Main conclusion
Plant and the soil-associated microbiome is important for imparting bacterial wilt disease tolerance in plants.
Abstract
Plants are versatile organisms that are endowed with the capacity to withstand various biotic and abiotic stresses despite having no locomotory abilities. Being the agent for bacterial wilt (BW) disease, Ralstonia solanacearum (RS) colonizes the xylem vessels and limits the water supply to various plant parts, thereby causing wilting. The havoc caused by RS leads to heavy losses in crop productivity around the world, for which a sustainable mitigation strategy is urgently needed. As several factors can influence plant–microbe interactions, comprehensive understanding of plant and soil-associated microbiome under the influence of RS and various environmental/edaphic conditions is important to control this pathogen. This review mainly focuses on microbiome dynamics associated with BW disease and also provide update on microbial/non-microbial approaches employed to control BW disease in crop plants.
Similar content being viewed by others
Data, material and/or code availability
Not required.
Abbreviations
- AHN:
-
Alkali hydrolysable nitrogen
- AK:
-
Available potassium
- AP:
-
Available phosphate
- ASi:
-
Available silicon
- BW:
-
Bacterial wilt
- CEC:
-
Cation exchange capacity
- MRS:
-
Microbial restoration substrates
- OM:
-
Organic matter
- RS:
-
Ralstonia solanacearum
- TK:
-
Total potassium
- WSOC:
-
Water-soluble organic carbon
References
Agarwal H, Dowarah B, Baruah PM, Bordoloi KS, Krishnatreya DB, Agarwala N (2020) Endophytes from Gnetum gnemon L. can protect seedlings against the infection of the phytopathogenic bacterium Ralstonia solanacearum as well as promote plant growth in tomatoes. Microbiol Res 238:126503. https://doi.org/10.1016/j.micres.2020.126503
Ahmed W, Dai Z, Zhang J, Li S, Ahmed A, Munir S, Liu Q, Tan Y, Ji G, Zhao Z (2022a) Plant-microbe interaction: mining the impact of native Bacillus amyloliquefaciens WS-10 on tobacco bacterial wilt disease and rhizosphere microbial communities. Microbiology Spectrum 10(4):e0147122. https://doi.org/10.1128/spectrum.01471-22
Ahmed W, Yang J, Tan Y, Munir S, Liu Q, Zhang J et al (2022b) Ralstonia solanacearum, a deadly pathogen: revisiting the bacterial wilt biocontrol practices in tobacco and other Solanaceae. Rhizosphere. https://doi.org/10.1016/j.rhisph.2022.100479
Alam T, Khan RAA, Ali A, Sher H, Ullah Z, Ali M (2019) Biogenic synthesis of iron oxide nanoparticles via Skimmia laureola and their antibacterial efficacy against bacterial wilt pathogen Ralstonia solanacearum. Mater Sci Eng, C Mater Biol Appl 98:101–108. https://doi.org/10.1016/j.msec.2018.12.117
Almeida OAC, de Araujo NO, Dias BHS, de Sant’Anna Freitas C, Coerini LF, Ryu CM, de Castro Oliveira JV (2023) The power of the smallest: the inhibitory activity of microbial volatile organic compounds against phytopathogens. Front Microbiol 13:951130. https://doi.org/10.3389/fmicb.2022.951130
Azeem M, Pirjan K, Qasim M, Mahmood A, Javed T, Muhammad H, Yang S, Dong R, Ali B, Rahimi M (2023) Salinity stress improves antioxidant potential by modulating physio-biochemical responses in Moringa oleifera Lam. Sci Rep 13(1):2895. https://doi.org/10.1038/s41598-023-29954-6
Berg G (2009) Plant–microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture. Appl Microbiol Biotechnol 84:11–18. https://doi.org/10.1007/s00253-009-2092-7
