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Effects of earthworms and arbuscular mycorrhizal fungi on preventing Fusarium oxysporum infection in the strawberry plant

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Abstract

Background and aims

Fusarium wilt is a devastating fungal disease in strawberries caused by Fusarium spp. We aimed to determine the role of earthworms and arbuscular mycorrhizal (AM) fungi in preventing Fusarium oxysporum (Fof) infection in strawberry plants.

Methods

AM fungi, Fof and the copy number of Actinomyces genes were determined by a quantitative real-time polymerase chain reaction. The Shannon–Wiener index for microbial communities was determined by their terminal restriction fragment length polymorphism profiles. Structural equation modelling was used to establish the relationships between the disease index and abiotic/biotic variables.

Results

Earthworms and AM fungi could individually or interactively prevent the infection of strawberry plants by Fof. Earthworms significantly decreased the copy number of Fof in the soil. The AM fungi increased the copy number of Actinomycetes and bacterial diversity and decreased the disease index of Fusarium wilt. Correlation analysis indicated that the root Ca and shoot Mg contents and the number of AM gene copies in plant roots had a significant negative correlation with the disease index of Fusarium wilt and the number of gene copies of Fof in plant roots.

Conclusions

The addition of earthworms and AM fungi to soil is a promising biological control method for the prevention of Fusarium wilt in strawberries and acts via an increase in the soil organic matter content, regulation of the soil environment, and improved root (P, Ca, Mg and Fe) and shoot (N, P, K, Ca and Mg) nutrient contents.

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References

  • Akhtar MS, Siddiqui ZA, Wiemken A (2011) Arbuscular mycorrhizal fungi and Rhizobium to control plant fungal diseases. In: Alternative farming systems, biotechnology, drought stress and ecological fertilisation. Springer, Dordrecht, pp 263–292

    Google Scholar 

  • Arbuckle JL (2006) Amos (version 7.0) [computer program]. SPSS, Chicago

    Google Scholar 

  • Arroyo FT, Llergo Y, Aguado A, Romero F (2009) First report of Fusarium wilt caused by Fusarium oxysporum on strawberry in Spain. Plant Dis 93:323–323

    CAS  PubMed  Google Scholar 

  • Ayuke FO, Lagerlöf J, Jorge G, Söderlund S, Muturi JJ, Sarosh BR, Meijer J (2017) Effects of biocontrol bacteria and earthworms on the severity of Alternaria brassicae disease and the growth of oilseed rape plants (Brassica napus). Appl Soil Ecol 117:63–69

    Google Scholar 

  • Azcón-Aguilar C, Barea JM (1997) Arbuscular mycorrhizas and biological control of soil-borne plant pathogens–an overview of the mechanisms involved. Mycorrhiza 6:457–464

    Google Scholar 

  • Aznar A, Chen NW, Thomine S, Dellagi A (2015) Immunity to plant pathogens and iron homeostasis. Plant Sci 240:90–97

    CAS  PubMed  Google Scholar 

  • Berrocal-Lobo M, Molina A (2008) Arabidopsis defense response against Fusarium oxysporum. Trends Plant Sci 13:145–150

    CAS  PubMed  Google Scholar 

  • Bertrand M, Blouin M, Barot S, Charlier A, Marchand D, Roger-Estrade J (2015) Biocontrol of eyespot disease on two winter wheat cultivars by an anecic earthworm (Lumbricus terrestris). Appl Soil Ecol 96:33–41

    Google Scholar 

  • Bianco L, Lopez L, Scalone AG, Di Carli M, Desiderio A, Benvenuto E, Perrotta G (2009) Strawberry proteome characterization and its regulation during fruit ripening and in different genotypes. J Proteome 72:586–607

    CAS  Google Scholar 

  • Blouin M, Hodson ME, Delgado EA, Baker G, Brussaard L, Butt KR, Cluzeau D et al (2013) A review of earthworm impact on soil function and ecosystem services. Eur J Soil Sci 64:161–182

    Google Scholar 

  • Calvet C, Pera J, Barea JM (1993) Growth response of marigold (Tagetes erecta L.) to inoculation with Glomus mosseae, Trichoderma aureoviride and Pythium ultimum in a peat-perlite mixture. Plant Soil 148:1–6

    Google Scholar 

  • Cameron DD, Neal AL, van Wees SC, Ton J (2013) Mycorrhiza-induced resistance: more than the sum of its parts? Trends Plant Sci 18:539–545

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cao J, Ji D, Wang C (2015a) Interaction between earthworms and arbuscular mycorrhizal fungi on the degradation of oxytetracycline in soils. Soil Biol Biochem 90:283–292

