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What does it take to be a plant pathogen: genomic insights from Streptomyces species

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Abstract

Plant pathogenicity is rare in the genus Streptomyces, with only a dozen or so species possessing this trait out of the more than 900 species described. Nevertheless, such species have had a significant impact on agricultural economies throughout the world due to their ability to cause important crop diseases such as potato common scab, which is characterized by lesions that form on the potato tuber surface. All pathogenic species that cause common scab produce a family of phytotoxins called the thaxtomins, which function as cellulose synthesis inhibitors. In addition, the nec1 and tomA genes are conserved in several pathogenic streptomycetes, the former of which is predicted to function in the suppression of plant defense responses. Streptomyces scabies is the oldest plant pathogen described and has a world-wide distribution, whereas species such as S. turgidiscabies and S. acidiscabies are believed to be newly emergent pathogens found in more limited geographical locations. The genome sequence of S. scabies 87-22 was recently completed, and comparative genomic analyses with other sequenced microbial pathogens have revealed the presence of additional genes that may play a role in plant pathogenicity, an idea that is supported by functional analysis of one such putative virulence locus. In addition, the availability of multiple genome sequences for both pathogenic and nonpathogenic streptomycetes has provided an opportunity for comparative genomic analyses to identify the Streptomyces pathogenome. Such genomic analyses will contribute to the fundamental understanding of the mechanisms and evolution of plant pathogenicity and plant-microbe biology within this genus.

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References

  • Arnold K, Bordoli L, Kopp J, Schwede T (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195–201

    CAS  PubMed  Google Scholar 

  • Bender CL, Alarcon-Chaidez F, Gross DC (1999) Pseudomonas syringae phytotoxins: mode of action, regulation, and biosynthesis by peptide and polyketide synthetases. Microbiol Mol Biol Rev 63:266–292

    CAS  PubMed  Google Scholar 

  • Bentley SD, Chater KF, Cerdeno-Tarraga AM, Challis GL, Thomson NR, James KD et al (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–147

    PubMed  Google Scholar 

  • Bignell DR, Seipke RF, Huguet-Tapia JC, Chambers AH, Parry R, Loria R (2010) Streptomyces scabies 87–22 contains a coronafacic acid-like biosynthetic cluster that contributes to plant-microbe interactions. Mol Plant Microbe Interact 23:161–175

    CAS  PubMed  Google Scholar 

  • Bischoff V, Cookson SJ, Wu S, Scheible WR (2009) Thaxtomin A affects CESA-complex density, expression of cell wall genes, cell wall composition, and causes ectopic lignification in Arabidopsis thaliana seedlings. J Exp Bot 60:955–965

    CAS  PubMed  Google Scholar 

  • Bouarab K, Melton R, Peart J, Baulcombe D, Osbourn A (2002) A saponin-detoxifying enzyme mediates suppression of plant defenses. Nature 418:889–892

    CAS  PubMed  Google Scholar 

  • Bouchek-Mechiche K, Gardan L, Normand P, Jouan B (2000) DNA relatedness among strains of Streptomyces pathogenic to potato in France: description of three new species, S. europaeiscabiei sp. nov. and S. stelliscabiei sp. nov. associated with common scab, and S. reticuliscabiei sp. nov. associated with netted scab. Int J Syst Evol Microbiol 50(Pt 1):91–99

  • Bowyer P, Clarke BR, Lunness P, Daniels MJ, Osbourn AE (1995) Host range of a plant pathogenic fungus determined by a saponin detoxifying enzyme. Science 267:371–374

    CAS  PubMed  Google Scholar 

  • Brotman Y, Briff E, Viterbo A, Chet I (2008) Role of swollenin, an expansin-like protein from Trichoderma, in plant root colonization. Plant Physiol 147:779–789

    CAS  PubMed  Google Scholar 

  • Bukhalid RA, Loria R (1997) Cloning and expression of a gene from Streptomyces scabies encoding a putative pathogenicity factor. J Bacteriol 179:7776–7783

    CAS  PubMed  Google Scholar 

  • Bukhalid RA, Chung SY, Loria R (1998) nec1, a gene conferring a necrogenic phenotype, is conserved in plant-pathogenic Streptomyces spp. and linked to a transposase pseudogene. Mol Plant Microbe Interact 11:960–967

    CAS  PubMed  Google Scholar 

  • Bukhalid RA, Takeuchi T, Labeda D, Loria R (2002) Horizontal transfer of the plant virulence gene, nec1, and flanking sequences among genetically distinct Streptomyces strains in the Diastatochromogenes cluster. Appl Environ Microbiol 68:738–744

