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

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.

Keywords

Xanthomonas / two-component signal transduction system / virulence factor

References

[1] 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

[2] Andrade M O, Alegria M C, Guzzo C R, Docena C, Rosa M C, 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

[3] 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

[4] 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

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

[6] 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

[7] 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 M A, Almeida N F, Alves L M, 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

[8] 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

[9] 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

[10] 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 cell-cell signaling and is required for full virulence to plants. Proc Natl Acad Sci U S A, 100(19): 10995–11000

[11] 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

[12] 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

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

[14] 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

[15] 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

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

[17] 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

[18] 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

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

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

[21] 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

[22] 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

[23] 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

[24] 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

[25] He Y W, Zhang L H (2008). Quorum sensing and virulence regulation in Xanthomonas campestris. FEMS Microbiol Rev, 32(5): 842–857

[26] 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

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

[28] 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

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

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

[31] 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

[32] Lee S W, Han S W, 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

[33] 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

[34] 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

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

[36] 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

[37] 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

[38] 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

[39] 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

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

[41] 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

[42] 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

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

[44] 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

[45] 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

[46] 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 W Y, 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

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

[48] 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

[49] 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

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

[51] 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

[52] Slater H, Alvarez-Morales A, Barber C E, Daniels M J, Dow J M (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

[53] Song W Y, 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

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

[55] 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-light-activated histidine kinases: two-component sensors in bacteria. Science, 317(5841): 1090–1093

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

[57] 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

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

[59] 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 M J (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

[60] 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

[61] 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

[62] 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

[63] 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

[65] 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

[64] 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

[66] 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

[67] 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

[68] 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

[69] 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

[70] Zhang S S, He Y Q, Xu L M, Chen B W, 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

Acknowledgements

The authors thank two anonymous reviewers for their valuable comments on this manuscript. This work was supported by the National Natural Science Foundation of China (Grant No. 30771401) and The National Basic Research Program (No. 2011CB100700) from the Ministry of Science and Technology of China.

RIGHTS & PERMISSIONS

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg