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Journal of Integrative Agriculture  2020, Vol. 19 Issue (4): 906-920    DOI: 10.1016/S2095-3119(19)62883-2
Special Focus: Bleeding canker of pear-An emerging devastating disease Advanced Online Publication | Current Issue | Archive | Adv Search |
Genomic characteristics of Dickeya fangzhongdai isolates from pear and the function of type IV pili in the chromosome
CHEN Bin1, TIAN Yan-li1, ZHAO Yu-qiang2, WANG Yuan-jie1, CHUAN Jia-cheng3, LI Xiang3, HU Bai-shi
1 College of Plant Protection and Key Laboratory of Integrated Management of Crop Diseases and Pests, Ministry of Education, Nanjing Agricultural University, Nanjing 210095, P.R.China
2 Institute of Botany, Jiangsu Province and Chinese Academy of Sciences (Nanjing Botanical Garden Mem. Sun Yat-Sen)/Jiangsu Key Laboratory for the Research and Utilization of Plant Resources, Nanjing 210014, P.R.China
3 Charlottetown Laboratory, Canadian Food Inspection Agency, Charlottetown, PE C1A5T1, Canada
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Dickeya fangzhongdai, the causal agent of bleeding canker of pear, is a new member of the Dickeya genus and the only one that infects woody plants.  Recent studies have reclassified several Dickeya isolates as D. fangzhongdai, which were isolated from various environments, including water, Phalaenopsis sp. and Aglaonema sp.  To provide genomic characterization of D. fangzhongdai isolates from pear, the genomes of D. fangzhongdai strain JS5 (=China General Microbiological Culture Collection Center, CGMCC 1.15464T=DSM 101947T), along with two other isolates, LN1 and QZH3, were sequenced and compared to those of other Dickeya spp.  Homology greater than 99% was observed among three D. fangzhongdai strains.  Plasmid, type IV secretion system (T4SS) and type IV pili (TFPs) were found in genomes of D. fangzhongdai isolates.  Comparative analysis of the type III secretion systems (T3SS), type III secretion effectors (T3SE), plant cell wall degradation enzymes (PCWDE) and membrane transport proteins of Dickeya spp. showed some differences which might reflect the variations of virulence, phylogenetic and phenotypic characteristics of Dickeya spp.  In addition, deletion mutant of TFP in D. fangzhongdai JS5 showed no twitching motility and reduced virulence and biofilm formation.  The fingdings of the distinctive plasmid, T4SS and TFPs, as well as the differences of T3SE, PCWDE and membrane transport proteins make D. fangzhongdai isolates unique.  These results also suggested that acquisition of virulence genes by horizontal gene transfer might play some role in the genetic variation of D. fangzhongdai.
Keywords:  Dickeya fangzhongdai        comparative genomics        virulence        type IV pili  
Received: 13 November 2019   Accepted: 04 March 2020
Fund: This research was supported by the 111 International Cooperation Grant 2.0 (BP0719029) to Nanjing Agricultural University, China, from the Chinese government and Canadian Interdepartmental funding of Genomics Research and Development Initiatives (GRDI).
Corresponding Authors:  Correspondence HU Bai-shi, E-mail:; LI Xiang, E-mail:    
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CHEN Bin, TIAN Yan-li, ZHAO Yu-qiang, WANG Yuan-jie, CHUAN Jia-cheng, LI Xiang, HU Bai-shi. 2020. Genomic characteristics of Dickeya fangzhongdai isolates from pear and the function of type IV pili in the chromosome. Journal of Integrative Agriculture, 19(4): 906-920.

Alfano J R, Collmer A. 1997. The type III (Hrp) secretion pathway of plant pathogenic bacteria: Trafficking harpins, Avr proteins, and death. Journal of Bacteriology, 179, 5655–5662.
Ali? Š, Naglic T, Llop P, Toplak N, Koren S, Ravnikar M, Dreo T. 2015. Draft genome sequences of Dickeya sp. isolates B16 (NIB Z 2098) and S1 (NIB Z 2099) causing soft rot of Phalaenopsis orchids. Genome Announcements, 3, e00973-15.
Ali? Š, Pedron J, Dreo T, Van Gijsegem F. 2019. Genomic characterisation of the new Dickeya fangzhongdai species regrouping plant pathogens and environmental isolates. BMC Genomics, 20, 34.
Ali? Š, Van Gijsegem F, Pédron J, Ravnikar M, Dreo T. 2018. Diversity within the novel Dickeya fangzhongdai sp., isolated from infected orchids, water and pears. Plant Pathology, 67, 1612–1620.
Alvarez-Martinez C E, Christie P J. 2009. Biological diversity of prokaryotic type IV secretion systems. Microbiology and Molecular Biology Reviews, 73, 775–808.
Bahar O, Goffer T, Burdman S. 2009. Type IV pili are required for virulence, twitching motility, and biofilm formation of Acidovorax avenae subsp. citrulli. Molecular Plant-Microbe Interactions, 22, 909–920.
Bertani I, Passos da Silva D, Abbruscato P, Piffanelli P, Venturi V. 2013. Draft genome sequence of the plant pathogen Dickeya zeae DZ2Q, isolated from rice in Italy. Genome Announcements, 1, e00905-13.
Bertelli C, Laird M R, Williams K P, Lau B Y, Hoad G, Winsor G L, Brinkman F S L, Grp S F U R C. 2017. IslandViewer 4: Expanded prediction of genomic islands for larger-scale datasets. Nucleic Acids Research, 45, W30–W35.
Brady C L, Cleenwerck I, Denman S, Venter S N, Rodriguez-Palenzuela P, Coutinho T A, De Vos P. 2012. Proposal to reclassify Brenneria quercina (Hildebrand and Schroth 1967) Hauben et al. 1999 into a new genus, Lonsdalea gen. nov., as Lonsdalea quercina comb. nov., descriptions of Lonsdalea quercina subsp. quercina comb. nov., Lonsdalea quercina subsp. iberica subsp. nov. and Lonsdalea quercina subsp. britannica subsp. nov., emendation of the description of the genus Brenneria, reclassification of Dickeya dieffenbachiae as Dickeya dadantii subsp. dieffenbachiae comb. nov., and emendation of the description of Dickeya dadantii. International Journal of Systematic and Evolutionary Microbiology, 62, 1592–1602.
Carver T J, Rutherford K M, Berriman M, Rajandream M A, Barrell B G, Parkhill J. 2005. ACT: The artemis comparison tool. Bioinformatics, 21, 3422–3423.
Cascales E, Christie P J. 2003. The versatile bacterial type IV secretion systems. Nature Reviews Microbiology, 1, 137–149.
Chen X F, Zhang H L, Chen J. 2015. First report of Dickeya solani causing soft rot in imported bulbs of Hyacinthus orientalis in China. Plant Disease, 99, 155–155.
Coburn B, Sekirov I, Finlay B B. 2007. Type III secretion systems and disease. Clinical Microbiology Reviews, 20, 535–549.
Craig L, Li J. 2008. Type IV pili: Paradoxes in form and function. Current Opinion in Structural Biology, 18, 267–277.
Craig L, Pique M E, Tainer J A. 2004. Type IV pilus structure and bacterial pathogenicity. Nature Reviews Microbiology, 2, 363–378.
Felsenstein J. 1985. Confidence-limits on phylogenies - an approach using the bootstrap. Evolution, 39, 783–791.
Galan J E, Collmer A. 1999. Type III secretion machines: Bacterial devices for protein delivery into host cells. Science, 284, 1322–1328.
Glasner J D, Yang C H, Reverchon S, Hugouvieux-Cotte-Pattat N, Condemine G, Bohin J P, Van Gijsegem F, Yang S, Franza T, Expert D, Plunkett G 3rd, San Francisco M J, Charkowski A O, Py B, Bell K, Rauscher L, Rodriguez-Palenzuela P, Toussaint A, Holeva M C, He S Y, et al. 2011. Genome sequence of the plant-pathogenic bacterium Dickeya dadantii 3937. Journal of Bacteriology, 193, 2076–2077.
Golanowska M, Galardini M, Bazzicalupo M, Hugouvieux-Cotte-Pattat N, Mengoni A, Potrykus M, Slawiak M, Lojkowska E. 2015. Draft genome sequence of a highly virulent strain of the plant pathogen Dickeya solani, IFB0099. Genome Announcements, 3, e00109-15.
Hueck C J. 1998. Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiology and Molecular Biology Reviews, 62, 379–433.
