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Two-component signal transduction systems and regulation of virulence factors in Xanthomonas: a perspective

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Frontiers in Biology

Abstract

Two-component signal transduction systems (TCSTSs), consisting of a histidine kinase and a response regulator, play a critical role in regulating virulence gene expression in Gram-negative phytopathogenic bacteria Xanthomonas spp.. To date, 12 TCSTS genes have been identified, accounting for approximately 10% of the TCSTS genes in each genome that have been experimentally identified to be related to pathogenesis. These TCSTSs modulate the expression of a number of virulence factors through diverse molecular mechanisms such as interacting with DNA, protein-binding and involvement in second messenger metabolism, which generates a high level of regulatory versatility. Here we summarize the current knowledge in this field and discuss the emerging themes and remaining questions that are important in deciphering the signaling network of TCSTSs in Xanthomonas.

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References

  • Alfano J R, Collmer A (2004). Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu Rev Phytopathol, 42: 385–414

    Article  PubMed  CAS  Google Scholar 

  • Andrade MO, Alegria MC, Guzzo C R, Docena C, Rosa MC, Ramos C H, Farah C S (2006). The HD-GYP domain of RpfG mediates a direct linkage between the Rpf quorum-sensing pathway and a subset of diguanylate cyclase proteins in the phytopathogen Xanthomonas axonopodis pv citri. Mol Microbiol, 62(2): 537–551

    Article  PubMed  CAS  Google Scholar 

  • Barakat M, Ortet P, Jourlin-Castelli C, Ansaldi M, Méjean V, Whitworth D E (2009). P2CS: a two-component system resource for prokaryotic signal transduction research. BMC Genomics, 10: 315

    Article  PubMed  CAS  Google Scholar 

  • Burdman S, Shen Y, Lee S W, Xue Q, Ronald P (2004). RaxH/RaxR: a two-component regulatory system in Xanthomonas oryzae pv. oryzae required for AvrXa21 activity. Mol Plant Microbe Interact, 17(6): 602–612

    Article  PubMed  CAS  Google Scholar 

  • Büttner D, Bonas U (2010). Regulation and secretion of Xanthomonas virulence factors. FEMS Microbiol Rev, 34(2): 107–133

    Article  PubMed  CAS  Google Scholar 

  • Chatterjee S, Wistrom C, Lindow S E (2008). A cell-cell signaling sensor is required for virulence and insect transmission of Xylella fastidiosa. Proc Natl Acad Sci U S A, 105(7): 2670–2675

    Article  PubMed  Google Scholar 

  • da Silva A C, Ferro J A, Reinach F C, Farah C S, Furlan L R, Quaggio R B, Monteiro-Vitorello C B, Van Sluys MA, Almeida N F, Alves LM, do Amaral A M, Bertolini M C, Camargo L E, Camarotte G, Cannavan F, Cardozo J, Chambergo F, Ciapina L P, Cicarelli R M, Coutinho L L, Cursino-Santos J R, El-Dorry H, Faria J B, Ferreira A J, Ferreira R C, Ferro M I, Formighieri E F, Franco M C, Greggio C C, Gruber A, Katsuyama A M, Kishi L T, Leite R P, Lemos E G, Lemos M V, Locali E C, Machado M A, Madeira A M, Martinez-Rossi N M, Martins E C, Meidanis J, Menck C F, Miyaki C Y, Moon D H, Moreira L M, Novo M T, Okura V K, Oliveira M C, Oliveira V R, Pereira H A, Rossi A, Sena J A, Silva C, de Souza R F, Spinola L A, Takita M A, Tamura R E, Teixeira E C, Tezza R I, Trindade dos Santos M, Truffi D, Tsai S M, White F F, Setubal J C, Kitajima J P (2002). Comparison of the genomes of two Xanthomonas pathogens with differing host specificities. Nature, 417(6887): 459–463

    Article  PubMed  Google Scholar 

  • da Silva F G, Shen Y, Dardick C, Burdman S, Yadav R C, de Leon A L, Ronald P C (2004). Bacterial genes involved in type I secretion and sulfation are required to elicit the rice Xa21-mediated innate immune response. Mol Plant Microbe Interact, 17(6): 593–601

    Article  PubMed  Google Scholar 

  • Dekkers L C, Bloemendaal C J, de Weger L A, Wijffelman C A, Spaink H P, Lugtenberg B J (1998). A two-component system plays an important role in the root-colonizing ability of Pseudomonas fluorescens strain WCS365. Mol Plant Microbe Interact, 11(1): 45–56

