Abstract
Background and aims
Soil-borne diseases are an increasingly serious threat to agriculture systems. Organic fertilization would improve soil quality and microbial community as well, and thus is appreciated a promising control strategy for soil-borne diseases. Yet, how soil microbial communities mediate disease control under organic fertilization remains largely unknown. Here, we aimed to explore the microbial mechanism of controlling soil-borne diseases by organic fertilization.
Methods
We investigated the effects of various fertilization regimes on the soil suppressiveness toward pathogenic fungi in the peanut rhizosphere. The fertilization regimes tested were organic fertilizer, chemical fertilizers, and a combination of both.
Results
Uninterrupted application of organic fertilizer in peanut field plots for seven planting seasons resulted in a control of peanut root rot, with a significantly higher peanut yield. Upon organic fertilization, bacterial microbiome assembly in the rhizosphere played a key role in developing soil suppressiveness against peanut root rot; upon chemical fertilization, the potential fungal pathogens dominated the fungal microbiome assembly in the rhizosphere to boost root rot. Further, structural equation model revealed that the rhizosphere bacterial community contributed to the control of root rot. Furthermore, upon organic fertilization, the rhizosphere bacterial community strongly suppressed mycelial growth and spore germination of Fusarium sp. ACCC 36194.
Conclusions
Collectively, in a monocropping system, persistent organic fertilization favors the development of a protective microbial shield in the plant rhizosphere, maintaining the rhizosphere health.
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References
Berendsen RL, Pieterse CMJ, Bakker PAHM (2012) The rhizosphere microbiome and plant health. Trends Plant Sci 17(8):478–486
Bibi F, Strobel GA, Naseer MI, Yasir M, Al-Ghamdi AAK, Azhar EI (2018) Microbial flora associated with the halophyte-Salsola imbricate and its biotechnical potential. Front Microbiol 9:65
Bonanomi G, Antignani V, Capodilupo M, Scala F (2010) Identifying the characteristics of organic soil amendments that suppress soilborne plant diseases. Soil Biol Biochem 42(2):136–144
Bongiorno G, Bunemann EK, Oguejiofor CU, Meier J, Gort G, Comans R et al (2019a) Sensitivity of labile carbon fractions to tillage and organic matter management and their potential as comprehensive soil quality indicators across pedoclimatic conditions in Europe. Ecol Indic 99:38–50
Bongiorno G, Postma J, Buenemann EK, Brussaard L, de Goede RGM, Maeder P et al (2019b) Soil suppressiveness to Pythium ultimum in ten European long-term field experiments and its relation with soil parameters. Soil Biol Biochem 133:174–187
Bremner J, Mulvaney (1996) Nitrogen-total. Methods of soil analysis part 3–chemical methods. Madison: America Society of Agronomy, Inc. 1085–1121
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(1):807–838
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7(5):335–336
Cha J-Y, Han S, Hong H-J, Cho H, Kim D, Kwon Y, Kwon SK, Crüsemann M, Bok Lee Y, Kim JF, Giaever G, Nislow C, Moore BS, Thomashow LS, Weller DM, Kwak YS (2016) Microbial and biochemical basis of a Fusarium wilt-suppressive soil. ISME J 10(1):119–129
Chapelle E, Mendes R, Bakker PAHM, Raaijmakers JM (2016) Fungal invasion of the rhizosphere microbiome. ISME J 10(1):265–268
Compant S, Samad A, Faist H, Sessitsch A (2019) A review on the plant microbiome: ecology, functions, and emerging trends in microbial application. J Adv Res 19:29–37
Couteaudier Y, Alabouvette C (1990) Quantitative comparison of Fusarium oxysporum competitiveness in relation to carbon utilization. FEMS Microbiol Ecol 74(4):261–267
De Boer W (2017) Upscaling of fungal-bacterial interactions: from the lab to the field. Curr Opin Microbiol 37:35–41
De Boer W, Li XG, Meisner A, Garbeva P (2019) Pathogen suppression by microbial volatile organic compounds in soils. FEMS Microbiol Ecol 8:8