Bhunchoth A, Blanc-Mathieu R, Mihara T, Nishimura Y, Askora A, Phironrit N, Leksomboon C, Chatchawankanphanich O, Kawasaki T, Nakano M, Fujie M, Ogata H, Yamada T (2016) Two asian jumbo phages, ϕRSL2 and ϕRSF1, infect Ralstonia solanacearum and show common features of ϕKZ-related phages. Virology 494:56–66. https://doi.org/10.1016/j.virol.2016.03.028
Brader G, Compant S, Vescio K, Mitter B, Trognitz F, Ma LJ, Sessitsch A (2017) Ecology and genomic insights into plant-pathogenic and plant-nonpathogenic endophytes. Annu Rev Phytopathol 55:61–83. https://doi.org/10.1146/annurev-phyto-080516-035641
Chandwani S, Dewala S, Chavan SM, Paul D, Pachaiappan R, Gopi M, Amaresan N (2023) Complete genome sequencing of Bacillus subtilis (CWTS 5), a siderophore-producing bacterium triggers antagonistic potential against Ralstonia solanacearum. J Appl Microbiol 134(4):lxad066. https://doi.org/10.1093/jambio/lxad066
Chang X, Wang Y, Sun J, Xiang H, Yang Y, Chen S, Yu J, Yang C (2022) Mitigation of tobacco bacteria wilt with microbial degradation of phenolic allelochemicals. Sci Rep 12(1):20716. https://doi.org/10.1038/s41598-022-25142-0
Chen D, Liu X, Li C, Tian W, Shen Q, Shen B (2014) Isolation of Bacillus amyloliquefaciens S20 and its application in control of eggplant bacterial wilt. J Environ Manage 137:120–127. https://doi.org/10.1016/j.jenvman.2014.01.043
Chen S, Qi G, Ma G, Zhao X (2020) Biochar amendment controlled bacterial wilt through changing soil chemical properties and microbial community. Microbiol Res 231:126373. https://doi.org/10.1016/j.micres.2019.126373
Chu D, Ilyas N, Peng L, Wang X, Wang D, Xu Z, Gao Q, Tan X, Zhang C, Li Y, Yuan Y (2022) Genomic insights on fighting bacterial wilt by a novel Bacillus amyloliquefaciens strain Cas02. Microb Biotechnol 15(4):1152–1167. https://doi.org/10.1111/1751-7915.13925
de la Porte A, Schmidt R, Yergeau ÉÉ, Constant P (2020) A gaseous milieu: extending the boundaries of the rhizosphere. Trends Microbiol 28(7):536–542. https://doi.org/10.1016/j.tim.2020.02.016
Deng X, Zhang N, Shen Z, Zhu C, Li R, Salles JF, Shen Q (2020) Rhizosphere bacteria assembly derived from fumigation and organic amendment triggers the direct and indirect suppression of tomato bacterial wilt disease. Appl Soil Ecol 147:103364. https://doi.org/10.1016/j.apsoil.2019.103364
Deng X, Zhang N, Shen Z, Zhu C, Liu H, Xu Z, Li R, Shen Q, Salles JF (2021) Soil microbiome manipulation triggers direct and possible indirect suppression against Ralstonia solanacearum and Fusarium oxysporum. NPJ Biofilms Microbiomes 7(1):33. https://doi.org/10.1038/s41522-021-00204-9
Deng Q, Liu H, Lu Q, Gangurde SS, Du P, Li H, Li S, Liu H, Wang R, Huang L, Chen R, Fan C, Liang X, Chen X, Hong Y (2023) Silicon application for the modulation of rhizosphere soil bacterial community structures and metabolite profiles in peanut under Ralstonia solanacearum inoculation. Int J Mol Sci 24(4):3268. https://doi.org/10.3390/ijms24043268
Dong CJ, Wang LL, Li Q, Shang QM (2019) Bacterial communities in the rhizosphere, phyllosphere and endosphere of tomato plants. PLoS ONE 14(11):e0223847. https://doi.org/10.1371/journal.pone.0223847
Dowarah B, Agarwal H, Krishnatreya DB, Sharma PL, Kalita N, Agarwala N (2021) Evaluation of seed associated endophytic bacteria from tolerant chilli cv. Firingi Jolokia for their biocontrol potential against bacterial wilt disease. Microbiol Res 248:126751. https://doi.org/10.1016/j.micres.2021.126751
Durán P, Thiergart T, Garrido-Oter R, Agler M, Kemen E, Schulze-Lefert P, Hacquard S (2018) Microbial interkingdom interactions in roots promote Arabidopsis survival. Cell 175(4):973-983.e14. https://doi.org/10.1016/j.cell.2018.10.020