    Article  PubMed  CAS  Google Scholar 

  • Dow J M, Crossman L, Findlay K, He Y Q, Feng J X, Tang J L (2003). Biofilm dispersal in Xanthomonas campestris is controlled by cellcell signaling and is required for full virulence to plants. Proc Natl Acad Sci U S A, 100(19): 10995–11000

    Article  PubMed  CAS  Google Scholar 

  • Dow J M, Daniels M J (1994). Pathogenicity determinants and global regulation of pathogenicity of Xanthomonas campestris pv. campestris. Curr Top Microbiol Immunol, 192: 29–41

    PubMed  CAS  Google Scholar 

  • Dow M (2008). Diversification of the function of cell-to-cell signaling in regulation of virulence within plant pathogenic xanthomonads. Sci Signal, 1(21): pe23

    Article  PubMed  Google Scholar 

  • Flor H H (1974). Current status of the gene-for-gene concept. Annu Rev Phytopathol, 9: 275–296

    Article  Google Scholar 

  • Furutani A, Tsuge S, Ohnishi K, Hikichi Y, Oku T, Tsuno K, Inoue Y, Ochiai H, Kaku H, Kubo Y (2004). Evidence for HrpXo-dependent expression of type II secretory proteins in Xanthomonas oryzae pv. oryzae. J Bacteriol, 186(5): 1374–1380

    Article  PubMed  CAS  Google Scholar 

  • Galperin M Y (2005). A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. BMC Microbiol, 5: 35

    Article  PubMed  CAS  Google Scholar 

  • Gao R, Stock A M (2009). Biological insights from structures of two-component proteins. Annu Rev Microbiol, 63: 133–154

    Article  PubMed  CAS  Google Scholar 

  • Goodman A L, Merighi M, Hyodo M, Ventre I, Filloux A, Lory S (2009). Direct interaction between sensor kinase proteins mediates acute and chronic disease phenotypes in a bacterial pathogen. Genes Dev, 23(2): 249–259

    Article  PubMed  CAS  Google Scholar 

  • Gotoh Y, Eguchi Y, Watanabe T, Okamoto S, Doi A, Utsumi R (2010). Two-component signal transduction as potential drug targets in pathogenic bacteria. Curr Opin Microbiol, 13(2): 232–239

    Article  PubMed  CAS  Google Scholar 

  • Goulian M (2010). Two-component signaling circuit structure and properties. Curr Opin Microbiol, 13(2): 184–189

    Article  PubMed  CAS  Google Scholar 

  • Grebe T W, Stock J B (1999). The histidine protein kinase superfamily. Adv Microb Physiol, 41: 139–227

    Article  PubMed  CAS  Google Scholar 

  • Gudesblat G E, Torres P S, Vojnov A A (2009). Xanthomonas campestris overcomes Arabidopsis stomatal innate immunity through a DSF cell-to-cell signal-regulated virulence factor. Plant Physiol, 149(2): 1017–1027

    Article  PubMed  CAS  Google Scholar 

  • He Y W, Boon C, Zhou L, Zhang L H (2009). Co-regulation of Xanthomonas campestris virulence by quorum sensing and a novel two-component regulatory system RavS/RavR. Mol Microbiol, 71(6): 1464–1476

    Article  PubMed  CAS  Google Scholar 

  • He Y W, Ng A Y, Xu M, Lin K, Wang L H, Dong Y H, Zhang L H (2007). Xanthomonas campestris cell-cell communication involves a putative nucleotide receptor protein Clp and a hierarchical signalling network. Mol Microbiol, 64(2): 281–292

    Article  PubMed  CAS  Google Scholar 

  • He Y W, Wang C, Zhou L, Song H, Dow J M, Zhang L H (2006). Dual signaling functions of the hybrid sensor kinase RpfC of Xanthomonas campestris involve either phosphorelay or receiver domain-protein interaction. J Biol Chem, 281(44): 33414–33421

    Article  PubMed  CAS  Google Scholar 

  • He YW, Zhang L H (2008). Quorum sensing and virulence regulation in Xanthomonas campestris. FEMS Microbiol Rev, 32(5): 842–857

    Article  PubMed  CAS  Google Scholar 

  • Hefti M H, Françoijs K J, de Vries S C, Dixon R, Vervoort J (2004). The PAS fold. A redefinition of the PAS domain based upon structural prediction. Eur J Biochem, 271(6): 1198–1208

    Article  PubMed  CAS  Google Scholar 

  • Hõrak R, Ilves H, Pruunsild P, Kuljus M, Kivisaar M (2004). The ColRColS two-component signal transduction system is involved in regulation of Tn4652 transposition in Pseudomonas putida under starvation conditions. Mol Microbiol, 54(3): 795–807