    CAS  Google Scholar 

  • Cao J, Wang C, Huang Y (2015b) Interactive impacts of earthworms (Eisenia fetida) and arbuscular mycorrhizal fungi (Funneliformis mosseae) on the bioavailability of calcium phosphates. Plant Soil 396:45–57

    CAS  Google Scholar 

  • Cao J, Wang C, Dou Z, Ji D (2016) Independent and combined effects of oxytetracycline and antibiotic-resistant Escherichia coli O157: H7 on soil microbial activity and partial nitrification processes. Soil Biol Biochem 98:138–147

    CAS  Google Scholar 

  • Cha JY, Han S, Hong HJ, Cho H, Kim D, Kwon Y, Giaever G (2016) Microbial and biochemical basis of a Fusarium wilt-suppressive soil. ISME J 10:119–129

    CAS  PubMed  Google Scholar 

  • de la Lastra E, Basallote-Ureba MJ, De los Santos B, Miranda L, Vela-Delgado MD, Capote N (2018) A TaqMan real-time polymerase chain reaction assay for accurate detection and quantification of Fusarium solani in strawberry plants and soil. Sci Hortic 237:128–134

    Google Scholar 

  • Debona D, Rios JA, Nascimento KJT, Silva LC, Rodrigues FA (2016) Influence of magnesium on physiological responses of wheat infected by Pyricularia oryzae. Plant Pathol 65:114–123

    CAS  Google Scholar 

  • Dinler H, Benlioglu S, Benlioglu K (2016) Occurrence of Fusarium wilt caused by Fusarium oxysporum on strawberry transplants in Aydın Province in Turkey. Australas Plant Dis Notes 11:10

    Google Scholar 

  • Du H, Lu H, Xu Y, Du X (2013) Community of environmental Streptomyces related to geosmin development in Chinese liquors. J Agric Food Chem 61:1343–1348

    CAS  PubMed  Google Scholar 

  • Eisenhauer N, Bowker MA, Grace JB, Powell JR (2015) From patterns to causal understanding: structural equation modeling (SEM) in soil ecology. Pedobiologia 58:65–72

    Google Scholar 

  • Elmer WH (2009) Influence of earthworm activity on soil microbes and soilborne diseases of vegetables. Plant Dis 93:175–179

    PubMed  Google Scholar 

  • Elmer WH, Ferrandino FJ (2009) Suppression of Verticillium wilt of eggplant by earthworms. Plant Dis 93:485–489

    PubMed  Google Scholar 

  • Estrada B, Aroca R, Barea JM, Ruiz-Lozano JM (2013) Native arbuscular mycorrhizal fungi isolated from a saline habitat improved maize antioxidant systems and plant tolerance to salinity. Plant Sci 201: 42–51

    CAS  PubMed  Google Scholar 

  • Fang X, Phillips D, Li H, Sivasithamparam K, Barbetti MJ (2011) Comparisons of virulence of pathogens associated with crown and root diseases of strawberry in Western Australia with special reference to the effect of temperature. Sci Hortic 131:39–48

    Google Scholar 

  • Fang X, Kuo J, You MP, Finnegan PM, Barbetti MJ (2012) Comparative root colonisation of strawberry cultivars Camarosa and Festival by Fusarium oxysporum f. sp. fragariae. Plant Soil 358:75–89

    CAS  Google Scholar 

  • Garg N, Chandel S (2010) Arbuscular mycorrhizal networks: process and functions. A review. Agron Sustain Dev 30:581–599

    CAS  Google Scholar 

  • Gordon TR (2017) Fusarium oxysporum and the Fusarium wilt syndrome. Annu Rev Phytopathol 55:23–39

    CAS  PubMed  Google Scholar 

  • Goudjal Y, Toumatia O, Yekkour A, Sabaou N, Mathieu F, Zitouni A (2014) Biocontrol of Rhizoctonia solani damping-off and promotion of tomato plant growth by endophytic actinomycetes isolated from native plants of Algerian Sahara. Microbiol Res 169:59–65

    CAS  PubMed  Google Scholar 

  • Henry PM, Kirkpatrick SC, Islas CM, Pastrana AM, Yoshisato JA, Koike ST, Gordon TR et al (2017) The population of Fusarium oxysporum f. sp. fragariae, cause of Fusarium wilt of strawberry, in California. Plant Dis 101:550–556

    CAS  PubMed  Google Scholar 

  • Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413: 297–299

    CAS  PubMed  Google Scholar 

  • Huber DM, Jones JB (2013) The role of magnesium in plant disease. Plant Soil 368:73–85

