Skip to main content

Advertisement

SpringerLink
Log in

Arbuscular mycorrhizal fungus suppresses tomato (Solanum lycopersicum Mill.) Ralstonia wilt via establishing a soil–plant integrated defense system

  • Soils, Sec 2 • Global Change, Environ Risk Assess, Sustainable Land Use • Research Article
  • Published:
Journal of Soils and Sediments Aims and scope Submit manuscript

Abstract

Purpose

Continuous cropping of tomato (Solanum lycopersicum Mill.) causes soil degradation, accumulating Ralstonia solanacearum that induce Ralstonia wilt notably in plastic shed soils. Arbuscular mycorrhizal (AM) fungi play a crucial role in protecting hosts against such soil-borne pathogens, but comprehensive understanding of the soil–plant defense systems upon mycorrhization is not clear yet, especially at the later period of fruit production. The aim of this study was to investigate the underlining mechanisms in both soil and plant.

Materials and methods

A 10-week greenhouse pot experiment with four treatments, including control and inoculation with Funneliformis caledonium (Fc), R. solanacearum (Rs), and both strains (Rs + Fc), was carried out on a sterilized soil. Pots with two tomato plants each were randomly arranged with six replicates per treatment. The wilt severity; the tissue biomass and nutrient content; the root mycorrhizal colonization and total phenolic compounds; the leaf peroxidase (POD), polyphenol oxidase (PPO), and phenylalanine ammonia lyase (PAL) activities; and soil AM fungi and R. solanacearum abundances, soil pH, organic C and nutrient concentrations, and phosphatase activity were all tested. Both redundancy analysis (RDA) and structural equation modeling (SEM) were performed to illustrate plant overall performance among treatments and to elucidate the major influencing pathways of AM fungi.

Results and discussion

The additional inoculation with F. caledonium resulted in significant decreases of soil R. solanacearum abundance and Olsen-P concentration, as well as increases of soil pH, organic C concentration, and phosphatase activity, as compared to the soil only inoculated with R. solanacearum. Mycorrhizal inoculation also increased root total phenolic compound content, and leaf POD and PPO activities, but reduced shoot/root K ratio in plants under the attack of R. solanacearum, thereby alleviating Ralstonia wilt severity by 65.7% and yield loss by 46.5%. The RDA and SEM results revealed significant variation in plant overall performance among treatments, and the contribution of AM fungi in suppressing tomato Ralstonia wilt and yield damage particularly via ameliorating soil quality and alleviating plant metabolic pressure.

Conclusions

This study verified the bio-protection of AM fungi in both soil and plant systems against tomato Ralstonia wilt. Mycorrhization shifted the soil environment and suppressed soil R. solanacearum population, and also modulated plant nutrient translocation, increased phenolic compounds synthetization, and activated defense enzymes. Through establishing the integrated defense systems in both rhizosphere and plant, AM fungi alleviated the severity of Ralstonia disease and ameliorated yield damage in tomato.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aloyce A, Ndakidemi PA, Mbega ER (2019) Survey and conventional management methods of bacterial wilt disease in open fields and greenhouses in Tanzania. J Plant Pathol 101:1107–1114

    Article  Google Scholar 

  • Azcon-Aguilar C, Barea JM (1996) Arbuscular mycorrhizas and biological control of soil-borne plant pathogens-an overview of the mechanisms involved. Mycorrhiza 6:457–464

    Article  Google Scholar 

  • Bernsdorff F, Doring AC, Gruner K, Schuck S, Brautigam A, Zeier J (2016) Pipecolic acid orchestrates plant systemic acquired resistance and defense priming via salicylic acid-dependent and -independent pathways. Plant Cell 28:102–129

    Article  CAS  Google Scholar 

  • Baum C, El-Tohamy W, Gruda N (2015) Increasing the productivity and product quality of vegetable crops using arbuscular mycorrhizal fungi: A review. Sci Hortic 187:131–141