Ek-Ramos MJ, Gomez-Flores R, Orozco-Flores AA, Rodríguez-Padilla C, González-Ochoa G, Tamez-Guerra P (2019) Bioactive products from plant-endophytic gram-positive bacteria. Front Microbiol 10:463. https://doi.org/10.3389/fmicb.2019.00463
Elsayed TR, Jacquiod S, Nour EH, Sørensen SJ, Smalla K (2020) Biocontrol of bacterial wilt disease through complex interaction between tomato plant, antagonists, the indigenous rhizosphere microbiota, and Ralstonia solanacearum. Front Microbiol 10:2835. https://doi.org/10.3389/fmicb.2019.02835
Fu Q, Lai JL, Ji XH, Luo ZX, Wu G, Luo XG (2022) Alterations of the rhizosphere soil microbial community composition and metabolite profiles of Zea mays by polyethylene-particles of different molecular weights. J Hazard Mater 423:127062. https://doi.org/10.1016/j.jhazmat.2021.127062
García-Rodríguez RO, Thiessen LD (2020) Plant-microbiome interactions for bacterial wilt suppression in modern tobacco production. Plant Health Progress 22(1):2–10. https://doi.org/10.1094/PHP-08-20-0069-RV
Genin S, Denny TP (2012) Pathogenomics of the Ralstonia solanacearum species complex. Annu Rev Phytopathol 50:67–89. https://doi.org/10.1146/annurev-phyto-081211-173000
Gu Z, Eils R, Schlesner M (2016) Complex heatmaps reveal patterns and correlations in multidimensional genomic data. Bioinformatics (oxford, England) 32(18):2847–2849. https://doi.org/10.1093/bioinformatics/btw313
Gu Y, Banerjee S, Dini-Andreote F, Xu Y, Shen Q, Jousset A, Wei Z (2022) Small changes in rhizosphere microbiome composition predict disease outcomes earlier than pathogen density variations. ISME J 16(10):2448–2456. https://doi.org/10.1038/s41396-022-01290-z
Hu Q, Tan L, Gu S, Xiao Y, Xiong X, Zeng WA, Feng K, Wei Z, Deng Y (2020) Network analysis infers the wilt pathogen invasion associated with non-detrimental bacteria. NPJ Biofilms Microbiomes 6(1):8. https://doi.org/10.1038/s41522-020-0117-2
Hu Y, Zhao W, Li X, Feng J, Li C, Yang X, Guo Q, Wang L, Chen S, Li Y, Yang Y (2021) Integrated biocontrol of tobacco bacterial wilt by antagonistic bacteria and marigold. Sci Rep 11(1):16360. https://doi.org/10.1038/s41598-021-95741-w
Jiang G, Wei Z, Xu J, Chen H, Zhang Y, She X, Macho AP, Ding W, Liao B (2017) Bacterial wilt in China: history, current status, and future perspectives. Front Plant Sci 8:1549. https://doi.org/10.3389/fpls.2017.01549
Jiang G, Wang N, Zhang Y et al (2021) The relative importance of soil moisture in predicting bacterial wilt disease occurrence. Soil Ecol Lett 3:356–366. https://doi.org/10.1007/s42832-021-0086-2
Jiang G, Zhang Y, Gan G, Li W, Wan W, Jiang Y, Yang T, Zhang Y, Xu Y, Wang Y, Shen Q, Wei Z, Dini-Andreote F (2022) Exploring rhizo-microbiome transplants as a tool for protective plant-microbiome manipulation. ISME Commun 2(1):10. https://doi.org/10.1038/s43705-022-00094-8
Jose J, Éva C, Bozsó Z, Hamow KÁ, Fekete Z, Fábián A, Bánfalvi Z, Sági L (2023) Global transcriptome and targeted metabolite analyses of roots reveal different defence mechanisms against Ralstonia solanacearum infection in two resistant potato cultivars. Front Plant Sci 13:1065419. https://doi.org/10.3389/fpls.2022.1065419
Karim Z, Hossain MS (2018) Management of bacterial wilt (Ralstonia solanacearum) of potato: focus on natural bioactive compounds. J Biodivers Conserv Bioresour Manag 4(1):73–92. https://doi.org/10.3329/jbcbm.v4i1.37879
Khairy AM, Tohamy MRA, Zayed MA, Mahmoud SF, El-Tahan AM, El-Saadony MT, Mesiha PK (2022) Eco-friendly application of nano-chitosan for controlling potato and tomato bacterial wilt. Saudi J Biol Sci 29(4):2199–2209. https://doi.org/10.1016/j.sjbs.2021.11.041