    CAS  Google Scholar 

  • Huber D, Römheld V, Weinmann M (2012) Relationship between nutrition, plant diseases and pests. In: Marschner P (ed) Marschner's mineral nutrition of higher plants, 3rd edn. Science Press, Beijing, pp 283–298

    Google Scholar 

  • Hume EA, Horrocks AJ, Fraser PM, Curtin D, Meenken ED, Chng S, Beare MH (2015) Alleviation of take-all in wheat by the earthworm Aporrectodea caliginosa (Savigny). Appl Soil Ecol 90:18–25

    Google Scholar 

  • Jansa J, Mozafar A, Kuhn G, Anken T, Ruh R, Sanders IR, Frossard E (2003) Soil tillage affects the community structure of mycorrhizal fungi in maize roots. Ecol Appl 13:1164–1176

    Google Scholar 

  • Johansson JF, Paul LR, Finlay RD (2004) Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol Ecol 48:1–13

    CAS  PubMed  Google Scholar 

  • Juber KS, Al-Juboory HH, Al-Juboory SB (2014) Fusarium wilt disease of strawberry caused by Fusarium oxysporum f. sp. Fragariae in Iraq and its control. J Exp Biol Agric Sci 2:419–427

    Google Scholar 

  • Klosterman SJ, Subbarao KV, Kang S, Veronese P, Gold SE, Thomma BP, Garcia-Pedrajas MD et al (2011) Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens. PLoS Pathog 7:e1002137. https://doi.org/10.1371/journal.ppat.1002137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koike ST, Gordon TR (2015) Management of Fusarium wilt of strawberry. Crop Prot 73:67–72

    CAS  Google Scholar 

  • Lang J, Hu J, Ran W, Xu Y, Shen Q (2012) Control of cotton Verticillium wilt and fungal diversity of rhizosphere soils by bio-organic fertilizer. Biol Fertil Soils 48:191–203

    Google Scholar 

  • Lecomte C, Edel-Hermann V, Cannesan MA, Gautheron N, Langlois A, Alabouvette C, Steinberg C et al (2016) Fusarium oxysporum f. sp. cyclaminis: underestimated genetic diversity. Eur J Plant Pathol 145:421–431

    Google Scholar 

  • Leplat J, Friberg H, Abid M, Steinberg C (2013) Survival of Fusarium graminearum, the causal agent of Fusarium head blight. A review. Agron Sustain Dev 33:97–111

    Google Scholar 

  • Li M, Asano T, Suga H, Kageyama K (2011) A multiplex PCR for the detection of Phytophthora nicotianae and P. cactorum, and a survey of their occurrence in strawberry production areas of Japan. Plant Dis 95:1270–1278

    CAS  PubMed  Google Scholar 

  • Li Y, Mao L, Yan D, Ma T, Shen J, Guo M, Cao A (2014) Quantification of Fusarium oxysporum in fumigated soils by a newly developed real-time PCR assay to assess the efficacy of fumigants for Fusarium wilt disease in strawberry plants. Pest Manag Sci 70:1669–1675

    CAS  PubMed  Google Scholar 

  • Lievens B, Brouwer M, Vanachter AC, Cammue BP, Thomma BP (2006) Real-time PCR for detection and quantification of fungal and oomycete tomato pathogens in plant and soil samples. Plant Sci 171:155–165

    CAS  Google Scholar 

  • Martin FN, Bull CT (2002) Biological approaches for control of root pathogens of strawberry. Phytopathology 92:1356–1362

    CAS  PubMed  Google Scholar 

  • McInnes TB, Black LL, Gatti JM Jr (1992) Disease-free plants for management of strawberry anthracnose crown rot. Plant Dis 76:260–264

    Google Scholar 

  • McMullen M, Bergstrom G, De Wolf E, Dill-Macky R, Hershman D, Shaner G, Van Sanford D (2012) A unified effort to fight an enemy of wheat and barley: Fusarium head blight. Plant Dis 96:1712–1728

    PubMed  Google Scholar 

  • Meyer-Wolfarth F, Schrader S, Oldenburg E, Weinert J, Brunotte J (2017) Biocontrol of the toxigenic plant pathogen Fusarium culmorum by soil fauna in an agroecosystem. Mycotoxin Res 33:237–244

    PubMed  Google Scholar 

  • Milleret R, Le Bayon RC, Gobat JM (2009) Root, mycorrhiza and earthworm interactions: their effects on soil structuring processes, plant and soil nutrient concentration and plant biomass. Plant Soil 316:1–12