    Article  Google Scholar 

  • Bhai RS, Prameela TP, Vincy K, Biju CN, Srinivasan V, Babu KN (2019) Soil solarization and amelioration with calcium chloride or Bacillus licheniformis-an effective integrated strategy for the management of bacterial wilt of ginger incited by Ralstonia pseudosolanacearum. Eur J Plant Pathol 154:903–917

    Article  CAS  Google Scholar 

  • Chave M, Crozilhac P, Deberdt P, Plouznikoff K, Declerck S (2017) Rhizophagus irregularis MUCL 41833 transitorily reduces tomato bacterial wilt incidence caused by Ralstonia solanacearum under in vitro conditions. Mycorrhiza 27:719–723

    Article  Google Scholar 

  • Chen M, Arato M, Borghi L, Nouri E, Reinhardt D (2018) Beneficial services of arbuscular mycorrhizal fungi - From ecology to application. Front Plant Sci 9:1270

    Article  Google Scholar 

  • Cordier C, Gianinazzi S, Gianinazzi-Pearson V (1996) Colonisation patterns of root tissues by Phytophthora nicotianae var. parasitica related to reduced disease in mycorrhizal tomato. Plant Soil 185:223–232

    Article  CAS  Google Scholar 

  • Cordier C, Pozo MJ, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (1998) Cell defense responses associated with localized and systemic resistance to Phytophthora parasitica induced in tomato by an arbuscular mycorrhizal fungus. Mol Plant Microbe Interact 11:1017–1028

    Article  CAS  Google Scholar 

  • Cui XC, Hu JL, Lin XG, Wang FY, Chen RR, Wang JH, Zhu JG (2013) Arbuscular mycorrhizal fungi alleviate ozone stress on nitrogen nutrition of field wheat. J Agric Sci Technol 15:1043–1052

    CAS  Google Scholar 

  • Costa KDD, dos Santos PR, dos Santos AMM, Silva AMF, Chagas JTB, de Carvalho JLS, Pereira JWD, Silva MD, da Silva JR, Menezes D (2019) Genetic control of tomato resistance to Ralstonia solanacearum. Euphytica 215:136

    Article  CAS  Google Scholar 

  • De Coninck B, Timmermans P, Vos C, Cammue BPA, Kazan K (2015) What lies beneath: belowground defense strategies in plants. Trends Plant Sci 20:91–101

    Article  CAS  Google Scholar 

  • Eke P, Chatue GC, Wakam LN, Kouipou RMT, Fokou PVT, Boyom FF (2016) Mycorrhiza consortia suppress the Fusarium root rot (Fusarium solani f. sp Phaseoli) in common bean (Phaseolus vulgaris L.). Biol Control 103:240–250

    Article  Google Scholar 

  • Elazouni I, Abdel-Aziz S, Rabea A (2019) Microbial efficacy as biological agents for potato enrichment as well as bio-controls against wilt disease caused by Ralstonia solanacearum. World J Microbiol Biotechnol 35:30

    Article  CAS  Google Scholar 

  • Elphinstone J, Allen C, Prior P, Hayward A (2005) The current bacterial wilt situation: a global overview. In: Allen C, Prior P, Hayward AC (eds) Bacterial wilt disease and the Ralstonia solanacearum species complex. American Phytophatological Society Press, St. Paul, Minnesota, pp 9–28

    Google Scholar 

  • Elsayed TR, Jacquiod S, Nour EH, Sorensen SJ, Smalla K (2020) Biocontrol of bacterial wilt disease through complex interaction between tomato plant, antagonists, the indigenous rhizosphere microbiota, and Ralstonia solanacearum. Front Microbiol 10:15

    Article  Google Scholar 

  • Fox J, Weisberg S (2019). An R companion to Applied Regression (3rd ed). Sage Publications

  • Ghareeb H, Bozso Z, Ott PG, Repenning C, Stahl F, Wydra K (2011) Transcriptome of silicon-induced resistance against Ralstonia solanacearum in the silicon non-accumulator tomato implicates priming effect. Physiol Mol Plant Pathol 75:83–89

    Article  CAS  Google Scholar 

  • Gianinazzi S, Gollotte A, Binet MN, van Tuinen D, Redecker D, Wipf D (2010) Agroecology: the key role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530