Kim DR, Kwak YS (2022) Roads to construct and re-build plant microbiota community. Plant Pathol J 38(5):425–431. https://doi.org/10.5423/PPJ.RW.05.2022.0065
Kwak MJ, Kong HG, Choi K, Kwon SK, Song JY, Lee J, Lee PA, Choi SY, Seo M, Lee HJ, Jung EJ, Park H, Roy N, Kim H, Lee MM, Rubin EM, Lee SW, Kim JF (2018) Rhizosphere microbiome structure alters to enable wilt resistance in tomato. Nat Biotechnol. https://doi.org/10.1038/nbt.4232
Law JW, Ser HL, Khan TM, Chuah LH, Pusparajah P, Chan KG, Goh BH, Lee LH (2017) The potential of Streptomyces as biocontrol agents against the rice blast fungus, Magnaporthe oryzae (Pyricularia oryzae). Front Microbiol 8:3. https://doi.org/10.3389/fmicb.2017.00003
Le KD, Kim J, Yu NH, Kim B, Lee CW, Kim JC (2020) Biological control of tomato bacterial wilt, kimchi cabbage soft rot, and red pepper bacterial leaf spot using Paenibacillus elgii JCK-5075. Front Plant Sci 11:775. https://doi.org/10.3389/fpls.2020.00775
Lee CG, Iida T, Inoue Y, Muramoto Y, Watanabe H, Nakaho K, Ohkuma M (2017a) Prokaryotic communities at different depths between soils with and without tomato bacterial wilt but pathogen-present in a single greenhouse. Microbes Environ 32(2):118–124. https://doi.org/10.1264/jsme2.ME16136
Lee CG, Iida T, Uwagaki Y, Otani Y, Nakaho K, Ohkuma M (2017b) Comparison of prokaryotic and eukaryotic communities in soil samples with and without tomato bacterial wilt collected from different fields. Microbes Environ 32(4):376–385. https://doi.org/10.1264/jsme2.ME17131
Li J, Zhao Q, Wuriyanghan H, Yang C (2021a) Biocontrol bacteria strains Y4 and Y8 alleviate tobacco bacterial wilt disease by altering their rhizosphere soil bacteria community. Rhizosphere 19:100390. https://doi.org/10.1016/j.rhisph.2021.100390
Li P, Liu M, Li G, Liu K, Liu T, Wu M, Saleem M, Li Z (2021b) Phosphorus availability increases pathobiome abundance and invasion of rhizosphere microbial networks by Ralstonia. Environ Microbiol 23(10):5992–6003. https://doi.org/10.1111/1462-2920.15696
Li C, Ahmed W, Li D, Yu L, Xu L, Xu T, Zhao Z (2022a) Biochar suppresses bacterial wilt disease of flue-cured tobacco by improving soil health and functional diversity of rhizosphere microorganisms. Appl Soil Ecol 171:104314. https://doi.org/10.1016/j.apsoil.2021.104314
Li M, Pommier T, Yin Y et al (2022b) Indirect reduction of Ralstonia solanacearum via pathogen helper inhibition. ISME J 16:868–875. https://doi.org/10.1038/s41396-021-01126-2
Li Y, Qi G, Xie Z, Li B, Wang R, Tan J, Shi H, Xiang B, Zhao X (2023a) The endophytic root microbiome is different in healthy and Ralstonia solanacearum-infected plants and is regulated by a consortium containing beneficial endophytic bacteria. Microbiol Spectrum 11(1):e0203122. https://doi.org/10.1128/spectrum.02031-22
Li Y, Zhang P, Li M, Shakoor N, Adeel M, Zhou P, Guo M, Jiang Y, Zhao W, Lou B, Rui Y (2023b) Application and mechanisms of metal-based nanoparticles in the control of bacterial and fungal crop diseases. Pest Manag Sci 79(1):21–36. https://doi.org/10.1002/ps.7218
Li Z, Guo W, Mo C, Tang R, He L, Du L, Li M, Wu H, Tang X, Huang Z, Wu X (2023c) Root metabolism and effects of root exudates on the growth of Ralstonia solanacearum and Fusarium moniliforme were significantly different between the two genotypes of peanuts. Genes 14(2):528. https://doi.org/10.3390/genes14020528
Liu H, Brettell LE (2019) Plant defense by VOC-induced microbial priming. Trends Plant Sci 24(3):187–189. https://doi.org/10.1016/j.tplants.2019.01.008
Liu H, Brettell LE, Qiu Z, Singh BK (2020) Microbiome-mediated stress resistance in plants. Trends Plant Sci 25(8):733–743. https://doi.org/10.1016/j.tplants.2020.03.014
