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Pseudomonas fluorescens HC1-07 transformed with phenazine-1-carboxylic acid biosynthesis genes has improved biocontrol activity against Rhizoctonia root rot and Fusarium crown rot of wheat

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Abstract

Wheat root diseases are typically caused by complex soilborne fungal pathogens. Biocontrol can be effective, but it can be difficult for a single biocontrol strain to achieve a good control effect. Previously, the gene for antibiotic phenazine-1-carboxylic acid (PCA) from Pseudomonas synxantha 2-79 was introduced into Pseudomonas fluorescens HC1-07, which produces cyclic lipopeptide (CLP) naturally. In the present study, recombinant strain HC1-07PHZ produced both PCA and CLP and maintained a similar population size as wild type strain HC1-07 in the wheat rhizosphere. Compared with that of HC1-07, the recombinant strain had a stronger inhibitory effect on pathogens of Rhizoctonia solani AG-8 C1, AG-2-1, Rhizoctonia cerealis R0301, and Fusarium graminearum Schwabe in vitro. When used as a seed-coating treatment, the recombinant strain inhibited  Rhizoctonia root rot of wheat, as did strain HC1-07. However, the dose of HC1-07PHZ was 1000-fold less. Liquid chromatography-tandem mass spectrometry (LC–MS/MS) revealed compounds such as pipecolic acid, arachidonic acid, and acetylcysteine in wheat root soil inoculated with three strains (2-79, HC1-07, and HC1-07PHZ) used as seed-coating agents, respectively. The composition of these molecules was very different for different bacteria. These metabolites may trigger plant defense responses, promote plant growth, or combat pathogenic fungi, but analysis of the enrichment pathway showed that these metabolites were mainly from signal pathways involved in plant detoxification and various biochemical processes. In summary, our study showed that recombinant strain HC1-07PHZ greatly improved the biocontrol effect against Rhizoctonia root rot and  Fusarium crown rot of wheat.

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Data availability

The datasets generated for this study are available on request to the corresponding author.

References

  • Alahmad S, Simpfendorfer S, Bentley AR, Hickey LT (2018) Crown rot of wheat in Australia: Fusarium pseudograminearum taxonomy, population biology and disease management. Australas Plant Pathol 47:285–299

    Article  Google Scholar 

  • Brooker NL, Kuzimichev Y, Laas J, Pavlis R (2007) Evaluation of coumarin derivatives as anti-fungal agents against soil-borne fungal pathogens. Commun Agric Appl Biol Sci 72:785–793

    PubMed  CAS  Google Scholar 

  • Cai J, Jozwiak A, Holoidovsky L, Meijler MM, Meir S, Rogachev I, Aharoni A (2021) Glycosylation of N-hydroxy-pipecolic acid equilibrates between systemic acquired resistance response and plant growth. Mol Plant 14:440–455

    Article  PubMed  CAS  Google Scholar 

  • Carlucci A, Raimondo ML, Colucci D, Lops F (2022) Streptomyces albidoflavus strain CARA17 as a biocontrol agent against fungal soil-borne pathogens of fennel plants. Plants 11:1420

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chen C, Li S, McKeever DR, Beattie GA (2013) The widespread plant-colonizing bacterial species Pseudomonas syringae detects and exploits an extracellular pool of choline in hosts. Plant J 75:891–902

    Article  PubMed  CAS  Google Scholar 

  • Chen YC, Holmes EC, Rajniak J, Kim JG, Tang S, Fischer CR, Mudgett MB, Sattely ES (2018) N-hydroxy-pipecolic acid is a mobile metabolite that induces systemic disease resistance in Arabidopsis. Proc Natl Acad Sci USA 115:4920–4929

  • D’aes J, Hoang Hua GK, De Maeyer K, Pannecoucque J, Forrez I, Ongena M, Dietrich LEP, Thomashow LS, Mavrodi DV, Höfte M (2011) Biological control of Rhizoctonia root rot on bean by phenazine and cyclic lipopeptide-producing Pseudomonas CMR12a. Phytopathology 101:996–1004

    Article  PubMed  Google Scholar 

  • Dahuja A, Kumar RR, Sakhare A, Watts A, Singh B, Goswami S, Sachdev A, Praveen S (2021) Role of ATP-binding cassette transporters in maintaining plant homeostasis under abiotic and biotic stresses. Physiol Plant 171:785–801

    Article  PubMed  CAS  Google Scholar 

  • del Río LE, Bradley CA, Henson RA, Endres GJ, Hanson BK, McKay K, Halvorson M, Porter PM, Le Gare DG, Lamey HA (2007) Impact of Sclerotinia stem rot on yield of canola. Plant Dis 91:191–194