    Article  Google Scholar 

  • Giovannetti M, Mosse B (1980) An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500

    Article  Google Scholar 

  • Hartz TK, Miyao G, Mullen RJ, Cahn MD, Brittan KL (1999) Potassium requirements for maximum yield and fruit quality of processing tomato. J Am Soc Hortic Sci 124:199–204

    Article  Google Scholar 

  • Hou S, Zhang Y, Li M, Liu H, Wu F, Hu J, Lin X (2020) Concomitant biocontrol of pepper Phytophthora blight by soil indigenous arbuscular mycorrhizal fungi via upfront film-mulching with reductive fertilizer and tobacco waste. J Soils Sediments 20:452–460

    Article  CAS  Google Scholar 

  • Hu J, Lin X, Wang J, Shen W, Wu S, Peng S, Mao T (2010) Arbuscular mycorrhizal fungal inoculation enhances suppression of cucumber Fusarium wilt in greenhouse soils. Pedosphere 20:586–593

    Article  CAS  Google Scholar 

  • Hu J, Hou S, Li M, Wang J, Wu F, Lin X (2020) The better suppression of pepper Phytophthora blight by arbuscular mycorrhizal (AM) fungus than Purpureocillium lilacinum alone or combined with AM fungus. J Soils Sediments 20:792–800

    Article  CAS  Google Scholar 

  • Jaiti F, Meddich A, Hadrami IE (2017) Effectiveness of arbuscular mycorrhizal fungi in the protection of date palm (Phoenix dactylifera L.) against bayoud disease. Physiol Mol Plant Pathol 71:166–173

    Article  CAS  Google Scholar 

  • Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38:651–664

    Article  CAS  Google Scholar 

  • Karagiannidis N, Bletsos F, Stavropoulos N (2002) Effect of Verticillium wilt (Verticillium dahliae Kleb.) and mycorrhiza (Glomus mosseae) on root colonization, growth and nutrient uptake in tomato and eggplant seedlings. Sci Hortic 94:145–156

    Article  CAS  Google Scholar 

  • Kelman Z, Farkas FI, Lovredkovich I (1954) Hypersensitive reaction induced by phytophathogenic bacteria in the tobacoo leaf. Phytopathology 54:474–477

    Google Scholar 

  • Kempe J, Sequeira L (1983) Biological-control of bacterial wilt of potatoes – attempts to induce resistance by treating tubers with bacteria. Plant Dis 67:499–503

    Article  Google Scholar 

  • Keys E (2004) Commercial agriculture as creative destruction or destructive creation: a case study of chili cultivation and plant-pest disease in the southern Yucatan region. Land Degrad Dev 15:397–409

    Article  Google Scholar 

  • Kim BS, French E, Caldwell D, Harrington EJ, Iyer-Pascuzzi AS (2016) Bacterial wilt disease: host resistance and pathogen virulence mechanisms. Physiol Mol Plant Pathol 95:37–43

    Article  Google Scholar 

  • Kline RB (2015) Principles and practice of structural equation modeling. Guilford Publications.

  • Liao JP, Lin XG, Cao ZH, Shi YQ, Wong MH (2003) Interactions between arbuscular mycorrhizae and heavy metals under sand culture experiment. Chemosphere 50:847–853

    Article  CAS  Google Scholar 

  • Liu JJ, Liu JL, Liu JH, Cui MM, Huang YJ, Tian Y, Chen AQ, Xu GH (2019a) The potassium transporter SIHAK10 is involved in mycorrhizal potassium uptake. Plant Physiol 180:465–479

    Article  CAS  Google Scholar 

  • Liu J, Yao Q, Li Y, Zhang W, Mi G, Chen X, Yu Z, Wang G (2019b) Continuous cropping of soybean alters the bulk and rhizospheric soil fungal communities in a Mollisol of Northeast PR China. Land Degrad Dev 30:1725–1738

    Article  Google Scholar 

  • Liu YJ, He JX, Shi GX, An LZ, Feng OM, HY, (2011) Diverse communities of arbuscular mycorrhizal fungi inhabit sites with very high altitude in Tibet Plateau. FEMS Microbiol Ecol 78:355–365

