Abstract
Fungi belonging to the genus Phoma form a phylogenetically heterogeneous group with a broad range of possible plant hosts. Most of them do not interfere with cultivation of crops; others, especially Phoma lingam with its perfect form Leptosphaeria maculans, are the causative agent of devastating field losses in rapeseed cultivation. Efficient disease management requires profound fundamental knowledge on biology and genetics of these organisms, which needs to be transferred into practical rules, effective for disease control in the field.
Good disease management implies reliable diagnosis tools, and reasonable procedures taking into account knowledge on infection pathways, the secretion of enzymes and toxins, and on the effects that these Phoma-specific substances cause in plants. Phoma forecasting, together with reasonable fungicide and cultivation regimes, are indispensable to avoid losses. Conventional breeding programmes for resistance have already been helpful in the past. Knowledge of various avirulence genes from Leptosphaeria maculans, together with the tremendously useful information from the genome sequence, will facilitate efficient plant breeding programmes in the future.
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References
Abeln ECA, Stax AM, De Gruyter J, van der Aa HA (2002) Genetic differentiation of Phoma exigua varieties by means of AFLP fingerprints. Mycol Res 106:419–427
Alabouvette C, Brunin B (1970) Recherches sur la maladie de colza due a Leptosphaeria maculans (Desm.): Ces. et de Not. I. Rôle des restes de culture dans la conservation et la dissemination du parasite. Ann Phytopathol 6:463–475
Annis SL, Goodwin PH (1996) Comparison of cell wall-degrading enzymes produced by highly and weakly virulent isolates of Leptosphaeria maculans in culture. Microbiol Res 151:401–406
Annis SL, Goodwin PH (1997) Inhibition of polygalacturonase activity produced by Leptosphaeria maculans with stem extracts of canola, and the relationship of inhibition to resistance. J Phytopathol 145:217–223
Ansan-Melayah D, Balesdent MH, Buée M, Rouxel T (1995) Genetic characterization of AvrLm1, the first avirulence gene of Leptosphaeria maculans. Phytopathol 85:1525–1529
Ansan-Melayah D, Balesdent MH, Delourme R, Pilet ML, Tanguy X, Renard M, Rouxel T (1998) Genes for race-specific resistance against blackleg disease in Brassica napus L. Plant Breed 117:373–378
Attard A, Gourges M, Gout L, Schmit J, Roux J, Narcy JP, Balesdent MH, Rouxel T (2001) Molecular characterisation and polymorphism of MinLm1, a minisatellite from the phytopathogenic ascomycete Leptosphaeria maculans. Curr Genet 40:54–64
Attard A, Gout L, Gourgues M, Kühn ML, Schmit J, Laroche S, Ansan-Melayah D, Billault A, Cattolico L, Balesdent MH, Rouxel T (2002) Analysis of molecular markers genetically linked to the Leptosphaeria maculans avirulence gene AvrLm1 in field populations indicates a highly conserved event leading to virulence on Rlm1 genotypes. Mol Plant Microbe Interact 15:672–682
Aubertot JN, West JS, Bousset-Vaslin L, Salam MU, Barbetti MJ, Diggle AJ (2006) Improved resistance management for durable disease control: a case study of Phoma stem canker of oilseed rape (Brassica napus). Eur J Plant Pathol 114:91–106
Aveskamp MM, De Gruyter J, Crous PW (2008) Biology and recent development in the systematics of Phoma, a complex genus of major quarantine significance. Fungal Divers 31:1–18
Aveskamp MM, De Gruyter J, Woudenberg JHC, Verkley GJM, Crous PW (2010) Highlights of the Didymellaceae: a polyphasic approach to characterize Phoma and related pleosporalean genera. Stud Mycol 65:1–60
Badawy HMA, Hoppe HH (1989a) Production of phytotoxic sirodesmins by aggressive strains of Leptosphaeria maculans differing in interactions with oil seed rape genotypes. J Phytopathol 127:146–157
Badawy HMA, Hoppe HH (1989b) Nonspecific phytotoxic effects of sirodesmins on host and nonhost plants of Leptosphaeria maculans. J Phytopathol 127:137–145
Balesdent MH, Gall C, Robin P, Rouxel T (1992) Intraspecific variation in soluble mycelial protein and esterase patterns of Leptosphaeria maculans French isolates. Mycol Res 96:677–684
Balesdent MH, Attard A, Ansan-Melayah D, Delourme R, Renard M, Rouxel T (2001) Genetic control and host range of avirulence toward Brassica napus cultivars Quinta and Jet Neuf in Leptosphaeria maculans. Phytopathology 91:70–76
Balesdent MH, Attard A, Kühn ML, Rouxel T (2002) New avirulence genes in the phytopathogenic fungus Leptosphaeria maculans. Phytopathology 92:1122–1133