    CAS  PubMed  Google Scholar 

  • Chague V, Elad Y, Barakat R, Tudzynski P, Sharon A (2002) Ethylene biosynthesis in Botrytis cinerea. FEMS Microbiol Ecol 40:143–149

    CAS  PubMed  Google Scholar 

  • Clark CA, Watson B (1983) Susceptibility of weed species of Convolvulaceae to root-infecting pathogens of sweet potato. Plant Dis 67:907–909

    Google Scholar 

  • Conrath U (2006) Systemic acquired resistance. Plant Signal Behav 1:179–184

    PubMed  Google Scholar 

  • Cullen DW, Lees AK (2007) Detection of the nec1 virulence gene and its correlation with pathogenicity in Streptomyces species on potato tubers and in soil using conventional and real-time PCR. J Appl Microbiol 102:1082–1094

    CAS  PubMed  Google Scholar 

  • Deising H, Nicholson RL, Haug M, Howard RJ, Mendgen K (1992) Adhesion pad formation and the involvement of cutinase and esterases in the attachment of uredospores to the host cuticle. Plant Cell 4:1101–1111

    CAS  PubMed  Google Scholar 

  • Dickman MB, Patil SS (1986) Cutinase deficient mutants of Colletotrichum gloeosporioides are non-pathogenic to papaya fruit. Physiol Mol Plant Pathol 28:235–242

    CAS  Google Scholar 

  • Dickman MB, Podila GK, Kolattukudy PE (1989) Insertion of cutinase gene into a wound pathogen enables it to infect intact host. Nature 342:446–448

    CAS  Google Scholar 

  • Duval I, Beaudoin N (2009) Transcriptional profiling in response to inhibition of cellulose synthesis by thaxtomin A and isoxaben in Arabidopsis thaliana suspension cells. Plant Cell Rep 28:811–830

    CAS  PubMed  Google Scholar 

  • Duval I, Brochu V, Simard M, Beaulieu C, Beaudoin N (2005) Thaxtomin A induces programmed cell death in Arabidopsis thaliana suspension-cultured cells. Planta 222:820–831

    CAS  PubMed  Google Scholar 

  • El-Sayed MA, Valadon LR, El-Shanshoury A (1987) Biosynthesis and metabolism of indole-3-acetic acid in Streptomyces mutabilis and Streptomyces atroolivaceus. Microbiol Lett 36:85–95

    CAS  Google Scholar 

  • El-Shanshoury AR (1991) Biosynthesis of indole-3- acetic acid in Streptomyces atroolivaceus and its changes during spore germination and mycelial growth. Microbios 67:159–164

    CAS  Google Scholar 

  • Errakhi R, Dauphin A, Meimoun P, Lehner A, Reboutier D, Vatsa P, Briand J, Madiona K, Rona JP, Barakate M, Wendehenne D, Beaulieu C, Bouteau F (2008) An early Ca2+ influx is a prerequisite to thaxtomin A-induced cell death in Arabidopsis thaliana cells. J Exp Bot 59:4259–4270

    CAS  PubMed  Google Scholar 

  • Ettinger WF, Thurkral SK, Kolattukudy PE (1987) Structure of cutinase gene, cDNA and the derived amino acid sequence from phytopathogenic fungi. Biochemistry 26:7883–7892

    CAS  Google Scholar 

  • Faucher E, Savard T, Bealieu C (1992) Characterization of actinomycetes isolated from common scab lesions on potato tubers. Can J Plant Pathol 14:197–202

    Google Scholar 

  • Fernandez C, Szyperski T, Bruyere T, Ramage P, Mosinger E, Wuthrich K (1997) NMR solution structure of the pathogenesis-related protein P14a. J Mol Biol 266:576–593

    CAS  PubMed  Google Scholar 

  • Fernando G, Zimmerman W, Kolattukudy PE (1984) Suberin-grown Fusarium solani f. sp. pisi generates a cutinase-like esterase which depolymerizes the aliphatic components of suberin. Physiol Plant Pathol 24:143–155

    CAS  Google Scholar 

  • Fett WF, Gerard HC, Moreau RA, Osman SF, Jones LE (1992) Cutinase production by Streptomyces spp. Curr Microbiol 25:165–171