    Article  PubMed  CAS  Google Scholar 

  • Huang D L, Tang D J, Liao Q, Li X Q, He Y Q, Feng J X, Jiang B L, Lu G T, Tang J L (2009). The Zur of Xanthomonas campestris is involved in hypersensitive response and positively regulates the expression of the hrp cluster via hrpX but not hrpG. Mol Plant Microbe Interact, 22(3): 321–329

    Article  PubMed  CAS  Google Scholar 

  • Jones J D, Dangl J L (2006). The plant immune system. Nature, 444(7117): 323–329

    Article  PubMed  CAS  Google Scholar 

  • Laub M T, Goulian M (2007). Specificity in two-component signal transduction pathways. Annu Rev Genet, 41: 121–145

    Article  PubMed  CAS  Google Scholar 

  • Leduc J L, Roberts G P (2009). Cyclic di-GMP allosterically inhibits the CRP-like protein (Clp) of Xanthomonas axonopodis pv. citri. J Bacteriol, 191(22): 7121–7122

    Article  PubMed  CAS  Google Scholar 

  • Lee SW, Han SW, Bartley L E, Ronald P C (2006). From the Academy: Colloquium review. Unique characteristics of Xanthomonas oryzae pv. oryzae AvrXa21 and implications for plant innate immunity. Proc Natl Acad Sci U S A, 103(49): 18395–18400

    Article  PubMed  CAS  Google Scholar 

  • Lee S W, Han S W, Sririyanum M, Park C J, Seo Y S, Ronald P C (2009). A type I-secreted, sulfated peptide triggers XA21-mediated innate immunity. Science, 326(5954): 850–853

    Article  PubMed  CAS  Google Scholar 

  • Lee S W, Jeong K S, Han S W, Lee S E, Phee B K, Hahn T R, Ronald P (2008). The Xanthomonas oryzae pv. oryzae PhoPQ two-component system is required for AvrXA21 activity, hrpG expression, and virulence. J Bacteriol, 190(6): 2183–2197

    Article  PubMed  CAS  Google Scholar 

  • Ng W L, Bassler B L (2009). Bacterial quorum-sensing network architectures. Annu Rev Genet, 43: 197–222

    Article  PubMed  CAS  Google Scholar 

  • Ninfa A J, Magasanik B (1986). Covalent modification of the glnG product, NRI, by the glnL product, NRII, regulates the transcription of the glnALG operon in Escherichia coli. Proc Natl Acad Sci U S A, 83(16): 5909–5913

    Article  PubMed  CAS  Google Scholar 

  • Nixon B T, Ronson C W, Ausubel F M (1986). Two-component regulatory systems responsive to environmental stimuli share strongly conserved domains with the nitrogen assimilation regulatory genes ntrB and ntrC. Proc Natl Acad Sci U S A, 83(20): 7850–7854

    Article  PubMed  CAS  Google Scholar 

  • Noël L, Thieme F, Nennstiel D, Bonas U (2001). cDNA-AFLP analysis unravels a genome-wide hrpG-regulon in the plant pathogen Xanthomonas campestris pv. vesicatoria. Mol Microbiol, 41(6): 1271–1281

    Article  PubMed  Google Scholar 

  • Osbourn A E, Clarke B R, Stevens B J, Daniels M J (1990). Use of oligonucleotide probes to identify members of two-component regulatory systems in Xanthomonas campestris pathovar campestris. Mol Gen Genet, 222(1): 145–151

    PubMed  CAS  Google Scholar 

  • Parkinson J S, Kofoid E C (1992). Communication modules in bacterial signaling proteins. Annu Rev Genet, 26: 71–112

    Article  PubMed  CAS  Google Scholar 

  • Paul R, Jaeger T, Abel S, Wiederkehr I, Folcher M, Biondi E G, Laub M T, Jenal U (2008). Allosteric regulation of histidine kinases by their cognate response regulator determines cell fate. Cell, 133(3): 452–461

    Article  PubMed  CAS  Google Scholar 

  • Perez J C, Shin D, Zwir I, Latifi T, Hadley T J, Groisman E A (2009). Evolution of a bacterial regulon controlling virulence and Mg(2+) homeostasis. PLoS Genet, 5(3): e1000428

    Article  PubMed  CAS  Google Scholar 

  • Prost L R, Miller S I (2008). The Salmonellae PhoQ sensor: mechanisms of detection of phagosome signals. Cell Microbiol, 10(3): 576–582

    Article  PubMed  CAS  Google Scholar 

  • Qian W, Han Z J, He C (2008a). Two-component signal transduction systems of Xanthomonas spp.: a lesson from genomics. Mol Plant Microbe Interact, 21(2): 151–161

