Watermelon Root Exudates Enhance Root Colonization of Bacillus amyloliquefaciens TR2.
Journal
Current microbiology
ISSN: 1432-0991
Titre abrégé: Curr Microbiol
Pays: United States
ID NLM: 7808448
Informations de publication
Date de publication:
18 Feb 2023
18 Feb 2023
Historique:
received:
12
08
2022
accepted:
30
01
2023
entrez:
21
2
2023
pubmed:
22
2
2023
medline:
25
2
2023
Statut:
epublish
Résumé
Bacillus amyloliquefaciens TR2, one of plant growth-promoting rhizobacteria (PGPR), is capable of colonizing plant roots in a large population size. However, the interaction of watermelon root exudates and colonization of the strain TR2 has not yet been clearly elucidated. In this investigation, we demonstrated that B. amyloliquefaciens TR2 promoted watermelon plants growth and exhibited biocontrol efficacy against watermelon Fusarium wilt under greenhouse conditions. Collected watermelon root exudates significantly induced chemotaxis, swarming motility, and biofilm formation of the strain TR2. We also tested the components of root exudates (organic acids: malic acid, citric acid, succinic acid, and fumaric acid; amino acids: methionine, glutamic acid, alanine, and aspartic acid; phenolic acid: benzoic acid) and the results showed that a majority of these compounds could promote chemotactic response, swarming motility, and biofilm formation in a different degree. Benzoic acid induced the strongest chemotactic response; however, the swarming motility and biofilm formation of the strain TR2 were maximumly enhanced by supplement of fumaric acid and glutamic acid, respectively. In addition, the root colonization examination indicated that the population of B. amyloliquefaciens TR2 colonized on watermelon root surfaces was dramatically increased by adding concentrated watermelon root exudates. In summary, our studies provide evidence suggesting that root exudates are important for colonization of B. amyloliquefaciens TR2 on plant roots and help us to understand the interaction between plants and beneficial bacteria.
Identifiants
pubmed: 36802037
doi: 10.1007/s00284-023-03206-2
pii: 10.1007/s00284-023-03206-2
doi:
Substances chimiques
fumaric acid
88XHZ13131
Plant Exudates
0
Glutamates
0
Benzoates
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
110Subventions
Organisme : Beijing Municipal Education Commission
ID : KM201910020011
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Beneduzi A, Ambrosini A, Passaglia L (2012) Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genet Mol Biol 35(suppl 4):1044–1051. https://doi.org/10.1590/s1415-47572012000600020
doi: 10.1590/s1415-47572012000600020
pubmed: 23411488
pmcid: 3571425
Jin Y, Zhu H, Luo S, Yang W, Zhang L, Li S, Jin Q, Cao Q, Sun S, Xiao M (2019) Role of maize root exudates in promotion of colonization of Bacillus velezensis strain S3–1 in rhizosphere soil and root tissue. Curr Microbiol 76(7):855–862. https://doi.org/10.1007/s00284-019-01699-4
doi: 10.1007/s00284-019-01699-4
pubmed: 31073734
Li B, Li Q, Xu ZH, Zhang N, Shen Q, Zhang R (2014) Responses of beneficial Bacillus amyloliquefaciens SQR9 to different soilborne fungal pathogens through the alteration of antifungal compounds production. Front Microbiol 5:636. https://doi.org/10.3389/fmicb.2014.00636
doi: 10.3389/fmicb.2014.00636
pubmed: 25484880
pmcid: 4240174
Weng J, Wang Y, Li J, Shen Q, Zhang R (2013) Enhanced root colonization and biocontrol activity of Bacillus amyloliquefaciens SQR9 by abrB gene disruption. Appl Microbiol Biotechnol 97(17):8823–8830. https://doi.org/10.1007/s00253-012-4572-4