Hugouvieux-Cotte-Pattat N, Jacot-des-Combes C, Briolay J. 2019. Dickeya lacustris sp. nov., a water-living pectinolytic bacterium isolated from lakes in France. International Journal of Systematic and Evolutionary Microbiology, 69, doi: 10.1099/ijsem.0.003208.
Jehl M A, Arnold R, Rattei T. 2011. Effective - a database of predicted secreted bacterial proteins. Nucleic Acids Research, 39, D591–D595.
Khayi S, Blin P, Pedron J, Chong T M, Chan K G, Moumni M, Helias V, Van Gijsegem F, Faure D. 2015. Population genomics reveals additive and replacing horizontal gene transfers in the emerging pathogen Dickeya solani. BMC Genomics, 16, 788.
Khayi S, Mondy S, Beury-Cirou A, Moumni M, Helias V, Faure D. 2014. Genome sequence of the emerging plant pathogen Dickeya solani strain RNS Genome Announcements, 2, e01270-13.
Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones S J, Marra M A. 2009. Circos: An information aesthetic for comparative genomics. Genome Research, 19, 1639–1645.
Kumar S, Stecher G,Tamura K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874.
Lawley T D, Klimke W A, Gubbins M J, Frost L S. 2003. F factor conjugation is a true type IV secretion system. FEMS Microbiology Letters, 224, 1–15.
Li B, Shi Y, Ibrahim M, Liu H, Shan C, Wang Y, Kube M, Xie G L, Sun G. 2012. Genome sequence of the rice pathogen Dickeya zeae strain ZJU1202. Journal of Bacteriology, 194, 4452–4453.
Li, M, Shen X, Yan J, Han H, Zheng B, Liu D, Cheng H, Zhao Y, Rao X, Wang C, Tang J, Hu F, Gao G F. 2011. GI-type T4SS-mediated horizontal transfer of the 89K pathogenicity island in epidemic Streptococcus suis serotype 2. Molecular Microbiology, 79, 1670–1683.
Lombard V, Golaconda Ramulu H, Drula E, Coutinho P M, Henrissat B. 2014. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Research, 42, D490–D495.
Lowe T M, Eddy S R. 1997. tRNAscan-SE: A program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Research, 25, 955–964.
Meier-Kolthoff J P, Auch A F, Klenk H P, Goker M. 2013. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics, 14, 60.
Ng S Y, Wu J, Nair D B, Logan S M, Robotham A, Tessier L, Kelly J F, Uchida K, Aizawa S, Jarrell K F. 2011. Genetic and mass spectrometry analyses of the unusual type IV-like pili of the archaeon Methanococcus maripaludis. Journal of Bacteriology, 193, 804–814.
Niu X N, Wei Z Q, Zou H F, Xie G G, Wu F, Li K J, Jiang W, Tang J L, He Y Q. 2015. Complete sequence and detailed analysis of the first indigenous plasmid from Xanthomonas oryzae pv. oryzicola. BMC Microbiology, 15, 233.
Parkinson N, DeVos P, Pirhonen M, Elphinstone J. 2014. Dickeya aquatica sp. nov., isolated from waterways. International Journal of Systematic and Evolutionary Microbiology, 64, 2264–2266.
Pritchard L, Humphris S, Baeyen S, Maes M, Van Vaerenbergh J, Elphinstone J, Saddler G, Toth I K. 2013a. Draft genome sequences of four Dickeya dianthicola and four Dickeya solani strains. Genome Announcements, 1, e00087-12.
Pritchard L, Humphris S, Saddler G S, Elphinstone J G, Pirhonen M, Toth I K. 2013b. Draft genome sequences of 17 isolates of the plant pathogenic bacterium Dickeya. Genome Announcements, 1, e00978-13.
Raoul des Essarts Y, Mondy S, Helias V, Faure D. 2015. Genome sequence of the potato plant pathogen Dickeya dianthicola strain RNS04.9. Genome Announcements, 3, e00581-15.
Remaut H, Waksman G. 2004. Structural biology of bacterial pathogenesis. Current Opinion in Structural Biology, 14, 161–170.
Richter M, Rossello-Mora R. 2009. Shifting the genomic gold standard for the prokaryotic species definition. Proceedings of the National Academy of Sciences of the United States of America, 106, 19126–19131.