Derakhshani H, Tun HM, Khafipour E (2016) An extended single-index multiplexed 16S rRNA sequencing for microbial community analysis on MiSeq Illumina platforms. J Basic Microb 56(3):321–326
Dignam BEA, O'Callaghan M, Condron LM, Raaijmakers JM, Kowalchuk GA, Wakelin SA (2016) Challenges and opportunities in harnessing soil disease suppressiveness for sustainable pasture production. Soil Biol Biochem 95:100–111
Dixon P (2003) VEGAN, a package of R functions for community ecology. J Veg Sci 14(6):927–930
Dobermann A, Dawe D, Roetter RP, Cassman KG (2000) Reversal of rice yield decline in a long-term continuous cropping experiment. Agron J 92(4):633–643
Dutta S, Mishra AK, Kumar BSD (2008) Induction of systemic resistance against fusarial wilt in pigeon pea through interaction of plant growth promoting rhizobacteria and rhizobia. Soil Biol Biochem 40(2):452–461
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10(10):996–998
Feng K, Zhang Z, Cai W, Liu W, Xu M, Yin H, Wang A, He Z, Deng Y (2017) Biodiversity and species competition regulate the resilience of microbial biofilm community. Mol Ecol 26(21):6170–6182
Garbeva P, Van Veen JA, Van Elsas JD (2004) Microbial diversity in soil: selection of microbial populations by plant and soil type and implications for disease suppressiveness. Annu Rev Phytopathol 42:243–270
Garbeva P, Hordijk C, Gerards S, De Boer W (2014) Volatiles produced by the mycophagous soil bacterium Collimonas. FEMS Microbiol Ecol 87:639–649
Gómez Expósito R, de Bruijn I, Postma J, Raaijmakers JM (2017) Current insights into the role of rhizosphere bacteria in disease suppressive soils. Front Microbiol 8:2529–2529
Gustafsson JE, Martenson R (2002) Structural equation modeling with AMOS: basic concepts, applications, and programming. Contemporary Psychology-Apa Review of Books 47:478–480
Hoitink HAJ, Boehm MJ (1999) Biocontrol within the context of soil microbial communities: a substrate-dependent phenomenon. Annu Rev Phytopathol 37:427–446
Hol WHG, Garbeva P, Hordijk C, Hundscheid MPJ, Gunnewiek PJAK, Agtmaal V et al (2015) Non-random species loss in bacterial communities reduces antifungal volatile production. Ecology 96(8):2042–2048
Hu LT, Bentler PM (1999) Cutoff criteria for fit indexes in covariance structure analysis: conventional criteria versus new alternatives. Struct Equ Model 6(1):1–55
Huang XQ, Wen T, Zhang JB, Meng L, Zhu TB, Liu LL, Cai ZC (2015) Control of soil-borne pathogen Fusarium oxysporum by biological soil disinfestation with incorporation of various organic matters. Eur J of Plant Pathol 143(2):223–235
Kolde R (2015) Pheatmap: pretty Heatmaps. R Package. http://cran.r-project.org/web/packages/pheatmap/index.html, Version 1.0.8
Koljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M et al (2013) Towards a unified paradigm for sequence-based identification of fungi. Mol Ecol 22(21):5271–5277
Lazcano C, Gomez-Brandon M, Revilla P, Dominguez J (2013) Short-term effects of organic and inorganic fertilizers on soil microbial community structure and function. Biol Fert Soils 49(6):723–733
Li XG, Zhang TL, Wang XX, Hua K, Zhao L, Han ZM (2013) The composition of root exudates from two different resistant peanut cultivars and their effects on the growth of soil-borne pathogen. Int J Biol Sci 9(2):164–173
Li XG, Ding CF, Zhang TL, Wang XX (2014) Fungal pathogen accumulation at the expense of plant-beneficial fungi as a consequence of consecutive peanut monoculturing. Soil Biol Biochem 72:11–18
Li XG, Zhang YN, Ding CF, Jia ZJ, He ZL, Zhang TL et al (2015) Declined soil suppressiveness to Fusarium oxysporum by rhizosphere microflora of cotton in soil sickness. Biol Fert Soils 51(8):935–946
Li XG, De Boer W, Zhang YN, Ding CF, Zhang TL, Wang XX (2018) Suppression of soil-borne Fusarium pathogens of peanut by intercropping with the medicinal herb Atractylodes lancea. Soil Biol Biochem 116:120–130
Lu RK (2000) Methods for soil agro-chemistry analysis. China agricultural science and technology press. Beijing, China (in Chinese)
