Induced Systemic Resistance and the Rhizosphere Microbiome |
Bakker, Peter A.H.M.
(Plant-Microbe Interactions, Department of Biology, Faculty of Science, Utrecht University)
Doornbos, Rogier F. (Plant-Microbe Interactions, Department of Biology, Faculty of Science, Utrecht University) Zamioudis, Christos (Plant-Microbe Interactions, Department of Biology, Faculty of Science, Utrecht University) Berendsen, Roeland L. (Plant-Microbe Interactions, Department of Biology, Faculty of Science, Utrecht University) Pieterse, Corne M.J. (Plant-Microbe Interactions, Department of Biology, Faculty of Science, Utrecht University) |
1 | Pozo, M. J., Verhage, A., García-Andrade, J., García, J. M. and Azcon-Aguilar, C. 2009. Priming plant defences against pathogens by arbuscular mycorrhizal fungi. In: Mycorrhizas:Functional processes and ecological impact, ed by C. Azcon-Aguilar, J. M. Barea, S. Gianinazzi, and V. Gianinazzi-Pearson, pp. 137−149. Springer-Verlag Heidelberg. |
2 | Press, C. M., Wilson, M., Tuzun, S. and Kloepper, J. W. 1997. salicylic acid produced by Serratia marcescens 90−166 is not the primary determinant of induced systemic resistance in cucumber or tobacco. Mol. Plant-Microbe Interact. 10:761−768. |
3 | Raaijmakers, J. M., Leeman, M., Van Oorschot, M. M. P., Van der Sluis, I., Schippers, B. and Bakker, P. A. H. M. 1995. Doseresponse relationships in biological control of fusarium wilt of radish by Pseudomonas spp. Phytopathology 85:1075−1081. DOI ScienceOn |
4 | Raaijmakers, J. M., Paulitz, T. C., Steinberg, C., Alabouvette, C. and Moënne-Loccoz, Y. 2009. The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321:341−361. DOI |
5 | Raaijmakers, J. M., Vlami, M. and De Souza, T. J. 2002. Antibiotic production by bacterial biocontrol agents. Anton. Leeuw. Int. J. G. 81:537−547. |
6 | Raaijmakers, J. M. and Weller, D. M. 1998. Natural plant protection by 2,4-diacetylphloroglucinol-producing Pseudomonas spp. in take-all decline soils. Mol. Plant-Microbe Interact. 11: 144−152. |
7 | Ran, L. X., Li, Z. N., Wu, G. J., Van Loon, L. C. and Bakker, P. A. H. M. 2005. Induction of systemic resistance against bacterial wilt in Eucalyptus urophylla by fluorescent Pseudomonas spp. Eur. J. Plant Pathol. 113:59−70. |
8 | Reglinski, T. and Walters, D. 2009. Induced resistance for plant disease control. In: Disease Control in Crops, ed by D. Walters, pp. 62-92. Wiley-Blackwell, Oxford UK. |
9 | Rosenzweig, N., Tiedje, J. M., Quensen, J. F., III, Meng, Q. and Hao, J. J. 2012. Microbial communities associated with potato common scab-suppressive soil determined by pyrosequencing analyses. Plant Dis. 96:718−725. |
10 | Van Dongen, J. T., Frohlich, A., Ramirez-Aguilar, S. J., Schauer, N., Fernie, A. R., Erban, A., Kopka, J., Clark, J., Langer, A. and Geigenberger, P. 2009. Transcript and metabolite profiling of the adaptive response to mild decreases in oxygen concentration in the roots of Arabidopsis plants. Annals Bot. 103: 269−280. DOI |
11 | Van der Heijden, M. G. A., Bradgett, R. D. and Van Straalen, N. M. 2008. The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecology Letters 11:296−310. DOI ScienceOn |
12 | Van der Heijden, M. G. A., Streitwolf-Engel, R., Riedl, R., Siegrist, S., Neudecker, A., Ineichen, K., Boller, T., Wiemken, A. and Sanders, I. R. 2006. The mycorrhizal contribution to plant productivity, plant nutrition and soil structure in experimental grassland. New Phytol. 172:739−752. DOI ScienceOn |
