Genetic and Proteomic Analyses of a Xanthomonas campestris pv. campestris purC Mutant Deficient in Purine Biosynthesis and Virulence

Zhihui Yuan; Li Wang; Shutao Sun; Yao Wu; Wei Qian

doi:10.1016/j.jgg.2013.05.003

Volume 40 Issue 9

Sep. 2013

Turn off MathJax

Article Contents

Abstract

References

Article Navigation > Journal of Genetics and Genomics > 2013 > 40(9): 473-487

PDF( 1000 KB)

Genetic and Proteomic Analyses of a Xanthomonas campestris pv. campestris purC Mutant Deficient in Purine Biosynthesis and Virulence

doi: 10.1016/j.jgg.2013.05.003

Zhihui Yuan^{a, b, #},
Li Wang^{a, #},
Shutao Sun^c,
Yao Wu^a,
Wei Qian^a

a
State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China
b
University of Chinese Academy of Sciences, Beijing 100049, China
c
Center of Core Facility, Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China

More Information

Corresponding author: E-mail address: qianw@im.ac.cn (Wei Qian)
Received Date: 2013-03-11
Accepted Date: 2013-05-23
Rev Recd Date: 2013-05-21

Available Online: 2013-06-01

Publish Date: 2013-09-20

Abstract

Abstract

Bacterial proliferation in hosts requires activation of a number of housekeeping pathways, including purine de novo biosynthesis. Although inactivation of purine biosynthesis genes can attenuate virulence, it is unclear which biochemical or virulence factors are associated with the purine biosynthesis pathway in vivo. We report that inactivation of purC, a gene encoding phosphoribosylaminoimidazole-succinocarboxamide synthase, caused complete loss of virulence inXanthomonas campestris pv. campestris, the causal agent of black rot disease of cruciferous plants. The purC mutant was a purine auxotroph; it could not grow on minimal medium, whereas addition of purine derivatives, such as hypoxanthine or adenine plus guanine, restored growth of the mutant. The purC mutation also significantly enhanced the production of an unknown purine synthesis associated pigment and extracellular polysaccharides by the bacterium. In addition, comparative proteomic analyses of bacteria grown on rich and minimal media revealed that the purC mutation affected the expression levels of diverse proteins involved in purine and pyrimidine synthesis, carbon and energy metabolisms, iron uptake, proteolysis, protein secretion, and signal transduction. These results provided clues to understanding the contributions of purine synthesis to bacterial virulence and interactions with host immune systems.
- Purine biosynthesis,
- Virulence,
- Proteomics

These authors contributed equally to this work.

FullText(HTML)

References(54)

