Detection of potential suberinase-encoding genes in streptomyces scabiei strains and other actinobacteria

Canadian Journal of Microbiology

Volumn 59, Issue 5, 2013, Pages 294-303

  Komeil, Doaa ^a,b   Simao Beaunoir, Anne Marie ^a   Beaulieu, Carole ^a  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

^b ALEXANDRIA UNIVERSITY   (Egypt)

Author keywords

Common scab; Esterase; Streptomyces scabies; Suberin

Indexed keywords

ESTERASE; LIGNIN; SUBERIN; XYLAN;

BACTERIAL DISEASE; BACTERIUM; BIODEGRADATION; DETECTION METHOD; DISEASE PREVALENCE; ENZYME ACTIVITY; GENE EXPRESSION; HOST PLANT; HYBRIDIZATION; LIGNIN; POLYMER; POLYMERASE CHAIN REACTION; POTATO; PROTEIN; SECRETION;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GENE; BACTERIAL VIRULENCE; BACTERIUM DETECTION; BIODEGRADATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC CODE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SOUTHERN BLOTTING; STREPTOMYCES; STREPTOMYCES SCABIEI;

ACTINOBACTERIA; ESTERASES; GENE EXPRESSION; LIPID METABOLISM; LIPIDS; SOLANUM TUBEROSUM; STREPTOMYCES;

EID: 84877351305     PISSN: 00084166     EISSN: 14803275     Source Type: Journal    
DOI: 10.1139/cjm-2012-0741     Document Type: Article

References (83)

