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Secreted metabolite-mediated interactions between rhizosphere bacteria and Trichoderma biocontrol agents


Autoři: Ningxiao Li aff001;  Md Tariqul Islam aff001;  Seogchan Kang aff001
Působiště autorů: Department of Plant Pathology and Environmental Microbiology, The Pennsylvania State University, University Park, Pennsylvania, United States of America aff001
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0227228

Souhrn

Trichoderma has been used as an alternative to synthetic pesticides to control a variety of phytopathogenic fungi, oomycetes, and nematodes. Although its mechanism of pathogen suppression has been extensively studied, how Trichoderma interacts with non-target microbes is not well understood. Here, we investigated how two Trichoderma biological control agents (BCAs) interact with rhizosphere bacteria isolated from a tomato plant via secreted proteins, metabolites, and volatile compounds (VCs). Culture filtrates (CFs) of T. virens and T. harzianum, containing secreted proteins and metabolites, strongly inhibited (>75% reduction in growth) 39 and 19, respectively, out of 47 bacterial strains tested. Their CFs inhibited the remaining strains at lower degrees. Both metabolites and proteins are involved in inhibiting bacteria, but they seem to antagonize each other in inhibiting some strains. Trichoderma and bacteria suppressed the growth of each other using VCs. The secretion of antibacterial and antifungal molecules by T. virens and T. harzianum was significantly affected by VCs from some bacteria, suggesting that both Trichoderma BCAs and rhizosphere bacteria use VCs to influence each other in multiple ways. In light of these results, we discuss how metabolite-mediated interactions can potentially affect the effectiveness of biocontrol.

Klíčová slova:

Actinobacteria – Antibacterials – Antifungals – Bacterial growth – Metabolites – Protein metabolism – Rhizosphere – Secretion


Zdroje

1. National Research Council. Toward Sustainable Agricultural Systems in the 21st Century. Washington, D.C.: National Academies Press; 2010 Jun. doi: 10.17226/12832

2. Reid A, Greene SE. How microbes can help feed the world. American Society for Micriobiology; 2012. doi: 10.1093/biosci/biu163

3. Velivelli SLS, De Vos P, Kromann P, Declerck S, Prestwich BD. Biological control agents: from field to market, problems, and challenges. Trends Biotechnol. 2014;32: 493–496. doi: 10.1016/j.tibtech.2014.07.002 25246168

4. Berg G. Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol. 2009;84: 11–8. doi: 10.1007/s00253-009-2092-7 19568745

5. Calistru C, McLean M, Berjak P. In vitro studies on the potential for biological control of Aspergillus flavus and Fusarium moniliforme by Trichoderma species. A study of the production of extracellular metabolites by Trichoderma species. Mycopathologia. 1997;137: 115–124. doi: 10.1023/A:1006802423729 16284721

6. Ejechi B. Biological control of wood decay in an open tropical environment with Penicillium sp. and Trichoderma viride. Int Biodeterior Biodegradation. 1997;39: 295–299. doi: 10.1016/S0964-8305(97)00023-1

7. Yedidia I, Benhamou N, Chet I. Induction of defense responses in cucumber plants (Cucumis sativus L.) by the biocontrol agent Trichoderma harzianum. Appl Environ Microbiol. 1999;65: 1061–1070. 10049864

8. Mukherjee PK, Horwitz BA, Herrera-Estrella A, Schmoll M, Kenerley CM. Trichoderma research in the genome era. Annu Rev Phytopathol. 2013;51: 105–29. doi: 10.1146/annurev-phyto-082712-102353 23915132

9. Singh A, Shukla N, Kabadwal BC, Tewari AK, Kumar J. Review on plant-Trichoderma-pathogen interaction. Int J Curr Microbiol Appl Sci. 2018;7: 2382–2397. doi: 10.20546/ijcmas.2018.702.291