Liu X, Liu L, Gong J et al (2022a) Soil conditions on bacterial wilt disease affect bacterial and fungal assemblage in the rhizosphere. AMB Expr 12:110. https://doi.org/10.1186/s13568-022-01455-1
Liu Y, Tan X, Pan Y, Yu J, Du Y, Liu X, Ding W (2022b) Mutation in phcA enhanced the adaptation of Ralstonia solanacearum to long-term acid stress. Front Microbiol 13:829719. https://doi.org/10.3389/fmicb.2022.829719
Liu L, Chen Z, Su Z et al (2023) Soil pH indirectly determines Ralstonia solanacearum colonization through its impacts on microbial networks and specific microbial groups. Plant Soil 482:73–88. https://doi.org/10.1007/s11104-022-05671-3
Lundberg DS, Lebeis SL, Paredes SH, Yourstone S, Gehring J, Malfatti S, Tremblay J, Engelbrektson A, Kunin V, Del Rio TG, Edgar RC, Eickhorst T, Ley RE, Hugenholtz P, Tringe SG, Dangl JL (2012) Defining the core Arabidopsis thaliana root microbiome. Nature 488(7409):86–90. https://doi.org/10.1038/nature11237
Ma L, Zhang HY, Zhou XK, Yang CG, Zheng SC, Duo JL, Mo MH (2018) Biological control tobacco bacterial wilt and black shank and root colonization by bio-organic fertilizer containing bacterium Pseudomonas aeruginosa NXHG29. Appl Soil Ecol 129:136–144. https://doi.org/10.1016/j.apsoil.2018.05.011
Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M, Ronald P et al (2012) Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol 13:614–629. https://doi.org/10.1111/j.1364-3703.2012.00804.x
Md Meftaul I, Venkateswarlu K, Dharmarajan R, Annamalai P, Megharaj M (2020) Pesticides in the urban environment: a potential threat that knocks at the door. Sci Total Environ 711:134612. https://doi.org/10.1016/j.scitotenv.2019.134612
Mohamed BF, Sallam NM, Alamri SA, Abo-Elyousr KA, Mostafa YS, Hashem M (2020) Approving the biocontrol method of potato wilt caused by Ralstonia solanacearum (Smith) using Enterobacter cloacae PS14 and Trichoderma asperellum T34. Egyptian J Biol Pest Control 30:1–13. https://doi.org/10.1186/s41938-020-00262-9
Mohammed AF, Oloyede AR, Odeseye AO (2020) Biological control of bacterial wilt of tomato caused by Ralstonia solanacearum using Pseudomonas species isolated from the rhizosphere of tomato plants. Arch Phytopathol Plant Prot 53(1–2):1–16. https://doi.org/10.1080/03235408.2020.1715756
Morcillo RJL, Manzanera M (2021) The effects of plant-associated bacterial exopolysaccharides on plant abiotic stress tolerance. Metabolites 11:337. https://doi.org/10.3390/metabo11060337
Morita T, Tanaka I, Ryuda N, Ikari M, Ueno D, Someya T (2019) Antifungal spectrum characterization and identification of strong volatile organic compounds produced by Bacillus pumilus TM-R. Heliyon 5(6):e01817. https://doi.org/10.1016/j.heliyon.2019.e01817
Narasimhamurthy K, Udayashankar AC, De Britto S, Lavanya SN, Abdelrahman M, Soumya K, Shetty HS, Srinivas C, Jogaiah S (2022) Chitosan and chitosan-derived nanoparticles modulate enhanced immune response in tomato against bacterial wilt disease. Int J Biol Macromol 220:223–237. https://doi.org/10.1016/j.ijbiomac.2022.08.054
Nicolopoulou-Stamati P, Maipas S, Kotampasi C, Stamatis P, Hens L (2016) Chemical pesticides and human health: the urgent need for a new concept in agriculture. Front Public Health 4:148. https://doi.org/10.3389/fpubh.2016.00148
Niu J, Chao J, Xiao Y, Chen W, Zhang C, Liu X, Rang Z, Yin H, Dai L (2017) Insight into the effects of different cropping systems on soil bacterial community and tobacco bacterial wilt rate. J Basic Microbiol 57(1):3–11. https://doi.org/10.1002/jobm.201600222