References

[1]	Alcantara, R.B., Read, R.D., Valderas, M.W. et al. Infect. Immun., 72 (2004),pp. 4911-4917
[2]	Andrews, S.C., Robinson, A.K., Rodriguez-Quinones, F. Bacterial iron homeostasis FEMS Microbiol. Rev., 27 (2003),pp. 215-237
[3]	Beyer, N.H., Roepstorff, P., Hammer, K. et al. Proteomics, 3 (2003),pp. 786-797
[4]	Bigot, A., Botton, E., Dubail, I. et al. Appl. Environ. Microbiol., 72 (2006),pp. 6623-6631
[5]	Bingel-Erlenmeyer, R., Kohler, R., Kramer, G. et al. A peptide deformylase-ribosome complex reveals mechanism of nascent chain processing Nature, 452 (2008),pp. 108-111
[6]	Buttner, D., Bonas, U. FEMS Microbiol. Rev., 34 (2010),pp. 107-133
[7]	Cattoir, V., Narasimhan, G., Skurnik, D. et al. MBio, 3 (2013),pp. e00410-e00412
[8]	Chatterjee, S., Sonti, R.V. Can. J. Microbiol., 51 (2005),pp. 575-581
[9]	Chiang, S.L., Mekalanos, J.J., Holden, D.W. Annu. Rev. Microbiol., 53 (1999),pp. 129-154
[10]	Clatworthy, A.E., Pierson, E., Hung, D.T. Targeting virulence: a new paradigm for antimicrobial therapy Nat. Chem. Biol., 3 (2007),pp. 541-548
[11]	da Silva, A.C., Ferro, J.A., Reinach, F.C. et al. Comparison of the genomes of two Xanthomonas pathogens with differing host specificities Nature, 417 (2002),pp. 459-463
[12]	Daum, R.S. N. Engl. J. Med., 359 (2008),pp. 85-87
[13]	Dow, J.M., Clarke, B.R., Milligan, D.E. et al. Appl. Environ. Microbiol., 56 (1990),pp. 2994-2998
[14]	Eriksson, S., Lucchini, S., Thompson, A. et al. Mol. Microbiol., 47 (2003),pp. 103-118
[15]	He, Y.W., Boon, C., Zhou, L. et al. Mol. Microbiol., 71 (2009),pp. 1464-1476
[16]	He, Y.W., Wu, J., Zhou, L. et al. Mol. Plant Microbe Interact., 24 (2011),pp. 948-957
[17]	Innes, R.W., Hirose, M.A., Kuempel, P.L. J. Bacteriol., 170 (1988),pp. 3793-3802
[18]	Jansen, A., Yu, J. Differential gene expression of pathogens inside infected hosts Curr. Opin. Microbiol., 9 (2006),pp. 138-142
[19]	Jenkins, A., Cote, C., Twenhafel, N. et al. Infect. Immun., 79 (2011),pp. 153-166
[20]	Klarsfeld, A.D., Goossens, P.L., Cossart, P. Mol. Microbiol., 13 (1994),pp. 585-597
[21]	Krewulak, K.D., Vogel, H.J. Structural biology of bacterial iron uptake Biochim. Biophys. Acta, 1778 (2008),pp. 1781-1804
[22]	Lan, L., Cheng, A., Dunman, P.M. et al. J. Bacteriol., 192 (2010),pp. 3068-3077
[23]	Liautard, J.P., Jubier-Maurin, V., Boigegrain, R.A. et al. Antimicrobials: targeting virulence genes necessary for intracellular multiplication Trends Microbiol., 14 (2006),pp. 109-113
[24]	Liu, G.Y., Nizet, V. Color me bad: microbial pigments as virulence factors Trends Microbiol., 17 (2009),pp. 406-413
[25]	Lowe, A.M., Beattie, D.T., Deresiewicz, R.L. Mol. Microbiol., 27 (1998),pp. 967-976
[26]	Lu, G.T., Tang, Y.Q., Li, C.Y. et al. J. Bacteriol., 191 (2009),pp. 3639-3648
[27]	Mansfield, J., Genin, S., Magori, S. et al. Top 10 plant pathogenic bacteria in molecular plant pathology Mol. Plant Pathol., 13 (2012),pp. 614-629
