee, S., and Taylor, J. (1990). "Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics, " in PCR Protocols: a Guide to Methods and Applications, eds M. A. Innis, G. D. H., J. J. Sninsky and T. J. White (New York, NY: Academic Press), 315-322.
Yusran, Y., Roemheld, V., and Mueller, T. (2009). Effects of Pseudomonas sp. "Proradix" and Bacillus amyloliquefaciens FZB42 on the Establishment of AMF Infection, Nutrient Acquisition and Growth of Tomato Affected by Fusarium oxysporum Schlecht f.sp. radicis-lycopersici Jarvis and Shoemaker. eScholoarship Repository, University of California 1106.
Zdor, R. E. (2015). Bacterial cyanogenesis: impact on biotic interactions. J. Appl. Microbiol. 118, 267-274. doi: 10.1111/jam.12697
