Abstract
It was hypothesized that disruption of the root–microbiome association creates empty rhizosphere niches that could be filled by both soilborne pathogens and beneficial microbes. The effect of de-coupling root–microbiome associations related to improve soil suppressiveness was investigated in cucumber using the pathogen Fusarium oxysporum f. sp. Cucumerinum (FOC) and its antagonist Bacillus amyloliquefaciens SQR9 (SQR9) system. The root–soil microbiome association of cucumber was disrupted by applying the fungicide carbendazim to the soil, and then FOC or/and its antagonist SQR9 were inoculated in the rhizosphere. In the fungicide treatment, the FOC wilt disease incidence was significantly increased by 13.3 % on average compared to the FOC treatment without fungicide. However, when the fungicide treatment was applied to the soil with SQR9 and FOC, the SQR9 effectively reduced the disease incidence, and improved cucumber plant growth compared to a no fungicide control. These results indicate that de-coupling of root–microbiome associations followed by antagonist inoculation can improve rhizosphere soil suppressiveness, which may help to develop strategies for efficient application of rhizosphere beneficial microbes in agriculture.
Similar content being viewed by others
References
Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681
Badri DV, Weir TL, van der Lelie D, Vivanco JM (2009) Rhizosphere chemical dialogues: plant-microbe interactions. Curr Opin Biotech 20(6):642–650
Bakker MG, Manter DK, Sheflin AM, Weir TL, Vivanco JM (2012) Harnessing the rhizosphere microbiome through plant breeding and agricultural management. Plant Soil 360:1–13
Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17:478–486
Berg G (2009) Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotech 84:11–18
Berg G, Opelt K, Zachow C, Lottmann J, Gotz M, Costa R, Smalla K (2006) The rhizosphere effect on bacteria antagonistic towards the pathogenic fungus Verticillium differs depending on plant species and site. FEMS Microbiol Ecol 56:250–261
Berg G, Smalla K (2009) Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol Ecol 68:1–13
Bever JD, Platt TG, Morton ER (2012) Microbial population and community dynamics on plant roots and their feedbacks on plant communities. Annu Rev Microbiol 66:265–283
Broeckling CD, Broz AK, Bergelson J, Manter DK, Vivanco JM (2008) Root exudates regulate soil fungal community composition and diversity. Appl Environ Microbiol 74:738–744
Bulgarelli D, Rott M, Schlaeppi K, van Themaat EVL, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E, Peplies J, Gloeckner FO, Amann R, Eickhorst T, Schulze-Lefert P (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95
Cao Y, Zhang Z, Ling N, Yuan Y, Zheng X, Shen B, Shen Q (2011) Bacillus subtilis SQR9 can control Fusarium wilt in cucumber by colonizing plant roots. Biol Fertil Soils 47:495–506
Case TJ (1983) Niche overlap and the assembly of island lizard communities. Oikos 41:427–433
Chaparro JM, Sheflin AM, Manter DK, Vivanco JM (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fertil Soils 48:489–499
Chen L, Huang X, Zhang F, Zhao D, Yang X, Shen Q (2012) Application of Trichoderma harzianum SQR-T037 bio-organic fertilizer significantly controls Fusarium wilt and affects the microbial communities of continuously cropped soil of cucumber. J Sci Food Agric 92:2465–2470
Crowder DW, Northfield TD, Strand MR, Snyder WE (2010) Organic agriculture promotes evenness and natural pest control. Nature 466:109–112
Diamond JM (1975) Assembly of species communities. In: Cody ML, Diamond JM (eds) Ecology and evolution of communities. Harvard University Press, Cambridge, MA, pp 342–444
De Ridder-Duine AS, Kowalchuk GA, Klein Gunnewied PJA, Smant W, van Veen JA, de Boer W (2005) Rhizosphere bacterial community composition in natural stands of Carex arenaria (sand sedge) is determined by bulk soil community composition. Soil Biol Biochem 37:349–357
Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149
Duffy B, Keel C, Defago G (2004) Potential role of pathogen signaling in multitrophic plant-microbe interactions involved in disease protection. Appl Environ Microbiol 70:1836–1842
Egamberdieva D, Kamilova F, Validov S, Gafurova L, Kucharova Z, Lugtenberg B (2008) High incidence of plant growth-stimulating bacteria associated with the rhizosphere of wheat grown on salinated soil in Uzbekistan. Environ Microbiol 10:1–9
