Skip to main content

Promoting soil microbial-mediated suppressiveness against Fusarium wilt disease by the enrichment of specific fungal taxa via crop rotation

Abstract

A pineapple-banana rotation was studied as a model system to investigate the potential emergence of a fungal-mediated disease-suppression in a soil highly infested with the pathogen Fusarium oxysporum causing the banana wilt disease. By using both field and pot experiments, the pineapple-banana rotation system resulted in a significant decrease of the pathogen number and next-stubble banana disease incidence (P < 0.05). This pathogen-suppression phenomenon was linked with detectable shifts in the soil resident fungal taxa tracked in the pineapple season. Most importantly, taxa affiliated with Talaromyces pinophilus and Clonostachys rossmaniae were found to be significantly enriched in the bulk soils due to the pineapple cultivation (P < 0.05). The taxon T. pinophilus was also significantly enriched in the rhizosphere of banana after the rotation (P < 0.05). Later, we used fungal isolation and pot inoculation to validate that both T. pinophilus and C. rossmaniae taxa are able to significantly decrease the pathogen number in the banana rhizosphere soil (P < 0.05), thus confirming their biocontrol effects suppressing the disease. Taken together, this study provides evidence on how crop rotation affects the resident soil microbiome and the development of disease suppressiveness. Besides, this study highlights the importance of understanding the dynamic changes in soil biology mediated by crop rotation and validates the mechanisms underpinning suppression toward promoting practical and directed manipulation of protective microbiomes in agroecosystems.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  • Amato KR, Sanders JG, Song SJ, Nute M, Metcalf JL, Thompson LR, Morton JT, Amir A, Mckenzie VJ, Humphrey G, Gogul G, Gaffney J, Baden AL, Britton GAO, Cuozzo FP, Fiore AD, Dominy NJ, Goldberg AG, Kowalewski MM, Lewis RJ, Link A, Sauther ML, Tecot S, White BA, Nelson KE, Stumpf RM, Knight R, Leigh SR (2019) Evolutionary trends in host physiology outweigh dietary niche in structuring primate gut microbiomes. ISME J 13:576–587

    CAS  PubMed  Article  Google Scholar 

  • Banerjee S, Schlaeppi K, Van der Heijden MGA (2018) Keystone taxa as drivers of microbiome structure and functioning. Nat Rev Microbiol 16:567–576

    CAS  PubMed  Article  Google Scholar 

  • Bao SD, Su HY, An ZS et al (1986) Soil agrochemical analysis, 2nd edn. China agriculture Press, Beijing

    Google Scholar 

  • Bashan Y, Prabhu SR, de-Bashan LE, Kloepper JW, (2020) Disclosure of exact protocols of fermentation, identity of microorganisms within consortia, formation of advanced consortia with microbe-based products. Biol Fertil Soils 56:443–445

    Article  Google Scholar 

  • Berendsen RL, Vismans G, Yu K, Song Y, De Jonge R, Burgman WP, Burmølle M, Herschend J, Bakker PAHM, Pieterse CMJ (2018) Disease-induced assemblage of a plant-beneficial bacterial consortium. ISME J 12:1496–1507

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Bernard E, Larkin RP, Tavantzis S, Alyokhin EMS, A, Gross SD, (2014) Rapeseed rotation, compost and biocontrol amendments reduce soilborne diseases and increase tuber yield in organic and conventional potato production systems. Plant Soil 374:611–627

    CAS  Article  Google Scholar 

  • Bokulich N, Subramanian S, Faith J, Gevers D, Gordon JI, Knight R, Mills DA, Caporaso JG (2013) Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing. Nat Methods 10:57–59

    CAS  PubMed  Article  Google Scholar 

  • Bulgarelli D, Garrido-Oter R, Münch PC, Weiman A, Dröge J, Pan Y, CMHardy A, Schulze-Lefert P, (2015) Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host Microbe 17:392–403

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Bulgarelli D, Rott M, Schlaeppi K, Van der 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

    CAS  PubMed  Article  Google Scholar 

  • Butler D (2013) Fungus threatens top banana. Nature 504:195–196

    CAS  PubMed  Article  Google Scholar 

  • Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Chapelle E, Mendes R, Bakker PAH, Rainmakers JM (2016) Fungal invasion of the rhizosphere microbiome. ISME J 10:265–268

    CAS  PubMed  Article  Google Scholar 

  • de-Bashan LE, Nannipieri P, Antoun H, Lindermann RG (2020) Application of beneficial microorganisms and their effects on soil, plants, and the environment: the scientific legacy of Professor Yoav Bashan. Biol Fertil Soils 56:439–442

    Article  Google Scholar 

  • Delgado-Baquerizo M, Maestre FT, Reich PB, Jeffries TC, Gaitan JJ, Encinar D, Berdugo M, Campbell CD, Singh BK (2016) Microbial diversity drives multi-functionality in terrestrial ecosystems. Nat Commun 7:10541

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Deshpande V, Wang Q, Greenfield P, Charleston M, Porras-Alfaro A, Kuske CR, Cole JR, Midgley DJ, Tran-Dinh N (2014) Fungal identification using a Bayesian classifier and the Warcup training set of internal transcribed spacer sequences. Mycologia 108:1–5

    Article  Google Scholar 

  • Fang Y, Zhang L, Jiao Y, Liao J, Luo L, Ji S, Li J, Dai K, Zhu S, Yang M (2016) Tobacco Rotated with Rapeseed for Soil-Borne Phytophthora Pathogen Biocontrol: Mediated by Rapeseed Root Exudates. Front Microbiol 7:894

    PubMed  PubMed Central  Article  Google Scholar 

  • Fizpatrick CR, Copeland J, Wang PW, Guttman DS, Kotanen PM, Johnson MTJ (2018) Assembly of ecological function of the root microbiome across angiosperm plant species. Proc Natl Acad Sci USA 115:E1157–E1165

    Article  CAS  Google Scholar 

  • Frindte K, Pape R, Werner K, Löffler J, Knief C (2019) Temperature and soil moisture control microbial community composition in an arctic–alpine ecosystem along elevational and micro-topographic gradients. ISME J 13:2031–2043

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Fu L, Ruan Y, Tao C, Li R, Shen Q (2016) Continuous application of bioorganic fertilizer induced resilient culturable bacteria community associated with banana Fusarium wilt suppression. Sci Rep-UK 6:27731

    CAS  Article  Google Scholar 

  • Garcia-Pichel F, Loza V, Marusenko Y, Mateo PM (2013) Potrafka R. Temperature drives the continental-scale distribution of key microbes in topsoil communities. Science 340:1574–1577

    CAS  PubMed  Article  Google Scholar 

  • Ghoul M, Mitri S (2016) The Ecology and evolution of microbial competition. Trends Microbiol 24:833–845

    CAS  PubMed  Article  Google Scholar 

  • Hall M, Beiko RG (2018) 16S rRNA gene analysis with QIIME2. Microbiome Analysis: Methods in Molecular Biology 1849:113–129

    CAS  Article  Google Scholar 

  • Hartman K, Van der Heijden MGA, Wittwer RA, Banerjee S, Walser JC, Schlaeppi K (2018) Cropping practices manipulate abundance, patterns of root and soil microbiome members paving the way to smart farming. Microbiome 6:14

    PubMed  PubMed Central  Article  Google Scholar 

  • Haskett TL, Tkacz A, Poole PS (2021) Engineering rhizobacteria for sustainable agriculture. ISME J 15:949–964

    PubMed  Article  Google Scholar 

  • Hong S, Jv H, Lu M, Wang B, Zhao Y, Ruan Y (2020) Significant decline in banana Fusarium wilt disease is associated with soil microbiome reconstruction under chilli pepper-banana rotation. Eur J Soil Biol. 97:103154

    CAS  Article  Google Scholar 

  • Hope RM (2013) Package 'Rmisc': Ryan Miscellaneous. Version 1.5. https://cran.rproject.org/web/packages/Rmisc/index.html.