    CAS  Google Scholar 

  • Nam MH, Jung SK, Kim NG, Yoo SJ, Kim HG (2005) Resistance analysis of cultivars and occurrence survey of Fusarium wilt on strawberry. Res Plant Dis 11:35–38

    Google Scholar 

  • Niu L, Liao W (2016) Hydrogen peroxide signaling in plant development and abiotic responses: crosstalk with nitric oxide and calcium. Front Plant Sci 7:230

    PubMed  PubMed Central  Google Scholar 

  • Nunan N, Lerch TZ, Pouteau V, Mora P, Changey F, Kätterer T, Herrmann AM et al (2015) Metabolising old soil carbon: simply a matter of simple organic matter? Soil Biol Biochem 88:128–136

    CAS  Google Scholar 

  • Palaniyandi SA, Yang SH, Zhang L, Suh JW (2013) Effects of actinobacteria on plant disease suppression and growth promotion. Appl Microbiol Biotechnol 97:9621–9636

    CAS  PubMed  Google Scholar 

  • Paudel S, Longcore T, MacDonald B, McCormick MK, Szlavecz K, Wilson GW, Loss SR (2016) Belowground interactions with aboveground consequences: invasive earthworms and arbuscular mycorrhizal fungi. Ecology 97:605–614

    PubMed  Google Scholar 

  • Paynter ML, De Faveri J, Herrington ME (2014) Resistance to Fusarium oxysporum f. sp. fragariae and predicted breeding values in strawberry. J Am Soc Hortic Sci 139:178–184

    Google Scholar 

  • Pérez-Jiménez RM, De Cal A, Melgarejo P, Cubero J, Soria C, Zea-Bonilla T, Larena I (2012) Resistance of several strawberry cultivars against three different pathogens. Span J Agric Res 10:502–512

    Google Scholar 

  • Pincot DD, Poorten TJ, Hardigan MA, Harshman JM, Acharya CB, Cole GS, Knapp SJ et al (2018) Genome-wide association mapping uncovers fw1, a dominant gene conferring resistance to Fusarium wilt in strawberry. G3 Genesgenetics 8:1817–1828

    CAS  Google Scholar 

  • Plavšin I, Velki M, Ečimović S, Vrandečić K, Ćosić J (2017) Inhibitory effect of earthworm coelomic fluid on growth of the plant parasitic fungus Fusarium oxysporum. Eur J Soil Biol 78:1–6

    Google Scholar 

  • Porcel R, Redondo-Gómez S, Mateos-Naranjo E, Aroca R, Garcia R, Ruiz-Lozano JM (2015) Arbuscular mycorrhizal symbiosis ameliorates the optimum quantum yield of photosystem II and reduces non-photochemical quenching in rice plants subjected to salt stress. J Plant Physiol 185:75–83

    CAS  PubMed  Google Scholar 

  • Ragab MM, Ashour AMA, Abdel-Kader MM, El-Mohamady R, Abdel-Aziz A (2012) In vitro evaluation of some fungicides alternatives against Fusarium oxysporum the causal of wilt disease of pepper (Capsicum annum L.). Inter J Agric For 2:70–77

    Google Scholar 

  • Ragab MM, Abada KA, Abd-El-Moneim ML, Abo-Shosha YZ (2015) Effect of different mixtures of some bioagents and rhizobium phaseoli on bean damping-off under field condition. Int J Sci Eng Res 6:1009–1106

    Google Scholar 

  • Rashid MI, Mujawar LH, Shahzad T, Almeelbi T, Ismail IM, Oves M (2016) Bacteria and fungi can contribute to nutrients bioavailability and aggregate formation in degraded soils. Microbiol Res 183:26–41

    CAS  PubMed  Google Scholar 

  • Ravindran B, Contreras-Ramos SM, Wong JWC, Selvam A, Sekaran G (2014) Nutrient and enzymatic changes of hydrolysed tannery solid waste treated with epigeic earthworm Eudrilus eugeniae and phytotoxicity assessment on selected commercial crops. Environ Sci Pollut Res 21:641–651

    CAS  Google Scholar 

  • Rousidou C, Papadopoulou ES, Kortsinidou M, Giannakou IO, Singh BK, Menkissoglu-Spiroudi U, Karpouzas DG (2013) Bio-pesticides: harmful or harmless to ammonia oxidizing microorganisms? The case of a Paecilomyces lilacinus-based nematicide. Soil Biol Biochem 67:98–105

