Abstract
Aim
The secretion of allelochemicals from plant roots plays a key role in soil sickness and soil-borne disease. The goal of this study was to investigate the role of allelopathic chemicals in Ralstonia solanacearum-infected tobacco roots.
Methods
The organic acids investigated in the present study are major components of tobacco root exudates. Through a swarming assay, we assessed the chemotaxis and colonization of R. solanacearum in response to organic acids.
Results
Fumaric acid was detected, and the results showed that this acid could serve as a semiochemical for attracting R. solanacearum and inducing the formation of biofilms of this species. The results also revealed that cinnamic and myristic acids play significant roles on swarming motility and chemotaxis. In addition, cinnamic, myristic and fumaric acids could enhance the expression of chemotaxis- and motility-related genes in R. solanacearum cultured in minimal medium. Furthermore, these three acids promote R. solanacearum colonization and accelerate disease progression in tobacco.
Conclusion
Cinnamic, myristic and fumaric acids could serve as semiochemical attractants to induce the colonization and infection of R. solanacearum. The results of the present study enhance our understanding of the ecological effects of plant root exudates in plant-microbe interactions and help to reveal the relationship between tobacco bacterial wilt and the autotoxins and allelochemicals that accumulate from root exudates.
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References
Alexandre G, Zhulin IB (2001) More than one way to sense chemicals. J Bacteriol 183:4681–4686
Andersen PC, Brodbeck BV, Oden S, Shriner A, Leite B (2007) Influence of xylem fluid chemistry on planktonic growth, biofilm formation and aggregation of Xylella fastidiosa. FEMS Microbiol Lett 274:210–217
Antúnez-Lamas M, Cabrera-Ordóñez E, López-Solanilla E, Raposo R, Trelles-Salazar O, Rodríguez-Moreno A, Rodríguez-Palenzuela P (2009) Role of motility and chemotaxis in the pathogenesis of Dickeya dadantii 3937 (ex Erwinia chrysanthemi 3937. Microbiology 155:434–442
Bacilio-Jiménez M, Aguilar-Flores S, Ventura-Zapata E, Pérez-Campos E, Bouquelet S, Zenteno E (2003) Chemical characterization of root exudates from rice (Oryza sativa) and their effects on the chemotactic response of endophytic bacteria. Plant Soil 249:271–277
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
Beauregard PB, Chai Y, Vlamakis H, Losick R, Kolter R (2013) Bacillus subtilis biofilm induction by plant polysaccharides. Proc Natl Acad Sci 110:E1621–E1630
Bertin C, Yang X, Weston LA (2003) The role of root exudates and allelochemicals in the rhizosphere. Plant Soil 256:67–83
Chaparro JM, Sheflin AM, Manter DK, Vivanco JM (2012) Manipulating the soil microbiome to increase soil health and plant fertility. Biol Fertil Soils 48:489–499
Chen S, Zhou B, Lin S, Li X, Ye X (2011) Accumulation of cinnamic acid and vanillin in eggplant root exudates and the relationship with continuous cropping obstacle. Afr J Biotechnol 10:2659–2665
Chow S, Gu K, Jiang L, Nassour A (2011) Salicylic acid affects swimming, twitching and swarming motility in Pseudomonas aeruginosa, resulting in decreased biofilm formation. Journal of Experimental Microbiology and Immunology 15:22–29
Compant S, Clément C, Sessitsch A (2010) Plant growth-promoting bacteria in the rhizo- and endosphere of plants: their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678
de Weert S, Vermeiren H, Mulders IH, Kuiper I, Hendrickx N, Bloemberg GV, BJ L (2002) Flagella-driven chemotaxis towards exudate components is an important trait for tomato root colonization by Pseudomonas fluorescens. Mol Plant-Microbe Interact 15:1173–1180
Davies DG, Marques CN (2009) A fatty acid messenger is responsible for inducing dispersion in microbial biofilms. J Bacteriol 191:1393–1403
Dong L, Li X, Huang L, Gao Y, Zhong L, Zheng Y, Zuo Y (2013) Lauric acid in crown daisy root exudate potently regulates root-knot nematode chemotaxis and disrupts mi-flp-18 expression to block infection. J Exp Bot 65:131–141
Doornbos RF, van Loon LC, Bakker PA (2012) Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. A review. Agron Sustain Dev 32:227–243
Dutta S, Rani T, Podile A (2013) Root exudate-induced alterations in Bacillus cereus cell wall contribute to root colonization and plant growth promotion. PloS One 8:e78369. doi:10.1371/journal.pone.0078369