Saier Jr M H, Reddy V S, Tsu B V, Ahmed M S, Li C, Moreno-Hagelsieb G. 2016. The transporter classification database (TCDB): Recent advances. Nucleic Acids Research, 44, D372–D379.
Saier Jr M H, Tran C V, Barabote R D. 2006. TCDB: The Transporter Classification Database for membrane transport protein analyses and information. Nucleic Acids Research, 34, D181–D186.
Saier Jr M H, Yen M R, Noto K, Tamang D G, Elkan C. 2009.The Transporter Classification Database: Recent advances. Nucleic Acids Research, 37, D274–D278.
Saier M R, Tamang D, Vastermark A. 2014. The transporter classification database. Nucleic Acids Research, 42, D251–D258.
Saitou N, Nei M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406–425.
Samson R, Legendre J B, Christen R, Fischer-Le Saux M, Achouak W, Gardan L. 2005. Transfer of Pectobacterium chrysanthemi (Burkholder et al. 1953) Brenner et al. 1973 and Brenneria paradisiaca to the genus Dickeya gen. nov as Dickeya chrysanthemi comb. nov and Dickeya paradisiaca comb. nov and delineation of four novel species, Dickeya dadantii sp nov., Dickeya dianthicola sp nov., Dickeya dieffenbachiae sp nov and Dickeya zeae sp nov. International Journal of Systematic and Evolutionary Microbiology, 55, 1415–1427.
Scherzinger E, Lurz R, Otto S, Dobrinski B. 1992. In vitro cleavage of double- and single-stranded DNA by plasmid RSF1010-encoded mobilization proteins. Nucleic Acids Research, 20, 41–48.
Scott J R, Zahner D. 2006. Pili with strong attachments: Gram-positive bacteria do it differently. Molecular Microbiology, 62, 320–330.
Tian Y L, Zhao Y Q, Yuan X L, Yi J P, Fan J Q, Xu Z G, Hu B S, De Boer S H, Li X. 2016. Dickeya fangzhongdai sp. nov., a plant-pathogenic bacterium isolated from pear trees (Pyrus pyrifolia). International Journal of Systematic and Evolutionary Microbiology, 66, 2831–2835.
Wang Y, Zhang Q, Sun M A, Guo D. 2011. High-accuracy prediction of bacterial type III secreted effectors based on position-specific amino acid composition profiles. Bioinformatics, 27, 777–784.
van der Wolf J M, Nijhuis E H, Kowalewska M J, Saddler G S, Parkinson N, Elphinstone J G, Pritchard L, Toth I K, Lojkowska E, Potrykus M, Waleron M, De Vos P, Cleenwerck I, Pirhonen M, Garlant L, Helias V, Pothier J F, Pfluger V, Duffy B, Tsror L, et al. 2014. Dickeya solani sp. nov., a pectinolytic plant-pathogenic bacterium isolated from potato (Solanum tuberosum). International Journal of Systematic and Evolutionary Microbiology, 64, 768–774.
Yin G Y, Xu Y G. 1973. Study on the occurrence and control of the bleeding canker of pear. Xuzhou Horticulture, 1, 15–19. (in Chinese)
Zuckerkandl E. 1965. Evolutionary divergence and convergence in proteins. Evolving Genes aud Proteins, doi: 10.1016/B978-1-4832-2734-4.50017-6
Zhang J X, Hu J, Shen H F, Zhang Y C, Sun D, Pu X M, Yang Q Y, Fan Q R, Lin B R. 2018. Genomic analysis of the Phalaenopsis pathogen Dickeya sp. PA1, representing the emerging species Dickeya fangzhongdai. BMC Genomics, 19, 782.
Zhang J X, Lin B R, Shen H F, Pu X M. 2013. Genome sequence of the banana pathogen Dickeya zeae strain MS1, which causes bacterial soft rot. Genome Announcements, 1, e00317-13.
Zhao Y Q, Tian Y L, Li X, Hu B S. 2018. Complete genome sequence of a Dickeya fangzhongdai type strain causing bleeding canker of pear tree trunks. Genome Announcements, 6, e00177-18.
Zhou J N, Cheng Y Y, Lv M F, Liao L S, Chen Y F, Gu Y F, Liu S Y, Jiang Z D, Xiong Y Y, Zhang L H. 2015. The complete genome sequence of Dickeya zeae EC1 reveals substantial divergence from other Dickeya strains and species. BMC Genomics, 16, 571.
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