    CAS  Google Scholar 

  • Schouteden N, De Waele D, Panis B, Vos CM (2015) Arbuscular mycorrhizal fungi for the biocontrol of plant-parasitic nematodes: a review of the mechanisms involved. Front Microbiol 6:1280

    PubMed  PubMed Central  Google Scholar 

  • Singh A, Singh JN (2009) Effect of biofertilizers and bioregulators on growth, yield and nutrient status of strawberry cv. Sweet Charlie. Indian J Hortic 66:220–224

    Google Scholar 

  • Singh VK, Khan AW, Saxena RK, Kumar V, Kale SM, Sinha P, ... Sameer Kumar CV (2016) Next‐generation sequencing for identification of candidate genes for Fusarium wilt and sterility mosaic disease in pigeonpea (Cajanus cajan). Plant Biotechnol J 14: 1183–1194

    PubMed  PubMed Central  Google Scholar 

  • Smith SE, Read DJ (2008) Mineral nutrition, toxic element accumulation and water relations of arbuscular mycorrhizal plants. In: Mycorrhizal symbiosis, 3rd edn. Academic Press, London, pp 145–187

    Google Scholar 

  • Stael S, Kmiecik P, Willems P, Van Der Kelen K, Coll NS, Teige M, Van Breusegem F (2015) Plant innate immunity–sunny side up? Trends Plant Sci 20:3–11

    CAS  PubMed  Google Scholar 

  • Stephens PM, Davoren CW (1997) Influence of the earthworms Aporrectodea trapezoides and A. rosea on the disease severity of Rhizoctonia solani on subterranean clover and ryegrass. Soil Biol Biochem 29:511–516

    CAS  Google Scholar 

  • Teng SK, Aziz NAA, Mustafa M, Aziz SA, Yan YW (2012) Evaluation on physical, chemical and biological properties of casts of geophagous earthworm, Metaphire tschiliensis tschiliensis. Sci Res Essays 7:1169–1174

    CAS  Google Scholar 

  • Torres LFC, Magallón RF, Gálvez GV (2014) Utilization of vermicompost in greenhouses to produce tomatoes and control for Fusarium oxysporum f. sp. lycopersici. e-CUCBA 1:27–35

    Google Scholar 

  • Uppal AK, El Hadrami A, Adam LR, Tenuta M, Daayf F (2008) Biological control of potato Verticillium wilt under controlled and field conditions using selected bacterial antagonists and plant extracts. Biol Control 44:90–100

    Google Scholar 

  • Veresoglou SD, Barto EK, Menexes G, Rillig MC (2013) Fertilization affects severity of disease caused by fungal plant pathogens. Plant Pathol 62:961–969

    Google Scholar 

  • Walkley A (1947) A critical examination of a rapid method for determining organic carbon in soils—effect of variations in digestion conditions and of inorganic soil constituents. Soil Sci 63:251–264

    CAS  Google Scholar 

  • Yuan S, Wang L, Wu K, Shi J, Wang M, Yang X, ... Shen B (2014) Evaluation of Bacillus–fortified organic fertilizer for controlling tobacco bacterial wilt in greenhouse and field experiments. Appl Soil Ecol 75: 86–94

    Google Scholar 

  • Zhang YJ, Fan PS, Zhang X, Chen CJ, Zhou MG (2009) Quantification of Fusarium graminearum in harvested grain by real-time polymerase chain reaction to assess efficacies of fungicides on Fusarium head blight, deoxynivalenol contamination, and yield of winter wheat. Phytopathology 99:95–100

    CAS  PubMed  Google Scholar 

  • Zhang W, Cao J, Zhang S, Wang C (2016a) Effect of earthworms and arbuscular mycorrhizal fungi on the microbial community and maize growth under salt stress. Appl Soil Ecol 107:214–223

    Google Scholar 

  • Zhang L, Xu M, Liu Y, Zhang F, Hodge A, Feng G (2016b) Carbon and phosphorus exchange may enable cooperation between an arbuscular mycorrhizal fungus and a phosphate-solubilizing bacterium. New Phytol 210:1022–1032

    CAS  PubMed  Google Scholar 

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Acknowledgements

This work was funded by the National Key R & D Program of China (2016YFE0101100)and the National Natural Science Foundation of China (Project 31570514).

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Correspondence to Chong Wang.

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Li, N., Wang, C., Li, X. et al. Effects of earthworms and arbuscular mycorrhizal fungi on preventing Fusarium oxysporum infection in the strawberry plant. Plant Soil 443, 139–153 (2019). https://doi.org/10.1007/s11104-019-04224-5

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