    Article  PubMed  CAS  Google Scholar 

  • Qian W, Han Z J, Tao J, He C Z (2008b). Genome-scale mutagenesis and phenotypic characterization of two-component signal transduction systems in Xanthomonas campestris pv. campestris ATCC 33913. Mol Plant Microbe Interact, 21(8): 1128–1138

    Article  PubMed  CAS  Google Scholar 

  • Qian W, Jia Y, Ren S X, He Y Q, Feng J X, Lu L F, Sun Q, Ying G, Tang D J, Tang H, Wu W, Hao P, Wang L, Jiang B L, Zeng S, Gu WY, Lu G, Rong L, Tian Y, Yao Z, Fu G, Chen B, Fang R, Qiang B, Chen Z, Zhao G P, Tang J L, He C (2005). Comparative and functional genomic analyses of the pathogenicity of phytopathogen Xanthomonas campestris pv. campestris. Genome Res, 15(6): 757–767

    Article  PubMed  CAS  Google Scholar 

  • Raghavan V, Groisman E A (2010). Orphan and hybrid two-component system proteins in health and disease. Curr Opin Microbiol, 13(2): 226–231

    Article  PubMed  CAS  Google Scholar 

  • Ryan R P, Fouhy Y, Lucey J F, Crossman L C, Spiro S, He Y W, Zhang L H, Heeb S, Cámara M, Williams P, Dow J M (2006). Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc Natl Acad Sci U S A, 103(17): 6712–6717

    Article  PubMed  CAS  Google Scholar 

  • Ryan R P, McCarthy Y, Andrade M, Farah C S, Armitage J P, Dow J M (2010). Cell-cell signal-dependent dynamic interactions between HD-GYP and GGDEF domain proteins mediate virulence in Xanthomonas campestris. Proc Natl Acad Sci U S A, 107(13): 5989–5994

    Article  PubMed  Google Scholar 

  • Silversmith R E (2010). Auxiliary phosphatases in two-component signal transduction. Curr Opin Microbiol, 13(2): 177–183

    Article  PubMed  CAS  Google Scholar 

  • Skerker J M, Prasol M S, Perchuk B S, Biondi E G, Laub M T (2005). Two-component signal transduction pathways regulating growth and cell cycle progression in a bacterium: a system-level analysis. PLoS Biol, 3(10): e334

    Article  PubMed  CAS  Google Scholar 

  • Slater H, Alvarez-Morales A, Barber C E, Daniels MJ, Dow JM (2000). A two-component system involving an HD-GYP domain protein links cell-cell signalling to pathogenicity gene expression in Xanthomonas campestris. Mol Microbiol, 38(5): 986–1003

    Article  PubMed  CAS  Google Scholar 

  • Song WY, Wang G L, Chen L L, Kim H S, Pi L Y, Holsten T, Gardner J, Wang B, Zhai W X, Zhu L H, Fauquet C, Ronald P (1995). A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science, 270(5243): 1804–1806

    Article  PubMed  CAS  Google Scholar 

  • Stock A M, Robinson V L, Goudreau P N (2000). Two-component signal transduction. Annu Rev Biochem, 69: 183–215

    Article  PubMed  CAS  Google Scholar 

  • Swartz T E, Tseng T S, Frederickson M A, Paris G, Comerci D J, Rajashekara G, Kim J G, Mudgett M B, Splitter G A, Ugalde R A, Goldbaum F A, Briggs W R, Bogomolni R A (2007). Blue-lightactivated histidine kinases: two-component sensors in bacteria. Science, 317(5841): 1090–1093

    Article  PubMed  CAS  Google Scholar 

  • Swings J G, Civerolo E L (1993). Xanthomonas. London: Chapman & Hall

    Google Scholar 

  • Szczesny R, Jordan M, Schramm C, Schulz S, Cogez V, Bonas U, Büttner D (2010). Functional characterization of the Xcs and Xps type II secretion systems from the plant pathogenic bacterium Xanthomonas campestris pv vesicatoria. New Phytol, 187(4): 983–1002

    Article  PubMed  CAS  Google Scholar 

  • Tamayo R, Pratt J T, Camilli A (2007). Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu Rev Microbiol, 61: 131–148

    Article  PubMed  CAS  Google Scholar 

  • Tang J L, Feng J X, Li Q Q, Wen H X, Zhou D L, Wilson T J, Dow J M, Ma Q S, Daniels MJ (1996). Cloning and characterization of the rpfC gene of Xanthomonas oryzae pv. oryzae: involvement in exopolysaccharide production and virulence to rice. Mol Plant Microbe Interact, 9(7): 664–666