Paudel S, Dobhal S, Alvarez AM, Arif M (2020) Taxonomy and phylogenetic research on Ralstonia solanacearum species complex: a complex pathogen with extraordinary economic consequences. Pathogens (basel, Switzerland) 9(11):886. https://doi.org/10.3390/pathogens9110886
Pohjanen J, Koskimäki JJ, Pirttilä AM (2014) Interactions of meristem-associated endophytic bacteria. Adv Endophytic Res. https://doi.org/10.1007/978-81-322-1575-2_5
Poria V, Dębiec-Andrzejewska K, Fiodor A, Lyzohub M, Ajijah N, Singh S, Pranaw K (2022) Plant Growth-Promoting Bacteria (PGPB) integrated phytotechnology: a sustainable approach for remediation of marginal lands. Front Plant Sci 13:999866. https://doi.org/10.3389/fpls.2022.999866
Qi G, Ma G, Chen S, Lin C, Zhao X (2019) Microbial network and soil properties are changed in bacterial wilt-susceptible soil. Appl Environ Microbiol 85(13):e00162-e219. https://doi.org/10.1128/AEM.00162-19
Raza W, Ling N, Liu D, Wei Z, Huang Q, Shen Q (2016a) Volatile organic compounds produced by Pseudomonas fluorescens WR-1 restrict the growth and virulence traits of Ralstonia solanacearum. Microbiol Res 192:103–113. https://doi.org/10.1016/j.micres.2016.05.014
Raza W, Ling N, Yang L, Huang Q, Shen Q (2016b) Response of tomato wilt pathogen Ralstonia solanacearum to the volatile organic compounds produced by a biocontrol strain Bacillus amyloliquefaciens SQR-9. Sci Rep 6:24856. https://doi.org/10.1038/srep24856
Raza W, Wang J, Wu Y, Ling N, Wei Z, Huang Q, Shen Q (2016c) Effects of volatile organic compounds produced by Bacillus amyloliquefaciens on the growth and virulence traits of tomato bacterial wilt pathogen Ralstonia solanacearum. Appl Microbiol Biotechnol 100(17):7639–7650. https://doi.org/10.1007/s00253-016-7584-7
Sharma I, Kashyap S, Agarwala N (2023) Biotic stress-induced changes in root exudation confer plant stress tolerance by altering rhizospheric microbial community. Front Plant Sci 14:1132824. https://doi.org/10.3389/fpls.2023.1132824
Shen T, Lei Y, Pu X, Zhang S, Du Y (2021) Identification and application of Streptomyces microflavus G33 in compost to suppress tomato bacterial wilt disease. Appl Soil Ecol 157:103724. https://doi.org/10.1016/j.apsoil.2020.103724
Simon JC, Marchesi JR, Mougel C, Selosse MA (2019) Host-microbiota interactions: from holobiont theory to analysis. Microbiome 7(1):5. https://doi.org/10.1186/s40168-019-0619-4
Su L, Zhang L, Nie D, Kuramae EE, Shen B, Shen Q (2020) Bacterial tomato pathogen Ralstonia solanacearum invasion modulates rhizosphere compounds and facilitates the cascade effect of fungal pathogen Fusarium solani. Microorganisms 8(6):806. https://doi.org/10.3390/microorganisms8060806
Sui X, Han X, Cao J, Li Y, Yuan Y, Gou J, Zheng Y, Meng C, Zhang C (2022) Biocontrol potential of Bacillus velezensis EM-1 associated with suppressive rhizosphere soil microbes against tobacco bacterial wilt. Front Microbiol 13:940156. https://doi.org/10.3389/fmicb.2022.940156
Tahir HAS, Gu Q, Wu H, Raza W, Safdar A, Huang Z, Rajer FU, Gao X (2017a) Effect of volatile compounds produced by Ralstonia solanacearum on plant growth promoting and systemic resistance inducing potential of Bacillus volatiles. BMC Plant Biol 17(1):133. https://doi.org/10.1186/s12870-017-1083-6
Tahir HA, Gu Q, Wu H, Niu Y, Huo R, Gao X (2017b) Bacillus volatiles adversely affect the physiology and ultra-structure of Ralstonia solanacearum and induce systemic resistance in tobacco against bacterial wilt. Sci Rep 7:40481. https://doi.org/10.1038/srep40481