10. Guzmán-Guzmán P, Porras-Troncoso MD, Olmedo-Monfil V, Herrera-Estrella A. Trichoderma species: versatile plant symbionts. Phytopathology. 2019;109: 6–16. doi: 10.1094/PHYTO-07-18-0218-RVW 30412012

11. Monte E. Understanding Trichoderma: between biotechnology and microbial ecology. Int Microbiol. 2001;4: 1–4. doi: 10.1007/s101230100001 11770814

12. Samuels GJ. Trichoderma: systematics, the sexual state, and ecology. Phytopathology. 2006;96: 195–206. doi: 10.1094/PHYTO-96-0195 18943925

13. Chaverri P, Samuels GJ. Evolution of habitat preference and nutrition mode in a cosmopolitan fungal genus with evidence of interkingdom host jumps and major shifts in ecology. Evolution. 2013;67: 2823–2837. doi: 10.1111/evo.12169 24094336

14. Adams PB. The potential of mycoparasites for biological control of plant diseases. Annu Rev Phytopathol. 1990;28: 59–72. doi: 10.1146/annurev.py.28.090190.000423 20540607

15. Ghisalberti EL, Sivasithamparam K. Antifungal antibiotics produced by Trichoderma spp. Soil Biol Biochem. 1991;23: 1011–1020.

16. Harman GE. Overview of mechanisms and uses of Trichoderma spp. Phytopathology. 2006;96: 190–194. doi: 10.1094/PHYTO-96-0190 18943924

17. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M. Trichoderma species—Opportunistic, avirulent plant symbionts. Nat Rev Microbiol. 2004;2: 43–56. doi: 10.1038/nrmicro797 15035008

18. Koike N, Hyakumachi M, Kageyama K, Tsuyumu S, Doke N. Induction of systemic resistance in cucumber against several diseases by plant growth-promoting fungi: lignification and superoxide generation. Eur J Plant Pathol. 2001;107: 523–533.

19. Yedidia I, Shoresh M, Kerem Z, Benhamou N, Kapulnik Y, Chet I. Concomitant induction of systemic resistance to Pseudomonas syringae pv. lachrymans in cucumber by Trichoderma asperellum (T-203) and accumulation of phytoalexins. Appl Environ Microbiol. 2003;69: 7343–7353. doi: 10.1128/AEM.69.12.7343-7353.2003 14660384

20. Seaman A. Efficacy of OMRI-Approved Products for Tomato Foliar Disease Control. New York State Integr Pest Manag Progr Publ. 2003.

21. Mazzola M, Freilich S. Prospects for biological soilborne disease control: application of indigenous versus synthetic microbiomes. Phytopathology. 2017;107: 256–263. doi: 10.1094/PHYTO-09-16-0330-RVW 27898265

22. Mendes R, Garbeva P, Raaijmakers JM. The rhizosphere microbiome: Significance of plant beneficial, plant pathogenic, and human pathogenic microorganisms. FEMS Microbiol Rev. 2013;37: 634–663. doi: 10.1111/1574-6976.12028 23790204

23. Raaijmakers JM, Paulitz TC, Steinberg C, Alabouvette C, Moënne-Loccoz Y. The rhizosphere: a playground and battlefield for soilborne pathogens and beneficial microorganisms. Plant Soil. 2009;321: 341–361. doi: 10.1007/s11104-008-9568-6

24. Saito M. Symbiotic exchange of nutrients in arbuscular mycorrhizas: transport and transfer of phosphorus. Arbuscular Mycorrhizas: Physiology and Function. Dordrecht: Springer Netherlands; 2000. pp. 85–106. doi: 10.1007/978-94-017-0776-3_5

25. Mendoza-Mendoza A, Zaid R, Lawry R, Hermosa R, Monte E, Horwitz BA, et al. Molecular dialogues between Trichoderma and roots: Role of the fungal secretome. Fungal Biol Rev. 2018;32: 62–85. doi: 10.1016/j.fbr.2017.12.001