  • Hu J, Wei Z, Weidner S, Friman VP, Xu YC, Shen QR, Jousset A (2017) Probiotic Pseudomonas communities enhance plant growth and nutrient assimilation via diversity-mediated ecosystem functioning. Soil Biol Biochem 113:122–129

    CAS  Article  Google Scholar 

  • Hu L, Robert CAM, Cadot S, Zhang X, Ye M, Li B, Manzo D, Chervet N, Steinger T, Van der Heijden MGA, Schlaeppi K, Erb M (2018) Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nat Commun 9:2738

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Huang XQ, Wen T, Zhang JB, Meng L, Zhu TB, Liu LL (2015) Control of soilborne pathogen Fusarium oxysporum by biological soil disinfestation with incorporation of various organic matters. Eur J Plant Pathol 143:223–235

    CAS  Article  Google Scholar 

  • Huang YH, Wang RC, Li CH, Zuo CW, Wei YR, Zhang L, Yi GJ (2012) Control of Fusarium wilt in banana with Chinese leek. Eur J Plant Pathol 134:87–95

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Kamilova F, Kravchenko LV, Shaposhnikov AI, Makarova N, Lugtenberg B (2006) Effects of the tomato pathogen Fusarium oxysporum f. sp. Radicis-lycopersici and of the biocontrol bacterium Pseudomonas fluorescens WCS365 on the composition of organic acids and sugars in tomato root exudate. Mol Plant Microbe in 19:1121–1126

    CAS  Article  Google Scholar 

  • Kazerooni EA, Rethinasamy V, Al-Sadi AM (2019) Talaromyces pinophilus inhibits Pythium and Rhizoctonia-induced damping-off of cucumber. J Plant Pathol 101:377–383

    Article  Google Scholar 

  • Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD (2013) Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the miseq Illumina sequencing platform. Appl Environ Microb 79:5112–5120

    CAS  Article  Google Scholar 

  • Larkin RP, Lynch RP (2018) Use and Effects of Different brassica and other rotation crops on soil borne diseases and yield of potato. Horticulturae 4:37

    Article  Google Scholar 

  • Lebeis SL, Paredes SH, Lundberg DS, Breakfield N, Gehring J, McDonald M, Malfatiti S, Del Rio TG, Jones CD, Tringe SG, Dangl JL (2015) Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa. Science 349:860–864

    CAS  PubMed  Article  Google Scholar 

  • Li C, Tian Q, Rahman MK, Wu F (2020) Effect of anti-fungal compound phytosphingosine in wheat root exudates on the rhizosphere soil microbial community of watermelon. Plant Soil 456:223–240

    CAS  Article  Google Scholar 

  • Li CY, Mostert G, Zuo CW, Beukes I, Yang QS, Sheng O, Kuang RB, Wei YR, Hu CH, Rose L, Karangwa P, Yang J, Deng GM, Liu SW, Gao J, Viljoen A, Yi GJ (2013) Diversity and distribution of the banana wilt pathogen Fusarium oxysporum f. Sp. Cubense in China. Fungal Genom Biol: 1–16. https://doi.org/10.4172/2165-8056.1000111

  • Li H, Qiu Y, Wang X, Liu W, Chen G, Ma Y, Xing B (2016) Suspension stability and aggregation of multi-walled carbon nanotubes as affected by dissolved organic matters extracted from agricultural. Environ Pollut 210:323–329

    CAS  PubMed  Article  Google Scholar 

  • Lin F, Gao J, Zeng T, Zeng H (2010) Isolation and identification of banana vasicular wilt in Hainan Province and determination of biological characteristics of strains Focr1 and Focr4. Genom Appl Biol 29:314–321

    Google Scholar 

  • Lin Y, Ye G, Kuzyakov Y, Liu D, Fan J, Ding W (2019) Long-term manure application increases soil organic matter and aggregation, and alters microbial community structure and keystone taxa. Soil Biol Biochem 134:187–196

    CAS  Article  Google Scholar 

  • Lori M, Symnaczik S, Mäder P, Deyn DG, Gattinger A (2017) Organic farming enhances soil microbial abundance and activity-a metaanalysis and meta-Regression. PLoS ONE 12:1–25

    Article  CAS  Google Scholar 

  • Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with deseq2. Genome Biol 15:550