    Article  PubMed  Google Scholar 

  • Eccleston L, Brambilla A, Vlot AC (2022) New molecules in plant defence against pathogens. Essays Biochem 66:683–693

    Article  PubMed  CAS  Google Scholar 

  • Ginn AN, Evans T, Ernest E, Koehler AM (2022) First report of Rhizoctonia solani AG 4 causing brown bean of lima bean in Delaware. Plant Dis 107:214

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • He W, Zhong Q, He B, Wu B, Din MU, A, Han J, Ding Y, Liu Z, Li W, Jiang Y, Li G, (2022) N-acetylcysteine priming alleviates the transplanting injury of machine-transplanted rice by comprehensively promoting antioxidant and photosynthetic systems. Plants 11:1311

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Huang Z, Bonsall RF, Mavrodi DV, Weller DM, Thomashow LS (2004) Transformation of Pseudomonas fluorescens with genes for biosynthesis of phenazine-1-carboxylic acid improves biocontrol of rhizoctonia root rot and in situ antibiotic production. FEMS Microbiol Ecol 49:243–251

    Article  PubMed  CAS  Google Scholar 

  • Jaaffar AKM, Parejko J, Paulitz TC, Weller DM, Thomashow, (2017) Sensitivity of Rhizoctonia isolates to phenazine-1-carboxylic acid and biological control by phenazine-producing Pseudomonas spp. Phytopathology 107:692–703

    Article  PubMed  CAS  Google Scholar 

  • Khedr MA, Massarotti A, Mohamed ME (2018) Rational discovery of (+) (S) abscisic acid as a potential antifungal agent: a repurposing approach. Sci Rep 8:8565

    Article  PubMed  PubMed Central  Google Scholar 

  • King EO, Ward MK, Raney DE (1954) Two simple media for the demonstration of pyocyanin and fluorescein. J Lab Clin Med 44:301–307

    PubMed  CAS  Google Scholar 

  • Kretzschmar T, Burla B, Lee Y, Martinoia E, Nagy R (2011) Functions of ABC transporters in plants. Essays Biochem 50:145–160

    Article  PubMed  CAS  Google Scholar 

  • Le CN, Kruijt M, Raaijmakers JM (2012) Involvement of phenazines and lipopeptides in interactions between Pseudomonas species and Sclerotium rolfsii, causal agent of stem rot disease on groundnut. J Appl Microbiol 112:390–403

    Article  PubMed  CAS  Google Scholar 

  • LeTourneau MK, Marshall MJ, Grant M, Freeze PM, Strawn DG, Lai B, Dohnalkova AC, Harsh JB, Weller DM, Thomashow LS (2019) Phenazine-1-carboxylic acid-producing bacteria enhance the reactivity of iron minerals in dryland and irrigated wheat rhizospheres. Environ Sci Technol 53:14273–14284

    Article  PubMed  CAS  Google Scholar 

  • Li X, Gruber MY, Hegedus DD, Lydiate DJ, Gao MJ (2011) Effects of a coumarin derivative, 4-methylumbelliferone, on seed germination and seedling establishment in Arabidopsis. J Chem Ecol 37:880–890

    Article  PubMed  CAS  Google Scholar 

  • Li ZY, Dong ZP, Wang N, Dong L, Bai H, Quan JZ, Liu L (2014) First report of foxtail millet seedling damping-off caused by binucleate Rhizoctonia AG-A in China. Plant Dis 98:1587

    Article  PubMed  CAS  Google Scholar 

  • Lim GH, Singhal R, Kachroo A, Kachroo P (2017) Fatty acid- and lipid-mediated signaling in plant defense. Annu Rev Phytopathol 55:505–536

    Article  PubMed  CAS  Google Scholar 

  • MacNish GC, Neate SM (1996) Rhizoctonia bare patch of cereals: An Australian perspective. Plant Dis 80:965–971

    Article  Google Scholar 

  • Marian M, Shimizu M (2019) Improving performance of microbial biocontrol agents against plant diseases. J Gen Plant Pathol 85:329–336

    Article  Google Scholar 

  • Mavrodi OV, Mavrodi DV, Park AA, Weller DM, Thomashow LS (2006) The role of dsbA in colonization of the wheat rhizosphere by Pseudomonas fluorescens Q8r1-96. Microbiology 152:863–872

    Article  PubMed  CAS  Google Scholar 

  • Muranaka LS, Giorgiano TE, Takita MA, Forim MR, Silva LF, Coletta-Filho HD, Machado MA, de Souza AA (2013) N-acetylcysteine in agriculture, a novel use for an old molecule: focus on controlling the plant-pathogen Xylella fastidiosa. PLoS ONE 8(8):e72937

