Skip to main content
SpringerLink
Log in

Regulatory network of hrp gene expression in Xanthomonas oryzae pv. oryzae

  • REVIEW FOR THE 100TH ANNIVERSARY
  • Published:
Journal of General Plant Pathology Aims and scope Submit manuscript

Abstract

Like other plant-pathogenic bacteria, Xanthomonas oryzae pv. oryzae, the causal agent of bacterial leaf blight of rice, has hrp genes that are indispensable for its virulence. The hrp genes are involved in the construction of the type III secretion (T3S) apparatus, through which dozens of virulence-related proteins, called effectors, are directly secreted into plant cells to suppress and disturb plant immune systems and/or induce plant susceptibility genes. The expression of hrp genes is strictly regulated and induced only in plants and in certain nutrient-poor media. Two proteins, HrpG and HrpX, are known as key regulators for hrp gene expression. Great efforts by many researchers have revealed unexpectedly that, besides HrpG and HrpX, many regulators are involved in this regulation, some of which also regulate the expression of virulence-related genes other than hrp. Moreover, it has been found that HrpG and HrpX regulate not only hrp genes and effector genes but also genes unrelated to the T3S system. These findings suggest that the expression of the hrp gene is orchestrally regulated with other virulence-related genes by a complicated, sophisticated regulatory network in X. oryzae pv. oryzae.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Aldrick SJ, Buddenhagen IW, Reddy APK (1973) The occurrence of bacterial leaf blight in wild and cultivated rice in northern Australia. Aust J Agric Res 24:219–227

    Article  Google Scholar 

  • Alfano JR, Collmer A (1997) The type III (Hrp) secretion pathway of plant pathogenic bacteria: trafficking harpins, Avr proteins, and death. J Bacteriol 179:5655–5662

    CAS  PubMed Central  PubMed  Google Scholar 

  • An SQ, Lu GT, Su HZ, Li RF, He YQ, Jiang BL, Tang DJ, Tang JL (2011) Systematic mutagenesis of all predicted gntR genes in Xanthomonas campestris pv. campestris reveals a GntR family transcriptional regulator controlling hypersensitive response and virulence. Mol Plant Microbe Interact 24:1027–1039

    Article  CAS  PubMed  Google Scholar 

  • Arlat M, Gough CL, Barber CE, Boucher C, Daniels MJ (1991) Xanthomonas campestris contains a cluster of hrp genes related to the larger hrp cluster of Pseudomonas solanacearum. Mol Plant Microbe Interact 4:593–601

    Article  CAS  PubMed  Google Scholar 

  • Astua-Monge G, Minsavage GV, Stall RE, Davis MJ, Bonas U, Jones JB (2000) Resistance of tomato and pepper to T3 strains of Xanthomonas campestris pv. vesicatoria is specified by a plant-inducible avirulence gene. Mol Plant Microbe Interact 13:911–921

    Article  CAS  PubMed  Google Scholar 

  • Barber CE, Tang JL, Feng JX, Pan MQ, Wilson TJG, Slater H, Dow JM, Williams P, Daniels MJ (1997) A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule. Mol Microbiol 24:555–566

    Article  CAS  PubMed  Google Scholar 

  • Boch J, Bonas U (2010) Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annu Rev Phytopathol 48:419–436

    Article  CAS  PubMed  Google Scholar 

  • Bretz J, Losada L, Lisboa K, Hutcheson SW (2002) Lon protease functions as a negative regulator of type III protein secretion in Pseudomonas syringae. Mol Microbiol 45:397–409

    Article  CAS  PubMed  Google Scholar 

  • Burdman S, Shen Y, Lee SW, 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 17:602–612

    Article  CAS  PubMed  Google Scholar 

  • Büttner D, Bonas U (2002) Getting across—bacterial type III effector proteins on their way to the plant cell. EMBO J 21:5313–5322

    Article  PubMed Central  PubMed  Google Scholar 

  • Büttner D, He SY (2009) Type III protein secretion in plant pathogenic bacteria. Plant Physiol 150:1656–1664