el Zahar Haichar F, Santaella C, Heulin T, Achouak W (2014) Root exudates mediated interactions belowground. Soil Biol Biochem 77:69–80
Englert DL, Jayaraman A, Manson MD (2009) Microfluidic techniques for the analysis of bacterial chemotaxis. Chemotaxis: Methods and Protocols 571:1–23
Faure D, Vereecke D, Leveau JH (2009) Molecular communication in the rhizosphere. Plant Soil 321:279–303
Hao W, Ren L, Ran W, Shen Q (2010) Allelopathic effects of root exudates from watermelon and rice plants on Fusarium oxysporum f. Sp. niveum. Plant Soil 336:485–497
Harwood CS, Rivelli M, Ornston LN (1984) Aromatic acids are chemoattractants for Pseudomonas putida. J Bacteriol 160:622–628
Huang L, Song L, Xia X, Mao W, Shi K, Zhou Y, Yu Q (2013) Plant-soil feedbacks and soil sickness: from mechanisms to application in agriculture. J Chem Ecol 39:232–242
Huang X, Chaparro JM, Reardon KF, Zhang R, Shen Q, Vivanco JM (2014) Rhizosphere interactions: root exudates, microbes, and microbial communities1. Botany 92:267–275
Inoue T, Shingaki R, Fukui K (2008) Inhibition of swarming motility of Pseudomonas aeruginosa by branched-chain fatty acids. FEMS Microbiol Lett 281:81–86
Jia Z, Yi J, Su Y, Shen H (2011) Autotoxic substances in the root exudates from continuous tobacco cropping. Allelopath J 27:87–96
Kamilova F, Kravchenko LV, Shaposhnikov AI, 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 19:250–256
Kato-Noguchi H, Ino T, Ota K (2008) Secretion of momilactone a from rice roots to the rhizosphere. J Plant Physiol 165:691–696
Li X, Ding C, Hua K, Zhang T, Zhang Y, Zhao L, Wang X (2014) Soil sickness of peanuts is attributable to modifications in soil microbes induced by peanut root exudates rather than to direct allelopathy. Soil Biol Biochem 78:149–159
Liaw S, Lai H, Wang B (2004) Modulation of swarming and virulence by fatty acids through the RsbA protein in Proteus mirabilis. Infect Immun 72:6836–6845
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 47:374–379
Liu X, Parales RE (2008) Chemotaxis of Escherichia coli to pyrimidines: a new role for the signal transducer tap. J Bacteriol 190:972–979
Liu Y, Zhang N, Qiu M, Feng H, Vivanco JM, Shen Q, Zhang R (2014) Enhanced rhizosphere colonization of beneficial Bacillus amyloliquefaciens SQR9 by pathogen infection. FEMS Microbiol Lett 353:49–56
Liu Y, Li X, Cai K, Cai L, Lu N, Shi J (2015) Identification of benzoic acid and 3-phenylpropanoic acid in tobacco root exudates and their role in the growth of rhizosphere microorganisms. Appl Soil Ecol 93:78–87
Mark GL, Dow JM, Kiely PD, Higgins H, Haynes J, Baysse C, Abbas A, Foley T, Franks A, Morrissey J, O'Gara F (2005) Transcriptome profiling of bacterial responses to root exudates identifies genes involved in microbe-plant interactions. Proc Natl Acad Sci U S A 102:17454–17459
McCully M (2005) The rhizosphere: the key functional unit in plant/soil/microbial interactions in the field. Implications for the understanding of allelopathic effects. Proceedings of the 4th World Congress on Allelopathy:21–26
Neal A, Ton J (2013) Systemic defense priming by Pseudomonas putida KT2440 in maize depends on benzoxazinoid exudation from the roots. Plant Signaling & Behavior 8:e22655. doi:10.4161/psb.22655
Neal AL, Ahmad S, Gordon-Weeks R, Ton J (2012) Benzoxazinoids in root exudates of maize attract Pseudomonas putida to the rhizosphere. PloS One 7:e35498. doi:10.1371/journal.pone.005498
Oku S, Komatsu A, Nakashimada Y, Tajima T, Kato J (2014) Identification of Pseudomonas fluorescens chemotaxis sensory proteins for malate, succinate, and fumarate, and their involvement in root colonization. Microbes Environ 29:413–419
Overhage J, Lewenza S, Marr AK, Hancock RE (2007) Identification of Genes Involved in Swarming Motility Using a Pseudomonas aeruginosa PAO1 Mini-Tn5-lux Mutant Library. J Bacteriol 189:2164–2169
Park S, Takano Y, Matsuura H, Yoshihara T (2004) Antifungal compounds from the root and root exudate of Zea mays. Biosci Biotechnol Biochem 68:1366–1368
Peeters E, Nelis HJ, Coenye T (2008) Comparison of multiple methods for quantification of microbial biofilms grown in microtiter plates. J Microbiol Methods 72:157–165
Porter SL, Wadhams GH, Armitage JP (2011) Signal processing in complex chemotaxis pathways. Nature reviews. Microbiology 9:153–165
Rudrappa T, Czymmek KJ, Paré PW, Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148:1547–1556
Singh T, Arora DK (2001) Motility and chemotactic response of Pseudomonas fluorescens toward chemoattractants present in the exudate of Macrophomina phaseolina. Microbiol Res 156:343–351