13 | Van Hulten, M., Pelser, M., Van Loon, L. C., Pieterse, C. M. J. and Ton, J. 2006. Costs and benefits of priming for defense in Arabidopsis. Proc. Natl. Acad. Sci. USA 103:5602−5607. |
14 | Van Loon, L. C. and Bakker, P. A. H. M. 2005. Induced systemic resistance as a mechanism of disease suppression by rhizobacteria. In: PGPR: Biocontrol and biofertilization, ed by Z.A. Siddiqui, pp. 39-66. Springer, Dordrecht, the Netherlands. |
15 | Van Loon, L. C., Bakker, P. A. H. M. and Pieterse, C. M. J. 1998. Systemic resistance induced by rhizosphere bacteria. Annu. Rev. Phytopathol. 36:453−483. |
16 | Van Peer, R. and Schippers, B. 1992. Lipopolysaccharides of plant-growth promoting Pseudomonas sp. strain WCS417r induce resistance in carnation to Fusarium wilt. Neth. J. Plant Pathol. 98:129−139. |
17 | Van Peer, R., Niemann, G. J. and Schippers, B. 1991. Induced resistance and phytoalexin accumulation in biological control of fusarium wilt of carnation by Pseudomonas sp. strain WCS417r. Phytopathology 81:728−734. |
18 | Van Pelt, J. A., Van der Sluis, I., Pieterse, C. M. J. and Bakker, P. A. H. M. 2008. Induced systemic resistance Bioassays in Arabidopsis thaliana. In: Prospects and applications for plantassociated microbes A laboratory manual Part A: Bacteria, ed by S. Sorvari and A. M. Pirttila, pp. 113−118. BBI Piikkio, Finland. |
19 | Weller, D. M., Mavrodi, D. V., Van Pelt, J. A., Pieterse, C. M. J., Van Loon, L. C. and Bakker, P. A. H. M. 2012. Induced systemic resistance (ISR) in Arabidopsis thaliana against Pseudomonas syringae pv. tomato by 2,4-diacetylphloroglucinol-producing Pseudomonas fluorescens. Phytopathology 102:403−412. |
20 | Weller, D. M., Raaijmakers, J. M., McSpadden Gardener, B. B. and Thomashow, L. S. 2002. Microbia populations responsible for specific soil suppressiveness to plant pathogens. Annu. Rev. Phytopathol. 40:309−348. |
21 | Williams, B. L., Hornig, M., Parekh, T. and Lipkin, W. I. 2012. Application of novel PCR-based methods for detection, quantitation, and phylogenetic characterization of Sutterella species in intestinal biopsy samples from children with autism and gastrointestinal disturbances. mBio 3:e00261−11. |
22 | Yang, J., Kloepper, J. W. and Ryu, C.-M. 2008. Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci. 14:1−4. |
23 | Zamioudis, C. and Pieterse, C. M. J. 2012. Modulation of host immunity by beneficial microbes. Mol. Plant-Microbe Interact. 25:139−150. DOI ScienceOn |
24 | Thamer, S., Schädler, M., Bonte, D. and Ballhorn, D. J. 2011. Dual benefit from a belowground symbiosis: nitrogen fixing rhizobia promote growth and defense against a specialist herbivore in a cyanogenic plant. Plant Soil 341:209−219. DOI |
25 | Ton, J., Davison, S., Van Wees, S. C. M., Van Loon, L. C. and Pieterse, C. M. J. 2001. The Arabidopsis ISR1 locus controlling rhizobacteria-mediated induced systemic resistance is involved in ethylene signaling. Plant Physiol. 125:652−661. DOI ScienceOn |
26 | Ton, J., Pieterse, C. M. J. and Van Loon, L. C. 1999. Identification of a locus in Arabidopsis controlling both the expression of rhizobacteria-mediated induced systemic resistance (ISR) and basal resistance against Pseudomonas syringae pv. tomato. Mol. Plant-Microbe Interact. 12:911−918. |
27 | Tran, H., Ficke, A., Asiimwe, T., Hofte, M. and Raaijmakers, J. M. 2007. Role of the cyclic lipopeptide massetolide A in biological control of Phytophthora infestans and in colonization of tomato plants by Pseudomonas fluorescens. New Phytol. 175:731−742. |
28 | Turnbaugh, P. J., Hamady, M., Yatsunenko, T., Cantarel, B. L., Duncan, A., Ley, R. E., Sogin, M. L., Jones, W. J., Roe, B. A., Affourtit, J. P., Egholm, M., Henrissat, B., Heath, A. C., Knoght, R. and Gordon, J. I. 2009. A core gut microbiome in obese and lean twins. Nature 457:480−486. |
29 | Turnbaugh, P. J., Ley, R. E., Mahowald, M. A., Magrini, V., Mardis, E. R. and Gordon, J. I. 2006. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444:1027−1031. |
30 | Van der Ent, S., Verhagen, B. W. M., Van Doorn, R., Bakker, D., Verlaan, M. G., Pel, M. J. C., Joosten, R. G., Proveniers, M. C. G., Van Loon, L. C., Ton, J. and Pieterse, C. M. J. 2008. MYB72 is required in early signaling steps of rhizobacteriainduced systemic resistance in Arabidopsis. Plant Physiol. 146:1293−1304. DOI ScienceOn |
31 | Ongena, M., Jourdan, E., Schafer, M., Kech, C., Budzikiewicz, H., Luxen, A. and Thonart, P. 2005. Isolation of an N-alkylated benzylamine derivative from Pseudomonas putida BTP1 as elicitor of induced systemic resistance in bean. Mol. Plant-Microbe Interact. 18:562−569. |
32 | Vartoukian, S. R., Palmer, R. M. and Wade, W .G. 2010. Strategies for culture of 'unculturable' bacteria. FEMS Microbiol. Lett. 309:1−7. |
33 | Venturi, V. and Passos da Silva, D. 2012. Incoming pathogens team up with harmless "resident'' bacteria. Trends Microbiol. 20:160−164. DOI ScienceOn |
34 | Wei, G., Kloepper, J. W. and Tuzun, S. 1991. Induction of systemic resistance of cucumber to Colletotrichum orbiculare by select strains of plant growth-promoting rhizobacteria. Phytopathology 81:1508−1512. |
35 | Wei, G., Kloepper, J. W. and Tuzun, S. 1996. Induced systemic resistance to cucumber diseases and increased plant growth by plant growth-promoting rhizobacteria under field conditions. Phytopathology 86:221−224. |
36 | Weller, D. M. 2007. Pseudomonas biocontrol agents of soilborne pathogens: looking back over 30 years. Phytopathology 97:250−256. |
37 | Schreiner, K., Hagn, A., Kyselkova, M., Moenne-Loccoz, Y., Welzl, G., Munch, J. C. and Schloter, M. 2010. Comparison of barley succession and take-all disease as environmental factors shaping the rhizobacterial community during take-all decline. Appl. Environ. Microbiol. 76:4703−4712. |
38 | Schuhegger, R., Ihring, A., Gantner, S., Bahnweg, G., Knappe, C., Vogg, G., Hutzler, P., Schmid, M., Van Breusegem, F., Eberl, L., Hartmann, A. and Langebartels, C. 2006. Induction of systemic resistance in tomato by N-acyl-L-homoserine lactoneproducing rhizosphere bacteria. Plant Cell Environm. 29:909−918. |
39 | Segarra, G., Van der Ent, S., Trillas, I. and Pieterse, C. M. J. 2009. MYB72, a node of convergence in induced systemic resistance triggered by a fungal and a bacterial beneficial microbe. Plant Biology 11:90−96. |
40 | Shoresh, M., Harman, G. E. and Mastouri, F. 2010. Induced systemic resistance and plant responses to fungal biocontrol agents. Annu. Rev. Phytopathol. 48:21−43. DOI ScienceOn |
41 | Sultana, S., Hossian, Md. M., Kubota, M. and Hyakumachi, M. 2009. Induction of systemic resistance in Arabidopsis thaliana in response to a culture filtrate from a plant growth-promoting fungus, Phoma sp. GS8-3. Plant Biology 11:97−104. DOI ScienceOn |
42 | Johnson, K. B. and DiLeone, J. A. 1999. Effect of antibiosis on antagonist dose-plant disease response relationships for the biological control of crown gall of tomato and cherry. Phytopathology 89:974−980. |
43 | Jourdan, E., Henry, G., Duby, F., Dommes, J., Barthelemy, J. P., Thonart, P. and Ongena, M. 2009. Insights into the defenserelated events occurring in plant cells following perception of surfactin-type lipopeptide from Bacillus subtilis. Mol. Plant-Microbe Interact. 22:456−468. |
44 | Katznelson, H., Lochhead, A. G. and Timonin, M. I. 1948. Soil microorganisms and the rhizosphere. Bot. Rev. 14:543−586. |
45 | Khan, M. S., Zaidi, A. and Wani, P. A. 2009. Role of phosphate solubilizing microorganisms in sustainable agriculture - a review. Agron. Sustain. Dev. 27:29−43. |
46 | Khoruts, A., Dicksved, J., Jansson, J. K. and Sadowsky, M. J. 2010. Changes in the composition of the human fecal microbiome after bacteriotherapy for recurrent Clostridium difficileassociated diarrhea. J. Clin. Gastroenterol. 44:354−360. |
47 | Kloepper, J. W., Ryu, C.-M. and Zhang, S. 2004. Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259−1266. DOI ScienceOn |
48 | Koike, N., Hyakumachi, M., Kageyama, K., Tsuyumu, S. and Doke, N. 2001. Induction of systemic resistance in cucumber against several diseases by plant growth-promoting fungi: lignification and superoxide generation. Eur. J. Plant Pathol. 108:187−196. |
49 | Kraiser, T., Gras, D. E., Gutierrez, A. G., Gonzalez, B. and Gutierrez, R. A. 2011. A holistic view of nitrogen acquisition in plants. J. Exp. Bot. 62:1455−1466. |
50 | Kyselkova, M., Kopecky, J., Frapolli, M., Defago, G., Sagova-Mareckova, M., Grundmann, G. L. and Moenne-Loccoz, Y. 2009. Comparison of rhizobacterial community composition in soil suppressive or conducive to tobacco black root rot disease. ISME J. 3:1127−1138. DOI ScienceOn |
51 | Mazurier, S., Corberand, T., Lemanceau, P. and Raaijmakers, J. M. 2009. Phenazine antibiotics produced by fluorescent pseudomonads contribute to natural soil suppressiveness to Fusarium wilt. ISME J. 3:977−991. |
52 | Mazzola, M. 2002. Mechanisms of natural soil suppressiveness to soilborne diseases. Anton. Leeuw. Int. J. G. 81:557−564. |
53 | Mendes, R., Kruijt, M., De Bruijn, I., Dekkers, E., Van der Voort, M., Schneider, J. H. M., Piceno, Y. M., DeSantis, T. Z., Andersen, G. L., Bakker, P. A. H. M. and Raaijmakers, J. M. 2011. Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097−1100. |
54 | Meziane, H., Van der Sluis, I., Van Loon, L. C., Hofte, M. and Bakker, P. A. H. M. 2005. Determinants of Pseudomonas putida WCS358 involved in inducing systemic resistance in plants. Mol. Plant Pathol. 6:177−185. |
55 | Micallef, S. A., Shiaris, M. P. and Colon-Carmona, A. 2009. Influence of Arabidopsis thaliana accessions on rhizobacterial communities and natural variation in root exudates. J. Exp. Bot. 60:1729-1742. DOI ScienceOn |
56 | Montesinos, E. and Bonaterra, A. 1996. Dose-response models in biological control of plant pathogens: an empirical verification. Phytopathology 86:464−472. |
57 | Ongena, M., Jourdan, E., Adam, A., Paquot, M., Brans, A., Joris, B., Arpigny, J.-L. and Thonart, P. 2007. Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environ. Microbiol. 9:1084−1090. |
58 | Hein, J. W., Wolfe, G. V. and Blee, K. A. 2008. Comparison of rhizosphere bacterial communities in Arabidopsis thaliana mutants for systemic acquired resistance. Microb. Ecol. 55:333-343. DOI |
59 | Iavicoli, A., Boutet, E., Buchala, A. and Metraux, J. P. 2003. Induced systemic resistance in Arabidopsis thaliana in response to root inoculation with Pseudomonas fluorescens CHA0. Mol. Plant-Microbe Interact. 16:851−858. |