    Article  CAS  Google Scholar 

  • Lopez-Raez JA, Flors V, Garcia JM, Pozo MJ (2010a) AM symbiosis alters phenolic acid content in tomato roots. Plant Signal Behav 5:1138–1140

    Article  CAS  Google Scholar 

  • Lopez-Raez JA, Verhage A, Fernandez I, Garcia JM, Azcon-Aguilar C, Flors V, Pozo MJ (2010b) Hormonal and transcriptional profiles highlight common and differential host responses to arbuscular mycorrhizal fungi and the regulation of the oxylipin pathway. J Exp Bot 61:2589–2601

    Article  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    Article  CAS  Google Scholar 

  • Lu R (2000) Analyticle methods for soil and agro-chemistry. China Agicultural Science and Technology Press, Beijing

    Google Scholar 

  • Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M, Ronald P, Dow M, Verdier V, Beer SV, Machado MA, Toth I, Salmond G, Foster GD (2012) Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol 13:614–629

    Article  Google Scholar 

  • Mariutto M, Duby F, Adam A, Bureau C, Fauconnier ML, Ongena M, Thonart P, Dommes J (2011) The elicitation of a systemic resistance by Pseudomonas putida BTP1 in tomato involves the stimulation of two lipoxygenase isoforms. BMC Plant Biol 11:29

    Article  CAS  Google Scholar 

  • Matern U, Grimmig B, Kneusel RE (1995) Plant cell wall reinforcement in the disease-resistance response: molecular composition and regulation. Can J Bot 73:511–517

    Article  Google Scholar 

  • Mebius LJ (1960) A rapid method for the determination of organic carbon in soil. Anal Chim Acta 22:120–124

    Article  CAS  Google Scholar 

  • Meisinger JJ, Bandel VA, Angle JS, O’Keefe BE, Reynolds CM (1992) Presidedress soil nitrate test evaluation in Maryland. Soil Sci Soc Am J 56:575–578

    Article  Google Scholar 

  • Mori Y, Inoue K, Ikeda K, Nakayashiki H, Higashimoto C, Ohnishi K, Kiba A, Hikichi Y (2016) The vascular plant-pathogenic bacterium Ralstonia solanacearum produces biofilms required for its virulence on the surfaces of tomato cells adjacent to intercellular spaces. Mol Plant Pathol 17:890–902

    Article  CAS  Google Scholar 

  • Nair A, Kolet SP, Thulasiram HV, Bhargava S (2015) Role of methyl jasmonate in the expression of mycorrhizal induced resistance against Fusarium oxysporum in tomato plants. Physiol Mol Plant Pathol 92:139–145

    Article  CAS  Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens H, Szocs E, Wagner H (2018) vegan: Community Ecology Package. Ordination methods, diversity analysis and other functions for community and vegetation ecologists. Ver 2.5–1

  • Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. US Department of Agriculture, Washington

    Google Scholar 

  • Pankhurst CE, Lynch JM (2005) Biocontrol of soil-borne plant diseases. In: Hillel D (ed) Encyclopedia of soils in the environment. Elsevier, Oxford, pp 129–136

    Chapter  Google Scholar 

  • Perez-de-Luque A, Tille S, Johnson I, Pascual-Pardo D, Ton J, Cameron DD (2017) The interactive effects of arbuscular mycorrhiza and plant growth-promoting rhizobacteria synergistically enhance host plant defences against pathogens. Sci Rep 7:16409

    Article  CAS  Google Scholar 

  • Peter MG (1989) Chemical modifications of bio-polymers by quinones and quinone methides. Angew Chem Int Ed 28:555–570

    Article  Google Scholar 

  • Pozo MJ, Azcon-Aguilar C (2007) Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol 10:393–398

    Article  CAS  Google Scholar 

  • Pozo MJ, Cordier C, Dumas-Gaudot E, Gianinazzi S, Barea JM, Azcon-Aguilar C (2002) Localized versus systemic effect of arbuscular mycorrhizal fungi on defense responses to Phytophthora infection in tomato plants. J Exp Bot 53:525–534