    Article  PubMed Central  PubMed  Google Scholar 

  • Chao NX, Wei K, Chen Q, Meng QL, Tang DJ, He YQ, Lu GT, Jiang BL, Liang XX, Feng JX, Chen B, Tang JL (2008) The rsmA-like gene rsmA Xcc of Xanthomonas campestris pv. campestris is involved in the control of various cellular processes, including pathogenesis. Mol Plant Microbe Interact 21:411–423

    Article  CAS  PubMed  Google Scholar 

  • Cunnac S, Boucher C, Genin S (2004a) Characterization of the cis-acting regulatory element controlling HrpB-mediated activation of the type III secretion system and effector genes in Ralstonia solanacearum. J Bacteriol 186:2309–2318

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cunnac S, Occhialini A, Barberis P, Boucher C, Genin S (2004b) Inventory and functional analysis of the large Hrp regulon in Ralstonia solanacearum: identification of novel effector proteins translocated to plant host cells through the type III secretion system. Mol Microbiol 53:115–128

    Article  CAS  PubMed  Google Scholar 

  • Dorman CJ (2004) H-NS: a universal regulator for a dynamic genome. Nat Rev Microbiol 2:391–400

    Article  CAS  PubMed  Google Scholar 

  • Dow JM, Crossman L, Findlay K, He YQ, Feng JX, Tang JL (2003) Biofilm dispersal in Xanthomonas campestrisis controlled by cell–cell signaling and is required for full virulence to plants. Proc Natl Acad Sci USA 100:10995–11000

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dow JM, Fouhy Y, Lucey JF, Ryan RP (2006) The HD-GYP domain, cyclic di-GMP signaling, and bacterial virulence to plants. Mol Plant Microbe Interact 19:1378–1384

    Article  CAS  PubMed  Google Scholar 

  • Doyle EL, Stoddard BL, Voytas DF, Bogdanove AJ (2013) TAL effectors: highly adaptable phytobacterial virulence factors and readily engineered DNA-targeting proteins. Trends Cell Biol 23:390–398

    Article  CAS  PubMed  Google Scholar 

  • Fang FC, Rimsky S (2008) New insights into transcriptional regulation by H-NS. Curr Opin Microbiol 11:113–120

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Feng JX, Song ZZ, Duan CJ, Zhao S, Wu YQ, Wang C, Dow JM, Tang JL (2009) The xrvA gene of Xanthomonas oryzae pv. oryzae, encoding an H-NS-like protein, regulates virulence in rice. Microbiology 155:3033–3044

    Article  CAS  PubMed  Google Scholar 

  • Fenselau S, Bonas U (1995) Sequence and expression analysis of the hrpB pathogenicity operon of Xanthomonas campestris pv. vesicatoria which encodes eight proteins with similarity to components of the Hrp, Ysc, Spa and Fli secretion systems. Mol Plant Microbe Interact 8:845–854

    Article  CAS  PubMed  Google Scholar 

  • Furutani A, Tsuge S, Oku T, Tsuno K, Inoue Y, Ochiai H, Kaku H, Kubo Y (2003) Hpa1 secretion via type III secretion system in Xanthomonas oryzae pv. oryzae. J Gen Plant Pathol 69:271–275

    Article  CAS  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 186:1374–1380

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Furutani A, Nakayama T, Ochiai H, Kaku H, Kubo Y, Tsuge S (2006) Identification of novel HrpXo regulons preceded by two cis-acting elements, a plant-inducible promoter box and a −10 box-like sequence, from the genome database of Xanthomonas oryzae pv. oryzae. FEMS Microbiol Lett 259:133–141

    Article  CAS  PubMed  Google Scholar 

  • Furutani A, Takaoka M, Sanada H, Noguchi Y, Oku T, Tsuno K, Ochiai H, Tsuge S (2009) Identification of novel type III secretion effectors in Xanthomonas oryzae pv. oryzae. Mol Plant Microbe Interact 22:96–106

    Article  CAS  PubMed  Google Scholar 

  • Ge C, He C (2008) Regulation of the type II secretion structural gene xpsE in Xanthomonas campestris pathovar campestris by the global transcription regulator Clp. Curr Microbiol 56:122–127

    Article  CAS  PubMed  Google Scholar 

  • Genin S, Denny TP (2012) Pathogenomics of the Ralstonia solanacearum species complex. Annu Rev Phytopathol 50:67–89