Balesdent MH, Barbetti MJ, Li H, Sivasithamparam K, Gout L, Rouxel T (2005) Analysis of Leptosphaeria maculans race structure in a worldwide collection of isolates. Phytopathology 95:1061–1071
Balesdent MH, Louvard K, Pinochet X, Rouxel T (2006) A large-scale survey of races of Leptosphaeria maculans occurring on oilseed rape in France. Eur J Plant Pathol 114:53–65
Balmas V, Scherm B, Ghignone S, Salem AOM, Cacciola AO, Migheli Q (2005) Characterisation of Phoma tracheiphila by RAPD-PCR, microsatellite-primed PCR and ITS rDNA sequencing and development of specific primers for in planta PCR detection. Eur J Plant Pathol 111:235–247
Bansal VK, Thiagarajah MR, Stringam GR, Hardin RT (1998) Haploid plantlet screening in the development of blackleg resistant DH lines of Brassica napus. Plant Breed 117:103–106
Bayraktar H, Dolar FS, Tor M (2007) Determination of genetic diversity within Ascochyta rabiei (Pass.) Labr., the cause of Ascochyta blight of chickpea in Turkey. J Plant Pathol 89:341–347
Boerema GH (1997) Contributions towards a monograph of Phoma (coelomycetes). 5. Subdivision of the genus in sections. Mycotaxon 64:321–333
Boerema GH, Dorenbosch MMJ, Leffring L (1965a) A comparative study of the black stem fungi on lucerne and red clover and the footrot fungus on pea. Neth J Plant Pathol 71:79–89
Boerema GH, Dorenbosch MMJ, van Kesteren HA (1965b) Remarks on species of Phoma referred to Peyronellaea. Persoonia 4:47–68
Bohman S, Wang M, Dixelius C (2002) Arabidopsis thaliana-derived resistance against Leptosphaeria maculans in a Brassica napus genomic background. Theor Appl Genet 105:498–504
Bose AK, Khanchan KS, Tavares R, Funke PT (1968) Biochemical studies II. The mode of incorporation of phenylalanine into gliotoxin. J Am Chem Soc 90:3593–3594
Boudart G (1978) Phytotoxine et nécrose des hypocotyles de crucifères infectées par Leptosphaeria maculans (Ces. et de Not.) et sa forme imparfaite Phoma lingam. Phytopathology 92:76–82
Boudart G (1989) Antibacterial activity of sirodesmin PL phytotoxin: application to the selection of phytotoxin-deficient mutants. Appl Environ Microbiol 55:1555–1559
Bousquet JF, Férézou JP, Devys M, Barbier M (1977) Sur une toxine produite par le champignon Phoma lingam Tode, parasite du colza: isolement et propriétés. C R Acad Sci Paris, Ser D 284:927–928
Brock M (2009) Fungal metabolism in host niches. Curr Opin Microbiol 12:371–376
Bugbee WM (1990) Combined resistance in sugar beet to Rhizoctonia solani, Phoma betae, and Botrytis cinerera. Plant Dis 74:353–355
Bugbee WM (1993) A pectin lyase inhibitor protein from cell walls of sugar beet. Phytopathology 83:63–68
Castell-Miller CV, Szabo LJ, Gale LR, O’Neill NR, Samac DA (2008) Molecular variability of a Minnesota population of Phoma medicaginis var. medicaginis, the causal agent of spring black stem and leaf spot of alfalfa. Can J Plant Pathol 30:85–96
Cozijnsen AJ, Howlett BJ (2003) Characterisation of the mating-type locus of the plant pathogenic ascomycete Leptosphaeria maculans. Curr Genet 43:351–357
Crouch JH, Lewis BG, Mithen RF (1994) The effect of a genome substitution on the resistance of Brassica napus to infection by Leptosphaeria maculans. Plant Breed 112:265–278
Curtis PJ, Greatbanks D, Hesp B, Forbes Cameron A, Freer AA (1977) Sirodesmins A, B, C, and G, antiviral epipolythiopiperazine-2,5-diones of fungal origin: X-ray analysis of sirodesmin A diacetate. J Chem Soc Perkin I:180–189
De March G, Séguin-Swartz G, Petrie GA (1986) Virulence and culture filtrate phytotoxicity in Leptosphaeria maculans: perspectives for in vitro selection. Can J Plant Pathol 8:422–428
Demontis MA, Cacciola SO, Orrù M, Balmas V, Chessa V, Maserti BE, Mascia L, Raudino F, di San Lio GM, Migheli Q (2008) Development of real-time PCR systems based on SYBR® Green I and TaqMan® technologies for specific quantitative detection of Phoma tracheiphila in infected Citrus. Eur J Plant Pathol 120:339–351
Devys M, Férézou JP, Topgi RS, Barbier M, Bousquet JF, Kollmann A (1984) Structure and biosynthesis of phomenoic acid, an antifungal compound isolated from Phoma lingam Tode. J Chem Soc Perkin Trans I:2133–2137
Devys M, Topgi RS, Férézou JP, Quaino L, Bousquet JF, Kollman A, Barbier M (1986) Phomenolactone, an antifungal substance from Phoma lingam. Phytochemistry 25:531–532
Diederichsen E, Sacristán MD (1996) Disease response of resynthesized Brassica napus L. lines carrying different combinations of resistance to Plasmodiophora brassicae Wor. Plant Breed 115:5–10
Dixelius C (1999) Inheritance of the resistance to Leptosphaeria maculans of Brassica nigra and B. juncea in near-isogenic lines of B. napus. Plant Breed 118:151–156