doi: 10.1007/s00253-012-4572-4
pubmed: 23196984
Qin Y, Shang Q, Zhang Y, Li P, Chai Y (2017) Bacillus amyloliquefaciens L-S60 reforms the rhizosphere bacterial community and improves growth conditions in cucumber plug seedling. Front Microbiol 8:2620. https://doi.org/10.3389/fmicb.2017.02620
doi: 10.3389/fmicb.2017.02620
pubmed: 29312278
pmcid: 5744474
Chen Y, Cao S, Chai Y, Clardy J, Kolter R, Guo J, Losick R (2012) A Bacillus subtilis sensor kinase involved in triggering biofilm formation on the roots of tomato plants. Mol Microbiol 85(3):418–430. https://doi.org/10.1111/j.1365-2958.2012.08109.x
doi: 10.1111/j.1365-2958.2012.08109.x
pubmed: 22716461
pmcid: 3518419
Gao T, Ding M, Wang Q (2020) The recA gene is crucial to mediate colonization of Bacillus cereus 905 on wheat roots. Appl Microbiol Biotechnol 104(21):9251–9265. https://doi.org/10.1007/s00253-020-10915-2
doi: 10.1007/s00253-020-10915-2
pubmed: 32970180
Huang R, Feng H, Xu Z, Zhang N, Liu Y, Shao J, Shen Q, Zhang R (2022) Identification of adhesions in plant beneficial rhizobacteria Bacillus velezensis SQR9 and their effect on root colonization. Mol Plant Microbe Interact 35(1):64–72. https://doi.org/10.1094/MPMI-09-21-0234-R
doi: 10.1094/MPMI-09-21-0234-R
pubmed: 34698535
Yuan J, Zhang N, Huang Q, Raza W, Li R, Vivanco J, Shen Q (2015) Organic acids from root exudates of banana help root colonization of PGPR strain Bacillus amyloliquefaciens NJN-6. Sci Rep 5:13438–13447. https://doi.org/10.1038/srep13438
doi: 10.1038/srep13438
pubmed: 26299781
pmcid: 4547103
Gao T, Ding M, Yang C-H, Fan H, Chai Y, Li Y (2019) The phosphotransferase system gene ptsH plays an important role in MnSOD production, biofilm formation, swarming motility, and root colonization in Bacillus cereus 905. Res Microbiol 170(2):86–96. https://doi.org/10.1016/j.resmic.2018.10.002
doi: 10.1016/j.resmic.2018.10.002
pubmed: 30395927
Sood SG (2003) Chemotactic response of plant-growth-promoting bacteria towards roots of vesicular-arbuscular mycorrhizal tomato plants. FEMS Microbiol 45(3):219–227. https://doi.org/10.1016/S0168-6496(03)00155-7
doi: 10.1016/S0168-6496(03)00155-7
Sharma M, Saleh D, Charron J-B, Jabaji S (2020) A crosstalk between Brachypodium root exudates, organic acids, and Bacillus velezensis B26, a growth promoting bacterium. Front Microbiol 11:575578. https://doi.org/10.3389/fmicb.2020.575578
doi: 10.3389/fmicb.2020.575578
pubmed: 33123106
pmcid: 7573104
Fan H, Zhan Z, Li Y, Zhang X, Duan Y, Wang Q (2017) Biocontrol of bacterial fruit blotch by Bacillus subtilis 9407 via surfactin-mediated antibacterial activity and colonization. Front Microbiol 8:1973. https://doi.org/10.3389/fmicb.2017.01973
doi: 10.3389/fmicb.2017.01973
pubmed: 29075242
pmcid: 5641556
Kearns DB, Losick R (2003) Swarming motility in undomesticated Bacillus subtilis. Mol Microbiol 49(3):581–590. https://doi.org/10.1046/j.1365-2958.2003.03584.x
doi: 10.1046/j.1365-2958.2003.03584.x
pubmed: 12864845
López D, Vlamakis H, Koter R (2010) Biofilms. Cold Spring Harb Perspect Biol 2(7):398. https://doi.org/10.1101/cshperspect.a000398
doi: 10.1101/cshperspect.a000398
Beauregard P, Chai Y, Vlamakis H, Losick R, Kolter R (2013) Bacillus subtilis biofilm induction by plant polysaccharides. Proc Natl Acad Sci USA 110(17):1621–1630. https://doi.org/10.1073/pnas.1218984110
doi: 10.1073/pnas.1218984110
Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32(6):666–681. https://doi.org/10.1111/j.1365-3040.2008.01926.x