    Article  CAS  PubMed  Google Scholar 

  • Genin S, Brito B, Denny TP, Boucher C (2005) Control of the Ralstonia solanacearum type III secretion system (Hrp) genes by the global virulence regulator PhcA. FEBS Lett 579:2077–2081

    Article  CAS  PubMed  Google Scholar 

  • Gophna U, Ron EZ, Graur D (2003) Bacterial type III secretion systems are ancient and evolved by multiple horizontal-transfer events. Gene 312:151–163

    Article  CAS  PubMed  Google Scholar 

  • Guo Y, Figueiredo F, Jones J, Wang N (2011) HrpG and HrpX play global roles in coordinating different virulence traits of Xanthomonas axonopodis pv. citri. Mol Plant Microbe Interact 24:649–661

    Article  CAS  PubMed  Google Scholar 

  • Guo W, Cai LL, Zou HS, Ma WX, Liu XL, Zou LF, Li YR, Chen XB, Chen GY (2012a) Ketoglutarate transport protein KgtP is secreted through the type III secretion system and contributes to virulence in Xanthomonas oryzae pv. oryzae. Appl Environ Microbiol 78:5672–5681

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Guo W, Zou LF, Li YR, Cui YP, Ji ZY, Cai LL, Zou HS, Hutchins WC, Yang CH, Chen GY (2012b) Fructose-bisphosphate aldolase exhibits functional roles between carbon metabolism and the hrp system in rice pathogen Xanthomonas oryzae pv. oryzicola. PLoS One 7:e31855

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • He YW, Ng AY, Xu M, Lin K, Wang LH, Dong YH, Zhang LH (2007) Xanthomonas campestris cell–cell communication involves a putative nucleotide receptor protein Clp and a hierarchical signalling network. Mol Microbiol 64:281–292

    Article  CAS  PubMed  Google Scholar 

  • Hoskisson PA, Rigali S (2009) Chapter 1. Variation in form and function: the helix-turn-helix regulators of the GntR superfamily. Adv Appl Microbiol 69:1–22

    Article  CAS  PubMed  Google Scholar 

  • Hsiao YM, Liao HY, Lee MC, Yang TC, Tseng YH (2005) Clp upregulates transcription of engA gene encoding a virulence factor in Xanthomonas campestris by direct binding to the upstream tandem Clp sites. FEBS Lett 579:3525–3533

    Article  CAS  PubMed  Google Scholar 

  • Hsiao YM, Fang MC, Sun PF, Tseng YH (2009) Clp and RpfF up-regulate transcription of pelA1 gene encoding the major pectate lyase in Xanthomonas campestris pv. campestris. J Agric Food Chem 57:6207–6215

    Article  CAS  PubMed  Google Scholar 

  • Huang HC, Hutcheson SW, Collmer A (1991) Characterization of the hrp cluster from Pseudomonas syringae pv. syringae 61 and TnphoA tagging of genes encoding exported or membrane-spanning Hrp proteins. Mol Plant Microbe Interact 4:469–476

    Article  CAS  Google Scholar 

  • Huang DL, Tang DJ, Liao Q, Li XQ, He YQ, Feng JX, Jiang BL, Lu GT, Tang JL (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 22:321–329

    Article  PubMed  Google Scholar 

  • Hutcheson SW, Bretz J, Sussan T, Jin S, Pak K (2001) Enhancer-binding proteins HrpR and HrpS interact to regulate hrp-encoded type III protein secretion in Pseudomonas syringae strains. J Bacteriol 183:5589–5598

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Jones RK, Barnes LW, Gonzalez CF, Leach JE, Alvarez AM, Benedict AA (1989) Identification of low-virulence strains of Xanthomonas campestris pv. oryzae from rice in the United States. Phytopathology 79:984–990

    Article  CAS  Google Scholar 

  • Kamdar HV, Kamoun S, Kado CI (1993) Restoration of pathogenicity of avirulent Xanthomonas oryzae pv. oryzae and X. campestris pathovars by reciprocal complementation with the hrpXo and hrpXc genes and identification of HrpX function by sequence analyses. J Bacteriol 175:2017–2025

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kametani-Ikawa Y, Tsuge S, Furutani A, Ochiai H (2011) An H-NS-like protein involved in the negative regulation of hrp genes in Xanthomonas oryzae pv. oryzae. FEMS Microbiol Lett 319:58–64