Dixelius C, Wahlberg S (1999) Resistance to Leptosphaeria maculans is conserved in a specific region of the Brassica B genome. Theor Appl Genet 99:368–372
Dusabenyagasani M, Fernando WGD (2008) Development of a SCAR marker to track canola resistance against blackleg caused by Leptosphaeria maculans pathogenicity group 3. Plant Dis 92:903–908
Easton CJ, Rossall S (1985) The production of certain cell wall-degrading enzymes by Leptosphaeria maculans in culture and in stem canker lesions of oilseed rape. Physiol Plant Pathol 26:185–197
Eckert M, Gout L, Rouxel T, Blaise F, Jedryczka M, Fitt B, Balesdent MH (2005) Identification and characterization of polymorphic minisatellites in the phytopathogenic ascomycete Leptosphaeria maculans. Curr Genet 47:37–48
Eckert MR, Rossall S, Selley A, Fitt BDL (2009) Effects of fungicides on in vitro spore germination and mycelial growth of the phytopathogens Leptosphaeria maculans and L. biglobosa (Phoma stem canker of oilseed rape). Pest Manag Sci 66:396–405
Elliott CE, Gardiner DM, Thomas GD, Cozijnsen A, van de Wouw A, Howlett BJ (2007) Production of the toxin sirodesmin PL by Leptosphaeria maculans during infection of Brassica napus. Mol Plant Pathol 8:791–802
Elliott CA, Fox EM, Jarvis RS, Howlett BJ (2011) The cross-pathway control system regulates production of the secondary metabolite toxin, sirodesmin PL, in the ascomycete, Leptosphaeria maculans. BMC Microbiol 11:169
Ezra D, Kroitor T, Sadowsky A (2007) Molecular characterization of Phoma tracheiphila, causal agent of mal secco disease in Citrus, in Israel. Eur J Plant Pathol 118:183–191
Farman ML, Oliver RP (1988) The transformation of protoplasts of Leptosphaeria maculans to hygromycin B resistance. Curr Genet 13:327–330
Farman ML, Oliver RP (1992) Transformation frequencies are enhanced and vector DNA is targeted during retransformation of Leptosphaeria maculans, a fungal plant pathogen. Mol Gen Genet 231:243–247
Feldman TS, O’Brien HE, Arnold AE (2008) Moths that vector a plant pathogen also transport endophytic fungi and mycoparasitic antagonists. Microb Ecol 56:742–750
Férézou JP, Riche C, Quesneau-Thierry A, Pascard-Billy C, Barbier M, Bousquet JF, Boudart G (1977) Structures de deux toxins isolées des cultures du champignon Phoma lingam Tode: La sirodesmine PL et la désacétylsirodesmine PL. Nouv J Chim 1:327–333
Férézou JP, Quesneau-Thierry A, Barbier M, Kollmann A, Bousquet JF (1980a) Structure and synthesis of phomamide, a new piperazine-2,5-dione related to the sirodesmins, isolated from the culture medium of Phoma lingam Tode. J Chem Soc Perkin I:113–115
Férézou JP, Quesneau-Thierry A, Servy C, Zissmann E, Barbier M (1980b) Sirodesmin PL biosynthesis in Phoma lingam Tode. J Chem Soc Perkin I:1739–1746
Fogliano V, Marchese A, Scaloni A, Ritieni A, Visconti A, Randazzo G, Graniti A (1998) Characterization of a 60 kDa phytotoxic glycoprotein produced by Phoma tracheiphila and its relation to malseccin. Physiol Mol Plant Pathol 53:149–161
Fox EM, Gardiner DM, Keller NP, Howlett BJ (2008) A Zn(II)2Cys6 DNA binding protein regulates the sirodesmin PL biosynthetic gene cluster in Leptosphaeria maculans. Fung Genet Biol 45:671–682
Gabrielson RL (1983) Blackleg disease of crucifers caused by Leptosphaeria maculans (Phoma lingam) and its control. Seed Sci Technol 11:749–780
Gall C, Balesdent MH, Desthieux I, Robin P, Rouxel T (1995) Polymorphism of Tox0 Leptosphaeria maculans isolates as revealed by soluble protein and isozyme electrophoresis. Mycol Res 99:221–229
Gardiner DM, Cozijnsen AJ, Wilson LM, Pedras MSC, Howlett BJ (2004a) The sirodesmin biosynthetic gene cluster of the plant pathogenic fungus Leptosphaeria maculans. Mol Microbiol 53:1307–1318
Gardiner DM, Jarvis RS, Howlett BJ (2004b) The ABC transporter gene in the sirodesmin biosynthetic gene cluster of Leptosphaeria maculans is not essential for sirodesmin production but facilitates self-protection. Fungal Genet Biol 42:257–263
Ghanbarnia K, Lydiate DJ, Rimmer SR, Li G, Kutcher HR, Larkan NJ, McVetty PBE, Fernando WGD (2012) Genetic mapping of the Leptosphaeria maculans avirulence gene corresponding to the LepR1 resistance gene of Brassica napus. Theor Appl Genet 124:505–513
Goodwin PH, Annis SL (1991) Rapid identification of genetic variation and pathotype of Leptosphaeria maculans by random amplified polymorphic DNA assay. Appl Environ Microbiol 57:2482–2486
Gout L, Fudal I, Kuhn ML, Blaise F, Eckert M, Cattolico L, Balesdent M-H, Rouxel T (2006) Lost in the middle of nowhere: the AvrLm1 avirulence gene of the dothideomycete Leptosphaeria maculans. Mol Microbiol 60:67–80