1. Adams, M.J. 1975. Potato tuber lenticels: development and structure. Ann. Appl. Biol. 79(3): 267-273. doi:110.1111/j.1744-7348.1975.tb01582.x.
2. Bajar, A., Podila, G.K., and Kolattukudy, P.E. 1991. Identification of a fungal cutinase promoter that is inducible by a plant signal via a phosphorylated trans-acting factor. Proc. Natl. Acad. Sci. U.S.A. 88(18): 8208-8212. doi:110.1073/pnas.88.18.8208. PMID:1896470.
3. Beausejour, J., Goyer, C., Vachon, J., and Beaulieu, C. 1999. Production of thaxtomin A by Streptomyces scabies strains in plant extract containing media. Can. J. Microbiol. 45(9): 764-768. doi:110.1139/w99-072.
4. Belanger, P.-A., Beaudin, J., and Roy, S. 2011. High-throughput screening of microbial adaptation to environmental stress. J. Microbiol. Methods, 85(2): 92-97. doi:110.1016/j.mimet.2011.01.028. PMID:21315114.
5. Belbahri, L., Calmin, G., Mauch, F., and Andersson, J.O. 2008. Evolution of the cutinase gene family: evidence for lateral gene transfer of a candidate Phytophthora virulence factor. Gene, 408(1-2): 1-8. doi:110.1016/j.gene.2007.10.019. PMID:18024004.
6. Bendtsen, J.D., Nielsen, H., von Heijne, G., and Brunak, S. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340(4): 783-795. doi:110. 1016/j.jmb.2004.05.028. PMID:15223320.
7. Bernards, M.A. 2002. Demystifying suberin. Can. J. Bot. 80(3): 227-240. doi:110.1139/B02-017.
8. Berneche-D'Amours, A., Ghinet, M.G., Beaudin, J., Brzezinski, R., and Roy, S. 2011. Sequence analysis of rpoB and rpoD gene fragments reveals the phylogenetic diversity of actinobacteria of genus Frankia. Can. J. Microbiol. 57(3): 244-249. doi:110.1139/W10-106. PMID:21358766.
9. Bibb, M.J., Freeman, R.F., and Hopwood, D.A. 1977. Physical and genetical characterisation of a second sex factor, SCP2, for Streptomyces coelicolor A3(2). Mol. Gen. Genet. 154(2): 155-166. doi:110.1007/BF00330831.
10. Biely, P., MacKenzie, C.R., and Schneider, H. 1988. Acetylxylan esterase of Schizophyllum commune. Methods Enzymol. 160(c): 700-707. doi:110.1016/0076- 6879(88)60190-X.
11. Błaszczak, W., Chrzanowsk, M., Fornal, J., Zimnoch-Guzowsk, E., Palacios, M.C., and Vacek, J. 2005. Scanning electron microscopic investigation of different types of necroses in potato tubers. Food Control, 16(8): 747-752. doi:110.1016/ j.foodcont.2004.06.014.
12. Bonnen, A.M., and Hammerschmidt, R. 1989. Role of cutinolytic enzymes in infection of cucumber by Colletotrichum lagenarium. Physiol. Mol. Plant Pathol. 35(6): 475-481. doi:110.1016/0885-5765(89)90089-1.
13. Borgmeyer, J.A., and Crawford, D.L. 1985. Production and characterization of polymeric lignin degradation intermediates from two different Streptomyces spp. Appl. Environ. Microbiol. 49(2): 273-278. PMID:16346714.
14. Bouchek-Mechiche, K., Gardan, L., Normand, P., and 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(1): 91-99. doi:110.1099/00207713-50- 1-91. PMID:10826791.
15. Brody, J.R., and Kern, S.E. 2004. Sodium boric acid: a Tris-free, cooler conductive medium for DNA electrophoresis. Biotechniques, 36(2): 214-216. PMID:14989083.
16. Bukhalid, R.A., Chung, S.Y., and 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(10): 960-967. doi:110.1094/MPMI.1998.11.10.960.
17. de Klerk, A., McLeod, A., Faurie, R., and van Wyk, P.S. 1997. Net blotch and necrotic warts caused by Streptomyces scabies on pods of peanut (Arachis hypogaea). Plant Dis. 81(8): 958. doi:110.1094/PDIS.1997.81.8.958B.
18. de Vries, R.P., van Kuyk, P.A., Kester, H.C.M., and Visser, J. 2002. The Aspergillus niger faeB gene encodes a second feruloyl esterase involved in pectin and xylan degradation and is specifically induced in the presence of aromatic compounds. Biochem. J. 363(2): 377-386. doi:110.1042/0264-6021:3630377. PMID:11931668.
19. Dickman, M.B., and Patil, S.S. 1986. Cutinase deficient mutants of Colletotrichum gloeosporioides are non-pathogenic to papaya fruit. Physiol. Mol. Plant Pathol. 28(2): 235-242. doi:110.1016/S0048-4059(86)80067-4.
20. Dickman, M.B., Podila, G.K., and Kolattukudy, P.E. 1989. Insertion of cutinase gene into a wound pathogen enables it to infect intact host. Nature, 342: 446-448. doi:110.1038/342446a0.
21. Donnelly, P.K., and Crawford, D.L. 1988. Production by Streptomyces viridosporus T7A of an enzyme which cleaves aromatic acids from lignocellulose. Appl. Environ. Microbiol. 54(9): 2237-2244. PMID:16347736.
22. Doumbou, C.L., Akimov, V., Côté, M., Charest, P.M., and Beaulieu, C. 2001. Axonomic study on nonpathogenic streptomycetes isolated from common scab lesions on potato tubers. Syst. Appl. Microbiol. 24(3): 451-456. doi:110.1078/ 0723-2020-00051. PMID:11822683.
23. Faucher, E., Savard, T., and Beaulieu, C. 1992. Characterization of actinomycetes isolated from common scab lesions on potato tubers. Can. J. Plant Pathol. 14(3): 197-202. doi:110.1080/07060669209500874.