60 | Diaz Heijtz, R., Wang, S., Anuar, F., Qian, Y., Bjorkholm, B., Samuelsson, A., Hibberd, M. L., Forssberg, H. and Pettersson, V. 2011. Normal gut microbiota modulates brain development and behavior. Proc. Natl. Acad. Sc. U.S.A. 108:3047−3052. |
61 | Doornbos, R. F., Geraats, B. P. J., Kuramae, E. E., Van Loon, L. C. and Bakker, P. A. H. M. 2011. Effects of jasmonic acid, ethylene, and salicylic acid signaling on the rhizosphere bacterial community of Arabidopsis thaliana. Mol. Plant-Microbe Interact. 24:395−407. |
62 | Alabouvette, C. 1999. Fusarium wilt suppressive soils: an example of disease suppressive soils. Australas. Plant Pathol. 28: 57−64. |
63 | Anderson, I. C. and Cairney, J. W. G. 2004. Diversity and ecology of soil fungal communities: Increased understanding through the application of molecular techniques. Environ. Microbiol. 6:769−779. |
64 | Arumugam, M., Raes, J., Pelletier, E., Le Paslier, D., Yamada, T., Mende, D. R., Fernandes, G. R., Tap, J., Bruls, T., Batto, J.-M., Bertalan, M., Borruel, N., Casellas, F., Fernandez, L., Gautier, L., Hansen, T., Hattori, M., Hayashi, T., Kleerebezem, M., Kurokawa, K., Leclerc, M., Levenez, F., Manichanh, C., Nielsen, H. B., Nielsen, T., Pons, N., Poulain, J., Qin, J., Sicheritz-Ponten, T., Tims, S., Torrents, D., Ugarte, E., Zoetendal, E. G., Wang, J., Guarner, F., Pedersen, O., De Vos, W. M., Brunak, S., Dore, J., MetaHIT Consortium (additional members), Weissenbach, J., Ehrlich, S. D. and Bork, P. 2011. Enterotypes of the human gut microbiome. Nature 473:174−180. |
65 | Rudrappa, T., Czymmek, K. J., Pare, P. W. and Bais, H. P. 2008. Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol. 148:1547−1556. |
66 | Ryu, C. M., Farag, M. A., Hu, C. H., Reddy, M. S., Kloepper, J. W. and Pare, P. W. 2004. Bacterial volatiles induce systemic resistance in Arabidopsis. Plant Physiol. 134:1017−1026. DOI ScienceOn |
67 | Sanguin, H., Sarniguet, A., Gazengel, K., Moenne-Loccoz, Y. and Grundmann, G. L. 2009. Rhizosphere bacterial communities associated with disease suppressiveness stages of take-all decline in wheat monoculture. New Phytol. 184:694−707. DOI ScienceOn |
68 | Lemanceau, P., Corberand, T., Gardan, L., Latour, X., Laguerre, G., Boeufgras, J-M. and Alabouvette, C. 1995. Effect of two plant species, flax (Linum usitatissinum L.) and tomato (Lycopersicon esculentum Mill.) on the diversity of soilborne populations of fluorescent pseudomonads. Appl. Environ. Microbiol. 61:1004−1012. |
69 | Ling, N., Huang, Q., Guo, S. and Shen, Q. 2011. Paenibacillus polymyxa SQR-21 systemically affects root exudates of watermelon to decrease the conidial germination of Fusarium oxysporum f.sp. niveum. Plant Soil 341:485−493. |
70 | Mark, G. L., Dow, J. M., Kiely, P. D., Higgins, H., Haynes, J., Baysse, C., Abbas, A., Foley, T., Franks, A., Morrissey, J. and O'Gara, F. 2005. Transcriptome profiling of bacterial responses to root exudates identifies genes involved in microbe-plant interactions. Proc. Natl. Acad. Sc. USA 102: 17454−17459. |
71 | Maurhofer, M., Hase, C., Meuwly, P., Metraux, J. P. and Defago, G. 1994. Induction of systemic resistance of tobacco to tobacco necrosis virus by the root-colonizing Pseudomonas fluorescens strain CHA0: Influence of the gacA gene and of pyoverdine production. Phytopathology 84:39−146. |