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Lupwayi NZ, Larney FJ, Blackshaw RE, Kanashiro DA, Pearson DC (2017) Phospholipid fatty acid biomarkers show positive soil microbial community responses to conservation soil management of irrigated crop rotations. Soil till Res 168:1–10

    Article  Google Scholar 

  • Mamet SD, Redlick E, Brabant M, Lamb EG, Helgason BL, Stanley K, Siciliano SD (2019) Structural equation modeling of a winnowed soil microbiome identifies how invasive plants re-structure microbial networks. ISME J 13:1988–1996

    PubMed  PubMed Central  Article  Google Scholar 

  • Mawarda PC, Roux XL, van Elsas JD, Salles JF (2020) Deliberate introduction of invisible invaders: a critical appraisal of the impact of microbial inoculants on soil microbial communities. Soil Biol Biochem. 148:107874

    CAS  Article  Google Scholar 

  • Meena KK, Sorty AM, Bitla UM, Choudhary K, Gupta P, Pareek A, Singh DP, Prabha R, Sahu PK, Gupta VK, Singh HB, Krishanani KK, Minhas PS (2017) Abiotic stress responses and microbe-mediated mitigation in plants: the omics strategies. Front Plant Sci 8:172

    PubMed  PubMed Central  Article  Google Scholar 

  • Mendes LW, Kuramae EE, Navarrete AA, Van Veen JA, Tsai SM (2014) Taxonomical and functional microbial community selection in soybean rhizosphere. ISME J 8:1577–1587

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Mendes R, Garbeva P, Rainmakers JM (2013) The rhizosphere microbiome: significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev 37:634–663

    CAS  PubMed  Article  Google Scholar 

  • Mendes R, Kruijt M, De Bruijn I, Dekkers E, Van der Voort M, Schneider JHM, Piceno YM, Desantis TZ, Andersen GL, Bakker PAHM, Rainmakers JM (2011) Deciphering the rhizosphere microbiome for disease-suppressive bacteria. Science 332:1097–1100

    CAS  PubMed  Article  Google Scholar 

  • Monda H, Cozzolino V, Vinci G, Spaccini R, Piccolo A (2017) Molecular characteristics of water-extractable organic matter from different composted biomasses and their effects on seed germination and early growth of maize. Sci Total Environ 590–591:40–49

    PubMed  Article  CAS  Google Scholar 

  • Mukesh D, Heriberto V, Martin B, Funck JD, Magnus K (2020) Lysm proteins regulate fungal development and contribute to hyphal protection and biocontrol traits in Clonostachys rosea. Front Microbiol 11:679

    Article  Google Scholar 

  • Nilsson RH, Anslan S, Bahram M, Wurzbacher P Baldrian, Tedersoo L (2019) Mycobiome diversity: high-throughput sequencing and identification of fungi. Nat Rev Microbiol 17:95–109

    CAS  PubMed  Article  Google Scholar 

  • Nilsson RH, Larsson KH, Taylor AFS, Bengtsson-Palme J, Jeppesen TS, Schigel D, Kennedy P, Picard K, Glöckner FO, Tedersoo L, Saar I, Kõljalg U, Abarenkov K (2018) The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res 47:D259–D264

    PubMed Central  Article  CAS  Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens, MHH, Wagner H (2012) Vegan: community ecology package. R Package ed Version n 2.5–7. https://cran.r-project.org, https://github.com/vegandevs/vegan

  • Ploetz RC (2015) Fusarium wilt of banana. Phytopathology 105:1512–1521

    PubMed  Article  Google Scholar 

  • Rainmakers JM, Mazzola M (2016) Soil immune responses. Science 352:1392–1393

    Article  Google Scholar 

  • Revelle W (2014) Package psych: Procedures for personality and psychological research. R package version 1.4.3. http://cran.r-project.org/web/packages/psych/psych.pdf

  • Rivett DW, Scheuerl T, Culbert CT, Mombrikot SB, Johnstone E, Barraclough TG, Bell T (2016) Resource-dependent attenuation of species interactions during bacterial succession. ISME J 10:2259–2268

    PubMed  PubMed Central  Article  Google Scholar 

  • Roberti R, Veronesi A, Cesari A, Cascone A, Berardino ID, Bertini L, Caruso C (2008) Induction of PR proteins and resistance by the biocontrol agent Clonostachys rosea in wheat plants infected with Fusarium culmorum. Plant Sci 175:339–347

