Advertisement

Biocontrol of Root Diseases and Growth Promotion of the Tuberous Plant Aconitum carmichaelii Induced by Actinomycetes Are Related to Shifts in the Rhizosphere Microbiota

Abstract

Soil Actinomycetes have been used as biocontrol agents against soil-borne plant diseases, yet little is known about their effects on the structure of the rhizosphere microbiota and the long-term effects on crop yield and disease intensity after the application of Actinomycetes is stopped. Here, we conducted 3-year plot experiments to investigate the roles of two Actinomycetes strains (Streptomyces pactum Act12 and Streptomyces rochei D74) in the biocontrol of soil-borne root diseases and growth promotion of monkhood (Aconitum carmichaelii). We also examined their long-term effects after soil application of a mixed Actinomycetes preparation (spore powder) was completed. High-throughput sequencing was used to analyze shifts in the rhizosphere microbiota. The antifungal activity and root colonization ability of the two Actinomycetes were also tested. Disease severity of southern blight and root rot decreased following application of the Actinomycetes preparation, whereas biomass yield of tubers increased compared with the control group. Significant effects of disease control and plant growth promotion were also observed after application was stopped. The Actinomycetes preparation induced marked increases in the abundance of beneficial microbes and decreases in the abundance of harmful microbes in rhizosphere soil. Adding cell-free culture filtrates of both strains Act12 and D74 inhibited the growth of fungal pathogens capable of causing southern blight (Sclerotium rolfsii) and root rot (Fusarium oxysporum) in A. carmichaelii. A GFP-labeled strain was used to show that D74 can colonize roots of A. carmichaelii. In conclusion, a preparation of two Actinomycetes plays a role in the biocontrol of root diseases and growth promotion of A. carmichaelii by inhibiting pathogen growth and shaping the rhizosphere microbiota.

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

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 199

This is the net price. Taxes to be calculated in checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

References

  1. 1.

    Lewis JA, Papavizas GC (1991) Biocontrol of cotton damping-off caused by Rhizoctonia solani in the field with formulations of Trichoderma spp. and Gliocladium virens. Crop Protect 10:396–402

  2. 2.

    Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moenne-Loccoz Y (2009) The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil 321:341–361

  3. 3.

    Bruehl GW (1987) Soilborne plant pathogens. Macmillan, NY

  4. 4.

    Parra G, Ristaino JB (2001) Resistance to mefenoxam and metalaxyl among field isolates of Phytophthora capsici causing phytophthora blight of bell pepper. Plant Dis. 85:1069–1075

  5. 5.

    Cohen Y, Coffey MD (1986) Systemic fungicides and the control of oomycetes. Annu. Rev. Phytopathol. 24:311–338

  6. 6.

    Fu L, Penton CR, Ruan Y, Shen Z, Xue C, Li R, Shen Q (2017) Inducing the rhizosphere microbiome by biofertilizer application to suppress banana Fusarium wilt disease. Soil Biol. Biochem. 104:39–48

  7. 7.

    Subramanian P, Mageswari A, Kim K, Lee Y, Sa T (2015) Psychrotolerant endophytic Pseudomonas spp. OB155 and OS261 induced chilling resistance in tomato plants (Solanum lycopersicum Mill.) by activation of their antioxidant capacity. Mol Plant-Microbe In 28:1073–1081

  8. 8.

    Li S, Zhang N, Zhang Z, Luo J, Shen B, Zhang R, Shen Q (2013) Antagonist Bacillus subtilis HJ5 controls Verticillium wilt of cotton by root colonization and biofilm formation. Biol Fert Soils 49:295–303

  9. 9.

    Harman GE, Howell CR, Viterbo A, Chel I, Lorito M (2004) Trichoderma species—opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56

  10. 10.

    Viaene T, Langendries S, Beirinckx S, Maes M, Goormachtig S (2016) Streptomyces as a plant's best friend? FEMS Microbiol. Ecol. 92:fw119

  11. 11.

    Duan JL, Xue QH, Shu ZM, Wang DS, He F (2015) Effects of combined application of actinomycetes Act12 bio-control agents and potassium humate on growth and microbial flora in rooting zone of Salvia miltiorrhiza Bge. Acta Ecol. Sin. 35:1807–1819

  12. 12.

    Zhang HY, Xue QH, Shen GH, Wang DS (2013) Effects of actinomycetes agent on ginseng growth and rhizosphere soil microflora. Chin. J. Appl. Ecol. 8:2287–2293

  13. 13.

    Li JG, Ren GD, Jia ZJ, Dong YH (2014) Composition and activity of rhizosphere microbial communities associated with healthy and diseased greenhouse tomatoes. Plant Soil 380:337–347

  14. 14.

    Zhou G, Tang L, Zhou X, Wang T, Kou Z, Wang Z (2015) A review on phytochemistry and pharmacological activities of the processed lateral root of Aconitum carmichaelii Debeaux. J. Ethnopharmacol. 160:173–193

  15. 15.