doi: 10.1111/j.1365-3040.2008.01926.x
pubmed: 19143988
Bais HP, Weir TL, Perry LG, Gilroy S, Vivanco JM (2006) The role of root exudates in rhizosphere interactions with plants and other organisms. Annu Rev Plant Biol 57:233–266. https://doi.org/10.1146/annurev.arplant.57.032905.105159
doi: 10.1146/annurev.arplant.57.032905.105159
pubmed: 16669762
Hirsch AM, Bauer WD, Bird DM, Cullimore J, Tyler B, Yoder JI (2003) Molecular signals and receptors: controlling rhizosphere interactions between plants and other organisms. Ecology 84(4):858–868. https://doi.org/10.1890/0012-9658(2003)084[0858:MSARCR]2.0.CO;2
doi: 10.1890/0012-9658(2003)084[0858:MSARCR]2.0.CO;2
Shi S, Richardson A, O’Callaghan M, DeAngelis K, Jones E, Stewart A, Firestone MK, Condron L (2011) Effects of selected root exudates components on soil bacterial communities. FEMS Microbiol Ecol 77(3):600–610. https://doi.org/10.1111/j.1574-6941.2011.01150.x
doi: 10.1111/j.1574-6941.2011.01150.x
pubmed: 21658090
Zuo C, Li C, Li B, Wei Y, Hu C, Yang Q, Yang J, Sheng O, Kuang R, Deng G, Biswas M (2015) The toxic mechanism and bioactive components of Chinese leek root exudates acting against Fusarium oxysporum f. sp. cubense tropical race 4. Eur J Plant Pathol 143(3):447–460. https://doi.org/10.1007/s10658-015-0697-5
doi: 10.1007/s10658-015-0697-5
Bais HP, Fall R, Vivanco JM (2004) Biocontrol of Bacillus subtilis against infection of Arabidopsis roots by Pseudomonas syringae is facilitated by biofilm formation and surfactin production. Plant Physiol 134(1):307–319. https://doi.org/10.1104/pp.103.028712
doi: 10.1104/pp.103.028712
pubmed: 14684838
pmcid: 316310
de Weert S, Vermeiren H, Mulders IHM, Kuiper I, Hendrickx N, Bloemberg GV, Vanderleyden J, De Mot R, Lugtenberg BJJ (2002) Flagella-driven chemotaxis towards exudate components is an important trait for tomato root colonization by Pseudomonas fluorescens. Mol Plant Microbe Interact 15(11):1173–1180. https://doi.org/10.1094/MPMI.2002.15.11.1173
doi: 10.1094/MPMI.2002.15.11.1173
pubmed: 12423023
Kamilova F, Kravchenko L, Shaposhnikov A, Azarova T, Makarova N, Lugtenberg B (2006) Organic acids, sugars, and L-tryptophane in exudates of vegetables growing on stonewool and their effects on activities of rhizosphere bacteria. Mol Plant Microbe Interact 19(3):250–256. https://doi.org/10.1094/MPMI-19-0250
doi: 10.1094/MPMI-19-0250
pubmed: 16570655
Liu Y, Chen L, Wu G, Feng H, Zhang G, Shen Q, Zhang R (2017) Identification of root-secreted compounds involved in the communication between cucumber, the beneficial Bacillus amyloliquefaciens, and the soil-borne pathogen Fusarium oxysporum. Mol Plant Microbe Interact 30(1):53–62. https://doi.org/10.1094/MPMI-07-16-0131-R
doi: 10.1094/MPMI-07-16-0131-R
pubmed: 27937752
Li D, Li R, Qin W, Zhou Y, Shang Q, Ren Z, Wei Y, Zhao X (2018) Control effects and related biocontrol factors detection of two Bacillus amyloliquefaciens strains on watermelon Fusarium wilt. Chin J Biol control 34(05):729–737. https://doi.org/10.16409/j.cnki.2095-039x.2018.05.012 . (in Chinese)
doi: 10.16409/j.cnki.2095-039x.2018.05.012
Zhao Y, Miao P, Wang X, Gao T, Shi X, Jia S, Ren Z, Zhao X (2022) Influences of Bacillus amyloliquefaciens TR2 on soil enzyme activities and its effects on disease control and growth promotion in strawberry. Chinese J Biol Control 38(02):495–501. https://doi.org/10.16409/j.cnki.2095-039x.2022.02.014 . (in Chinese)
doi: 10.16409/j.cnki.2095-039x.2022.02.014