[28]	Marra, A. Targeting virulence for antibacterial chemotherapy: identifying and characterising virulence factors for lead discovery Drugs R. D., 7 (2006),pp. 1-16
[29]	Mazurkiewicz, P., Tang, C.M., Boone, C. et al. Signature-tagged mutagenesis: barcoding mutants for genome-wide screens Nat. Rev. Genet., 7 (2006),pp. 929-939
[30]	Mei, J.M., Nourbakhsh, F., Ford, C.W. et al. Mol. Microbiol., 26 (1997),pp. 399-407
[31]	Merrell, D.S., Hava, D.L., Camilli, A. Mol. Microbiol., 43 (2002),pp. 1471-1491
[32]	Mole, B.M., Baltrus, D.A., Dangl, J.L. et al. Global virulence regulation networks in phytopathogenic bacteria Trends Microbiol., 15 (2007),pp. 363-371
[33]	Park, Y.J., Song, E.S., Kim, Y.T. et al. FEMS Microbiol. Lett., 276 (2007),pp. 55-59
[34]	Pilatz, S., Breitbach, K., Hein, N. et al. Infect. Immun., 74 (2006),pp. 3576-3586
[35]	Poplawsky, A.R., Urban, S.C., Chun, W. Appl. Environ. Microbiol., 66 (2000),pp. 5123-5127
[36]	Price, M.N., Huang, K.H., Alm, E.J. et al. A novel method for accurate operon predictions in all sequenced prokaryotes Nucleic Acids Res., 33 (2005),pp. 880-892
[37]	Qian, W., Han, Z.J., He, C. Mol. Plant Microbe Interact., 21 (2008),pp. 151-161
[38]	Qian, W., Han, Z.J., Tao, J. et al. Mol. Plant Microbe Interact., 21 (2008),pp. 1128-1138
[39]	Qian, W., Jia, Y., Ren, S.X. et al. Genome Res., 15 (2005),pp. 757-767
[40]	Rediers, H., Rainey, P.B., Vanderleyden, J. et al. Microbiol. Mol. Biol. Rev., 69 (2005),pp. 217-261
[41]	Roberts, R.L., Metz, M., Monks, D.E. et al. Proc. Natl. Acad. Sci. USA, 100 (2003),pp. 6634-6639
[42]	Ryan, R.P., Vorholter, F.J., Potnis, N. et al. Nat. Rev. Microbiol., 9 (2011),pp. 344-355
[43]	Samant, S., Lee, H., Ghassemi, M. et al. Nucleotide biosynthesis is critical for growth of bacteria in human blood PLoS Pathog., 4 (2008),p. e37
[44]	Sambrook, F.F., Maniatis, T.
[45]	Schafer, A., Tauch, A., Jager, W. et al. Gene, 145 (1994),pp. 69-73
[46]	Smith, H. Trends Microbiol., 6 (1998),pp. 239-243
[47]	Song, Y., Liu, C.I., Lin, F.Y. et al. J. Med. Chem., 52 (2009),pp. 3869-3880
[48]	Symmons, M.F., Bokma, E., Koronakis, E. et al. The assembled structure of a complete tripartite bacterial multidrug efflux pump Proc. Natl. Acad. Sci. USA, 106 (2009),pp. 7173-7178
[49]	Tang, J.L., Liu, Y.N., Barber, C.E. et al. Mol. Gen. Genet., 226 (1991),pp. 409-417
[50]	Thammavongsa, V., Kern, J.W., Missiakas, D.M. et al. J. Exp. Med., 206 (2009),pp. 2417-2427
[51]	Vorholter, F.J., Schneiker, S., Goesmann, A. et al. J. Biotechnol., 134 (2008),pp. 33-45
[52]	Wu, H.J., Wang, A.H., Jennings, M.P. Discovery of virulence factors of pathogenic bacteria Curr. Opin. Chem. Biol., 12 (2008),pp. 93-101
[53]	Wu, T., Zhao, Z., Zhang, L. et al. Microb. Pathog., 51 (2011),pp. 69-76
[54]	Zrenner, R., Stitt, M., Sonnewald, U. et al. Pyrimidine and purine biosynthesis and degradation in plants Annu. Rev. Plant Biol., 57 (2006),pp. 805-836