Tan L, Zeng WA, Xiao Y, Li P, Gu S, Wu S, Zhai Z, Feng K, Deng Y, Hu Q (2021) Fungi-bacteria associations in wilt diseased rhizosphere and endosphere by interdomain ecological network analysis. Front Microbiol 12:722626. https://doi.org/10.3389/fmicb.2021.722626
Trivedi P, Leach JE, Tringe SG, Sa T, Singh BK (2020) Plant-microbiome interactions: from community assembly to plant health. Nat Rev Microbiol 18(11):607–621. https://doi.org/10.1038/s41579-020-0412-1
Velásquez AC, Oney M, Huot B, Xu S, He SY (2017) Diverse mechanisms of resistance to Pseudomonas syringae in a thousand natural accessions of Arabidopsis thaliana. New Phytol 214(4):1673–1687. https://doi.org/10.1111/nph.14517
Wang R, Zhang H, Sun L et al (2017) Microbial community composition is related to soil biological and chemical properties and bacterial wilt outbreak. Sci Rep 7:343. https://doi.org/10.1038/s41598-017-00472-6
Wang N, Wang L, Zhu K, Hou S, Chen L, Mi D, Gui Y, Qi Y, Jiang C, Guo JH (2019) Plant root exudates are involved in Bacillus cereus AR156 mediated biocontrol against Ralstonia solanacearum. Front Microbiol 10:98. https://doi.org/10.3389/fmicb.2019.00098
Wang L, Gao Y, Jiang N, Yan J, Lin W, Cai K (2022a) Silicon controls bacterial wilt disease in tomato plants and inhibits the virulence-related gene expression of Ralstonia solanacearum. Int J Mol Sci 23(13):6965. https://doi.org/10.3390/ijms23136965
Wang Z, Zhang Y, Bo G, Zhang Y, Chen Y, Shen M, Zhang P, Li G, Zhou J, Li Z, Yang J (2022b) Ralstonia solanacearum infection disturbed the microbiome structure throughout the whole tobacco crop niche as well as the nitrogen metabolism in soil. Front Bioeng Biotechnol 10:903555. https://doi.org/10.3389/fbioe.2022.903555
Wang J, Raza W, Jiang G, Yi Z, Fields B, Greenrod S, Friman VP, Jousset A, Shen Q, Wei Z (2023a) Bacterial volatile organic compounds attenuate pathogen virulence via evolutionary trade-offs. ISME J 17(3):443–452. https://doi.org/10.1038/s41396-023-01356-6
Wang Z, Luo W, Cheng S, Zhang H, Zong J, Zhang Z (2023b) Ralstonia solanacearum—a soil borne hidden enemy of plants: research development in management strategies, their action mechanism and challenges. Front Plant Sci 14:1141902. https://doi.org/10.3389/fpls.2023.1141902
Wei Z, Huang J, Yang T, Jousset A, Xu Y, Shen Q, Friman VP (2017) Seasonal variation in the biocontrol efficiency of bacterial wilt is driven by temperature-mediated changes in bacterial competitive interactions. J Appl Ecol 54(5):1440–1448. https://doi.org/10.1111/1365-2664.12873
Wen T, Zhao M, Liu T, Huang Q, Yuan J, Shen Q (2020) High abundance of Ralstonia solanacearum changed tomato rhizosphere microbiome and metabolome. BMC Plant Biol 20(1):166. https://doi.org/10.1186/s12870-020-02365-9
Wen D, Guo Q, Zhao W, Yang Y, Yang C, Yu J, Hu Y (2023) Effect and mechanism of NaHS on tobacco bacterial wilt caused by Ralstonia solanacearum. Sci Rep 13(1):2462. https://doi.org/10.1038/s41598-022-26697-8
Wu X, Li H, Wang Y, Zhang X (2020) Effects of bio-organic fertiliser fortified by Bacillus cereus QJ-1 on tobacco bacterial wilt control and soil quality improvement. Biocontrol Sci Tech 30(4):351–369. https://doi.org/10.1080/09583157.2020.1711870
Xiao XO, Lin W, Feng E, Ou X (2023) Transcriptome and metabolome response of eggplant against Ralstonia solanacearum infection. PeerJ 11:e14658. https://doi.org/10.7717/peerj.14658
Yamada T, Satoh S, Ishikawa H, Fujiwara A, Kawasaki T, Fujie M, Ogata H (2010) A jumbo phage infecting the phytopathogen Ralstonia solanacearum defines a new lineage of the Myoviridae family. Virology 398(1):135–147. https://doi.org/10.1016/j.virol.2009.11.043