Hammond KE, Lewis BG (1986) The timing and sequence of events leading to stem canker disease in populations of Brassica napus var. oleifera in the field. Plant Pathol 35:551–564
Hammond KE, Lewis BG (1987) The establishment of systemic infection in leaves of oilseed rape by Leptosphaeria maculans. Plant Pathol 36:135–147
Hammond KE, Lewis BG, Musa TM (1985) A systemic pathway in the infection of oilseed rape plants by Leptosphaeria maculans. Plant Pathol 34:557–565
Hassan AK, Schulz C, Sacristan MD, Wöstemeyer J (1991) Biochemical and molecular tools for the differentiation of aggressive and non-aggressive isolates of the oilseed rape pathogen, Phoma lingam. J Phytopathol 131:120–136
Hill CB, Xu XH, Williams PH (1984) Correlations of virulence, growth rate, pigment production and allozyme banding patterns which differentiate virulent and avirulent isolates of Leptosphaeria maculans. Cruciferae Newslett 9:79
Hoffmann W, Peters R (1958) Versuche zur Herstellung synthetischer und semisynthetischer Rapsformen. Der Züchter 28:40–51
Hosford RM (1975) Phoma glomerata, a new pathogen of wheat and Triticales, cultivar resistance related to wet period. Phytopathology 65:1236–1239
Howlett BJ (1997) Genome analysis of the fungal plant pathogen Leptosphaeria maculans using pulsed field gel electrophoresis. Electrophoresis 18:1544–1547
Howlett BJ (2004) Current knowledge of the Brassica napus – Leptosphaeria maculans interaction: a review. Can J Plant Pathol 26:245–252
Howlett BJ, Idnurm A, Pedras MSC (2001) Leptosphaeria maculans, the causal agent of blackleg disease of Brassicas. Fung Genet Biol 33:1–14
Hu Q, Andersen SB, Dixelius C, Hansen LN (2002) Production of fertile intergeneric somatic hybrids between Brassica napus and Sinapis arvensis for the enrichment of the rapeseed gene pool. Plant Cell Rep 21:147–152
Huang YJ, Hood JR, Eckert MR, Stonard JF, Cools HJ, King GJ, Rossall S, Ashworth M, Fitt BDL (2011) Effects of fungicide on growth of Leptosphaeria maculans and L. biglobosa in relation to development of Phoma stem canker on oilseed rape (Brassica napus). Plant Pathol 60:607–620
Humpherson-Jones FM, Burchill RT (1982) Chemical suppression of the sexual stage of Leptosphaeria maculans on oil-seed rape and turnip seed crop straw. Ann Appl Biol 100:281–288
Idnurm A, Howlett BJ (2002) Isocitrate lyase is essential for pathogenicity of the fungus Leptosphaeria maculans to canola (Brassica napus). Eukaryot Cell 1:719–724
Idnurm A, Howlett BJ (2003) Analysis of loss of pathogenicity mutants reveals that repeat-induced point mutations can occur in the Dothideomycete Leptosphaeria maculans. Fungal Genet Biol 39:31–37
Jestin C, Lodé M, Vallée P, Domin C, Falentin C, Horvais R, Coedel S, Manzanares-Dauleux MJ, Delourme R (2011) Association mapping of quantitative resistance for Leptosphaeria maculans in oilseed rape (Brassica napus L.). Mol Breed 27:271–287
Johnson RD, Lewis BG (1990) DNA polymorphism in Leptosphaeria maculans. Physiol Mol Plant Pathol 37:417–424
Kaczmarek J, Jedryczka M, Fitt BDL, Lucas JA, Latunde-Dada AO (2009) Analyses of air samples for ascospores of Leptosphaeria maculans and L. biglobosa by light microscopy and molecular techniques. J Appl Genet 50:411–419
Kaur S, Cogan NOI, Ye G, Baillie RC, Hand ML, Ling AE, Mcgeary AK, Kaur J, Hopkins CJ, Todorovic M, Mountford H, Edwards D, Batley J, Burton W, Salisbury P, Gororo N, Marcroft S, Kearney G, Smith KF, Forster JW, Spangenberg GC (2009) Genetic map construction and QTL mapping of resistance to blackleg (Leptosphaeria maculans) disease in Australian canola (Brassica napus L.) cultivars. Theor Appl Genet 120:71–83
Koch E, Badawy HMA, Hoppe HH (1989) Differences between aggressive and non-aggressive single spore lines of Leptosphaeria maculans in cultural characteristics and phytotoxin production. J Phytopathol 124:52–62
Koch E, Song K, Osborn TC, Williams PH (1991) Relationship between pathogenicity and phylogeny based on restriction fragment length polymorphism in Leptosphaeria maculans. Mol Plant-Microbe Interact 4:341–349
Kremer A, Li SM (2010) A tyrosine O-prenyltransferase catalyses the first pathway-specific step in the biosynthesis of sirodesmin PL. Microbiology 156:278–286
Kuhn ML, Gout L, Howlett BJ, Melayah D, Meyer M, Balesdent MH, Rouxel T (2006) Genetic linkage maps and genomic organization in Leptosphaeria maculans. Eur J Plant Pathol 114:17–31
Kuswinanti T, Koopmann B, Hoppe HH (1999) Virulence pattern of aggressive isolates of Leptosphaeria maculans on an extended set of Brassica differentials. J Plant Dis Protect 106:12–20