Fliessbach A, Winkler ME, Lutz MP, Oberholzer H, 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
Gao G, Yin D, Chen S, Xia F, Yang J, Li Q, Wang W (2012) Effect of biocontrol agent Pseudomonas fluorescens 2P24 on soil fungal community in cucumber rhizosphere using T-RFLP and DGGE. PLoS One 7:e31806. doi:10.1371/journal.pone.0031806
Gao X, Jackson TA, Lambert KN, Li S, Hartman GL, Niblack TL (2004) Detection and quantification of Fusarium solani f. sp. glycines in soybean roots with real-time quantitative polymerase chain reaction. Plant Dis 88:1372–1380
Garbeva P, van Elsas JD, van Veen JA (2008) Rhizosphere microbial community and its response to plant species and soil history. Plant Soil 302:19–32
Hartmann A, Rothballer M, Schmid M (2008) Lorenz Hiltner, a pioneer in rhizosphere microbial ecology and soil bacteriology research. Plant Soil 312:7–14
Hermansson A, Backman JSK, Svensson BH, Lindgren PE (2004) Quantification of ammonia-oxidising bacteria in limed and non-limed acidic coniferous forest soil using real-time PCR. Soil Biol Biochem 36:1935–1941
Hillebrand H, Bennett DM, Cadotte MW (2008) Consequences of dominance: a review of evenness effects on local and regional ecosystem processes. Ecology 89:1510–1520
Hiltner L (1904) Über neuere Erfahrungen und Probleme auf dem Gebiete der Bodenbakteriologie unter besonderer Berücksichtigung der Gründüngung und Brache. Arb DLG 98:59–78
Ibekwe AM, Kennedy AC, Frohne PS, Papiernik SK, Yang CH, Crowley DE (2002) Microbial diversity along a transect of agronomic zones. FEMS Microbiol Ecol 39:183–191
Jørgensen C, Leser TD (2007) Estimating amplification efficiency improves multiplex real-time PCR quantification of Bacillus licheniformis and Bacillus subtilis spores in animal feed. J Microbiol Meth 68:588–595
Klein E, Ofek M, Katan J, Minz D, Gamliel A (2013) Soil suppressiveness to fusarium disease: shifts in root microbiome associated with reduction of pathogen root colonization. Phytopathology 103:23–33
Larkin RP, Honeycutt CW (2006) Effects of different 3-year cropping systems on soil microbial communities and rhizoctonia diseases of potato. Phytopathology 96:68–79
Li S, Zhang N, Zhang Z, Luo J, Shen B, Zhang R, Shen Q (2013) Antagonist Bacillus subtilis HJ5 controls Verticillium wilt of cotton by root colonization and biofilm formation. Biol Fertil Soils 49:295–303
Lievens B, Claes L, Vakalounakis DJ, Vanachter ACRC, Thomma BPHJ (2007) A robust identification and detection assay to discriminate the cucumber pathogens Fusarium oxysporum f. sp. cucumerinum and f. sp. radicis-cucumerinum. Environ Microbiol 9:2145–2161
Ling N, Xue C, Huang Q, Yang X, Xu Y, Shen Q (2010) Development of a mode of application of bioorganic fertilizer for improving the biocontrol efficacy to Fusarium wilt. BioControl 55:673–683
Lugtenberg B, Chin-A-Woeng T, Bloemberg G (2002) Microbe-plant interactions: principles and mechanisms. Antonie Van Leeuwenhoek 81:373–383
Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, del Rio TG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488:86–90
Marx J (2004) The roots of plant-microbe collaborations. Science 304:234–236
Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JH, Piceno YM, DeSantis TZ, Andersen GL, Bakker PA, Raaijmakers JM (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–1100
Morgan JAW, Bending GD, White PJ (2005) Biological costs and benefits to plant-microbe interactions in the rhizosphere. J Exp Bot 56:1729–1739
Morrissey JP, Dow JM, Mark GL, O’Gara F (2004) Are microbes at the root of a solution to world food production? EMBO Rep 5:922–926
Nannipieri P, Ascher J, Ceccherini MT, Guerri G, Renella G, Pietramellara G (2008a) Recent advances in functional genomics and proteomics of plant associated microbes. In: Nautiyal CS, Dion P (eds) Molecular mechanisms of plant and microbe coexistence. Springer, Heidelberg, Germany, pp 215–241
Nannipieri P, Ascher J, Ceccherini MT, Landi L, Pietramellara G, Renella G, Valori F (2008b) Effects of root exudates on microbial diversity and activity in rhizosphere soils. In: Nautiyal CS, Dion P (eds) Molecular mechanisms of plant and microbe coexistence. Springer, Heidelberg, Germany, pp 339–365