    Article  PubMed  CAS  Google Scholar 

  • Tang J L, Liu Y N, Barber C E, Dow J M, Wootton J C, Daniels M J (1991). Genetic and molecular analysis of a cluster of rpf genes involved in positive regulation of synthesis of extracellular enzymes and polysaccharide in Xanthomonas campestris pathovar campestris. Mol Gen Genet, 226(3): 409–417

    Article  PubMed  CAS  Google Scholar 

  • Tao F, He Y W, Wu D H, Swarup S, Zhang L H (2010). The cyclic nucleotide monophosphate domain of Xanthomonas campestris global regulator Clp defines a new class of cyclic di-GMP effectors. J Bacteriol, 192(4): 1020–1029

    Article  PubMed  CAS  Google Scholar 

  • Tao J, He C (2010). Response regulator, VemR, positively regulates the virulence and adaptation of Xanthomonas campestris pv. campestris. FEMS Microbiol Lett, 304(1): 20–28

    Article  PubMed  CAS  Google Scholar 

  • Tsuge S, Nakayama T, Terashima S, Ochiai H, Furutani A, Oku T, Tsuno K, Kubo Y, Kaku H (2006). Gene involved in transcriptional activation of the hrp regulatory gene hrpG in Xanthomonas oryzae pv. oryzae. J Bacteriol, 188(11): 4158–4162

    Article  PubMed  CAS  Google Scholar 

  • Wang L, Rong W, He C (2008). Two Xanthomonas extracellular polygalacturonases, PghAxc and PghBxc, are regulated by type III secretion regulators HrpX and HrpG and are required for virulence. Mol Plant Microbe Interact, 21(5): 555–563

    Article  PubMed  CAS  Google Scholar 

  • Wang L H, He Y, Gao Y, Wu J E, Dong Y H, He C, Wang S X, Weng L X, Xu J L, Tay L, Fang R X, Zhang L H (2004). A bacterial cell-cell communication signal with cross-kingdom structural analogues. Mol Microbiol, 51(3): 903–912

    Article  PubMed  CAS  Google Scholar 

  • Wei K, Tang D J, He Y Q, Feng J X, Jiang B L, Lu G T, Chen B, Tang J L (2007). hpaR, a putative marR family transcriptional regulator, is positively controlled by HrpG and HrpX and involved in the pathogenesis, hypersensitive response, and extracellular protease production of Xanthomonas campestris pathovar campestris. J Bacteriol, 189(5): 2055–2062

    Article  PubMed  CAS  Google Scholar 

  • Wengelnik K, Bonas U (1996). HrpXv, an AraC-type regulator, activates expression of five of the six loci in the hrp cluster of Xanthomonas campestris pv. vesicatoria. J Bacteriol, 178(12): 3462–3469

    PubMed  CAS  Google Scholar 

  • Wengelnik K, Van den Ackerveken G, Bonas U (1996). HrpG, a key hrp regulatory protein of Xanthomonas campestris pv. vesicatoria is homologous to two-component response regulators. Mol Plant Microbe Interact, 9(8): 704–712

    Article  PubMed  CAS  Google Scholar 

  • Yamazaki A, Hirata H, Tsuyumu S (2008). HrpG regulates type II secretory proteins in Xanthomonas axonopodis pv. citri. J Gen Plant Pathol, 74: 138–150

    Article  CAS  Google Scholar 

  • Zhang S S, He Y Q, Xu L M, Chen BW, Jiang B L, Liao J, Cao J R, Liu D, Huang Y Q, Liang X X, Tang D J, Lu G T, Tang J L (2008). A putative colR(XC1049)-colS(XC1050) two-component signal transduction system in Xanthomonas campestris positively regulates hrpC and hrpE operons and is involved in virulence, the hypersensitive response and tolerance to various stresses. Res Microbiol, 159(7–8): 569–578

    Article  PubMed  CAS  Google Scholar 

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  1. State Key Laboratory of Plant Genomics, Institute of Microbiology, Chinese Academy of Sciences, Beijing, 100101, China

    Fang-Fang Wang, Li Wang & Wei Qian

  2. Graduate School, Chinese Academy of Sciences, Beijing, 100049, China

    Fang-Fang Wang

  3. National Plant Gene Research Center, Beijing, 100101, China

    Fang-Fang Wang, Li Wang & Wei Qian

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  2. Li Wang
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Wang, FF., Wang, L. & Qian, W. Two-component signal transduction systems and regulation of virulence factors in Xanthomonas: a perspective. Front. Biol. 5, 495–506 (2010). https://doi.org/10.1007/s11515-010-0750-x

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