Kutcher HR, van den Berg CGJ, Rimmer SR (1993) Variation in pathogenicity of Leptosphaeria maculans on Brassica spp. Based on cotyledon and stem reactions. Can J Plant Pathol 15:253–258
Licciardello G (2006) Identification and detection of Phoma tracheiphila, causal agent of Citrus mal secco disease, by real-time polymerase chain reaction. Plant Dis 90:1523–1530
Lieckfeldt E, Meyer W, Börner T (1993) Rapid identification and differentiation of yeasts by DNA and PCR fingerprinting. J Basic Microbiol 33:413–426
Lim L, Howlett BJ (1994) Linear plasmids, pLm9 and pLM10, can be isolated from the phytopathogenic ascomycete Leptosphaeria maculans by pulsed-field gel electrophoresis. Curr Genet 26:276–280
Liu SY, Liu Z, Fitt BDL, Evans N, Foster SJ, Huang YJ, Latunde-Dada AO, Lucas JA (2006) Resistance to Leptosphaeria maculans (Phoma stem canker) in Brassica napus (oilseed rape) induced by L. biglobosa and chemical defence activators in field and controlled environments. Plant Pathol 55:401–412
Long Y, Wang Z, Sun Z, Fernando DWG, McVetty PBE, Li G (2011) Identification of two blackleg resistance genes and fine mapping of one of these two genes in a Brassica napus canola cultivar ‘Surpass 400’. Theor Appl Genet 122:1223–1231
Marcroft SJ, Potter TD (2008) The fungicide fluquinconazole applied as a seed dressing to canola reduces Leptosphaeria maculans (blackleg) severity in south-eastern Australia. Australas Plant Pathol 37:396–401
Marcroft SJ, Sprague SJ, Pymer SJ, Salisbury PA, Howlett BJ (2004) Crop isolation, not extended rotation length, reduces blackleg (Leptosphaeria maculans) severity of canola (Brassica napus) in south-eastern Australia. Aust J Exp Agric 44:601–606
Mayerhofer R, Bansal VK, Thiagarajah MR, Stringam GR, Good AG (1997) Molecular mapping of resistance to Leptosphaeria maculans in Australian cultivars of Brassica napus. Genome 40:294–301
McGee GC, Petrie GA (1978) Variability of Leptosphaeria maculans in relation to blackleg of oilseed rape. Phytopathology 68:625–630
Melouk HA, Horner CE (1972) Production of pectolytic and macerating enzyme by Phoma strasseri. Can J Microbiol 18:1065–1072
Mendes-Pereira E, Balesdent MH, Brun H, Rouxel T (2003) Molecular phylogeny of the Leptosphaeria maculans – L. biglobosa species complex. Mycol Res 107:1287–1304
Mengistu A, Rimmer SR, Koch E, Williams PH (1991) Pathogenicity grouping of isolates of Leptosphaeria maculans on Brassica napus cultivars and their disease reaction profiles on rapid-cycling brassicas. Plant Dis 75:1279–1282
Meyer W, Lieckfeldt E, Wöstemeyer J, Börner T (1992) DNA fingerprinting for differentiating aggressiveness groups of the rapeseed pathogen Leptosphaeria maculans. Mycol Res 96:651–657
Monte E, Bridge PD, Sutton BC (1991) An integrated approach to Phoma systematics. Mycopathologia 115:89–103
Morgan-Jones G, Burch KB (1988a) Studies in the genus Phoma XII. Concerning Phoma destructiva, a second species implicated as a pathogen of tomato. Mycotaxon 32:253–265
Morgan-Jones G, Burch KB (1988b) Studies in the genus Phoma XI. Concerning Phoma lycopersici, the anamorph of Didymella lycopersici, causal organism of stem canker and fruit rot of tomato. Mycotaxon 32:133–142
Morinaga T (1934) Interspecific hybridisation in Brassica. VI. The cytology of F1 hybrids of B. juncea and B. nigra. Cytologia 6:62–67
Munday R (1989) Toxicity of thiols and disulphides: involvement of free radical species. Free Radical Biol Med 7:659–673
Olsson G (1960) Species crosses within the genus Brassica. II. Artificial Brassica napus L. Hereditas 46:351–386
Parlange F, Daverdin G, Fudal I, Kuhn ML, Balesdent MH, Blaise F, Grezes-Besset B, Rouxel T (2009) Leptosphaeria maculans avirulence gene AvrLm4-7 confers a dual recognition specificity by the Rlm4 and Rlm7 resistance genes of oilseed rape, and circumvents Rlm4-mediated recognition through a single amino acid change. Mol Microbiol 71:851–863
Pažoutová S (2009) Genetic variation of Phoma sorghina isolates from Southern Africa and Texas. Folia Microbiol 54:217–229
Pedras MSC, Biesenthal CJ (2000a) HPLC analyses of cultures of Phoma spp.: differentiation among groups and species through secondary metabolite profiles. Can J Microbiol 46:685–691
Pedras MSC, Biesenthal CJ (2000b) Vital staining of plant cell suspension cultures: evaluation of the phytotoxic activity of the phytotoxins phomalide and destruxin B. Plant Cell Rep 19:1135–1138
Pedras MSC, Séguin-Swartz G (1990) Rapid high-performance liquid chromatographic analysis of phytotoxins from Phoma lingam. J Chromatogr 519:383–386