Magoc T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27(21):2957–2963
McPherson MR, Wang P, Marsh EL, Mitchell RB, Schachtman DP (2018) Isolation and analysis of microbial communities in soil, rhizosphere, and roots in perennial grass experiments[J]. Jove-J Vis Exp 137:e57932
Mendes R, Kruijt M, de Bruijn I, Dekkers E, van der Voort M, Schneider JHM, Piceno YM, DeSantis TZ, Andersen GL, Bakker PAHM, Raaijmakers JM (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–1100
Mendes R, Garbeva P, Raaijmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663
Meng TZ, Wang QJ, Abbasi P, Ma Y (2019) Deciphering differences in the chemical and microbial characteristics of healthy and Fusarium wilt-infected watermelon rhizosphere soils. Appl Microbiol Biot 103:1497–1509
Niu B, Paulson JN, Zheng XQ, Kolter R (2017) Simplified and representative bacterial community of maize roots. PNAS 114(12):E2450–E2459
Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate USDA Washington DC
Orgiazzi A, Lumini E, Nilsson RH, Girlanda M, Vizzini A, Bonfante P, Bianciotto V (2012) Unravelling soil fungal communities from different mediterranean land-use backgrounds. PLoS One 7:e34847
R Development Core Team (2014) R: A language and environment for statistical computing
Rousk J, Baath E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG et al (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME J 4(10):1340–1351
Sanchez C, Tortosa G, Granados A, Delgado A, Bedmar EJ, Delgado MJ (2011) Involvement of Bradyrhizobium japonicum denitrification in symbiotic nitrogen fixation by soybean plants subjected to flooding. Soil Biol Biochem 43(1):212–217
Scher FM, Baker R (1980) Mechanism of biological-control in a Fusarium-suppressive soil. Phytopathology 70(5):412–417
Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, van Horn DJ, Weber CF (2009) Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541
Shen ZZ, Zhong ST, Wang YG, Wang BB, Mei XL, Li R, Ruan Y, Shen Q (2013) Induced soil microbial suppression of banana fusarium wilt disease using compost and biofertilizers to improve yield and quality. Eur J Soil Biol 57:1–8
Shen ZZ, Ruan YZ, Chao X, Zhang J, Li R, Shen QR (2015) Rhizosphere microbial community manipulated by 2 years of consecutive biofertilizer application associated with banana Fusarium wilt disease suppression. Biol Fert Soils 51:553–562
Shi WC, Li MC, Wei GS, Tian RM, Li CP, Wang B, Lin R, Shi C, Chi X, Zhou B, Gao Z (2019) The occurrence of potato common scab correlates with the community composition and function of the geocaulosphere soil microbiome. Microbiome 7(1):14
Soman C, Li D, Wander MM, Kent AD (2017) Long-term fertilizer and crop-rotation treatments differentially affect soil bacterial community structure. Plant Soil 413(1–2):1–15
Sun RB, Dsouza M, Gilbert JA, Guo XS, Wang DZ, Guo ZB, Ni Y, Chu H (2016) Fungal community composition in soils subjected to long-term chemical fertilization is most influenced by the type of organic matter. Environ Microbiol 18:5137–5150
Trivedi P, He Z, Van Nostrand JD, Albrigo G, Zhou J, Wang N (2012) Huanglongbing alters the structure and functional diversity of microbial communities associated with citrus rhizosphere. ISME J 6(2):363–383
Trivedi P, Delgado-Baquerizo M, Trivedi C, Hamonts K, Anderson IC, Singh BK (2017) Keystone microbial taxa regulate the invasion of a fungal pathogen in agro-ecosystems. Soil Biol Biochem 111:10–14
Van Elsas JD, Chiurazzi M, Mallon CA, Elhottova D, Kristufek V, Salles JF (2012) Microbial diversity determines the invasion of soil by a bacterial pathogen. PNAS 109(4):1159–1164
Van Os GJ, Wijnker JPM, Van Gulik WJM (1999) Effects of soil fumigation and flooding on suppression of Pythium root rot in ornamental bulb culture. Eur J Plant Pathol 105(8):791–800
Wakelin SA, Macdonald LM, Rogers SL, Gregg AL, Bolger TP, Baldock JA (2008) Habitat selective factors influencing the structural composition and functional capacity of microbial communities in agricultural soils. Soil Biol Biochem 40(3):803–813
Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73(16):5261–5267
Wei Z, Yang TJ, Friman V-P, Xu YC, Shen QR, Jousset A (2015) Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health. Nat Commun 6:8413
Wei Z, Hu J, Gu YA, Yin S, Xu Y, Jousset A et al (2018) Ralstonia solanacearum pathogen disrupts bacterial rhizosphere microbiome during an invasion. Soil Biol Biochem 118:8–17
Wright PJ, Falloon RE, Hedderley D (2017) A long-term vegetable crop rotation study to determine effects on soil microbial communities and soilborne diseases of potato and onion. New Zeal J Crop Hort 45:29–54
Xiong W, Guo S, Jousset A, Zhao QY, Wu HS, Li R, Kowalchuk GA, Shen Q (2017a) Bio-fertilizer application induces soil suppressiveness against Fusarium wilt disease by reshaping the soil microbiome. Soil Biol Biochem 114:238–247
Xiong W, Li R, Ren Y, Liu C, Zhao QY, Wu HS, Jousset A, Shen Q (2017b) Distinct roles for soil fungal and bacterial communities associated with the suppression of vanilla Fusarium wilt disease. Soil Biol Biochem 107:198–207
Xun WB, Xiong W, Huang T, Ran W, Li DC, Shen QR, Li Q, Zhang R (2016) Swine manure and quicklime have different impacts on chemical properties and composition of bacterial communities of an acidic soil. Appl Soil Ecol 100:38–44
Yang YR, Li XG, Liu JG, Zhou ZG, Zhang TL, Wang XX (2017) Bacterial diversity as affected by application of manure in red soils of subtropical China. Biol Fert Soils 53(6):639–649
Yang YR, Li XG, Liu JG, Zhou ZG, Zhang TL, Wang XX (2019) Fungal community structure in relation to manure rate in red soil in southern China. Appl Soil Ecol 147:103442
Zhalnina K, Louie KB, Hao Z, Mansoori N, da Rocha UN, Shi SJ, Cho H, Karaoz U, Loqué D, Bowen BP, Firestone MK, Northen TR, Brodie EL (2018) Dynamic root exudate chemistry and microbial substrate preferences drive patterns in rhizosphere microbial community assembly. Nat Microbiol 3:470–480
Zhang QC, Shamsi IH, Xu DT, Wang GH, Lin XY, Jilani G, Hussain N, Chaudhry AN (2012) Chemical fertilizer and organic manure inputs in soil exhibit a vice versa pattern of microbial community structure. Appl Soil Ecol 57:1–8
Zhao S, Liu DY, Ling N, Chen FD, Fang WM, Shen QR (2014a) Bio-organic fertilizer application significantly reduces the Fusarium oxysporum population and alters the composition of fungi communities of watermelon Fusarium wilt rhizosphere soil. Biol Fert Soils 50(5):765–774
Zhao XQ, Chen RF, Shen RF (2014b) Coadaptation of plants to multiple stresses in acidic soils. Soil Sci 179(10–11):503–513
Acknowledgments
We are very grateful to Dr. Zhengfu Yue, Xu Liu and Lijun Chen (Institute of Soil Science, CAS) for suggestions on high-throughput sequencing and assistance in data analysis, and our colleagues from the research group (other than the authors) for help in conducting the field experiments. This research was supported by the National Key Research and Development Program of China (2017YFD0200604), the National Natural Science Foundation of China (41671306) and the Excellent Youth Foundation of Jiangsu Province (BK20190040).
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X.L. and X.W. conceived the project and designed this study; D.C. conducted the experiments; X.L. and D.C. analyzed the data with assistance from W.Z., Z.Z., C.D. and Y.L.; X.L. and D.C. contributed to drafting the initial manuscript, and all co-authors revised, read, and approved the final manuscript. The funder had no role in study design; in the collection, analysis, and interpretation of data; in the writing of the report; and in the decision to submit the article for publication.
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Chen, D., Wang, X., Zhang, W. et al. Persistent organic fertilization reinforces soil-borne disease suppressiveness of rhizosphere bacterial community. Plant Soil 452, 313–328 (2020). https://doi.org/10.1007/s11104-020-04576-3
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DOI: https://doi.org/10.1007/s11104-020-04576-3