    Article  CAS  PubMed  Google Scholar 

  • Koebnik R, Krüger A, Thieme F, Urban A, Bonas U (2006) Specific binding of the Xanthomonas campestris pv. vesicatoria AraC-type transcriptional activator HrpX to plant-inducible promoter boxes. J Bacteriol 188:7652–7660

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lee SW, Han SW, Bartley LE, Ronald PC (2006) Unique characteristics of Xanthomonas oryzae pv. oryzae AvrXa21 and implications for plant innate immunity. Proc Natl Acad Sci USA 103:18395–18400

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lee SW, Jeong KS, Han SW, Lee SE, Phee BK, Hahn TR, Ronald P (2008) The Xanthomonas oryzae pv. oryzae PhoPQ two-component system is required for AvrXA21 activity, hrpG expression, and virulence. J Bacteriol 190:2183–2197

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Li RF, Lu GT, Li L, Su HZ, Feng GF, Chen Y, He YQ, Jiang BL, Tang DJ, Tang JL (2013) Identification of a putative cognate sensor kinase for the two-component response regulator HrpG, a key regulator controlling the expression of the hrp genes in Xanthomonas campestris pv. campestris. Environ Microbiol doi: 10.1111/1462-2920.12207 [Epub ahead of print]

  • Lozano JC (1977) Identification of bacterial leaf blight in rice caused by Xanthomonas oryzae, in America. Plant Dis Rep 61:644–648

    Google Scholar 

  • Marenda M, Brito B, Callard D, Genin S, Barberis P, Boucher C, Arlat M (1998) PrhA controls a novel regulatory pathway required for the specific induction of Ralstonia solanacearum hrp genes in the presence of plant cells. Mol Microbiol 27:437–453

    Article  CAS  PubMed  Google Scholar 

  • Miyazaki E, Yamanaka S, Misawa T (1976) Studies on the bacterial leaf blight of rice II. A comparison of hydrolytic enzyme activity between diseased and healthy tissue (in Japanese with English abstract). Ann Phytopath Soc Japan 42:21–29

    Article  Google Scholar 

  • Mizukami T, Wakimoto S (1969) Epidemiology and control of bacterial leaf blight of rice. Annu Rev Phytopathol 7:51–72

    Article  CAS  Google Scholar 

  • Mukaihara T, Tamura N, Murata Y, Iwabuchi M (2004) Genetic screening of Hrp type III-related pathogenicity genes controlled by the HrpB transcriptional activator in Ralstonia solanacearum. Mol Microbiol 54:863–875

    Article  CAS  PubMed  Google Scholar 

  • Mukaihara T, Tamura N, Iwabuchi M (2010) Genome-wide identification of a large repertoire of Ralstonia solanacearum type III effector proteins by a new functional screen. Mol Plant Microbe Interact 23:251–262

    Article  CAS  PubMed  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 41:1271–1281

    Article  PubMed  Google Scholar 

  • Noël L, Thieme F, Nennstiel D, Bonas U (2002) Two novel type III-secreted proteins of Xanthomonas campestris pv. vesicatoria are encoded within the hrp pathogenicity island. J Bacteriol 184:1340–1348

    Article  PubMed Central  PubMed  Google Scholar 

  • Occhialini A, Cunnac S, Reymond N, Genin S, Boucher C (2005) Genome-wide analysis of gene expression in Ralstonia solanacearum reveals that the hrpB gene acts as a regulatory switch controlling multiple virulence pathways. Mol Plant Microbe Interact 18:938–949

    Article  CAS  PubMed  Google Scholar 

  • Ochiai H, Inoue Y, Takeya M, Sasaki A, Kaku H (2005) Genome sequence of Xanthomonas oryzae pv. oryzae suggests contribution of large numbers of effector genes and insertion sequences to its race diversity. Jpn Agric Res Q 39:275–287

    Article  CAS  Google Scholar 

  • Oku T, Tanaka K, Iwamoto M, Inoue Y, Ochiai H, Kaku H, Tsuge S, Tsuno K (2004) Structural conservation of the hrp gene cluster in Xanthomonas oryzae pv. oryzae. J Gen Plant Pathol 70:159–167