Pedras MSC, Yu Y (2008) Structure and biological activity of maculansin A, a phytotoxin from the phytopathogenic fungus Leptosphaeria maculans. Phytochemistry 69:2966–2971
Pedras MSC, Abrams SR, Séguin-Swartz G, Quail JW, Jia Z (1989) Phomalirazine, a novel toxin from the phytopathogenic fungus Phoma lingam. J Am Chem Soc 111:1904–1905
Pedras MSC, Morales VM, Taylor JL (1993a) Phomaligols and phomaligadiones: new metabolites from the blackleg fungus. Tetrahedron 49:8317–8322
Pedras MSC, Morales VM, Taylor JL (1993b) Phomapyrones: three metabolites from the blackleg fungus. Phytochemistry 36:1315–1318
Pedras MSC, Taylor JL, Morales VM (1995) Phomaligin A and other yellow pigments in Phoma lingam and P. wasabiae. Phytochemistry 38:1215–1222
Perrotta G, Graniti A (1988) Phoma tracheiphila (Petri) Kanchaveli and Gikashvili. In: Smith IM, Dunez J, Lelliott RA, Phillips DH, Archer SA (eds) European handbook of plant diseases. Blackwell Scientific, Oxford, pp 396–398
Persson M, Staal J, Oide S, Dixelius C (2009) Layers of defense responses to Leptosphaeria maculans below the RLM1- and camalexin-dependent resistances. New Phytol 182:470–482
Pertrie GA, Lewis PA (1985) Sexual compatibility of isolates of the rapeseed blackleg fungus Leptosphaeria maculans from Canada, Australia, and England. Can J Plant Pathol 7:253–255
Pethybridge SJ, Hay FS (2001) Influence of Phoma ligulicola on yield, and site factors on disease development, in Tasmanian pyrethrum crops. Australas Plant Pathol 30:17–20
Pethybridge SJ, Scott JB, Hay FS (2004) Genetic relationships among isolates of Phoma ligulicola from pyrethrum and chrysanthemum based on ITS sequences and its detection by PCR. Australas Plant Pathol 33:173–181
Pethybridge SJ, Hay FS, Clarkson RA, Groom T, Wilson CR (2008) Host range of Australian Phoma ligulicola var. inoxydablis isolates from pyrethrum. J Phytopathol 156:506–508
Plieske J, Struss D, Röbbelen G (1998) Inheritance of resistance derived from the B-genome of Brassica against Phoma lingam in rapeseed and the development of molecular markers. Theor Appl Genet 97:929–936
Plummer KM, Howlett BJ (1995) Inheritance of chromosomal length polymorphism in the ascomycete Leptosphaeria maculans. Mol Gen Genet 247:416–422
Poiret B, Kollmann A, Bousquet JF (1985) Activités antifongiques de la sirodesmine PL et de deux analogues naturels isolés de Phoma lingam (Tode) Desm. Action antagoniste du zinc. Agronomie 5:533–538
Pollero R, Gaspar ML, Cabello M (1997) Lipolytic activity in free and immobilized cells of Phoma glomerata. JAOCS 74:451–454
Pollero R, Gaspar ML, Cabello M (2001) Extracellular lipolytic activity in Phoma glomerata. World J Microbiol Biotechnol 17:805–809
Pongam P, Osborn TC, Williams PH (1999) Assessment of genetic variation among Leptosphaeria maculans isolates using pathogenicity data and AFLP analysis. Plant Dis 83:149–154
Purwantara A, Salisbury PA, Burton WA, Howlett BJ (1998) Reaction of Brassica juncea (Indian mustard) lines to Australian isolates of Leptosphaeria maculans under glasshouse and field conditions. Eur J Plant Pathol 104:895–902
Purwantara A, Barrins JM, Cozijnsen AJ, Ades PK, Howlett BJ (2000) Genetic diversity of isolates of the Leptosphaeria maculans species complex from Australia, Europe and North America using amplified fragment length polymorphism analysis. Mycol Res 104:772–781
Remy E, Meyer M, Blaise F, Chabirand M, Wolff N, Balesdent MH, Rouxel T (2008a) The Lmpma1 gene of Leptosphaeria maculans encodes a plasma membrane H+-ATPase isoform essential for pathogenicity towards oilseed rape. Fung Genet Biol 45:1122–1134
Remy E, Meyer M, Blaise F, Simon UK, Kuhn D, Chabirand M, Riquelme M, Balesdent MH, Rouxel T (2008b) The Lmgpi15 gene, encoding a component of the glycosylphosphatidylinositol anchor biosynthesis pathway, is required for morphogenesis and pathogenicity in Leptosphaeria maculans. New Phytol 179:1105–1120
Remy E, Meyer M, Blaise F, Simon UK, Kuhn D, Balesdent MH, Rouxel T (2009) A key enzyme of the Leloir pathway is involved in pathogenicity of Leptosphaeria maculans towards oilseed rape. Mol Plant Microbe Interact 22:725–736
Rosewich UL, Kistler HC (2000) Role of horizontal gene transfer in the evolution of fungi. Annu Rev Phytopathol 38:325–363
Roustaee A, Dechamp-Guillaume G, Gelie B, Savy C, Dargent R, Barrault G (2000) Ultrastructural studies of the mode of penetration by Phoma macdonaldii in sunflower seedlings. Phytopathology 90:915–920
Rouxel T, Chupeau Y, Fritz R, Kollmann A, Bousquet JF (1988) Biological effects of sirodesmin PL, a phytotoxin produced by Leptosphaeria maculans. Plant Sci 57:45–53