Relative Articles

[1]	Ruizhen Yang, Ziyi Yang, Meng Xing, Yexing Jing, Yunwei Zhang, Kewei Zhang, Yun Zhou, Huixian Zhao, Weihua Qiao, Jiaqiang Sun. TaBZR1 enhances wheat salt tolerance via promoting ABA biosynthesis and ROS scavenging[J]. Journal of Genetics and Genomics. doi: 10.1016/j.jgg.2023.09.006
[2]	Weiya Xu, Yongming Chen, Bin Liu, Qiuyuan Li, Yilan Zhou, Xuanshuang Li, Weilong Guo, Zhaorong Hu, Zhenshan Liu, Mingming Xin, Yingyin Yao, Mingshan You, Huiru Peng, Zhongfu Ni, Jiewen Xing. TaANR1-TaMADS25 module regulates lignin biosynthesis and root development in wheat (Triticum aestivum L.)[J]. Journal of Genetics and Genomics. doi: 10.1016/j.jgg.2023.08.011
[3]	Yingying Meng, Chongnan Wang, Qiqi Li, Wenkai Ji, Jiangqi Wen, Kirankumar S. Mysore, Yanxi Pei, Lifang Niu, Hao Lin. DPB3 and DPB4 proteins regulate Medicago flowering and leaf anthocyanin biosynthesis[J]. Journal of Genetics and Genomics, 2023, 50(6): 450-453. doi: 10.1016/j.jgg.2023.01.007
[4]	Jiaqi Li, Juan Tian, Huan Cao, Mengli Pu, Xiaxia Zhang, Yanjun Yu, Zhi Wang, Zhaosheng Kong. VdMKK1-mediated cell wall integrity is essential for virulence in vascular wilt pathogen Verticillium dahliae[J]. Journal of Genetics and Genomics, 2023, 50(8): 620-623. doi: 10.1016/j.jgg.2023.03.001
[5]	Yu Luo, Wei Liu, Juan Sun, Zheng-Rong Zhang, Wei-Cai Yang. Quantitative proteomics reveals key pathways in the symbiotic interface and the likely extracellular property of soybean symbiosome[J]. Journal of Genetics and Genomics, 2023, 50(1): 7-19. doi: 10.1016/j.jgg.2022.04.004
[6]	Xiaoyang Wang, Huicong Meng, Yuxi Tang, Yashi Zhang, Yunxia He, Jinggeng Zhou, Xiangzong Meng. Phosphorylation of an ethylene response factor by MPK3/MPK6 mediates negative feedback regulation of pathogen-induced ethylene biosynthesis in Arabidopsis[J]. Journal of Genetics and Genomics, 2022, 49(8): 810-822. doi: 10.1016/j.jgg.2022.04.012
[7]	Hong Fang, Fan Zhang, Chongyang Zhang, Dan Wang, Shuangqian Shen, Feng He, Hui Tao, Ruyi Wang, Min Wang, Debao Wang, Xionglun Liu, Jie Luo, Guo-Liang Wang, Yuese Ning. Function of hydroxycinnamoyl transferases for the biosynthesis of phenolamides in rice resistance to Magnaporthe oryzae[J]. Journal of Genetics and Genomics, 2022, 49(8): 776-786. doi: 10.1016/j.jgg.2022.02.008
[8]	Shunqi Pei, Xuehui Wang, Xuan Wang, Hao Huang, Huaping Tao, Binghua Xie, Aifen Yang, Mengsheng Qiu, Zhou Tan. Aberrant nuclear lamina contributes to the malignancy of human gliomas[J]. Journal of Genetics and Genomics, 2022, 49(2): 132-144. doi: 10.1016/j.jgg.2021.08.013
[9]	Jinlong Wang, Xiahe Huang, Haitao Ge, Yan Wang, Weiyang Chen, Limin Zheng, Chengcheng Huang, Haomeng Yang, Lingyu Li, Na Sui, Yu Wang, Yuanya Zhang, Dandan Lu, Longfa Fang, Wu Xu, Yuqiang Jiang, Fang Huang, Yingchun Wang. The quantitative proteome atlas of a model cyanobacterium[J]. Journal of Genetics and Genomics, 2022, 49(2): 96-108. doi: 10.1016/j.jgg.2021.09.007
[10]	Youshang Zhao, Ting Jiang, Lei Li, Xiaotuo Zhang, Tianyu Yang, Cuimei Liu, Jinfang Chu, Binglian Zheng. The chromatin remodeling complex imitation of switch controls stamen filament elongation by promoting jasmonic acid biosynthesis in Arabidopsis[J]. Journal of Genetics and Genomics, 2021, 48(2): 123-133. doi: 10.1016/j.jgg.2021.02.003
[11]	Yugang Li, Weihui Li, Zhiwei Xie, Hui Xu, Zheng-Guo He. MpbR, an essential transcriptional factor for Mycobacterium tuberculosis survival in the host, modulates PIM biosynthesis and reduces innate immune responses[J]. Journal of Genetics and Genomics, 2019, 46(12): 575-589. doi: 10.1016/j.jgg.2019.12.002
[12]	Jie Ye, Danping Chen, Yue Yu, Liming Wang. Neuronal insulin receptor mediates a positive feedback regulation of insulin biosynthesis in Drosophila[J]. Journal of Genetics and Genomics, 2017, 44(2): 123-125. doi: 10.1016/j.jgg.2016.12.006
[13]	Jing Yang, Xiaomu Zhang, Yunqing Huang, Yuqi Feng, Yangsheng Li. OsCBL1 Modulates Lateral Root Elongation in Rice via Affecting Endogenous Indole-3-Acetic Acid Biosynthesis[J]. Journal of Genetics and Genomics, 2015, 42(6): 331-334. doi: 10.1016/j.jgg.2015.03.004
[14]	Changxin Ma, Yang Gao, Guoliang Chai, Hanxia Su, Niejun Wang, Yigang Yang, Chunbo Li, Di Miao, Wei Wu. Djrho2 is involved in regeneration of visual nerves in Dugesia japonica[J]. Journal of Genetics and Genomics, 2010, 37(11): 713-723. doi: 10.1016/S1673-8527(09)60089-8
[15]	Fang Kong, Cailin Ge, Xiaoping Fang, Rod J. Snowdon, Youping Wang. Characterization of seedling proteomes and development of markers to distinguish the Brassica A and C genomes[J]. Journal of Genetics and Genomics, 2010, 37(5): 333-340. doi: 10.1016/S1673-8527(09)60051-5
[16]	Yanfei Ren, Jun Lv, Hua Wang, Linchuan Li, Yufa Peng, Li-Jia Qu. A comparative proteomics approach to detect unintended effects in transgenic Arabidopsis[J]. Journal of Genetics and Genomics, 2009, 36(10): 629-639. doi: 10.1016/S1673-8527(08)60155-1
[17]	Xun Huang, James T. Warren, Lawrence I. Gilbert. New players in the regulation of ecdysone biosynthesis[J]. Journal of Genetics and Genomics, 2008, 35(1): 1-10. doi: 10.1016/S1673-8527(08)60001-6