    Article  CAS  Google Scholar 

  • Qin M, Zhang Q, Pan J, Jiang S, Liu Y, Bahadur A, Peng Z, Yang Y, Feng H (2020) Effect of arbuscular mycorrhizal fungi on soil enzyme activity is coupled with increased plant biomass. Eur J Soil Sci 71:84–92

    CAS  Google Scholar 

  • R Development Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Ren LX, Lou YS, Sakamoto K, Inubushi K, Amemiya Y, Shen QR, Xu GH (2010) Effects of arbuscular mycorrhizal colonization on microbial community in rhizosphere soil and Fusarium wilt disease in tomato. Commun Soil Sci Plant Anal 41:1399–1410

    Article  CAS  Google Scholar 

  • Rivero J, Alvarez D, Flors V, Azcon-Aguilar C, Pozo MJ (2018) Root metabolic plasticity underlies functional diversity in mycorrhiza-enhanced stress tolerance in tomato. New Phytol 220:1322–1336

    Article  CAS  Google Scholar 

  • Rivero J, Gamir J, Aroca R, Pozo MJ, Flors V (2015) Metabolic transition in mycorrhizal tomato roots. Front Microbiol 6:598

    Article  Google Scholar 

  • Schonfeld J, Heuer H, van Elsas JD, Smalla K (2003) Specific and sensitive detection of Ralstonia solanacearum in soil on the basis of PCR amplification of fliC fragments. Appl Environ Microbiol 69:7248–7256

    Article  CAS  Google Scholar 

  • Singh R, Soni SK, Kalra A (2013) Synergy between Glomus fasciculatum and a beneficial Pseudomonas in reducing root diseases and improving yield and forskolin content in Coleus forskohlii Briq. under organic field conditions. Mycorrhiza 23:35–44

    Article  Google Scholar 

  • Smith FA, Smith SE (2015) How harmonious are arbuscular mycorrhizal symbioses? Inconsistent concepts reflect different mindsets as well as results. New Phytol 205:1381–1384

    Article  Google Scholar 

  • Smith SE, Facelli E, Pope S, Smith FA (2010) Plant performance in stressful environments: interpreting new and established knowledge of the roles of arbuscular mycorrhizas. Plant Soil 326:3–20

    Article  CAS  Google Scholar 

  • Smith SE, Read D (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press

    Google Scholar 

  • Song YY, Chen DM, Lu K, Sun ZX, Zeng RS (2015) Enhanced tomato disease resistance primed by arbuscular mycorrhizal fungus. Front Plant Sci 6:13

    Article  Google Scholar 

  • Tabatabai MA (1994) Soil enzymes. In: Weaver RW, Angle GS, Bottomley PS, Bezdicek D, Smith S, Tabatabai MA, Wollum A (eds) Methods of soil analysis. Soil Science Society of America, Madison, Wisconsin, pp 775–833

    Google Scholar 

  • Tahat MM, Sijam K, Othman R (2012) Ultrastructural changes of tomatoes (Lycopersicon esculentum) root colonizaed by Glomus mosseae and Ralstonia solanacearum. Afr J Biotechnol 11:6681–6686

    Google Scholar 

  • Taheri P, Kakooee T (2017) Reactive oxygen species accumulation and homeostasis are involved in plant immunity to an opportunistic fungal pathogen. J Plant Physiol 216:152–163

    Article  CAS  Google Scholar 

  • Taiwo L, Adebayo DT, Adebayo OS, Adediran JA (2007) Compost and Glomus mosseae for management of bacterial and Fusarium wilts of tomato. Int J Veg Sci 13:49–61

    Article  Google Scholar 

  • Vos CM, Yang Y, De Coninck B, Cammue BPA (2014) Fungal (-like) biocontrol organisms in tomato disease control. Biol Control 74:65–81

    Article  Google Scholar 

  • Wang YY, Yin QS, Qu Y, Li GZ, Hao L (2018) Arbuscular mycorrhiza-mediated resistance in tomato against Cladosporium fulvum-induced mould disease. J Phytopathol 166:67–74