Rouxel T, Kollmann A, Bousquet JF (1990) Zinc suppresses sirodesmin PL toxicity and protects Brassica napus plants against the blackleg disease caused by Leptosphaeria maculans. Plant Sci 68:77–86
Rouxel T, Grandaubert J, Hane JK, Hoede C, van de Wouw AP, Couloux A, Dominguez V, Anthouard V, Bally P, Bourras S, Cozijnsen AJ, Ciufetti LM, Degrave A, Dilmaghani A, Duret L, Fudal I, Goodwin SB, Gout L, Glaser N, Linglin J, Kema GHJ, Lapalu N, Lawrence CB, May K, Meyer M, Ollivier B, Poulain J, Schoch CL, Simon A, Spatafora JW, Stachowiak A, Turgeon BG, Tyler BM, Vincent D, Weissenbach J, Amselem J, Quesneville H, Oliver RP, Wincker P, Balesdent MH, Howlett BJ (2011) Effector diversification within compartments of the Leptosphaeria maculans genome affected by repeat-induced point mutations. Nat Commun 2:202. doi:10.1038/ncomms1189
Sacristán MD (1982) Resistance responses to Phoma lingam of plants regenerated from selected cell and embryogenic cultures of haploid Brassica napus. Theor Appl Genet 61:193–200
Sacristán MD (1985) Selection for disease resistance in Brassica cultures. Hereditas 3(Suppl):57–63
Sacristán MD, Gerdemann M (1986) Different behaviour of Brassica juncea and B. carinata as sources of Phoma lingam resistance in experiments of interspecific transfer to B. napus. Plant Breed 97:304–314
Saniewska A, Dyki B (1997) Development of Phoma narcissi within tissues of Hippeastrum leaves. Phytopathol Polonica 14:55–60
Schäfer C, Wöstemeyer J (1992) Random primer dependent PCR differentiates aggressive from non-aggressive isolates of the oilseed rape pathogen Phoma lingam (Leptosphaeria maculans). J Phytopathol 136:124–136
Scharf DH, Heinekamp T, Remme N, Hortschansky P, Brakhage AA, Hertweck C (2012) Biosynthesis and function of gliotoxin in Aspergillus fumigatus. Appl Microbiol Biotechnol 93:467–472
Schleier S, Voigt K, Wöstemeyer J (1997) RAPD-based molecular diagnosis of mixed fungal infections on oilseed rape (Brassica napus): Evidence for genus- and species-specific sequences in the fungal genomes. J Phytopathol 145:81–87
Scholze P, Krämer R, Ryschka U, Klocke E, Schumann G (2010) Somatic hybrids of vegetable Brassicas as source for new resistances to fungal and virus diseases. Euphytica 176:1–14
Sexton AC, Howlett BJ (2001) Green fluorescent protein as a reporter in the Brassica-Leptosphaeria maculans interaction. Physiol Mol Plant Pathol 58:13–21
Sexton AC, Paulsen M, Wöstemeyer J, Howlett BJ (2000) Cloning, characterization and chromosomal location of three genes encoding host-cell-wall-degrading enzymes in Leptosphaeria maculans, a fungal pathogen of Brassica spp. Gene 248:89–97
Shoemaker RA, Brun H (2001) The teleomorph of the weakly aggressive segregate of Leptosphaeria maculans. Can J Bot 79:412–419
Sippell DW, Hall R (1995) Glucose phosphate isomerase polymorphisms distinguish weakly from highly virulent strains of Leptosphaeria maculans. Can J Plant Pathol 17:1–6
Sjödin C, Glimelius K (1989a) Differences in response to the toxin sirodesmin PL produced by Phoma lingam (Tode ex Fr.) Desm. on protoplasts, cell aggregates and intact plants of resistant and susceptible Brassica accessions. Theor Appl Genet 77:76–80
Sjödin C, Glimelius K (1989b) Brassica naponigra, a somatic hybrid resistant to Phoma lingam. Theor Appl Genet 77:651–656
Sjödin C, Nyhammar T, Glimelius K (1988) Effects of toxic metabolites produced by Phoma lingam (Tode ex Fr.) Desm. on protoplasts, cells and plants of hosts and non-hosts of the pathogen. Physiol Mol Plant Pathol 32:301–312
Snowdon RJ, Winter H, Diestel A, Sacristán MD (2000) Development and characterisation of Brassica napus-Sinapis arvensis addition lines exhibiting resistance to Leptosphaeria maculans. Theor Appl Genet 101:1008–1014
Sock J, Hoppe HH (1999) Pathogenicity of sirodesmin-deficient mutants of Phoma lingam. J Phytopathol 147:169–173
Sock J, Mennen H, Hoppe HH (1995) Pathogenicity of sirodesmin-deficient mutants of Leptosphaeria maculans. In: Proceedings of the 9th international rapeseed congress, Cambridge, pp 613–615
Sprague SJ, Watt M, Kirkegaard JA, Howlett BJ (2007) Pathways of infection of Brassica napus roots by Leptosphaeria maculans. New Phytol 176:211–222
Sprague SJ, Howlett BJ, Kirkegaard JA (2009) Epidemiology of root rot caused by Leptosphaeria maculans in Brassica napus crops. Eur J Plant Pathol 125:189–202
Steed JM, Baierl A, Fitt BDL (2007) Relating plant and pathogen development to optimise fungicide control of Phoma stem canker (Leptosphaeria maculans) on winter oilseed rape (Brassica napus). Eur J Plant Pathol 118:359–373