Peters RD, Sturz AV, Carter MR, Sanderson JB (2003) Developing disease-suppressive soils through crop rotation and tillage management practices. Soil Till Res 72:181–192
Postma-Blaauw MB, de Goede RGM, Bloem J, Faber JH, Brussaard L (2010) Soil biota community structure and abundance under agricultural intensification and extensification. Ecology 91:460–473
Postma J, Schilder MT, Bloem J, van Leeumen-Haagsma WK (2008) Soil suppressiveness and functional diversity of the soil microflora in organic farming systems. Soil Biol Biochem 40:2394–2406
Qiu M, Zhang R, Xue C, Zhang S, Li S, Zhang N, Shen Q (2012) Application of bio-organic fertilizer can control Fusarium wilt of cucumber plants by regulating microbial community of rhizosphere soil. Biol Fertil Soils 48:807–816
Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moenne-Loccoz Y (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321:341–361
Selvakumar G, Panneerselvam P, Ganeshamurthy AN (2012) Bacterial mediated alleviation of abiotic stress in crops. In: Maheshwari DK (ed) Bacteria in agrobiology: stress management. Springer, Berlin, pp 205–224
Stachowicz JJ, Tilman D (2005) Species invasions and the relationships between species diversity, community saturation, and ecosystem functions. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution, and biogeography. Sinauer Sunderland, MA, pp 41–64
Sugiyama A, Vivanco JM, Jayanty SS, Manter DK (2010) Pyrosequencing assessment of soil microbial communities in organic and conventional potato farms. Plant Dis 94:1329–1335
van Bruggena AHC, Semenovb AM (2000) In search of biological indicators for soil health and disease suppression. Appl Soil Ecol 15:13–24
Weller DM, Raaijmakers JM, Gardener BB, Thomashow LS (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu Rev Phytopathol 40:309–348
Weng J, Wang Y, Li J, Shen Q, Zhang R (2013) Enhanced root colonization and biocontrol activity of Bacillus amyloliquefaciens SQR9 by abrB gene disruption. Appl Microbiol Biotech. doi:10.1007/s00253-012-4572-4
Xu Z, Shao J, Li B, Yan X, Shen Q, Zhang R (2013) Bacillomycin D in Bacillus amyloliquefaciens SQR9 contributes to antifungal activity and biofilm formation. Appl Environ Microbiol 79:808–815
Yao H, Wu F (2010) Soil microbial community structure in cucumber rhizosphere of different resistance cultivars to Fusarium wilt. FEMS Microbiol Ecol 72:456–463
Zamioudis C, Pieterse CMJ (2012) Modulation of host immunity by beneficial microbes. Mol Plant Microbe In 25:139–150
Zhang S, Raza W, Yang X, Hu J, Huang Q, Xu Y, Liu X, Ran W, Shen Q (2008) Control of Fusarium wilt disease of cucumber plants with the application of a bioorganic fertilizer. Biol Fertil Soils 44:1073–1080
Zhao Q, Dong C, Yang X, Mei X, Ran W, Shen Q, Xu Y (2011) Biocontrol of Fusarium wilt disease for Cucumis melo melon using bio-organic fertilizer. Appl Soil Ecol 47:67–75
Zhou X, Wu F (2012a) Dynamics of the diversity of fungal and Fusarium communities during continuous cropping of cucumber in the greenhouse. FEMS Microbiol Ecol 80:469–478
Zhou X, Wu F (2012b) p-Coumaric acid influenced cucumber rhizosphere soil microbial communities and the growth of Fusarium oxysporum f.sp. cucumerinum Owen. PLoS One 7:e48288
Zhou X, Yu G, Wu F (2012) Responses of soil microbial communities in the rhizosphere of cucumber (Cucumis sativus L.) to exogenously applied p-hydroxybenzoic acid. J Chem Ecol 38:975–983
Acknowledgments
This research was financially supported by the Chinese Ministry of Science and Technology (2013AA100802) and the National Natural Science Foundation of China (41271271). RZ and QS were also supported by the Priority Academic Program Development of Jiangsu Higher Education Institutions. JMV was supported by a grant from the National Science Foundation (MCB-0950857). RZ, QR, and JMV are part of the 111 Project (B12009).
Author information
Authors and Affiliations
Corresponding authors
Additional information
Meihua Qiu and Shuqing Li contributed equally to this paper
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOC 3988 kb)
Rights and permissions
About this article
Cite this article
Qiu, M., Li, S., Zhou, X. et al. De-coupling of root–microbiome associations followed by antagonist inoculation improves rhizosphere soil suppressiveness. Biol Fertil Soils 50, 217–224 (2014). https://doi.org/10.1007/s00374-013-0835-1
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-013-0835-1