Yang W, Xu Q, Liu HX, Wang YP, Wang YM, Yang HT, Guo JH (2012) Evaluation of biological control agents against Ralstonia wilt on ginger. Biol Control 62(3):144–151. https://doi.org/10.1016/j.biocontrol.2012.05.001
Yang S, Chen X, Jiang Z, Ding J, Sun X, Xu J (2020) Effects of biochar application on soil organic carbon composition and enzyme activity in paddy soil under water-saving irrigation. Int J Environ Res Public Health 17(1):333. https://doi.org/10.3390/ijerph17010333
Yang K, Wang X, Hou R, Lu C, Fan Z, Li J, Wang S, Xu Y, Shen Q, Friman VP, Wei Z (2023) Rhizosphere phage communities drive soil suppressiveness to bacterial wilt disease. Microbiome 11(1):16. https://doi.org/10.1186/s40168-023-01463-8
Yin J, Zhang Z, Zhu C, Wang T, Wang R, Ruan L (2022) Heritability of tomato rhizobacteria resistant to Ralstonia solanacearum. Microbiome 10(1):1–18. https://doi.org/10.1186/s40168-022-01413-w
Yoo SJ, Kim ST, Weon HY, Song J, Sang MK (2022) Biocontrol activity of anti-salinity Bacillus mesonae H20–5 against Bacterial wilt in different tomato cultivars. Biol Control 169:104869. https://doi.org/10.1016/j.biocontrol.2022.104869
Yuan S, Wang L, Wu K, Shi J, Wang M, Yang X, Shen Q, 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. https://doi.org/10.1016/j.apsoil.2013.11.004
Zhang Y, Hu A, Zhou J, Zhang W, Li P (2020) Comparison of bacterial communities in soil samples with and without tomato bacterial wilt caused by Ralstonia solanacearum species complex. BMC Microbiol 20:1–10. https://doi.org/10.1186/s12866-020-01774-y
Zhang S, Liu X, Zhou L, Deng L, Zhao W, Liu Y, Ding W (2022) Alleviating soil acidification could increase disease suppression of bacterial wilt by recruiting potentially beneficial rhizobacteria. Microbiol Spectr 10(2):e02333-e2421. https://doi.org/10.1128/spectrum.02333-21
Zhao Q, Cao J, Cai X, Wang J, Kong F, Wang D, Wang J (2023) Antagonistic activity of volatile organic compounds produced by acid-tolerant pseudomonas protegens CLP-6 as biological fumigants to control tobacco bacterial wilt caused by Ralstonia solanacearum. Appl Environ Microbiol 89(2):e0189222. https://doi.org/10.1128/aem.01892-22
Zheng X, Zhu Y, Wang J, Wang Z, Liu B (2019) Combined use of a microbial restoration substrate and avirulent Ralstonia solanacearum for the control of tomato bacterial wilt. Sci Rep 9(1):20091. https://doi.org/10.1038/s41598-019-56572-y
Zheng C, Li W, Zhou Y, Zhu Z, Wu X (2023) Physiochemical properties and microflora of the rhizosphere soil of tobacco plants with and without bacterial wilt. Sustainability 15(4):3661. https://doi.org/10.3390/su15043661
Acknowledgement
The authors would like to acknowledge Department of Science and Technology, Govt. of India for providing FIST-program to Department of Botany, Gauhati University. We sincerely apologise to our contemporaries whose work could not be discussed in this article due to space restrictions.
Funding
Start-Up grant provided by University Grant Commission, Govt. of India (grant number F.30-386/2017) and Scheme for promoting research among young faculty (GU/Acad./YFPGC/50/2018/1738-79/05) provided to NA by Gauhati University.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Ethics approval
Not required.
Consent for publication
Not required.
Additional information
Communicated by Gerhard Leubner.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Kashyap, S., Sharma, I., Dowarah, B. et al. Plant and soil-associated microbiome dynamics determine the fate of bacterial wilt pathogen Ralstonia solanacearum. Planta 258, 57 (2023). https://doi.org/10.1007/s00425-023-04209-w
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-023-04209-w