Gao T, Foulston L, Chai Y, Wang Q, Losick R (2015) Alternative modes of biofilm formation by plant-associated Bacillus cereus. Microbiologyopen 4(3):452–464. https://doi.org/10.1002/mbo3.251
doi: 10.1002/mbo3.251
pubmed: 25828975
pmcid: 4475387
Martyn RD (1987) Fusarium oxysporum f. sp. niveum race 2: a highly aggressive race new to the United States. Plant Dis 71:233–236
doi: 10.1094/PD-71-0233
Yaryura P, León M, Correa O, Kerber N, Pucheu N, García A (2008) Assessment of the role of chemotaxis and biofilm formation as requirements for colonization of roots and seeds of soybean plants by Bacillus amyloliquefaciens BNM339. Curr Microbiol 56(6):625–632. https://doi.org/10.1007/s00284-008-9137-5
doi: 10.1007/s00284-008-9137-5
pubmed: 18335278
Chauhan PS, Lata C, Tiwari S, Chauhan AS, Mishra SK, Agarwal L, Chakrabarty D, Nautiyal CS (2019) Transcriptional alterations reveal Bacillus amyloliquefaciens-rice cooperation under salt stress. Sci Rep 9(1):11912. https://doi.org/10.1038/s41598-019-48309-8
doi: 10.1038/s41598-019-48309-8
pubmed: 31417134
pmcid: 6695486
Gagné-Bourque F, Mayer BF, Charron JB, Vali H, Bertrand A, Jabaji S (2015) Accelerated growth rate and increased drought stress resilience of the model grass Brachypodium distachyon colonized by Bacillus subtilis B26. PLoS One 10(6):e0130456. https://doi.org/10.1371/journal.pone.0130456
doi: 10.1371/journal.pone.0130456
pubmed: 26103151
pmcid: 4477885
Rahman A, Uddin W, Wenner NG (2015) Induced systemic resistance responses in perennial ryegrass against Magnaporthe oryzae elicited by semipurified surfactin lipopeptides and live cells of Bacillus amyloliquefaciens. Mol Plant Pathol 16(6):546–558. https://doi.org/10.1111/mpp.12209
doi: 10.1111/mpp.12209
pubmed: 25285593
pmcid: 6638512
Wang Z, Li Y, Zhao Y, Zhuang L, Yu Y, Wang M, Liu J, Wang Q (2021) A microbial consortium-based product promotes potato yield by recruiting rhizosphere bacteria involved in nitrogen and carbon metabolisms. Microb Biotechnol 14(5):1961–1975. https://doi.org/10.1111/1751-7915.13876
doi: 10.1111/1751-7915.13876
pubmed: 34231972
pmcid: 8449676
Chen Y, Yan F, Chai Y, Liu H, Kolter R, Losick R, Guo J-H (2013) Biocontrol of tomato wilt disease by Bacillus subtilis isolates from natural environments depends on conserved genes mediating biofilm formation. Environ Microbiol 15(3):848–864. https://doi.org/10.1111/j.1462-2920.2012.02860.x
doi: 10.1111/j.1462-2920.2012.02860.x
pubmed: 22934631
Wang J, Xu S, Yang R, Zhao W, Zhu D, Zhang X, Huang Z (2021) Bacillus amyloliquefaciens FH-1 significantly affects cucumber seedlings and the rhizosphere bacterial community but not soil. Sci Rep 11(1):12055. https://doi.org/10.1038/s41598-021-91399-6
doi: 10.1038/s41598-021-91399-6
pubmed: 34103586
pmcid: 8187646
Cao Y, Zhang Z, Ling N, Yuan Y, Zheng X, Shen B, Shen Q (2011) Bacillus subtilis SQR9 can control Fusarium wilt in cucumber by colonizing plant roots. Bio Fertil Soils 47(5):495–506. https://doi.org/10.1007/s00374-011-0556-2
doi: 10.1007/s00374-011-0556-2
Feng H, Zhang N, Du W, Zhang H, Liu Y, Fu R, Shao J, Zhang G, Shen Q, Zhang R (2018) Identification of chemotaxis compounds in root exudates and their sensing chemoreceptors in plant-growth-promoting rhizobacteria Bacillus amyloliquefaciens SQR9. Mol Plant Microbe Interact 31(10):995–1005. https://doi.org/10.1094/MPMI-01-18-0003-R
doi: 10.1094/MPMI-01-18-0003-R
pubmed: 29714096