    Article  CAS  Google Scholar 

  • Ou SH (1985) Bacterial leaf blight. Rice diseases, 2nd edn. Commonwealth Mycological Institute, Kew, pp 70–74

    Google Scholar 

  • Ray SK, Rajeshwari R, Sonti RV (2000) Mutants of Xanthomonas oryzae pv. oryzae deficient in general secretory pathway are virulence deficient and unable to secrete xylanase. Mol Plant Microbe Interact 13:394–401

    Article  CAS  PubMed  Google Scholar 

  • Ryan RP, Fouhy Y, Lucey JF, Crossman LC, Spiro S, He YW, Zhang LH, Heeb S, Cámara M, Williams P, Dow JM (2006) Cell–cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc Natl Acad Sci USA 103:6712–6717

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ryan RP, Fouhy Y, Lucey JF, Jiang BL, He YQ, Feng JX, Tang JL, Dow JM (2007) Cyclic di-GMP signalling in the virulence and environmental adaptation of Xanthomonas campestris. Mol Microbiol 63:429–442

    Article  CAS  PubMed  Google Scholar 

  • Schechter LM, Roberts KA, Jamir Y, Alfano JR, Collmer A (2004) Pseudomonas syringae type III secretion system targeting signals and novel effectors studied with a Cya translocation reporter. J Bacteriol 186:543–555

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schulte R, Bonas U (1992a) Expression of the Xanthomonas campestris pv. vesicatoria hrp gene cluster, which determines pathogenicity and hypersensitivity on pepper and tomato, is plant inducible. J Bacteriol 174:815–823

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schulte R, Bonas U (1992b) A Xanthomonas pathogenicity locus is induced by sucrose and sulfur-containing amino acid. Plant Cell 4:79–86

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schwessinger B, Ronald PC (2012) Plant innate immunity: perception of conserved microbial signatures. Annu Rev Plant Biol 63:451–482

    Article  CAS  PubMed  Google Scholar 

  • Slater H, Alvarez-Morales A, Barber CE, 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 38:986–1003

    Article  CAS  PubMed  Google Scholar 

  • Stock AM, Robinson VL, Goudreau PN (2000) Two-component signal transduction. Annu Rev Biochem 69:183–215

    Article  CAS  PubMed  Google Scholar 

  • Tabei H (1977) Anatomical studies of rice plant affected with bacterial leaf blight, Xanthomonas oryzae (Uyeda et Ishiyama) Dowson. Bull Kyushu Agric Exp Stn 19:193–257

    Google Scholar 

  • Takeuchi Y, Tohbaru M, Sato A (1994) Polysaccharides in primary cell walls of rice cells in suspension culture. Phytochemistry 35:361–363

    Article  CAS  Google Scholar 

  • Tang JL, Liu YN, Barber CE, Dow JM, Wootton JC, Daniels MJ (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 226:409–417

    Article  CAS  PubMed  Google Scholar 

  • Tang X, Xiao Y, Zhou JM (2006) Regulation of the type III secretion system in phytopathogenic bacteria. Mol Plant Microbe Interact 19:1159–1166

    Article  CAS  PubMed  Google Scholar 

  • Tsuge S, Furutani A, Fukunaka R, Oku T, Tsuno K, Ochiai H, Inoue Y, Kaku H, Kubo Y (2002) Expression of Xanthomonas oryzae pv. oryzae hrp genes in XOM2, a novel synthetic medium. J Gen Plant Pathol 68:363–371

    Article  CAS  Google Scholar 

  • Tsuge S, Ochiai H, Inoue Y, Oku T, Tsuno K, Kaku H, Kubo Y (2004) Involvement of phosphoglucose isomerase in pathogenicity of Xanthomonas oryzae pv. oryzae. Phytopathology 94:478–483

    Article  CAS  PubMed  Google Scholar 

  • Tsuge S, Terashima S, Furutani A, Ochiai H, Oku T, Tsuno K, Kaku H, Kubo Y (2005) Effects on promoter activity of base substitutions in the cis-acting regulatory element of HrpXo regulons in Xanthomonas oryzae pv. oryzae. J Bacteriol 187:2308–2314

    Article  CAS  PubMed Central  PubMed  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 188:4158–4162

