Open Access
Subscription Access
Biological Control of Potato Tuber Soft Rot using N-Acyl-L-Homoserine Lactone-Degrading Endophytic Bacteria
Pectobacterium carotovorum (Pc) causing potato tuber soft rot uses N-acyl-L-homoserine lactones (AHLs) to control the production of virulence factors via quorum sensing (QS). Some bacteria produce enzymes to inactivate the AHL signals of pathogenic bacteria via a phenomenon known as quorum quenching. One hundred bacterial isolates from potato tubers were screened for AHL-degrading activity using biosensor strain Chromobacterium violaceum CV026. Of these isolates, 20 were able to inactivate AHLs from the pathogenic bacteria in vitro. Of the 20 isolates, 6 attenuated tissue maceration of potato tubers by Pc. Suppression of tuber soft rot was observed even when these isolates were applied 24 h after the pathogen was introduced. Their colonization in tubers was approximately 103–104 cfu/g tuber, 7 days after inoculation. These isolates were identified as Bacillus sp., Variovorax sp., Variovorax paradoxus and Agrobacterium tumefaciens. Four of these isolates showed putative AHL-lactonase activity and provided the most significant protection against Pc. Therefore, AHL-degrading endophytic bacteria can be utilized as a novel biocontrol agent of potato tuber soft rot in Vietnam.
Keywords
AHL, Pectobacterium carotovorum, Potato Tuber Soft Rot, Quorum Sensing, Quorum Quenching.
User
Font Size
Information
- Fuqua, W. C., Winans, S. C. and Greenberg, E. P., Quorum sensing in bacteria: The LuxR/LuxI family of cell density-responsive transcriptional regulators. J. Bacteriol., 1994, 176, 269–275.
- Ma, B. et al., Host range and molecular phylogenies of the soft rot enterobacterial genera Pectobacterium and Dickeya. Phytopathology, 2007, 97, 1150–1163.
- Perombelon, M. C. M., Potato diseases caused by soft rot Erwinias: an overview of pathogenesis. Plant Pathol., 2002, 51, 1–12.
- Jones, S. et al., The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa. EMBO J., 1993, 12, 2477–2482.
- Dong, Y. H., Xu, J. L., Li, X. Z. and Zhang, L. H., AiiA, an enzyme that inactivates the acylhomoserine lactone quorumsensing signal and attenuates the virulence of Erwinia carotovora. Proc. Natl. Acad. Sci. USA, 2000, 97, 3526–3531.
- Alagarasan, G., Aswathy, K. S. and Madhaiyan, M., Shoot the message, not the messenger – combating pathogenic virulence in plants by inhibiting quorum sensing mediated signaling molecules. Front. Plant Sci., 2017, 8, 556; doi:10.3389/fpls.2017.00556.
- Teplistki, M., Robinson, J. B. and Bauer, J. W., Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviours in associated bacteria. Mol. Plant Microbe Interact., 2000, 13, 637– 648.
- Uroz, S. and Heinonsalo, J., Degradation of N-acyl homoserine lactone quorum sensing signal molecules by forest ischolar_main-associated fungi. FEMS Microbiol. Ecol., 2008, 65, 271–278.
- Morohoshi, T., Someya, N. and Ikeda, T., Novel N-acylhomoserin lactone-degrading bacteria isolate from the leaf surface of Solanum tuberosum and their quorum quenching properties. Biosci. Biotechnol. Biochem., 2009, 73, 2124–2127.
- Ma, A., Lv, D., Zhuang, X. and Zhuang, G., Quorum quenching in culturable phyllosphere bacteria from tobacco. Int. J. Mol. Sci., 2013, 14, 14607–14619.
- Jafra, S., Przysowa, J., Czajkowski, R., Michta, A., Garbeva, P. and Vander Wolf, J. M., Detection and characterization of bacteria from the potato rhizosphere degrading N-acyl-homoserine lactone. Can. J. Microbiol., 2006, 52, 1006–1015.
- Zamani, M., Behboudi, K. and Ahmadzadeh, M., Quorum quenching by Bacillus cereus U92: A double-edged sword in biological control of plant diseases. Biocon. Sci. Technol., 2013, 23, 555– 573.
- Dong, Y. H., Wang, L. H., Xu, J. L., Zhang, H. B., Zhang, X. F., and Zhang, L. H., Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature, 2001, 411, 813–817.
- Hallmann, J., Quadt-Hallmann, A., Mahaffee, W. F. and Kloepper, J. W., Bacterial endophytes in agricultural crops. Can. J. Microbiol., 1997, 43(10), 895–914.
- Liu, H., Carvalhais, L. C., Crawford, M., Singh, E., Dennis, P. G., Pieterse, C. M. J. and Schenk, P. M., Inner plant values: diversity, colonization and benefits from endophytic bacteria. Front. Microbiol., 2017, 8, 2552; doi:10.3389/fmicb.2017.02552.
- Shekhawat, G. S., Piplani, S. and Ansari, M. M., Endophytic bacterial flora of potato plant in relation to soft rot disease. Indian Phytopathol., 1984, 37, 501–505.
- Sturz, A. V., Christie, B. R., Matheson, B. G., Arsenault, W. J. and Buchanan, N. A., Endophytic bacterial communities in the periderm of potato tubers and their potential to improve resistance to soil-borne plant pathogens. Plant Pathol., 1999, 48, 360–369.
- Chen, C., Bauske, E. M., Musson, G., Rodríguez-Kabana, R. and Kloepper, J. W., Biological control of Fusarium wilt on cotton by use of endophytic bacteria. Biol. Control., 1995, 5, 83–91.
- Ha, N. T. T., Dung, N. V., Ha, N. T., Hoi, P. X., Gioi, D. H. and Long, H. H., Isolation and characterization of AHL-producing bacterial isolates and their pathogenesis in potato tuber. J. Agric. Rural Dev. (In Vietnamese), 2014, 24, 11–18.
- Kato, T., Morohoshi, T., Tsushima, S. and Ikeda, T., Characterization of three types of Quorum-sensing mutants in Burkholderia glumae strains isolated in Japan. J. Agric. Sci., 2014, 6, 7.
- McClean, K. H. et al., Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acyl homoserine lactones. Microbiology, 1997, 143, 3703–3711.
- Morohoshi, T., Kato, M., Fukamachi, K., Kato, N. and Ikeda, T., N-Acyl homoserine lactone regulates violacein production in Chromobacterium violaceum type strain ATCC12472. FEMS Microbiol. Lett., 2008, 279, 124–130.
- Long, H. H., Furuya, N., Kurose, D., Takeshita, M. and Takanami, Y., Isolation of endophytic bacteria from Solanum sp and their antibacterial activity against plant pathogenic bacteria. J. Fac. Agric., Kyushu Univ., 2003, 48, 21–28.
- Long, H. H., Schmidt, D. D. and Baldwin, I. T., Native bacterial endophytes promote host growth in a species-specific manner; phytohormone manipulations do not result in common growth responses. PLoS ONE, 2008, 3(7), e2702; doi:10.1371/journal.pone.0002702.
- Diallo, M. D. et al., Phylogenetic analysis of partial bacterial 16S rDNA sequences of tropical grass pasture soil under Acacia tortilis subsp. raddiana in Senegal. Syst. Appl. Microbiol., 2004, 27, 238–252.
- Chen, W. Y. and Echandi, E., Effects of a virulent bacteriocinproducing strains of Pseudomonas solanacearum on the control of bacterial wilt of tobacco. Plant Pathol., 1984, 33, 245–253.
- Wakinoto, S., Hirayae, K., Tsuchiya, K., Kushirna, Y., Furuya, N., and Matsuyama, N., Production of antibiotics by plant pathogenic Pseudomonads. Ann. Phytopath. Soc. Jpn., 1986, 52, 835–842.
- Molina, L., Constantinescu, F., Michel, L., Reimmann, C., Duffy, B. and Défago, G., Degradation of pathogen quorum-sensing molecules by soil bacteria: a preventive and curative biological control mechanism. FEMS Microbiol. Ecol., 2003, 1522, 1–11.
- Inglis, D. A., Schroeder, B. K. and Johnson, D. A., Bacterial Soft Rot and Lenticel Spot on Potato Tubers. Washington State University Extension Fact Sheet FS066E, 2011.
- Sturz, A. V. and Matheson, B. G., Populations of endophytic bacteria which influence host-resistance to Erwinia induced bacterial soft rot in potato tubers. Plant Soil, 1996, 184, 265–271.
- Kalia, V. C., Quorum sensing inhibitors: An overview. Biotechnol. Adv., 2013, 31, 224–245.
- Dong, Y. H., Wang, L. H., Xu, J. L., Zhang, H. B., Zhang, X. F., and Zhang, L. H., Quenching quorum-sensing-dependent bacterial infection by an N-acyl homoserine lactonase. Nature, 2001, 411, 813–817.
- Lee, S. J., Park, S. Y., Lee, J. J., Yum, D. Y., Koo, B. T. and Lee, J. K., Genes encoding the N-acyl homoserine lactone-degrading enzyme are widespread in many subspecies of Bacillus thuringiensis. Appl. Environ. Microbiol., 2002, 68, 3919–3924.
- Alymanesh, M. R., Taheri, P. and Tarighi, S., Pseudomonas as a frequent and important quorum quenching bacterium with biocontrol capability against many phytopathogens. Biocontrol Sci. Technol., 2016, 26, 1719–1735.
- Rashid, R., Morohoshi, T., Someya, N. and Ikeda, T., Degradation of N-acyl homoserine lactone quorum sensing signaling molecules by potato ischolar_main surface-associated Chryseobacterium strains. Microbes Environ., 2011, 26, 144–148.
- Han, J. I. et al., Complete genome sequence of the metabolically versatile plant growth-promoting endophyte Variovorax paradoxus S110. J. Bacteriol., 2011, 193, 1183–1190.
- Belimov, A. A., Dodd, I. C., Hontzeas, N., Theobald, J. C., Safronova, V. I. and Davies, W. J., Rhizosphere bacteria containing 1-aminocyclo-propane-1-carboxylate deaminase increase yield of plants grown in drying soil via both local and systemic hormone signaling. New Phytol., 2009, 181, 413–423.
- Belimov, A. A., Hontzeas, N., Safronova, V. I., Demchinskaya, S. V., Piluzza, G., Bullitta, S. and Glick, B. R., Cadmium-tolerant plant growth-promoting bacteria associated with the ischolar_mains of Indian mustard (Brassica juncea L. Czern.). Soil Biol. Biochem., 2005, 37, 241–250.
- Garge, S. S. and Nerurkar, A. S., Evaluation of quorum quenching Bacillus spp. for their biocontrol traits against Pectobacterium carotovorum subsp. carotovorum causing soft rot. Biocatal. Agric. Biotechnol., 2017, 9, 48–57.
- Garge, S. S. and Nerurkar, A. S., Attenuation of quorum sensing regulated virulence of Pectobacterium carotovorum subsp. carotovorum through an AHL lactonase produced by Lysinibacillus sp. Gs50. PLoS ONE, 2016, 11(12), e0167344; doi:10.1371/journal.pone.0167344.
Abstract Views: 315
PDF Views: 110