    Tang L, Liang LJ, Hua-Zhi YE, Zeng YJ (2004) Study on pests plaguing Aconitum carmichaelii Debx. Res Practice Chin Med 18:29–32

  16. 16.

    Tang B, Zhao Y, Shi X, Xu H, Zhao Y, Dai C, Liu F (2018) Enhanced heat stable antifungal factor production by Lysobacter enzymogenes OH11 with cheap feedstocks: medium optimization and quantitative determination. Lett. Appl. Microbiol. 66:439–446

  17. 17.

    Li DY, Sun Y (1981) Studies on Sclerotium rolfsii Sacc of Chinese aconite (Aconitum carmichaelii Derx). J Plant Prot 8:259–264

  18. 18.

    Duan X, Zhao F, Yan X, Xue Q, Li X, Wen B, Jia L, Yan H (2016) Construction of SPA7074-deficient mutant of biocontrol strain Streptomyces pactum Act12 and characterization of its secondary metabolites. Acta Microbiol Sin. 56:1833–1891

  19. 19.

    He F, Zhang ZL, Cui M, Xue QH, Wang DS (2015) Disease prevention and growth promotion effects of actinomycete strain D74 on Amorphophallus konjac. [J] Acta Horticulturae Sinica 42:367–376

  20. 20.

    Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu. Rev. Microbiol. 63:541–556

  21. 21.

    Lagopodi AL, Ram AFJ, Lamers GEM, Punt PJ, Lugtenberg BJJ, Bloemberg GV (2002) Novel aspects of tomato root colonization and infection by Fusarium oxysporum f. sp. radicis-lycopersici revealed by confocal laser scanning microscopic analysis using the green fluorescent protein as a marker. Mol. Plant-Microbe Interact. 15:172–179a

  22. 22.

    Xiong W, Zhao Q, Xue C, Xun W, Zhao J, Wu H, Li R, Shen Q (2016) Comparison of fungal community in black pepper-vanilla and vanilla monoculture systems associated with Vanilla Fusarium wilt disease. Front in Microbiol 7:117

  23. 23.

    Fierer N, Jackson JA, Vilgalys R, Jackson RB (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl. Environ. Microbiol. 71:4117–4120

  24. 24.

    Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963

  25. 25.

    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena 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, Tumbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:335–336

  26. 26.

    Haas BJ, Gevers D, Earl AM, Feldgarden M, Ward DV, Giannoukos G, Ciulla D, Tabbaa D, Highlander SK, Sodergren E, Methe B, DeSantis TZ, Petrosino JF, Knight R, Birren BW, Human Microbiome C (2011) Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res. 21:494–504

  27. 27.

    Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10:996–998

  28. 28.

    Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 41:590–596

  29. 29.

    Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13:2498–2504

  30. 30.

    Haas D, Defago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Microbiol 3:307–319

  31. 31.

    Das K, Rajawat MVS, Saxena AK, Prasanna R (2017) Development of Mesorhizobium ciceri-based biofilms and analyses of their antifungal and plant growth promoting activity in chickpea challenged by Fusarium wilt. Indian J. Microbiol. 57:48–59

  32. 32.

    Yuen GY, Broderick KC, Jochum CC, Chen CJ, Caswell-Chen EP (2018) Control of cyst nematodes by Lysobacter enzymogenes strain C3 and the role of the antibiotic HSAF in the biological control activity. Biol. Control 117:158–163

  33. 33.

    Puopolo G, Tomada S, Pertot I (2018) The impact of the omics era on the knowledge and use of Lysobacter species to control phytopathogenic micro-organisms. J. Appl. Microbiol. 124:15–27

  34. 34.

    Han KS, Choi SK, Kim HH, Lee SC, Park JH, Cho MR, Park MJ (2014) First report of Myrothecium roridum causing leaf and stem rot disease on Peperomia quadrangularis in Korea. Mycobiology 42:203–205

  35. 35.

    Ye W, Liu T, Zhu M, Zhang W, Li H, Huang Z, Li S (2017) De novo transcriptome analysis of plant pathogenic fungus Myrothecium roridum and identification of genes associated with trichothecene mycotoxin biosynthesis. Int. J. Mol. Sci. 18:497

  36. 36.

    Cho H, Song ES, Lee YK, Lee S, Lee SW, Jo A, Lee BM, Kim JG, Hwang I (2018) Analysis of genetic and pathogenic diversity of Ralstonia solanacearum causing potato bacterial wilt in Korea. Plant Pathol. J. 34:23–34

  37. 37.

    Chen J, Guo TW, Tan XL, Zhu WB, Wei XL, Wang DS, Xue QH (2013) Comparison of microecological characterization in rhizosphere soil between healthy and diseased plants in continuous cropping potato fields. Acta Agron. Sin. 39:2055–2064

  38. 38.