72 | Mavrodi, O. V., Mavrodi, D. V., Parejko, J. A., Thomashow, L. S. and Weller, D. M. 2012. Irrigation differentially impacts populations of indigenous antibiotic-producing Pseudomonas spp. in the rhizosphere of wheat. Appl. Environ. Microbiol. 78: 3214−3220. |
73 | Audenaert, K., Pattery, T., Cornelis, P. and Hofte, M. 2002. Induction of systemic resistance to Botrytis cinerea in tomato by Pseudomonas aeruginosa 7NSK2: Role of salicylic acid, pyochelin, and pyocyanin. Mol. Plant-Microbe Interact. 15: 1147−1156. |
74 | Baker, K. F. and Cook, R. J. 1974. Biological Control of Plant Pathogens. W.H. Freeman, San Francisco. |
75 | Bakker, P. A. H. M., Pieterse, C. M. J. and Van Loon, L. C. 2007. Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 97:239−243. DOI ScienceOn |
76 | Bisseling, T., Dangl, J. L. and Schultze-Lefert, P. 2009. Next-generation communication. Science 324:691. DOI ScienceOn |
77 | Bull, C. T., Weller, D. M. and Thomashow, L. S. 1991. Relationship between root colonization and suppression of Gaeumannomyces graminis var. tritici by Pseudomonas fluorescens strain 2−79. Phytopathology 81:954−959. |
78 | Crow, J. M. 2011. That Healthy gut feeling. Nature 480:S88−S89. |
79 | Da Rocha, A. B. and Hammerschmidt, R. 2005. History and perspectives on the use of disease resistance inducers in horticultural crops. HortTechology 15:518−529. |
80 | Derrien, M., Van Passel, M. W. J., Van de Bovenkamp, J. H. B., Schipper, R. G., De Vos, W. M. and Dekker, J. 2010. Mucinbacterial interactions in the human oral cavity and digestive tract. Gut. Microbes 1:254−268. |
81 | De Boer, W., Wagenaar, A-M., Klein Gunnewiek, P. J. A. and Van Veen, J. A. 2007. In vitro suppression of fungi caused by combinations of apparently non-antagonistic soil bacteria. FEMS Microbiol. Ecol. 59:177−185. |
82 | De Souza, J. T., Weller, D. M. and Raaijmakers, J. M. 2003. Frequency, diversity, and activity of 2,4-diacetylphloroglucinolproducing fluorescent Pseudomonas spp. in Dutch take-all decline soils. Phytopathology 93:54−63. |
83 | De Vleesschauwer, D., Cornelis, P. and Hofte, M. 2006. Redoxactive pyocyanin secreted by Pseudomonas aeruginosa 7NSK2 triggers systemic resistance to Magnaporte grisea but enhances Rhizoctonia solani susceptibility in rice. Mol. Plant-Microbe Interact. 19:1406−1419. |
84 | De Vleesschauwer, D., Djavaheri, M., Bakker, P. A. H. M. and Hofte, M. 2008. Pseudomonas fluorescens WCS374r-induced systemic resistance in rice against Magnaporthe oryzae is based on pseudobactin-mediated priming for a salicylic acidrepressible multifaceted defense response. Plant Physiol. 148:1996−2012. |
85 | De Vleesschauwer, D. and Hofte, M. 2009. Rhizobacteria-induced systemic resistance. Adv. Bot. Res. 51: 223−281. |
86 | Gams, W. 2007. Biodiversity of soil-inhabiting fungi. Biodivers. Conserv. 16:69−72. |
87 | Glandorf, D. C. M., Peters, L. G. L., Van der Sluis, I., Bakker, P. A. H. M. and Schippers, B. 1993. Crop specificity of rhizosphere pseudomonads and the involvement of root agglutinins. Soil Biol. Biochem. 25:981−989. |
88 | Glandorf, D. C. M., Van der Sluis, I., Anderson, A. J., Bakker, P. A. H. M. and Schippers, B. 1994. Agglutination, adherence and root colonization by fluorescent pseudomonads. Appl. Environ. Microbiol. 60:1726−1733. |
89 | Grenham, S., Clarke, G., Cryan, J. F. and Dinan, T. G. 2011. Braingut-microbe communication in health and disease. Frontiers in Physiology 2: Article 94. DOI:10.3389/fphys.2011.00094. DOI ScienceOn |
90 | Hartmann, A., Rothballer, M. and Schmid, M. 2008. Lorentz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant Soil 312:7−14. |