26. Zeilinger S, Gruber S, Bansal R, Mukherjee PK. Secondary metabolism in Trichoderma–chemistry meets genomics. Fungal Biol Rev. 2016;30: 74–90. doi: 10.1016/j.fbr.2016.05.001

27. Li N, Alfiky A, Wang W, Islam M, Nourollahi K, Liu X, et al. Volatile compound-mediated recognition and inhibition between Trichoderma biocontrol agents and Fusarium oxysporum. Front Microbiol. 2018;9: 1–16. doi: 10.3389/fmicb.2018.00001

28. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, et al. Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol. 2006;2: 2006.0008. doi: 10.1038/msb4100050 16738554

29. Wilson K. Preparation of genomic DNA from bacteria. Curr Protoc Mol Biol. 2001;56: 2.4.1–2.4.5. doi: 10.1002/0471142727.mb0204s56 18265184

30. Huang XQ, Madan A. SymBioSys\rCAP3: A DNA sequence assembly program. Genome Res. 1999;9: 868–877. doi: 10.1101/gr.9.9.868 10508846

31. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2012;41: D590–D596. doi: 10.1093/nar/gks1219 23193283

32. Yilmaz P, Parfrey LW, Yarza P, Gerken J, Pruesse E, Quast C, et al. The SILVA and “All-species Living Tree Project (LTP)” taxonomic frameworks. Nucleic Acids Res. 2014;42: D643–D648. doi: 10.1093/nar/gkt1209 24293649

33. Kumar S, Stecher G, Tamura K. MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol. 2016;33: 1870–1874. doi: 10.1093/molbev/msw054 27004904

34. Etebarian HR, Scott ES, Wicks TJ. Trichoderma harzianum T39 and T. virens DAR 74290 as potential biological control agents for Phytophthora erythroseptica. Eur J Plant Pathol. 2000;106: 329–337. doi: 10.1023/A:1008736727259

35. Simon A, Sivasithamparam K. Interactions among Gaeumannomyces graminis var. tritici, Trichoderma koningii, and soil bacteria. Can J Microbiol. 1988;34: 871–876. doi: 10.1139/m88-150

36. Schirmbock M, Lorito M, Wang YL, Hayes CK, Arisan-Atac I, Scala F, et al. Parallel formation and synergism of hydrolytic enzymes and peptaibol antibiotics, molecular mechanisms involved in the antagonistic action of Trichoderma harzianum against phytopathogenic fungi. Appl Environ Microbiol. 1994;60: 4364–4370. 7811076

37. Bitas V, Kim H-S, Bennett JW, Kang S. Sniffing on microbes: diverse roles of microbial volatile organic compounds in plant health. Mol Plant Microbe Interact. 2013;26: 835–843. doi: 10.1094/MPMI-10-12-0249-CR 23581824

38. Li N, Alfiky A, Vaughan MM, Kang S. Stop and smell the fungi: fungal volatile metabolites are overlooked signals involved in fungal interaction with plants. Fungal Biol Rev. 2016;30: 134–144. doi: 10.1016/j.fbr.2016.06.004

39. Schmidt R, Cordovez V, de Boer W, Raaijmakers J, Garbeva P. Volatile affairs in microbial interactions. ISME J. 2015;9: 1–7. doi: 10.1038/ismej.2014.99

40. Lee S, Yap M, Behringer G, Hung R, Bennett JW. Volatile organic compounds emitted by Trichoderma species mediate plant growth. Fungal Biol Biotechnol. 2016;3: 7. doi: 10.1186/s40694-016-0025-7 28955466

41. Martínez-Medina A, Van Wees SCM, Pieterse CMJ. Airborne signals from Trichoderma fungi stimulate iron uptake responses in roots resulting in priming of jasmonic acid-dependent defences in shoots of Arabidopsis thaliana and Solanum lycopersicum. Plant Cell Environ. 2017;40: 2691–2705. doi: 10.1111/pce.13016 28667819