    Thano P, Akarapisan A (2018) Phylotype and sequevar of Ralstonia solanacearum which causes bacterial wilt in Curcuma alismatifolia gagnep. Lett. Appl. Microbiol. 66:384–393. https://doi.org/10.1111/lam.12857

  39. 39.

    Degruyter J, Vankesteren HA, Noordeloos ME, Paternotte SJ, Veenbaasrijks JW (1992) The association of humicola-fuscoatra with corky root symptoms in wilted glasshouse tomatoes. Neth. J. Plant Pathol. 98:257–260

  40. 40.

    Menzies JG, Ehret DL, Koch C, Bogdanoff C (1998) Humicola fuscoatra infects tomato roots, but is not pathogenic. Eur. J. Plant Pathol. 104:769–775

  41. 41.

    Pak D, You MP, Lanoiselet V, Barbetti MJ (2017) Reservoir of cultivated rice pathogens in wild rice in Australia. Eur. J. Plant Pathol. 147:295–311

  42. 42.

    Boukaew S, Prasertsan P (2014) Suppression of rice sheath blight disease using a heat stable culture filtrate from Streptomyces philanthi RM-1-138. Crop Protect 61:1–10

  43. 43.

    Lehr NA, Schrey SD, Hampp R, Tarkka MT (2008) Root inoculation with a forest soil streptomycete leads to locally and systemically increased resistance against phytopathogens in Norway spruce. New Phytol. 177:965–976

  44. 44.

    Manhas RK, Kaur T (2016) Biocontrol potential of Streptomyces hydrogenans strain DH16 toward Alternaria brassicicola to control damping off and black leaf spot of Raphanus sativus. Front. Plant Sci. 7:1869

  45. 45.

    El-Tarabily KA, Sivasithamparam K (2006) Non-streptomycete actinomycetes as biocontrol agents of soil-borne fungal plant pathogens and as plant growth promoters. Soil Biol. Biochem. 38:1505–1520

  46. 46.

    Rey T, Dumas B (2017) Plenty is no plague: Streptomyces symbiosis with crops. Trends Plant Sci. 22:30–37

  47. 47.

    Sathya A, Vijayabharathi R, Gopalakrishnan S (2017) Plant growth-promoting actinobacteria: a new strategy for enhancing sustainable production and protection of grain legumes. 3 Biotech 7:102

  48. 48.

    Ma JN, Liu YT, Li YL, Sun YY, Yang BM, Lai HX, Xue QH (2017) Effects and mechanism of two Streptomyces strains on promoting plant growth and increasing grain yield of maize. Chin. J. Appl. Ecol. 28:315–326

  49. 49.

    Yu ZY, Yu MM, Luo JY, Su C, Xue QH, Huang SX, Sun Y, Ma YT (2015) Isolation, identification and antimicrobial activity of secondary metabolites from a soil-derived Streptomyces from arid habitats of Qinghai. Nat Prod Res Dev 27:1900–1904

  50. 50.

    Li YL, He F, Lai HX, Xue QH (2017) Mechanism of in vitro antagonism of phytopathogenic Sclerotium rolfsii by actinomycetes. Eur. J. Plant Pathol. 149:299–311

  51. 51.

    Xie J, Shu P, Strobel G, Chen J, Wei J, Xiang Z, Zhou Z (2017) Pantoea agglomerans SWg2 colonizes mulberry tissues, promotes disease protection and seedling growth. Biol. Control 113:9–17

  52. 52.

    Coombs JT, Franco CM (2003) Visualization of an endophytic Streptomyces species in wheat seed. Appl. Environ. Microbiol. 69:4260–4262

  53. 53.

    Timmusk S, Grantcharova N, Wagner EGH (2005) Paenibacillus polymyxa invades plant roots and forms biofilms. Appl. Environ. Microbiol. 71:7292–7300

  54. 54.

    Millet YA, Danna CH, Clay NK, Songnuan W, Simon MD, Werck-Reichhart D, Ausubel FM (2010) Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns. Plant Cell 22:973–990

Download references

Acknowledgments

This work was supported by the Youth Fund of the National Natural Science Foundation of China (31600407), the Fundamental Research Funds for the Central Universities of China (Z109021616), and the National Key Technology R&D Program of China (2012BAD14B11). We thank Dr. Chaofeng Lin (TEC, Qingdao, China) for improving the English.

Author information

Correspondence to Quanhong Xue or Hangxian Lai.

Electronic Supplementary Material

ESM 1

(DOCX 615 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Li, Y., Guo, Q., He, F. et al. Biocontrol of Root Diseases and Growth Promotion of the Tuberous Plant Aconitum carmichaelii Induced by Actinomycetes Are Related to Shifts in the Rhizosphere Microbiota. Microb Ecol 79, 134–147 (2020) doi:10.1007/s00248-019-01388-6

Download citation

Keywords

  • Aconitum carmichaelii
  • Actinomycetes biocontrol agent
  • Sclerotium rolfsii
  • Fusarium oxysporum
  • Green fluorescent protein
  • Rhizosphere microbiota