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Plant and Soil

, Volume 443, Issue 1–2, pp 139–153 | Cite as

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

  • Nan Li
  • Chong WangEmail author
  • Xiaolin Li
  • Mengli Liu
Regular Article
  • 191 Downloads

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.

Keywords

Fusarium oxysporum Disease index of Fusarium wilt Nutrient uptake Quantitative real-time polymerase chain reaction (qPCR) Actinomyces Structural equation model 

Notes

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).

References

  1. 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 263–292CrossRefGoogle Scholar
  2. Arbuckle JL (2006) Amos (version 7.0) [computer program]. SPSS, ChicagoGoogle Scholar
  3. Arroyo FT, Llergo Y, Aguado A, Romero F (2009) First report of Fusarium wilt caused by Fusarium oxysporum on strawberry in Spain. Plant Dis 93:323–323CrossRefPubMedGoogle Scholar
  4. 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 117:63–69CrossRefGoogle Scholar
  5. Azcón-Aguilar C, Barea JM (1997) Arbuscular mycorrhizas and biological control of soil-borne plant pathogens–an overview of the mechanisms involved. Mycorrhiza 6:457–464CrossRefGoogle Scholar
  6. Aznar A, Chen NW, Thomine S, Dellagi A (2015) Immunity to plant pathogens and iron homeostasis. Plant Sci 240:90–97CrossRefPubMedGoogle Scholar
  7. Berrocal-Lobo M, Molina A (2008) Arabidopsis defense response against Fusarium oxysporum. Trends Plant Sci 13:145–150CrossRefPubMedGoogle Scholar
  8. 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 96:33–41CrossRefGoogle Scholar
  9. 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 72:586–607CrossRefGoogle Scholar
  10. 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 64:161–182CrossRefGoogle Scholar
  11. 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 148:1–6CrossRefGoogle Scholar
  12. Cameron DD, Neal AL, van Wees SC, Ton J (2013) Mycorrhiza-induced resistance: more than the sum of its parts? Trends Plant Sci 18:539–545CrossRefPubMedPubMedCentralGoogle Scholar
  13. Cao J, Ji D, Wang C (2015a) Interaction between earthworms and arbuscular mycorrhizal fungi on the degradation of oxytetracycline in soils. Soil Biol Biochem 90:283–292CrossRefGoogle Scholar
  14. 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 396:45–57CrossRefGoogle Scholar
  15. 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 98:138–147CrossRefGoogle Scholar
  16. 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 10:119–129CrossRefPubMedGoogle Scholar
  17. 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 237:128–134CrossRefGoogle Scholar
  18. 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 65:114–123CrossRefGoogle Scholar
  19. 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 11:10CrossRefGoogle Scholar
  20. Du H, Lu H, Xu Y, Du X (2013) Community of environmental Streptomyces related to geosmin development in Chinese liquors. J Agric Food Chem 61:1343–1348CrossRefPubMedGoogle Scholar
  21. Eisenhauer N, Bowker MA, Grace JB, Powell JR (2015) From patterns to causal understanding: structural equation modeling (SEM) in soil ecology. Pedobiologia 58:65–72CrossRefGoogle Scholar
  22. Elmer WH (2009) Influence of earthworm activity on soil microbes and soilborne diseases of vegetables. Plant Dis 93:175–179CrossRefPubMedGoogle Scholar
  23. Elmer WH, Ferrandino FJ (2009) Suppression of Verticillium wilt of eggplant by earthworms. Plant Dis 93:485–489CrossRefPubMedGoogle Scholar
  24. 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: 42–51Google Scholar
  25. 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 131:39–48CrossRefGoogle Scholar
  26. 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 358:75–89CrossRefGoogle Scholar
  27. Garg N, Chandel S (2010) Arbuscular mycorrhizal networks: process and functions. A review. Agron Sustain Dev 30:581–599CrossRefGoogle Scholar
  28. Gordon TR (2017) Fusarium oxysporum and the Fusarium wilt syndrome. Annu Rev Phytopathol 55:23–39CrossRefPubMedGoogle Scholar
  29. 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 169:59–65CrossRefPubMedGoogle Scholar
  30. 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 101:550–556CrossRefPubMedGoogle Scholar
  31. Hodge A, Campbell CD, Fitter AH (2001) An arbuscular mycorrhizal fungus accelerates decomposition and acquires nitrogen directly from organic material. Nature 413: 297–299Google Scholar
  32. Huber DM, Jones JB (2013) The role of magnesium in plant disease. Plant Soil 368:73–85CrossRefGoogle Scholar
  33. 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 283–298CrossRefGoogle Scholar
  34. 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 90:18–25CrossRefGoogle Scholar
  35. 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 13:1164–1176CrossRefGoogle Scholar
  36. Johansson JF, Paul LR, Finlay RD (2004) Microbial interactions in the mycorrhizosphere and their significance for sustainable agriculture. FEMS Microbiol Ecol 48:1–13CrossRefPubMedGoogle Scholar