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nesemann K, Braus-Stromeyer SA, Harting R, Höfer A, Kusch H, Ambrosio AB, Timpner C, Braus GH (2018) Fluorescent pseudomonads pursue media-dependent strategies to inhibit growth of pathogenic Verticillium fungi. Appl Microbiol Biotechnol 102:817–831

    Article  PubMed  CAS  Google Scholar 

  • Okubara PA, Schroeder KL, Abatzoglou JT, Paulitz TC (2014) Agroecological factors correlated to soil DNA concentrations of Rhizoctonia in dryland wheat production zones of Washington State, USA. Phytopathology 104:683–691

    Article  PubMed  Google Scholar 

  • Olorunleke FE, Hua GKH, Kieu NP, Ma Z, Höfte M (2015) Interplay between orfamides, sessilins and phenazinesin the control of Rhizoctonia diseases by Pseudomonas sp. CMR12a. Environ Microbiol Rep 7:774–781

    Article  PubMed  CAS  Google Scholar 

  • Ownley BH, Weller DM, Thomashow LS (1992) Influence of in situ and in vitro pH on suppression of Gaeumannomyces graminis var. tritici by Pseudomonas fluorescens 2-79. Phytopathology 82:178–184

    Article  CAS  Google Scholar 

  • Pazarlar S, Sanver U, Cetinkaya N (2021) Exogenous pipecolic acid modulates plant defence responses against Podosphaera xanthii and Pseudomonas syringae pv. lachrymans in cucumber (Cucumis sativus L.). Plant Biol 23:473–484

    Article  PubMed  CAS  Google Scholar 

  • Pierson EA, Weller DM (1994) Use of mixtures of fluorescent pseudomonads to suppress take-all and improve the growth of wheat. Phytopathology 84:940–947

    Article  Google Scholar 

  • Qiao K, Liu Q, Xia Y, Zhang S (2021) Evaluation of a small-molecule compound, N-acetylcysteine, for the management of bacterial spot of tomato caused by copper-resistant Xanthomonas perforans. Plant Dis 105:108–113

    Article  PubMed  CAS  Google Scholar 

  • Schillinger WF, Paulitz TC (2006) Reduction of Rhizoctonia bare patch in wheat with barley rotations. Plant Dis 90:302–306

    Article  PubMed  CAS  Google Scholar 

  • Shuang M, Wang Y, Teng W, Jin G (2022) Isolation and identification of an endophytic bacteria Bacillus sp. K-9 exhibiting biocontrol activity against potato common scab. Arch Microbiol 204:483

    Article  PubMed  CAS  Google Scholar 

  • Smith CA, Want EJ, O’Maille G, Abagyan R, Siuzdak G (2006) XCMS: processing mass spectrometry data for metabolite profiling using nonlinear peak alignment, matching, and identification. Anal Chem 78:779–787

    Article  PubMed  CAS  Google Scholar 

  • Stringlis IA, de Jonge R, Pieterse C (2019) The age of coumarins in plant-microbe interactions. Plant Cell Physiol 60:1405–1419

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Su J, Zhao J, Zhao S, Li M, Pang S, Kang Z, Zhen W, Chen S, Chen F, Wang X (2021) Genetics of resistance to common root rot (spot blotch), Fusarium crown rot, and sharp eyespot in wheat. Front Genet 12:699342

    Article  PubMed  PubMed Central  Google Scholar 

  • Thomashow LS, Weller DM (1988) Role of a phenazine antibiotic from Pseudomonas fluorescens in biological control of Gaeumannomyces graminis var. tritici. J Bacteriol 170:3499–3508

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vasilev N, Boccard J, Lang G, Grömping U, Fischer R, Goepfert S, Rudaz S, Schillberg S (2016) Structured plant metabolomics for the simultaneous exploration of multiple factors. Sci Rep 6:37390

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang C, Yang Q, Wang W, Li Y, Guo Y, Zhang D, Ma X, Song W, Zhao J, Xu M (2017) A transposon-directed epigenetic change in ZmCCT underlies quantitative resistance to Gibberella stalk rot in maize. New Phytol 215:1503–1515

    Article  PubMed  CAS  Google Scholar 

  • Wang C, Liu R, Lim GH, de Lorenzo L, Yu K, Zhang K, Hunt AG, Kachroo A, Kachroo P (2018) Pipecolic acid confers systemic immunity by regulating free radicals. Sci Adv. https://doi.org/10.1126/sciadv.aar4509

    Article  PubMed  PubMed Central  Google Scholar 

  • Want EJ, Masson P, Michopoulos F, Wilson ID, Theodoridis G, Plumb RS, Shockcor J, Loftus N, Holmes E, Nicholson JK (2013) Global metabolic profiling of animal and human tissues via UPLC-MS. Nat Protoc 8:17–32