    CAS  Google Scholar 

  • Feys B, Benedetti CE, Penfold CN, Turner JG (1994) Arabidopsis mutants selected for resistance to the phytotoxin coronatine are male sterile, insensitive to methyl jasmonate, and resistant to a bacterial pathogen. Plant Cell 6:751–759

    CAS  PubMed  Google Scholar 

  • Flores-Gonzalez R, Velasco I, Montes F (2008) Detection and characterization of Streptomyces causing potato common scab in Western Europe. Plant Pathol 57:162–169

    CAS  Google Scholar 

  • Fry BA, Loria R (2002) Thaxtomin A: evidence for a plant cell wall target. Physiol Mol Plant Pathol 60:1–8

    CAS  Google Scholar 

  • Fukuda H, Ogawa T, Ishihara K, Fujii T, Nagahama K, Omata T, Inoue Y, Tanase S, Morino Y (1992a) Molecular cloning in Escherichia coli, expression and nucleotide sequence of the gene for the ethylene forming enzyme of Pseudomonas syringae pv. phaseolicola PK2. Biochem Biophys Res Commun 188:826–832

    CAS  PubMed  Google Scholar 

  • Fukuda H, Ogawa T, Tazaki M, Nagahama K, Fujii T, Tanase S, Morino Y (1992b) Two reactions are simultaneously catalyzed by a single enzyme: The arginine-dependent simultaneous formation of two products, ethylene and succinate, from 2-oxoglutarate by an enzyme from Pseudomonas syringae. Biochem Biophys Res Commun 188:483–489

    CAS  PubMed  Google Scholar 

  • Gilbert RD, Johnson AM, Dean RA (1996) Chemical signals responsible for appressorium formation in the rice blast fungus Magnaporthe grisea. Physiol Mol Plant Pathol 48:335–346

    CAS  Google Scholar 

  • Goto M, Ishida Y, Takikawa Y, Hyodo H (1985) Ethylene production by the kudzu strains of Pseudomonas syringae pv. phaseolicola causing halo blight in Pueraria lobata (Willd.) Ohwi. Plant Cell Physiol 26:141–150

    CAS  Google Scholar 

  • Graca J, Santos S (2007) Suberin: a biopolymer of plants’ skin. Macromol Biosci 12:128–135

    Google Scholar 

  • Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18:2714–2723

    CAS  PubMed  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    PubMed  Google Scholar 

  • Haydock SF, Appleyard AN, Mironenko T, Lester J, Scott N, Leadlay PF (2005) Organization of the biosynthetic gene cluster for the macrolide concanamycin A in Streptomyces neyagawaensis ATCC 27449. Microbiology 151:3161–3169

    CAS  PubMed  Google Scholar 

  • Healy FG, Wach M, Krasnoff SB, Gibson DM, Loria R (2000) The txtAB genes of the plant pathogen Streptomyces acidiscabies encode a peptide synthetase required for phytotoxin thaxtomin A production and pathogenicity. Mol Microbiol 38:794–804

    CAS  PubMed  Google Scholar 

  • Healy FG, Krasnoff SB, Wach M, Gibson DM, Loria R (2002) Involvement of a cytochrome P450 monooxygenase in thaxtomin A biosynthesis by Streptomyces acidiscabies. J Bacteriol 184:2019–2029

    CAS  PubMed  Google Scholar 

  • Hedge Y, Kolattukudy PE (1997) Cuticular waxes relieve self-inhibition of germination and appressorium formation by the conidia of Magnaporthe grisea. Physiol Mol Plant Pathol 51:75–84

    Google Scholar 

  • Hottiger T, Boller T (1991) Ethylene biosynthesis in Fusarium oxysporum sp. tulipae proceeds from glutamate/2-oxoglutarate and requires oxygen and ferrous ions in vivo. Arch Microbiol 157:18–22

    CAS  Google Scholar 

  • Huss M, Wieczorek H (2009) Inhibitors of V-ATPases: old and new players. J Exp Biol 212:341–346

    CAS  PubMed  Google Scholar 

  • Ikeda H, Ishikawa J, Hanamoto A, Shinose M, Kikuchi H, Shiba T, Sakaki Y, Hattori M, Omura S (2003) Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat Biotechnol 21:526–531

    PubMed  Google Scholar 

  • Jahr H, Dreier J, Meletzus D, Bahro R, Eichenlaub R (2000) The endo-β-1,4-glucanase CelA of Clavibacter michiganensis subsp. michiganensis is a pathogenicity determinant required for induction of bacterial wilt of tomato. Mol Plant Microbe Interact 13:703–714