    Article  CAS  Google Scholar 

  • War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7:1306–1320

    Article  Google Scholar 

  • Wei Z, Gu Y, Friman VP, Kowalchuk GA, Xu Y, Shen Q, Jousset A (2019) Initial soil microbiome composition and functioning predetermine future plant health. Sci Adv 5:eaaw0759

    Article  CAS  Google Scholar 

  • Wei Z, Yang XM, Yin SX, Shen QR, Ran W, Xu YC (2011) Efficacy of Bacillus-fortified organic fertiliser in controlling bacterial wilt of tomato in the field. Appl Soil Ecol 48:152–159

    Article  Google Scholar 

  • Yang CL, Dong Y, Friman VP, Jousset A, Wei Z, Xu YC, Shen QR (2019) Carbon resource richness shapes bacterial competitive interactions by alleviating growth-antibiosis trade-off. Funct Ecol 33:868–875

    Article  Google Scholar 

  • Yabuuchi E, Kosako Y, Yano I, Hotta H, Nishiuchi Y (1995) Transfer of two Burkholderia and an Alcaligenes species to Ralstonia gen. Nov. and Ralstonia eutropha (Davis 1969) comb Nov. Microbiol Immunol 39:897–905

    Article  CAS  Google Scholar 

  • Yuan S, Li M, Fang Z, Liu Y, Shi W, Pan B, Wu K, Shi J, Shen B, Shen Q (2016) Biological control of tobacco bacterial wilt using Trichoderma harzianum amended bioorganic fertilizer and the arbuscular mycorrhizal fungi Glomus mosseae. Biol Control 92:164–171

    Article  Google Scholar 

  • Yuliar NYA, Toyota K (2015) Recent trends in control methods for bacterial wilt diseases caused by Ralstonia solanacearum. Microbes Environ 30:1–11

    Article  CAS  Google Scholar 

  • Zeist AR, de Resende JTV, Pozzebon BC, Gabriel A, da Silva AA, Zeist RA (2019) Combination of solarization, biofumigation and grafting techniques for the management of bacterial wilt in tomato. Hortic Bras 37:260–265

    Article  Google Scholar 

  • Zhu HH, Yao Q (2004) Localized and systemic increase of phenols in tomato roots induced by Glomus versiforme inhibits Ralstonia solanacearum. J Phytopathol 152:537–542

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to Dr. Zhong Wei for supplying the strain of Ralstonia solanacearum QL-Rs1115, and to Dr. Jiangang Li, Dr. Feifei Sun, and Ms. Qi Zhao for their assistance in field soil sampling. We also acknowledge two anonymous reviewers and the editor for their valuable suggestions on the manuscript revision.

Funding

This work was supported by the National Key R&D Program of China (2017YFD0200603), the National Natural Science Foundation of China (No. 41671265), and the Knowledge Innovation Program of Chinese Academy of Sciences (CAS) (ISSASIP1634). J. Hu is supported by the Youth Innovation Promotion Association, CAS (No. 2016285).

Author information

Authors and Affiliations

  1. State Key Laboratory of Soil and Sustainable Agriculture, Institute of Soil Science, Chinese Academy of Sciences, Nanjing, 210008, China

    Minghui Li, Shaowei Hou, Junhua Wang, Junli Hu & Xiangui Lin

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Junli Hu

Authors
  1. Minghui Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shaowei Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Junhua Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Junli Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xiangui Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Junli Hu.

Ethics declarations

Human participant and/or animal rights and informed consent

None.

Conflict of interest

The authors declare no competing interests.

Additional information

Responsible editor: Dulce Flores-Rentería

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, M., Hou, S., Wang, J. et al. Arbuscular mycorrhizal fungus suppresses tomato (Solanum lycopersicum Mill.) Ralstonia wilt via establishing a soil–plant integrated defense system. J Soils Sediments 21, 3607–3619 (2021). https://doi.org/10.1007/s11368-021-03016-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11368-021-03016-8

Keywords

Search

Navigation