Somers E, Vanderleyden J, Srinivasan M (2004) Rhizosphere bacterial signalling: a love parade beneath our feet. Crit Rev Microbiol 30:205–240
Soto MJ, Fernández-Pascual M, Sanjuan J, Olivares J (2002) A fadD mutant of Sinorhizobium meliloti shows multicellular swarming migration and is impaired in nodulation efficiency on alfalfa roots. Mol Microbiol 43:371–382
Stougaard J (2000) Regulators and regulation of legume root nodule development. Plant Physiol 124:531–540
Sun S, Wang J, Zhu L, Liao D, Gu M, Ren L, Kapulnik Y, Xu G (2012) An active factor from tomato root exudates plays an important role in efficient establishment of mycorrhizal symbiosis. PloS One 7:e43385. doi:10.1371/journal.pone.0043385
Tan W, Wu Y (2003) Pathology of tobacco. Beijing, China
Tan S, Yang C, Mei X, Shen S, Raza W, Shen Q, Xu Y (2013) The effect of organic acids from tomato root exudates on rhizosphere colonization of Bacillus amyloliquefaciens T-5. Appl Soil Ecol 64:15–22
Timmusk S, Grantcharova N, Wagner EG (2005) Paenibacillus polymyxa invades plant roots and forms biofilms. Appl Environ Microbiol 71:7292–7300
Toyomasu T, Kagahara T, Okada K, Koga J, Hasegawa M, Mitsuhashi W, Sassa T, Yamane H (2008) Diterpene phytoalexins are biosynthesized in and exuded from the roots of rice seedlings. Biosci Biotechnol Biochem 72:562–567. doi:10.1271/bbb.70677
Tsoligkas AN, Bowen J, Winn M, Goss RJ, Overton TW, Simmons MJ (2012) Characterisation of spin coated engineered Escherichia coli biofilms using atomic force microscopy. Colloids Surf B: Biointerfaces 89:152–160
Wu D, Ding W, Zhang Y, Liu X, Yang L (2015a) Oleanolic acid induces the type III secretion system of Ralstonia solanacearum. Front Microbiol 6. doi:10.3389/fmicb.2015.01466
Wu K, Yuan S, Xun G, Shi W, Pan B, Guan H, Shen B, Shen Q (2015b) Root exudates from two tobacco cultivars affect colonization of Ralstonia solanacearum and the disease index. Eur J Plant Pathol 141:667–677
Xiao X, Cheng Z, Meng H, Khan MA, Li H (2012) Intercropping with garlic alleviated continuous cropping obstacle of cucumber in plastic tunnel. Acta Agriculturae Scandinavica, Section B-Soil & Plant Science 62:696–705. doi:10.1080/09064710.2012.697571
Yang S, Peng Q, San Francisco M, Wang Y, Zeng Q, Yang C (2008) Type III secretion system genes of Dickeya dadantii 3937 are induced by plant phenolic acids. PloS One 3:e2973. doi:10.1371/journal.pone.0002973
Yang M, Zhang Y, Qi L, Mei X, Liao J, Ding X, Deng W, Fan L, He X, Vivanco JM, Li C, Zhu Y, Zhu S (2014) Plant-plant-microbe mechanisms involved in soil-borne disease suppression on a maize and pepper intercropping system. PloS One 9:e115052. doi:10.1371/journal.pone.0115052
Yao J, Allen C (2006) Chemotaxis is required for virulence and competitive fitness of the bacterial wilt pathogen Ralstonia solanacearum. J Bacteriol 188:3697–3708
Ye S, Yu J, Peng Y, Zheng J, Zou L (2004) Incidence of Fusarium wilt in Cucumis sativus L. is promoted by cinnamic acid, an autotoxin in root exudates. Plant and Soil 263:143–150
Yu H, Liang H, Shen G, Sampietro DA, Gao X (2014) Effects of allelochemicals from tobacco root exudates on seed germination and seedling growth of tobacco. Allelopath J 33:107–120
Yuan J, Zhang N, Huang Q, Raza W, Li R, Vivanco JM, Shen Q (2015) Organic acids from root exudates of banana help root colonization of PGPR strain Bacillus amyloliquefaciens NJN-6. Scientific reports 5:13438. doi:10.1038/srep13438
Zhang F, Zhu Z, Yang X, Ran W, Shen Q (2013) Trichoderma harzianum T-E5 significantly affects cucumber root exudates and fungal community in the cucumber rhizosphere. Appl Soil Ecol 72:41–48
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 374:689–700
Zhao X, Zhen W, Qi Y, Liu X, Yin B (2009) Coordinated effects of root autotoxic substances and Fusarium oxysporum Schl. f. sp. fragariae on the growth and replant disease of strawberry. Frontiers of Agriculture in China 3:34–39. doi:10.1007/s11703–009–0006-1
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This research was financially supported by a grant from the China National Tobacco Corporation (110201202002).
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Li, S., Xu, C., Wang, J. et al. Cinnamic, myristic and fumaric acids in tobacco root exudates induce the infection of plants by Ralstonia solanacearum . Plant Soil 412, 381–395 (2017). https://doi.org/10.1007/s11104-016-3060-5
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DOI: https://doi.org/10.1007/s11104-016-3060-5