    CAS  PubMed  Google Scholar 

  • Johnson EG, Sparks JP, Dzikovski B, Crane BR, Gibson DM, Loria R (2008) Plant-pathogenic Streptomyces species produce nitric oxide synthase-derived nitric oxide in response to host signals. Chem Biol 15:43–50

    CAS  PubMed  Google Scholar 

  • Johnson EG, Krasnoff SB, Bignell DR, Chung WC, Tao T, Parry RJ, Loria R, Gibson DM (2009) 4-Nitrotryptophan is a substrate for the non-ribosomal peptide synthetase TxtB in the thaxtomin A biosynthetic pathway. Mol Microbiol 73:409–418

    CAS  PubMed  Google Scholar 

  • Joshi MV, Loria R (2007) Streptomyces turgidiscabies possesses a functional cytokinin biosynthetic pathway and produces leafy galls. Mol Plant Microbe Interact 20:751–758

    CAS  PubMed  Google Scholar 

  • Joshi M, Rong X, Moll S, Kers J, Franco C, Loria R (2007a) Streptomyces turgidiscabies secretes a novel virulence protein, Nec1, which facilitates infection. Mol Plant Microbe Interact 20:599–608

    CAS  PubMed  Google Scholar 

  • Joshi MV, Bignell DR, Johnson EG, Sparks JP, Gibson DM, Loria R (2007b) The AraC/XylS regulator TxtR modulates thaxtomin biosynthesis and virulence in Streptomyces scabies. Mol Microbiol 66:633–642

    CAS  PubMed  Google Scholar 

  • Katsir L, Chung HS, Koo AJ, Howe GA (2008a) Jasmonate signaling: a conserved mechanism of hormone sensing. Curr Opin Plant Biol 11:428–435

    CAS  PubMed  Google Scholar 

  • Katsir L, Schilmiller AL, Staswick PE, He SY, Howe GA (2008b) COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci USA 105:7100–7105

    CAS  PubMed  Google Scholar 

  • Kaup O, Ines G, Zellerman E-M, Eichenlaub R, Gartemann K-H (2005) Identification of a tomatinase in the tomato-pathogenic actinomycete Clavibacter michiganensis subsp. michiganensis NCPPB382. Mol Plant Microbe Interact 18:1090–1098

    CAS  PubMed  Google Scholar 

  • Kende H, Bradford K, Brummell D, Cho HT, Cosgrove D, Fleming A, Gehring C, Lee Y, McQueen-Mason S, Rose J, Voesenek LA (2004) Nomenclature for members of the expansin superfamily of genes and proteins. Plant Mol Biol 55:311–314

    CAS  PubMed  Google Scholar 

  • Kerff F, Amoroso A, Herman R, Sauvage E, Petrella S, Filee P, Charlier P, Joris B, Tabuchi A, Nikolaidis N, Cosgrove DJ (2008) Crystal structure and activity of Bacillus subtilis YoaJ (EXLX1), a bacterial expansin that promotes root colonization. Proc Natl Acad Sci USA 105:16876–16881

    CAS  PubMed  Google Scholar 

  • Kers JA, Wach MJ, Krasnoff SB, Widom J, Cameron KD, Bukhalid RA, Gibson DM, Crane BR, Loria R (2004) Nitration of a peptide phytotoxin by bacterial nitric oxide synthase. Nature 429:79–82

    CAS  PubMed  Google Scholar 

  • Kers JA, Cameron KD, Joshi MV, Bukhalid RA, Morello JE, Wach MJ, Gibson DM, Loria R (2005) A large, mobile pathogenicity island confers plant pathogenicity on Streptomyces species. Mol Microbiol 55:1025–1033

    CAS  PubMed  Google Scholar 

  • Kinashi H, Someno K, Sakaguchi K (1984) Isolation and characterization of concanamycins A, B and C. J Antibiot (Tokyo) 37:1333–1343

    CAS  Google Scholar 

  • King RR, Calhoun LA (2009) The thaxtomin phytotoxins: sources, synthesis, biosynthesis, biotransformation and biological activity. Phytochemistry 70:833–841

    CAS  PubMed  Google Scholar 

  • King RR, Lawrence CH (1995) 4-Nitrotryptophans associated with the in vitro production of thaxtomin A by Streptomyces scabies. Phytochemistry 40:41–43