91 | Hartmann, A., Schmid, M., Van Tuinen, D. and Berg, G. 2009. Plant-driven selection of microbes. Plant Soil 321:235−257. |
92 | Hazen, T. C., Dubinsky, E. A., DeSantis, T. Z., Andersen, G. L., Piceno, Y. M., Singh, N., Jansson, J. K., Probst, A., Borglin, S. E., Fortney, J. L., Stringfellow, W. T., Bill, M., Conrad, M. E., Tom, L. M., Chavarria, K. L., Alusi, T. R., Lamendella, R., Joyner, D. C., Spier, C., Baelum, J., Auer, M., Zemla, M. L., Chakraborty, R., Sonnenthal, E. L., D'haeseleer, P., Holman, H-Y. N., Osman, S., Lu, Z., Van Nostrand, J. D., Deng, Y., Zhou, J. and Mason, O. U. 2010. Deep-sea oil plume enriches indigenous oil degrading bacteria. Science 330:204-208. DOI ScienceOn |
93 | Helbling, D. E., Ackermann, M., Fenner, K., Kohler, H-P. E. and Johnson, D. R. 2012. The activity level of a microbial community function can be predicted from its metatranscriptome. ISME J. 6:902−904. DOI |
94 | Bakker, P. A. H. M., Ran, L. X., Pieterse, C. M. J. and Van Loon, L. C. 2003. Understanding the involvement of induced systemic resistance in rhizobacteria-mediated biocontrol of plant diseases. Can. J. Plant Pathol. 25:5−9. |
95 | Berendsen, R. L., Pieterse, C. M. J. and Bakker P. A. H. M. 2012. The second genome and plant health. Trends Plant Sci. 17:478−486. |
96 | Lee, B., Lee, S. and Ryu, M. R. 2012. Foliar aphid feeding recruits rhizosphere bacteria and primes plant immunity against pathogenic and non-pathogenic bacteria in pepper. Ann. Bot. 110:281−290. |
97 | Leeman, M., Van Pelt, J.A., Den Ouden, F. M., Heinsbroek, M., Bakker, P. A. H. M. and Schippers, B. 1995a. Induction of systemic resistance against fusarium wilt of radish by lipopolysaccharides of Pseudomonas fluorescens. Phytopathology 85: 1021−1027. |
98 | Leeman, M., Van Pelt, J. A., Hendrickx, M. J., Scheffer, R. J., Bakker, P. A. H. M. and Schippers, B. 1995b. Biocontrol of fusarium wilt of radish in commercial greenhouse trials by seed treatment with Pseudomonas fluorescens WCS374. Phytopathology 85:1301−1305. DOI |
99 | Doornbos, R. F., Van Loon, L. C. and Bakker, P. A. H. M. 2009. Beneficial Pseudomonas spp. have altered root colonization on Arabidopsis thaliana mutants affected in the expression of induced systemic resistance. In: Molecular tools for understanding and improving biocontrol. ed by B. Duffy, M. Maurhofer, C. Keel, C. Gessler, Y. Elad, and S. Kiewnick, IOBC/wprs Bulletin 43:307−310. |
100 | Duijff, B. J., Recorbet, G., Bakker, P. A. H. M., Loper, J. E. and Lemanceau, P. 1999. Microbial antagonism at the root level is involved in the suppression of fusarium wilt by the combination of nonpathogenic Fusarium oxysporum Fo47 and Pseudomonas putida WCS358. Phytopathology 89:1073−1079. |
101 | Elsharkawy, M. M., Shimizu, M., Takahashi, H. and Hyakumachi, M. 2012. Induction of systemic resistance against Cucumber mosaic virus by Penicillium simplicissimum GP17-2 in Arabidopsis and tobacco. Plant Pathol. DOI: 10.1111/j.1365-3059.2011.02573.x DOI ScienceOn |
102 | Fagundes, C. T., Amaral, F. A., Teixeira, A. L., Souza, D. G. and Teixeira, M. M. 2012. Adapting to environmental stresses: the role of the microbiota in controlling innate immunity and behavioral responses. Immunol. Rev. 245:250−264. |
103 | Fravel, D., Olivain, C. and Alabouvette, C. 2003. Fusarium oxysporum and its biocontrol. New Phytol. 157:493−502. |
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