    CAS  Article  Google Scholar 

  • Sarma BK, Yadav SK, Singh S, Singh HB (2015) Microbial consortium-mediated plant defense against phytopathogens: readdressing for enhancing efficacy. Soil Biol Biochem 8:25–33

    Article  CAS  Google Scholar 

  • Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60

    PubMed  PubMed Central  Article  Google Scholar 

  • Shen Z, Xue C, Penton CR, Thomashow LS, Zhang N, Wang B, Ruan Y, Li R, Shen Q (2019) Suppression of banana Panama disease induced by soil microbiome reconstruction through an integrated agricultural strategy. Soil Biol Biochem 128:164–174

    CAS  Article  Google Scholar 

  • Singh A, Lasek-Nesselquist E, Chaturvedi V, Chaturvedi S (2018) Trichoderma polysporum selectively inhibits white-nose syndrome fungal pathogen Pseudogymnoascus destructans amidst soil microbes. Microbiome 6:139

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Somenahally A, dupont JI, Brady J, Mclawrence J, Northup B, Gowda P, (2018) Microbial communities in soil profile are more responsive to legacy effects of wheat-cover crop rotations than tillage systems. Soil Biol Biochem 123:126–135

    CAS  Article  Google Scholar 

  • Sutton JC, Liu W, Ma J, Brown WG, Stewart JF, Walker GD (2008) Evaluation of the fungal endophyte Clonostachys rosea as an inoculant to enhance growth, fitness and productivity of crop plants. Acta Hortic 782:279–286

    Article  Google Scholar 

  • Teste FP, Kardol P, Turner BL, Wardle DA, Zemunik G, Renton M, Laliberté E (2017) Plant–soil feedback and the maintenance of diversity in Mediterranean-climate shrublands. Science 355:73–176

    Article  CAS  Google Scholar 

  • Tian T, Li S, Sun M (2014) Synergistic effect of dazomet soil fumigation and Clonostachys rosea against cucumber Fusarium wilt. Phytopathology 104:1314–1321

    PubMed  Article  Google Scholar 

  • Toju H, Peay KG, Yamamichi M, Narisawa K, Hiruma K, Naito K, Fukuda S, Ushio M, Nakaoka S, Onoda Y, Yoshida K, Schlaeppi K, Bai Y, Sugiura R, Ichihashi Y, Minamisawa K, Kiers ET (2018) Core microbiomes for sustainable agroecosystems. Nat Plants 4:247–257

    PubMed  Article  Google Scholar 

  • Van der Heijden MGA, Bardgett RD, Van Straalen NM (2008) The unseen majority: soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett 11:296–310

    PubMed  Article  Google Scholar 

  • Vieira S, Sikorski J, Dietz S, Herz K, Schrump M, Bruelheide H, Scheel D, Friedrich MW, Overmann J (2020) Drivers of the composition of active rhizosphere bacterial communities in temperate grasslands. ISME J 14:463–475

    CAS  PubMed  Article  Google Scholar 

  • Wang B, Li R, Ruan Y, Ou Y, Zhao Y, Shen Q (2015) Pineapple-banana rotation reduced the amount of Fusarium oxysporum more than maize-banana rotation mainly through modulating fungal communities. Soil Biol Biochem 86:77–86

    CAS  Article  Google Scholar 

  • Wang B, Yuan J, Zhang J, Shen Z, Zhang M, Li R, Ruan Y, Shen Q (2013) Effects of novel bioorganic fertilizer produced by Bacillus amyloliquefaciens W19 on antagonism of Fusarium wilt of banana. Biol Fertil Soils 49:435–446

    Article  Google Scholar 

  • Wang H, Wang J, Chen Q, Wang M, Hsiang T, Shang S, Yu Z (2016) Metabolic effects of azoxystrobin and kresoxim-methyl against Fusarium kyushuense examined using the Biolog FF microplate. Pestic Biochem Physi 130:52–58

    CAS  Article  Google Scholar 

  • Wang K, Yin X, Mao H, Chu C, Tian Y (2018) Changes in structure and function of fungal community in cow manure composting. Bioresource Technol 255:123–130