    CAS  Google Scholar 

  • King RR, Lawrence CH, Clark MC, Calhoun LA (1989) Isolation and characterization of phytotoxins associated with Streptomyces scabies. J Chem Soc Chem Commun 13:849–850

    Google Scholar 

  • King RR, Lawrence CH, Calhoun LA, Ristaino JB (1994) Isolation and characterization of thaxtomin-type phytotoxins associated with Streptomyces ipomoeae. J Agric Food Chem 42:1791–1794

    CAS  Google Scholar 

  • Kolattukudy PE (1985) Enzymatic penetration of the plant cuticle by fungal pathogens. Annu Rev Phytopathol 23:223–250

    CAS  Google Scholar 

  • Koller W, Parker DM, Becker CM (1991) Role of cutinase in the penetration of apple leaves by Venturia inaequalis. Phytopathology 81:1375–1379

    CAS  Google Scholar 

  • Kreuze JF, Suomalainen S, Paulin L, Valkonen JP (1999) Phylogenetic analysis of 16SrRNA genes and PCR analysis of the nec1 gene from Streptomyces spp. causing common scab, pitted scab, and netted scab in Finland. Phytopathology 89:462–469

    CAS  PubMed  Google Scholar 

  • Laine MJ, Haapalainen M, Wahlroos T, Kankare K, Nissinen R, Kassuwi S, Metzler M (2000) The cellulase encoded by the native plasmid of Clavibacter michiganensis ssp. sepedonicus plays a role in virulence and contains an expansin-like domain. Physiol Mol Plant Pathol 57:221–233

    CAS  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    CAS  PubMed  Google Scholar 

  • Lautru S, Oves-Costales D, Pernodet JL, Challis GL (2007) MbtH-like protein-mediated cross-talk between non-ribosomal peptide antibiotic and siderophore biosynthetic pathways in Streptomyces coelicolor M145. Microbiology 153:1405–1412

    CAS  PubMed  Google Scholar 

  • Lawrence CH, Clark MC, King RR (1990) Induction of common scab symptoms in asceptically cultured potato tubers by the vivotoxin, thaxtomin. Phytopathology 80:606–608

    CAS  Google Scholar 

  • Lehtonen MJ, Rantala H, Kreuze JF, Bang H, Kuisma L, Koski P, Virtanen E, Vohlman K, Valkonen JP (2004) Occurrence and survival of potato scab pathogens (Streptomyces species) on tuber lesions: quick diagnosis based on a PCR-based assay. Plant Pathol 53:280–287

    Google Scholar 

  • Leiner RH, Fry B, Carling DE, Loria R (1996) Probable involvement of thaxtomin A in pathogencitiy of Streptomyces scabies on seedlings. Phytopathology 86:709–713

    CAS  Google Scholar 

  • Lerat S, Babana AH, El Oirdi M, El Hadrami A, Daayf F, Beaudoin N, Bouarab K, Beaulieu C (2009) Streptomyces scabiei and its toxin thaxtomin A induce scopoletin biosynthesis in tobacco and Arabidopsis thaliana. Plant Cell Rep 28:1985 1985

    Google Scholar 

  • Li Y, Darley CP, Ongaro V, Fleming A, Schipper O, Baldauf SL, McQueen-Mason SJ (2002) Plant expansins are a complex multigene family with an ancient evolutionary origin. Plant Physiol 128:854–864

    CAS  PubMed  Google Scholar 

  • Li D, Ashby AM, Johnstone K (2003) Molecular evidence that the extracellular cutinase Pbc1 is required for pathogenicity of Pyrenopeziza brassicae on oilseed rape. Mol Plant Microbe Interact 16:545–552

    CAS  PubMed  Google Scholar 

  • Lin TS, Kolattukudy PE (1980) Isolation and characterization of a cuticular polyester (cutin) hydrolyzing enzyme from phytopathogenic fungi. Physiol Mol Plant Pathol 17:1–15

    CAS  Google Scholar 

  • Loria R, Bukhalid RA, Fry BA, King RR (1997) Plant pathogenicity in the genus Streptomyces. Plant Dis 81:836–846

    Google Scholar 

  • Loria R, Coombs J, Yoshida M, Kers J, Bukhalid RA (2003) A paucity of bacterial root diseases: Streptomyces succeeds where others fail. Physiol Mol Plant Pathol 62:65–72

    Google Scholar 

  • Loria R, Kers J, Joshi M (2006) Evolution of plant pathogenicity in Streptomyces. Annu Rev Phytopathol 44:469–487