Subramanian B, Bansal VK, Kav NNV (2005) Proteome-level investigation of Brassica carinata-derived resistance to Leptosphaeria maculans. J Agric Food Chem 53:313–324
Taylor JL, Borgmann IE (1994) An unusual repetitive element from highly virulent isolates of Leptosphaeria maculans and evidence of its transfer to a weakly virulent isolate. Mol Plant Microbe Interact 7:181–188
Taylor JL, Borgmann I, Séguin-Swartz G (1991) Electrophoretic karyotyping of Leptosphaeria maculans differentiates highly virulent from weakly virulent isolates. Curr Genet 19:273–277
Thomas E, Hoffmann F, Potrykus I, Wenzel G (1976) Protoplast regeneration and stem embryogenesis of haploid androgenetic rape. Mol Gen Genet 145:245–247
Thürwächter F, Garbe V, Hoppe HH (1999) Ascospore discharge, leaf infestation and variation in pathogenicity as criteria to predict impact of Leptosphaeria maculans on oilseed rape. J Phytopathol 147:215–222
van de Graaf P, Joseph ME, Chartier-Hollis JM, O’Neill TM (2002) Prepenetration stages in infection of Clematis by Phoma clematidina. Plant Pathol 51:331–337
van de Wouw AP, Marcroft SJ, Barbetti MJ, Hua L, Salisbury PA, Gout L, Rouxel T, Howlett BJ, Balesdent MH (2009) Dual control of avirulence in Leptosphaeria maculans towards a Brassica napus cultivar with ‘sylvestris-derived’ resistance suggests involvement of two resistance genes. Plant Pathol 58:503–513
van der Aa HA, Noordeloos ME, De Gruyter J (1990) Species concepts in some larger genera of the coelomycetes. Stud Mycol 32:3–19
van der Aa HA, Boerema GH, de Gruyter J (2000) Contributions towards a monograph of Phoma (coelomycetes). 6–1 – section phyllostictoides: characteristics and nomenclature of its type species Phoma exigua. Persoonia 17:435–456
van Kan JAL, van den Ackerweken GFJM, de Wit PJGM (1991) Cloning and characterization of cDNA of avirulence gene avr9 of the fungal pathogen Cladosporium fulvum, causal agent of tomato leaf mold. Mol Plant Microbe Interact 4:52–59
Venn L (1979) The genetic control of sexual compatibility in Leptosphaeria maculans. Australas Plant Pathol 8:5–6
Versalovic J, Koeuth T, Lupski R (1991) Distribution of repetitive DNA sequences in eubacteria and application to fingerprinting of bacterial genomes. Nucleic Acids Res 19:6823–6831
Voigt K, Wöstemeyer J (1995) The combination of Gilbert/Maxam chemical sequencing and the dideoxynucleotide chain termination approach facilitates the construction of species specific PCR-primers based on diagnostic RAPD bands. Microbiol Res 150:373–377
Voigt K, Schleier S, Wöstemeyer J (1998) RAPD-based molecular probes for the blackleg fungus Leptosphaeria maculans (Phoma lingam): evidence for pathogenicity group-specific sequences in the fungal genomes. J Phytopathol 146:567–576
Voigt K, Jedryczka M, Wöstemeyer J (2001) Strain typing of Polish Leptosphaeria maculans isolates supports at the genomic level the multi-species concept of aggressive and non-aggressive strains. Microbiol Res 156:169–177
Voigt K, Cozijnsen AJ, Kroymann J, Pöggeler S, Howlett BJ (2005) Phylogenetic relationships between members of the crucifer pathogenic Leptosphaeria maculans species complex as shown by mating type (MAT1-2), actin, and β-tubulin sequences. Mol Phylogenet Evol 37:541–557
West JS, Biddulph JE, Fitt BD, Gladders P (1999) Epidemiology of Leptosphaeria maculans in relation to forecasting stem canker severity on winter oilseed rape in the UK. Ann Appl Biol 135:535–546
West JS, Kharbanda PD, Barbetti MJ, Fitt BDL (2001) Epidemiology and management of Leptosphaeria maculans (Phoma stem canker) on oilseed rape in Australia, Canada and Europe. Plant Pathol 50:10–27
West JS, Fitt BDL, Leech PK, Biddulph JE, Huang YJ (2002) Effects of timing of Leptosphaeria maculans ascospore release and fungicide regime on Phoma leaf spot and Phoma stem canker development on winter oilseed rape (Brassica napus) in southern England. Plant Pathol 51:454–463
Williams RH, Fitt BDL (1999) Differentiating A and B groups of Leptosphaeria maculans, causal agent of stem canker (blackleg) of oilseed rape. Plant Pathol 48:161–175
Wöstemeyer J, Kreibich A (2002) Repetitive DNA elements in fungi (Mycota): impact on genomic architecture and evolution. Curr Genet 41:189–198
Zou HX, Xie X, Zheng XD, Li SM (2011) The tyrosine O-prenyltransferase SirD catalyzes O-, N-, and C-prenylations. Appl Microbiol Biotechnol 89:1443–1451
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Wöstemeyer, J. (2013). 7 Disease Management of Phoma Infections. In: Kempken, F. (eds) Agricultural Applications. The Mycota, vol 11. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-36821-9_7
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