Wang Y, Wang H, Yang C-H, Wang Q, Mei R (2007) Two distinct manganese-containing superoxide dismutase genes in Bacillus cereus: their physiological characterizations and roles in surviving in wheat rhizosphere. FEMS Microbiol Lett 272(2):206–213. https://doi.org/10.1111/j.1574-6968.2007.00759.x
doi: 10.1111/j.1574-6968.2007.00759.x
pubmed: 17521361
Canarini A, Wanek W, Merchant A, Richter A, Kaiser C (2019) Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Front Plant Sci 10:157. https://doi.org/10.3389/fpls.2019.00157
doi: 10.3389/fpls.2019.00157
pubmed: 30881364
pmcid: 6407669
Rudrappa T, Czymmke KJ, Paré PW, Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148(3):1547–1556. https://doi.org/10.1104/pp.108.127613
doi: 10.1104/pp.108.127613
pubmed: 18820082
pmcid: 2577262
Bhattacharyya C, Bakshi U, Mallick I, Mukherji S, Bera B, Ghosh A (2017) Genome-guided insights into the plant growth promotion capabilities of the physiologically versatile Bacillus aryabhattai strain AB211. Front Microbiol 8:411. https://doi.org/10.3389/fmicb.2017.00411
doi: 10.3389/fmicb.2017.00411
pubmed: 28377746
pmcid: 5359284
Van de Broek A, Lambrecht M, Vanderleyden J (1998) Bacterial chemotactic motility is important for the initiation of wheat root colonization by Azospirillum brasilense. Microbiology 144(Pt 9):2599–2606. https://doi.org/10.1099/00221287-144-9-2599
doi: 10.1099/00221287-144-9-2599
pubmed: 9782509
Zhang N, Wang D, Liu Y, Li S, Shen Q, Zhang R (2014) Effects of different plant root exudates and their organic acid components on chemotaxis, biofilm formation and colonization by beneficial rhizosphere-associated bacterial strains. Plant Soil 374(1–2):689–700. https://doi.org/10.1007/s11104-013-1915-6
doi: 10.1007/s11104-013-1915-6
Ling N, Raza W, Ma J, Huang Q, Shen Q (2011) Identification and role of organic acids in watermelon root exudates for recruiting Paenibacillus polymyxa SQR-21 in the rhizosphere. Eur J Soil Biol 47(6):374–379. https://doi.org/10.1016/j.ejsobi.2011.08.009
doi: 10.1016/j.ejsobi.2011.08.009
Sang MK, Kim KD (2014) Biocontrol activity and root colonization by Pseudomonas corrugata strains CCR04 and CCR80 against Phytophthora blight of pepper. Biocontrol 59(4):437–448. https://doi.org/10.1007/s10526-014-9584-9
doi: 10.1007/s10526-014-9584-9
Keswani C, Prakash O, Bharti N, Vílchez JI, Sansinenea E, Lally RD, Borriss R, Singh SP, Gupta VK, Fraceto LF, de Lima R, Singh HB (2019) Re-addressing the biosafety issues of plant growth promoting rhizobacteria. Sci Total Environ 690:841–852. https://doi.org/10.1016/j.scitotenv.2019.07.046
doi: 10.1016/j.scitotenv.2019.07.046
pubmed: 31302549
Barros-Rodríguez A, Rangseekaew P, Lasudee K, Pathom-Aree W, Manzanera M (2020) Regulatory risks associated with bacteria as biostimulants and biofertilizers in the frame of the European regulation (EU) 2019/1009. Sci Total Environ 740:140239. https://doi.org/10.1016/j.scitotenv.2020.140239
doi: 10.1016/j.scitotenv.2020.140239
pubmed: 32563889
Rangseekaew P, Barros-Rodríguez A, Pathom-Aree W, Manzanera M (2022) Plant beneficial deep-sea actinobacterium, Dermacoccus abyssi MT1.1T promote growth of tomato (Solanum lycopersicum) under salinity stress. Biology (Basel) 11(2):191. https://doi.org/10.3390/biology11020191
doi: 10.3390/biology11020191
pubmed: 35205058
pmcid: 8869415
Rangseekaew P, Barros-Rodríguez A, Pathom-Aree W, Manzanera M (2021) Deep-sea actinobacterium mitigate salinity stress in tomato seedlings and their biosafety testing. Biology (Basel) 10(8):1687. https://doi.org/10.3390/plants10081687
doi: 10.3390/plants10081687
pmcid: 8401925