42. Wheatley R, Hackett C, Bruce A, Kundzewicz A. Effect of substrate composition on production of volatile organic compounds from Trichoderma spp. inhibitory to wood decay fungi. Int Biodeterior Biodegrad. 1997;39: 199–205. doi: 10.1016/S0964-8305(97)00015-2

43. Meena M, Swapnil P, Zehra A, Dubey MK, Upadhyay RS. Antagonistic assessment of Trichoderma spp. by producing volatile and non-volatile compounds against different fungal pathogens. Arch Phytopathol Plant Prot. 2017;50: 629–648. doi: 10.1080/03235408.2017.1357360

44. Weiwei L, Wie M, Bingyu Z, Feng Liu. Antifungal activities and components of VOCs produced by Bacillus subtilis G8. Curr Res Bacteriol. 2008;1: 28–34.

45. Zou C-S, Mo M-H, Gu Y-Q, Zhou J-P, Zhang K-Q. Possible contributions of volatile-producing bacteria to soil fungistasis. Soil Biol Biochem. 2007;39: 2371–2379. doi: 10.1016/j.soilbio.2007.04.009

46. Kai M, Effmert U, Berg G, Piechulla B. Volatiles of bacterial antagonists inhibit mycelial growth of the plant pathogen Rhizoctonia solani. Arch Microbiol. 2007;187: 351–360. doi: 10.1007/s00203-006-0199-0 17180381

47. Beneduzi A, Ambrosini A, Passaglia LMP. Plant growth-promoting rhizobacteria (PGPR): Their potential as antagonists and biocontrol agents. Genet Mol Biol. 2012;35: 1044–1051. doi: 10.1590/s1415-47572012000600020 23411488

48. Audrain B, Farag M a., Ryu C-M, Ghigo J-M. Role of bacterial volatile compounds in bacterial biology. FEMS Microbiol Rev. 2015;39: 222–233. doi: 10.1093/femsre/fuu013 25725014

49. Piechulla B, Lemfack MC, Kai M. Effects of discrete bioactive microbial volatiles on plants and fungi. Plant Cell Environ. 2017;40: 2042–2067. doi: 10.1111/pce.13011 28643880

50. Yuan J, Zhao M, Li R, Huang Q, Raza W, Rensing C, et al. Microbial volatile compounds alter the soil microbial community. Environ Sci Pollut Res. 2017;24: 22485–22493. doi: 10.1007/s11356-017-9839-y 28803260

51. Reino JL, Guerrero RF, Hernández-Galán R, Collado IG. Secondary metabolites from species of the biocontrol agent Trichoderma. Phytochem Rev. 2007;7: 89–123. doi: 10.1007/s11101-006-9032-2

52. Liu SY, Lo CT, Shibu MA, Leu YL, Jen BY, Peng KC. Study on the anthraquinones separated from the cultivation of Trichoderma harzianum strain Th-R16 and their biological activity. J Agric Food Chem. 2009;57: 7288–7292. doi: 10.1021/jf901405c 19650641

53. Rybakova D, Rack-Wetzlinger U, Cernava T, Schaefer A, Schmuck M, Berg G. Aerial warfare: a volatile dialogue between the plant pathogen Verticillium longisporum and its antagonist Paenibacillus polymyxa. Front Plant Sci. 2017;8: 1294. doi: 10.3389/fpls.2017.01294 28798756

54. Spraker JE, Wiemann P, Baccile JA, Venkatesh N, Schumacher J, Schroeder FC, et al. Conserved responses in a war of small molecules between a plant-pathogenic bacterium and fungi. Casadevall A, editor. MBio. 2018;9: 1–14. doi: 10.1128/mBio.00820-18 29789359

55. Spraker JE, Jewell K, Roze L V., Scherf J, Ndagano D, Beaudry R, et al. A volatile relationship: profiling an inter-kingdom dialogue between two plant pathogens, Ralstonia solanacearum and Aspergillus flavus. J Chem Ecol. 2014;40: 502–513. doi: 10.1007/s10886-014-0432-2 24801606


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