    CAS  Article  Google Scholar 

  • Wickham H (2012) reshape2: Flexibly reshape data: a reboot of the reshape package. R package version 1. http://cran.ms.unimelb.edu.au/

  • Wickham H, Chang W (2015) ggplot2: an implementation of the grammar of graphics. R package version 1. http://ggplot2.org, https://github.com/hadley/ggplot2

  • Yin C, Jones KL, Peterson DE, Garrett KA, Hulbert SH, Paulitz TC (2010) Members of soil bacterial communities sensitive to tillage and crop rotation. Soil Biol Biochem 42:2111–2118

    CAS  Article  Google Scholar 

  • Yuan J, Wen T, Zhang H, Penton ZM, CR, Thomashow LS, Shen Q, (2020) Predicting disease occurrence with high accuracy based on soil macroecological patterns of Fusarium wilt. ISME J 14:2936–2950

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  • Yuan J, Zhao J, Wen T, Zhao M, Li R, Goossens P, Huang Q, Bai Y, Vivanco JM, Kowalchuk GA, Berendsen RL, Shen Q (2018) Root exudates drive the soil-borne legacy of aboveground pathogen infection. Microbiome 6:156

    PubMed  PubMed Central  Article  Google Scholar 

  • Zhalnina K, Louie KB, Hao Z, Mansoori N, Da Rocha UN, Shi S, 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

    CAS  PubMed  Article  Google Scholar 

  • Zhao W, Shi X, Xian P, Feng Z, Yang J, Yang X (2021) A new fusicoccane diterpene and a new polyene from the plant endophytic fungus Talaromyces pinophilus and their antimicrobial activities. Nat Prod Res 35:124–130

    CAS  PubMed  Article  Google Scholar 

  • Zhao Z, He J, Geisen S, Han L, Wang J, Shen J, Wei W, Fang Y, Li P, Zhang L (2019) Protist communities are more sensitive to nitrogen fertilization than other microorganisms in diverse agricultural soils. Microbiome 7:33

    PubMed  PubMed Central  Article  Google Scholar 

  • Zheng T, Liang C, Xie H, Zhao J, Yan E, Zhou X, Bao X (2019) Rhizosphere effects on soil microbial community structure and enzyme activity in a successional subtropical forest. FEMS Microbiol Ecol 5:iz043

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We sincerely thank all those who have assisted us with any part of this paper and Hainan WanZhong Co., Ltd. for providing access to the experimental equipment and greenhouse facilities.

Funding

This work was supported by the National Natural Science Foundation of China (42090065 and 31972509), the Fundamental Research Funds for the Central Universities (KYXK202009 and KYXK202008), the Hainan Provincial Natural Science Foundation of China (320RC483), the Priority Academic Program Development of the Jiangsu Higher Education Institutions (PAPD), the 111 project (B12009), and the Innovative Research Team Development Plan of the Ministry of Education of China (IRT_17R56).

Author information

Authors and Affiliations

Authors

Contributions

The experiment was designed by Rong Li. All experiments were performed by Xianfu Yuan. Data collection, analysis, and writing were performed by Xianfu Yuan, Rong Li, and Francisco Dini-Andreote. Beibei Wang, Wu Xiong, Zongzhuan Shen, Yunze Ruan, Qirong Shen, Francisco Dini-Andreote, and Shan Hong contributed to the intellectual input and assistance to this study and manuscript preparation.

Corresponding author

Correspondence to Rong Li.

Ethics declarations

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

All authors have approved the manuscript in its entirety and agreed for its publication.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 17254 KB)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Yuan, X., Wang, B., Hong, S. et al. Promoting soil microbial-mediated suppressiveness against Fusarium wilt disease by the enrichment of specific fungal taxa via crop rotation. Biol Fertil Soils 57, 1137–1153 (2021). https://doi.org/10.1007/s00374-021-01594-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00374-021-01594-w

Keywords

  • Fusarium wilt disease
  • Crop rotation
  • Root exudates
  • Talaromyces pinophilus
  • Clonostachys rossmaniae
  • Disease suppression