    Article  PubMed  CAS  Google Scholar 

  • Weller DM (2007) Pseudomonas biocontrol agents of soilborne pathogens: looking back over 30 years. Phytopathology 97:250–256

    Article  PubMed  Google Scholar 

  • Weller DM, Thomashow LS (2015) Phytosanitation and the development of transgenic biocontrol agents. In: OECD (ed) Biosafety and the environmental uses of micro-organisms: conference proceedings, OECD, Paris, pp 35–45

  • Wu X, Cheng K, Zhao R, Zang S, Bie T, Jiang Z, Wu R, Gao D, Zhang B (2017) Quantitative trait loci responsible for sharp eyespot resistance in common wheat CI12633. Sci Rep 7:11799

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu F, Yang G, Wang J, Song Y, Liu L, Zhao K, Li Y, Han Z (2018) Spatial distribution of root and crown rot fungi associated with winter wheat in the North China Plain and its relationship with climate variables. Front Microbiol 9:1054

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang MM, Mavrodi DV, Mavrodi OV, Bonsall RF, Parejko JA, Paulitz TC, Thomashow LS, Yang HT, Weller DM, Guo JH (2011) Biological control of take-all by fluorescent Pseudomonas spp. from Chinese wheat fields. Phytopathology 101:1481–1491

    Article  PubMed  Google Scholar 

  • Yang MM, Wen SS, Mavrodi DV, Mavrodi OV, Thomashow LS, Guo JH, Weller DV (2014) Biological control of wheat root diseases by the CLP-producing strain Pseudomonas fluorescens HC1-07. Phytopathology 104:248–256

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang MM, Mavrodi DV, Mavrodi OV, Thomashow LS, Weller DM (2017) Construction of a recombinant strain of Pseudomonas fluorescens producing both phenazine-1-carboxylic acid and cyclic lipopeptide for the biocontrol of take-all disease of wheat. Eur J Plant Pathol 149:683–694

    Article  CAS  Google Scholar 

  • Zelena E, Dunn WB, Broadhurst D, Francis-McIntyre S, Carroll KM, Begley P, O’Hagan S, Knowles JD, Halsall A, HUSERMET Consortium, Wilson ID, Kell DB (2009) Development of a robust and repeatable UPLC-MS method for the long-term metabolomic study of human serum. Anal Chem 81:1357–1364

    Article  PubMed  Google Scholar 

  • Zhang JB, Dmitri MV, Yang MM, Thomashow LS, Mavrodi OV, Jason K, Weller DM (2020) Pseudomonas synxantha 2-79 transformed with pyrrolnitrin biosynthesis genes has improved biocontrol activity against soilborne pathogens of wheat and canola. Phytopathology 110:1010–1017

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Złotek U, Szymanowska U, Jakubczyk A, Sikora M, Świeca M (2019) Effect of arachidonic and jasmonic acid elicitation on the content of phenolic compounds and antioxidant and anti-inflammatory properties of wheatgrass (Triticum aestivum L.). Food Chem 288:256–261

    Article  PubMed  Google Scholar 

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Acknowledgements

This work was supported by The National Natural Science Foundation of China (31801443) and The National Foreign Experts Program (G2022172012L). Thanks for Dr. Linda Thomashow and David Weller that provided the strains and suggestions on the manuscript.

Funding

This article was funded by Young Scientists Fund, 31801443, Mingming Yang, High-end Foreign Experts Recruitment Plan of China, G2022172012L, Mingming Yang.

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Authors and Affiliations

  1. State Key Laboratory of Crop Stress Biology for Arid Areas, College of Agronomy, Northwest A&F University, Yangling, Shaanxi, China

    Quan Zeng, Chao Cui, Kaiyue Wang, Fang Li, Chenyang Li, Shanshan Wen & Mingming Yang

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  1. Quan Zeng
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  2. Chao Cui
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  3. Kaiyue Wang
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  4. Fang Li
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  5. Chenyang Li
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  6. Shanshan Wen
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  7. Mingming Yang
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Contributions

QZ, MY, and SW carried out the experiments. QZ, MY, CC, KW, FL, and CL analyzed the data. QZ MY wrote the manuscript. CC, KW, FL, CL, and SW corrected it.

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Correspondence to Shanshan Wen or Mingming Yang.

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Zeng, Q., Cui, C., Wang, K. et al. Pseudomonas fluorescens HC1-07 transformed with phenazine-1-carboxylic acid biosynthesis genes has improved biocontrol activity against Rhizoctonia root rot and Fusarium crown rot of wheat. BioControl 68, 669–679 (2023). https://doi.org/10.1007/s10526-023-10227-0

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