    CAS  PubMed  Google Scholar 

  • Loria R, Bignell DR, Moll S, Huguet-Tapia JC, Joshi MV, Johnson EG, Seipke RF, Gibson DM (2008) Thaxtomin biosynthesis: the path to plant pathogenicity in the genus Streptomyces. Antonie Van Leeuwenhoek 94:3–10

    PubMed  Google Scholar 

  • Maiti IB, Kolattukudy PE (1979) Prevention of fungal infection of plants by specific inhibition of cutinase. Science 205:507–508

    CAS  PubMed  Google Scholar 

  • Manulis S, Shafrir H, Epstein E, Lichter A, Barash I (1994) Biosynthesis of indole-3-acetic acid via the indole-3-acetamide pathway in Streptomyces spp. Microbiology 140(Pt 5):1045–1050

    CAS  PubMed  Google Scholar 

  • Manulis S, Haviv-Chesner A, Brandl MT, Lindow SE, Barash I (1998) Differential involvement of indole-3-acetic acid biosynthetic pathways in pathogenicity and epiphytic fitness of Erwinia herbicola pv. gypsophilae. Mol Plant Microbe Interact 11:634–642

    CAS  PubMed  Google Scholar 

  • Martinez C, Nicolas A, van Tilbeurgh H, Egloff MP, Cudrey C, Verger R, Cambillau C (1994) Cutinase, a lipolytic enzyme with a preformed oxyanion hole. Biochemistry 33:83–89

    CAS  PubMed  Google Scholar 

  • Mazzola M, White FF (1994) A mutation in the indole-3-acetic acid biosynthesis pathway of Pseudomonas syringae pv. syringae affects growth in Phaseolus vulgaris and syringomycin production. J Bacteriol 176:1374–1382

    CAS  PubMed  Google Scholar 

  • Meimoun P, Tran D, Baz M, Errakhi R, Dauphin A, Lehner A, Briand J, Biligui B, Madiona K, Beaulieu C, Bouteau F (2009) Two different signaling pathways for thaxtomin A-induced cell death in Arabidopsis and tobacco BY2. Plant Signal Behav 4:142–144

    CAS  PubMed  Google Scholar 

  • Melotto M, Mecey C, Niu Y, Chung HS, Katsir L, Yao J, Zeng W, Thines B, Staswick P, Browse J, Howe GA, He SY (2008) A critical role of two positively charged amino acids in the Jas motif of Arabidopsis JAZ proteins in mediating coronatine- and jasmonoyl isoleucine-dependent interactions with the COI1 F-box protein. Plant J 55:979–988

    CAS  PubMed  Google Scholar 

  • Natsume M, Ryu R, Abe H (1996) Production of phytotoxins, concanamycins A and B by Streptomyces spp. Ann Phytopathol Soc Jpn 62:411–413

    CAS  Google Scholar 

  • Natsume M, Yamada A, Tashiro N, Abe H (1998) Differential production of the phytotoxins thaxtomin A and concanamycins A and B by potato common scab-causing Streptomyces spp. Ann Phytopathol Soc Jpn 64:202–204

    CAS  Google Scholar 

  • Natsume M, Taki M, Tashiro N, Abe H (2001) Phytotoxin production and aerial mycelium formation by Streptomyces scabies and S. acidiscabies in vitro. J Gen Plant Pathol 67:299–302

    CAS  Google Scholar 

  • Natsume M, Komiya M, Koyanagi F, Tashiro N, Kawaide H, Abe H (2005) Phytotoxin produced by Streptomyces sp. causing potato russet scab. J Gen Plant Pathol 71:364–369

    CAS  Google Scholar 

  • Ohnishi Y, Ishikawa J, Hara H, Suzuki H, Ikenoya M, Ikeda H, Yamashita A, Hattori M, Horinouchi S (2008) Genome sequence of the streptomycin-producing microorganism Streptomyces griseus IFO 13350. J Bacteriol 190:4050–4060

    CAS  PubMed  Google Scholar 

  • Omura S, Imamura N, Hinotozawa K, Otaguro K, Hashimoto K, Nakagawa A (1982) AM-2604, a new antiviral antibiotic produced by a strain of Streptomyces. J Antibiot (Tokyo) 35:1632–1637

    CAS  Google Scholar 

  • Park DH, Kim JS, Kwon SW, Wilson C, Yu YM, Hur JH, Lim CK (2003a) Streptomyces luridiscabiei sp. nov., Streptomyces puniciscabiei sp. nov. and Streptomyces niveiscabiei sp. nov., which cause potato common scab disease in Korea. Int J Syst Evol Microbiol 53:2049–2054