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Valls M, Genin S, Boucher C (2006) Integrated regulation of the type III secretion system and other virulence determinants in Ralstonia solanacearum. PLoS Pathog 2:e82

    Article  PubMed Central  PubMed  Google Scholar 

  • Vauterin L, Hoste B, Kersters K, Swings J (1995) Reclassification of Xanthomonas. Int J Syst Bacteriol 45:472–489

    Article  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 21:555–563

    Article  PubMed  Google Scholar 

  • Watabe M, Yamaguchi M, Furusawa I, Horino O (1993) Virulence, and bacterial multiplication and movement in rice leaves of Xanthomonas campestris pv. oryzae mutants impaired in productivity of extracellular polysaccharide. Ann Phytopath Soc Japan 59:544–550

    Article  CAS  Google Scholar 

  • Wei ZM, Beer SV (1995) hrpL activates Erwinia amylovora hrp gene transcription and is a member of the ECF subfamily of sigma factors. J Bacteriol 177:6201–6210

    CAS  PubMed Central  PubMed  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 178:3462–3469

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wengelnik K, Marie C, Russel M, Bonas U (1996a) Expression and localization of HrpA1, a protein of Xanthomonas campestris pv. vesicatoria essential for pathogenicity and induction of the hypersensitive reaction. J Bacteriol 178:1061–1069

    CAS  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wengelnik K, Rossier O, Bonas U (1999) Mutations in the regulatory gene hrpG of Xanthomonas campestris pv. vesicatoria result in constitutive expression of all hrp genes. J Bacteriol 181:6828–6831

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xiao Y, Heu S, Yi J, Lu Y, Hutcheson SW (1994) Identification of a putative alternate sigma factor and characterization of a multicomponent regulatory cascade controlling the expression of Pseudomonas syringae pv. syringae Pss61 hrp and hrmA genes. J Bacteriol 176:1025–1036

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xiao YL, Li YR, Liu ZY, Xiang Y, Chen GY (2007) Establishment of the hrp-inducing systems for the expression of the hrp genes of Xanthomonas oryzae pv. oryzicola. Acta Microbiologica Sinica 47:396–401

    CAS  PubMed  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 

  • Yang F, Tian F, Sun L, Chen H, Wu M, Yang CH, He C (2012) A novel two-component system PdeK/PdeR regulates c-di-GMP turnover and virulence of Xanthomonas oryzae pv. oryzae. Mol Plant Microbe Interact 25:1361–1369

    Article  CAS  PubMed  Google Scholar 

  • Yoshimochi T, Hikichi Y, Kiba A, Ohnishi K (2009) The global virulence regulator PhcA negatively controls the Ralstonia solanacearum hrp regulatory cascade by repressing expression of the PrhIR signaling proteins. J Bacteriol 191:3424–3428

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang SS, He YQ, Xu LM, Chen BW, Jiang BL, Liao J, Cao JR, Liu D, Huang YQ, Liang XX, Tang DJ, Lu GT, Tang JL (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 159:569–578

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to Drs. Hirokazu Ochiai (National Institute of Agrobiological Sciences), Takashi Oku (Prefectural University of Hiroshima), Kazunori Tsuno (Miyazaki University), Yasuhiro Inoue (National Agricultural Research Center), Kouhei Ohnishi (Kochi University), Yasufumi Hikichi (Kochi University) and many graduate and undergraduate students for their collaboration. We are supported by Grants-in-Aid for Scientific Research from the Ministry of Education, Science, Sports and Culture, Japan.

Author information

Authors and Affiliations

  1. Laboratory of Plant Pathology, Kyoto Prefectural University, Kyoto, 606-8522, Japan

    Seiji Tsuge & Yumi Ikawa

  2. Gene Research Center, Ibaraki University, Inashiki, 300-0393, Japan

    Ayako Furutani

Authors
  1. Seiji Tsuge
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ayako Furutani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yumi Ikawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Seiji Tsuge.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tsuge, S., Furutani, A. & Ikawa, Y. Regulatory network of hrp gene expression in Xanthomonas oryzae pv. oryzae . J Gen Plant Pathol 80, 303–313 (2014). https://doi.org/10.1007/s10327-014-0525-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10327-014-0525-3

Keywords

Search

Navigation