Current Science

Open Access Open Access  Restricted Access Subscription Access

Biological Control of Potato Tuber Soft Rot using N-Acyl-L-Homoserine Lactone-Degrading Endophytic Bacteria


Affiliations
1 Agricultural Genetics Institute, Pham Van Dong, Tu Liem, Hanoi, Viet Nam
2 Soils and Fertilizers Research Institute, Dong Ngac, Tu Liem, Hanoi, Viet Nam
3 Ministry of Agriculture and Rural Development, Ngoc Ha, Ba Dinh, Hanoi, Viet Nam
4 Kyushu University, Hakozaki, Higashi-ku, Fukuoka 812-8581, Japan
 

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
Notifications
Font Size

  • 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: 326

PDF Views: 112




  • Biological Control of Potato Tuber Soft Rot using N-Acyl-L-Homoserine Lactone-Degrading Endophytic Bacteria

Abstract Views: 326  |  PDF Views: 112

Authors

Nguyen Thanh Ha
Agricultural Genetics Institute, Pham Van Dong, Tu Liem, Hanoi, Viet Nam
Tran Quang Minh
Soils and Fertilizers Research Institute, Dong Ngac, Tu Liem, Hanoi, Viet Nam
Pham Xuan Hoi
Agricultural Genetics Institute, Pham Van Dong, Tu Liem, Hanoi, Viet Nam
Nguyen Thi Thanh Thuy
Ministry of Agriculture and Rural Development, Ngoc Ha, Ba Dinh, Hanoi, Viet Nam
Naruto Furuya
Kyushu University, Hakozaki, Higashi-ku, Fukuoka 812-8581, Japan
Hoang Hoa Long
Agricultural Genetics Institute, Pham Van Dong, Tu Liem, Hanoi, Viet Nam

Abstract


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.

References





DOI: https://doi.org/10.18520/cs%2Fv115%2Fi10%2F1921-1927