    CAS  PubMed  Google Scholar 

  • Park DH, Yu YM, Kim JS, Cho JM, Hur JH, Lim CK (2003b) Characterization of streptomycetes causing potato common scab in Korea. Plant Dis 87:1290–1296

    CAS  Google Scholar 

  • Patten CL, Glick BR (1996) Bacterial biosynthesis of indole-3-acetic acid. Can J Microbiol 42:207–220

    CAS  PubMed  Google Scholar 

  • Quadri LE, Sello J, Keating TA, Weinreb PH, Walsh CT (1998) Identification of a Mycobacterium tuberculosis gene cluster encoding the biosynthetic enzymes for assembly of the virulence-conferring siderophore mycobactin. Chem Biol 5:631–645

    CAS  PubMed  Google Scholar 

  • Robert-Seilaniantz A, Navarro L, Bari R, Jones JD (2007) Pathological hormone imbalances. Curr Opin Plant Biol 10:372–379

    CAS  PubMed  Google Scholar 

  • Sampedro J, Cosgrove DJ (2005) The expansin superfamily. Genome Biol 6:242

    PubMed  Google Scholar 

  • Sato M, Urushizaki S, Nishiyama K, Sakai F, Ota Y (1987) Efficient production of ethylene by Pseudomonas syringae pv. glycinea which causes halo blight in soybeans. Agric Biol Chem 51:1177–1178

    CAS  Google Scholar 

  • Sato M, Watanabe K, Yazawa M, Takikawa Y, Nishiyama K (1997) Detection of new ethylene-producing bacteria, Pseudomonas syringae pvs. cannabina and sesami, by PCR amplification of genes for the ethylene-forming enzyme. Phytopathology 87:1192–1196

    CAS  PubMed  Google Scholar 

  • Scheible W-R, Fry B, Kochevenko A, Schindelasch D, Zimmerli L, Somerville S, Loria R, Somerville CR (2003) An Arabidopsis mutant resistant to thaxtomin A, a cellulose synthesis inhibitor from Streptomyces species. Plant Cell 15:1781–1794

    CAS  PubMed  Google Scholar 

  • Seipke RF, Loria R (2008) Streptomyces scabies 87–22 possesses a functional tomatinase. J Bacteriol 190:7684–7692

    CAS  PubMed  Google Scholar 

  • Seki-Asano M, Okazaki T, Yamagishi M, Sakai N, Hanada K, Mizoue K (1994) Isolation and characterization of new 18-membered macrolides FD-891 and FD-892. J Antibiot (Tokyo) 47:1226–1233

    CAS  Google Scholar 

  • Shaykh M, Soliday C, Kolattukudy PE (1977) Proof for the production of cutinase by Fusarium solani f. sp. pisi during penetration into its host, Pisum sativum. Plant Physiol 60:170–177

    CAS  PubMed  Google Scholar 

  • Skamnioti P, Gurr SJ (2007) Magnaporthe grisea Cutinase2 mediates appressorium differentiation and host penetration and is required for full virulence. Plant Cell 19:2674–2689

    CAS  PubMed  Google Scholar 

  • Song J, Lee SC, Kang JW, Baek HJ, Suh JW (2004) Phylogenetic analysis of Streptomyces spp. isolated from potato scab lesions in Korea on the basis of 16S rRNA gene and 16S-23S rDNA internally transcribed spacer sequences. Int J Syst Evol Microbiol 54:203–209

    CAS  PubMed  Google Scholar 

  • Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448

    CAS  PubMed  Google Scholar 

  • St-Onge R, Goyer C, Coffin R, Filion M (2008) Genetic diversity of Streptomyces spp. causing common scab of potato in eastern Canada. Syst Appl Microbiol 31:474–484

    CAS  PubMed  Google Scholar 

  • Surico G, Comai L, Kosuge T (1984) Pathogenicity of strains of Pseudomonas syringae pv. savastanoi and their idoleacetic acid-deficient mutants on olive and oleander. Phytopathology 74:490–493

    Google Scholar 

  • Tegg RS, Melian L, Wilson CR, Shabala S (2005) Plant cell growth and ion flux responses to the streptomycete phytotoxin thaxtomin A: calcium and hydrogen flux patterns revealed by the non-invasive MIFE technique. Plant Cell Physiol 46:638–648