  37. 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 2:419–427Google Scholar
  38. 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 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Koike ST, Gordon TR (2015) Management of Fusarium wilt of strawberry. Crop Prot 73:67–72CrossRefGoogle Scholar
  40. 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 48:191–203CrossRefGoogle Scholar
  41. 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 145:421–431CrossRefGoogle Scholar
  42. 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 33:97–111CrossRefGoogle Scholar
  43. 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 95:1270–1278CrossRefPubMedGoogle Scholar
  44. 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 70:1669–1675CrossRefPubMedGoogle Scholar
  45. 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 171:155–165CrossRefGoogle Scholar
  46. Martin FN, Bull CT (2002) Biological approaches for control of root pathogens of strawberry. Phytopathology 92:1356–1362CrossRefPubMedGoogle Scholar
  47. McInnes TB, Black LL, Gatti JM Jr (1992) Disease-free plants for management of strawberry anthracnose crown rot. Plant Dis 76:260–264CrossRefGoogle Scholar
  48. 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 96:1712–1728CrossRefPubMedGoogle Scholar
  49. 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 33:237–244CrossRefPubMedGoogle Scholar
  50. 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 316:1–12CrossRefGoogle Scholar
  51. 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 11:35–38CrossRefGoogle Scholar
  52. Niu L, Liao W (2016) Hydrogen peroxide signaling in plant development and abiotic responses: crosstalk with nitric oxide and calcium. Front Plant Sci 7:230PubMedPubMedCentralGoogle Scholar
  53. 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 88:128–136CrossRefGoogle Scholar
  54. Palaniyandi SA, Yang SH, Zhang L, Suh JW (2013) Effects of actinobacteria on plant disease suppression and growth promotion. Appl Microbiol Biotechnol 97:9621–9636CrossRefPubMedGoogle Scholar
  55. 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 97:605–614CrossRefPubMedGoogle Scholar
  56. 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 139:178–184CrossRefGoogle Scholar
  57. 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 10:502–512CrossRefGoogle Scholar
  58. 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 8:1817–1828CrossRefGoogle Scholar
  59. 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 78:1–6CrossRefGoogle Scholar
  60. 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 185:75–83CrossRefPubMedGoogle Scholar
  61. 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 2:70–77Google Scholar
  62. 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 6:1009–1106Google Scholar
  63. 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 183:26–41CrossRefPubMedGoogle Scholar
  64. 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 21:641–651CrossRefGoogle Scholar
  65. 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 67:98–105CrossRefGoogle Scholar
  66. 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 6:1280CrossRefPubMedPubMedCentralGoogle Scholar
  67. Singh A, Singh JN (2009) Effect of biofertilizers and bioregulators on growth, yield and nutrient status of strawberry cv. Sweet Charlie. Indian J Hortic 66:220–224Google Scholar
  68. 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: 1183–1194Google Scholar
  69. 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 145–187CrossRefGoogle Scholar
  70. 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 20:3–11CrossRefPubMedGoogle Scholar
  71. 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 29:511–516CrossRefGoogle Scholar
  72. 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 7:1169–1174Google Scholar
  73. 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 1:27–35Google Scholar
  74. 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 44:90–100CrossRefGoogle Scholar
  75. Veresoglou SD, Barto EK, Menexes G, Rillig MC (2013) Fertilization affects severity of disease caused by fungal plant pathogens. Plant Pathol 62:961–969CrossRefGoogle Scholar
  76. 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 63:251–264CrossRefGoogle Scholar
  77. 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: 86–94Google Scholar
  78. 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 99:95–100CrossRefPubMedGoogle Scholar
  79. 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 107:214–223CrossRefGoogle Scholar
  80. 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 210:1022–1032CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.College of Resources and Environmental SciencesChina Agricultural UniversityBeijingPeople’s Republic of China
  2. 2.Beijing Key Laboratory of Biodiversity and Organic FarmingBeijingChina
  3. 3.Key Laboratory of Plant-Soil InteractionsMinistry of EducationBeijingChina

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