    CAS  PubMed  Google Scholar 

  • Thilmony R, Underwood W, He SY (2006) Genome-wide transcriptional analysis of the Arabidopsis thaliana interaction with the plant pathogen Pseudomonas syringae pv. tomato DC3000 and the human pathogen Escherichia coli O157:H7. Plant J 46:34–53

    CAS  PubMed  Google Scholar 

  • Uppalapati SR, Ayoubi P, Weng H, Palmer DA, Mitchell RE, Jones W, Bender CL (2005) The phytotoxin coronatine and methyl jasmonate impact multiple phytohormone pathways in tomato. Plant J 42:201–217

    CAS  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 Pathogens 2:0798–0807

    CAS  Google Scholar 

  • van Loon LC, van Strien EA (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 55:85–97

    Google Scholar 

  • van Loon LC, Geraats BP, Linthorst HJ (2006a) Ethylene as a modulator of disease resistance in plants. Trends Plant Sci 11:184–191

    PubMed  Google Scholar 

  • van Loon LC, Rep M, Pieterse CM (2006b) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162

    PubMed  Google Scholar 

  • Vandeputte O, Oden S, Mol A, Vereecke D, Goethals K, El Jaziri M, Prinsen E (2005) Biosynthesis of auxin by the Gram-positive phytopathogen Rhodococcus fascians is controlled by compounds specific to infected plant tissues. Appl Environ Microbiol 71:1169–1177

    CAS  PubMed  Google Scholar 

  • VanEtten HD, Mansfield JW, Bailey JA, Farmer EE (1994) Two classes of plant antibiotics: phytoalexins versus “phytoanticipins”. Plant Cell 6:1191–1192

    CAS  PubMed  Google Scholar 

  • Wanner LA (2006) A survey of genetic variation in Streptomyces isolates causing potato common scab in the United States. Phytopathology 96:1363–1371

    CAS  PubMed  Google Scholar 

  • Wanner LA (2007) A new strain of Streptomyces causing common scab in potato. Plant Dis 91:352–359

    CAS  Google Scholar 

  • Wanner LA (2009) A patchwork of Streptomyces species isolated from potato common scab lesions in North America. Am J Pot Res 86:247–264

    Google Scholar 

  • Weingart H, Volksch B, Ullrich MS (1999) Comparison of ethylene production by Pseudomonas syringae and Ralstonia solanacearum. Phytopathology 89:360–365

    CAS  PubMed  Google Scholar 

  • Wolpert M, Gust B, Kammerer B, Heide L (2007) Effects of deletions of mbtH-like genes on clorobiocin biosynthesis in Streptomyces coelicolor. Microbiology 153:1413–1423

    CAS  PubMed  Google Scholar 

  • Yang S, Zhang Q, Guo J, Charkowski AO, Glick BR, Ibekwe AM, Cooksey DA, Yang CH (2007) Global effect of indole-3-acetic acid biosynthesis on multiple virulence factors of Erwinia chrysanthemi 3937. Appl Environ Microbiol 73:1079–1088

    CAS  PubMed  Google Scholar 

  • Zhao Y, Thilmony R, Bender CL, Schaller A, He SY, Howe GA (2003) Virulence systems of Pseudomonas syringae pv. tomato promote bacterial speck disease in tomato by targeting the jasmonate signaling pathway. Plant J 36:485–499

    CAS  PubMed  Google Scholar 

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Acknowledgement

This work was supported by the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service, grant numbers 2008-35319-19202 (to R. Loria) and 2007-35600- 17813 (to G. Pettis).

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Authors and Affiliations

  1. Department of Plant Pathology and Plant-Microbe Biology, Cornell University, Ithaca, NY, 14853, USA

    Dawn R. D. Bignell, José C. Huguet-Tapia, Madhumita V. Joshi & Rosemary Loria

  2. Department of Biological Sciences, Louisiana State University, Baton Rouge, LA, 70803, USA

    Gregg S. Pettis

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  1. Dawn R. D. Bignell
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  2. José C. Huguet-Tapia
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  3. Madhumita V. Joshi
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  4. Gregg S. Pettis
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  5. Rosemary Loria
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Correspondence to Rosemary Loria.

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Bignell, D.R.D., Huguet-Tapia, J.C., Joshi, M.V. et al. What does it take to be a plant pathogen: genomic insights from Streptomyces species. Antonie van Leeuwenhoek 98, 179–194 (2010). https://doi.org/10.1007/s10482-010-9429-1

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