24. Faucher, E., Paradis, E., Goyer, C., Hodge, N.C., Hogue, R., Stall, R.E., and Beaulieu, C. 1995. Characterization of streptomycetes causing deep-pitted scab of potato in Quebec Canada. Int. J. Syst. Bacteriol. 45(2): 222-225. doi:110. 1099/00207713-45-2-222.
25. Fernando, G., Zimmermann, W., and Kolattukudy, P.E. 1984. Suberin-grown Fusarium solani f. sp. pisi generates a cutinase-like esterase which depolymerises the aliphatic components of suberin. Physiol. Plant Pathol. 24(2): 143-155. doi:110.1016/0048-4059(84)90022-5.
26. Fett, W.F., Wijey, C., Moreau, R.A., and Osman, S.F. 1999. Production of cutinase by Thermomonospora fusca ATCC 27730. J. Appl. Microbiol. 86(4): 561-568. doi:1 10.1046/j.1365-2672.1999.00690.x.
27. Fett, W.F., Wijey, C., Moreau, R.A., and Osman, S.F. 2000. Production of cutinolytic esterase by filamentous bacteria. Lett. Appl. Microbiol. 31(1): 25-29. doi:110.1046/j.1472-765x.2000.00752.x. PMID:10886609.
28. Francis, S., Dewey, F., and Gurr, S. 1996. The role of cutinase in germling development and infection by Erysiphe graminis f.sp. hordei. Physiol. Mol. Plant Pathol. 49(3): 201-211. doi:110.1006/pmpp.1996.0049.
29. Franke, R., and Schreiber, L. 2007. Suberin-a biopolyester forming apoplastic plant interfaces. Curr. Opin. Plant Biol. 10(3): 252-259. doi:110.1016/j.pbi.2007. 04.004. PMID:17434790.
30. Gao, M., and Chamuris, G.P. 1993. Microstructural and histochemical changes in Acer platanoides rhytidome caused by Dendrothele acerina (Aphyllophorales) and Mycena meliigena (Agaricales). Mycologia, 85(6): 987-995. Available from http://www.jstor.org/stable/3760682. doi:110.2307/3760682.
31. García-Lepe, R., Nuero, O.M., Reyes, F., and Santamaría, F. 1997. Lipase in autolysed cultures of filamentous fungi. Lett. Appl. Microbiol. 25(2): 127-130. doi:110.1046/j.1472-765X.1997.00187.x. PMID:9281862.
32. Gérard, H.C., Fett, W.F., Osman, S.F., and Moreau, R.A. 1993. Evaluation of cutinase activity of various industrial lipases. Biotechnol. Appl. Biochem. 17(2): 181-189. doi:110.1111/j.1470-8744.1993.tb00238.x.
33. Goyer, C. 2005. Isolation and characterization of phages Stsc1 and Stsc3 infecting Streptomyces scabiei and their potential as biocontrol agent. Can. J. Plant Pathol. 27(2): 210-216. doi:110.1080/07060660509507218.
34. Goyer, C., and Beaulieu, C. 1997. Host range of streptomycete strains causing common scab. Plant Dis. 81(8): 901-904. doi:110.1094/PDIS.1997.81.8.901.
35. Goyer, C., Faucher, E., and Beaulieu, C. 1996. Streptomyces caviscabies sp. nov., from deep-pitted lesions in potatoes in Quebec, Canada. Int. J. Syst. Evol. Microbiol. 46(3): 635-639. doi:110.1099/00207713-46-3-635.
36. Graça, J., and Pereira, H. 2000. Suberin structure in potato periderm: glycerol, long-chain monomers, and glyceryl and feruloyl dimers. J. Agric. Food Chem. 48(11): 5476-5483. doi:110.1021/jf0006123. PMID:11087505.
37. Graça, J., and Santos, S. 2007. Suberin: a biopolyester of plants' skin. Macromol. Biosci. 7(2): 128-135. doi:110.1002/mabi.200600218. PMID:17295399.
38. Green, R., Schottel, J.L., Swenson, L., Wei, Y., and Derwenda, Z. 1992. Crystallization and preliminary crystallographic data of a Streptomyces scabies extracellular esterase. J. Mol. Biol. 227(2): 569-571. doi:110.1016/0022-2836(92)90908-3. PMID: 1404370.
39. Heredia, A. 2003. Biophysical and biochemical characteristics of cutin, a plant barrier biopolymer. Biochim. Biophys. Acta, 1620(1-3): 1-7. doi:110.1016/S0304-4165(02)00510-X. PMID:12595066.
40. Hill, J., and Lazarovits, G. 2005. A mail survey of growers to estimate potato common scab prevalence and economic loss in Canada. Can. J. Plant Pathol. 27(1): 46-52. doi:110.1080/07060660509507192.
41. Joshi, M.V., Bignell, D.R.D., Johnson, E.G., Sparks, J.P., Gibson, D.M., and Loria, R. 2007. The AraC/XylS regulator TxtR modulates thaxtomin biosynthesis and virulence in Streptomyces scabies. Mol. Microbiol. 66(3): 633-642. doi:110.1111/j. 1365-2958.2007.05942.x. PMID:17919290.
42. Khatri, B.B., Tegg, R.S., Brown, P.H., and Wilson, C.R. 2011. Temporal association of potato tuber development with susceptibility to common scab and Streptomyces scabiei-induced responses in the potato periderm. Plant Pathol. 60(4): 776-786. doi:110.1111/j.1365-3059.2011.02435.x.
43. Kieser, T., Bibb, M.J., Buttner, M.J., Chater, K.F., and Hopwood, D.A. 2000. Practical Streptomyces genetics. John Innes Foundation, Norwich, UK.
44. King, R.R., Lawrence, C.H., and Clark, M.C. 1991. Correlation of phytotoxin production with pathogenicity of Streptomyces scabies isolates from scab infected potato tubers. Am. Potato J. 68(10): 675-680. doi:110.1007/BF02853743.
45. Kolattukudy, P.E. 1980. Biopolyester membranes of plants-cutin and suberin. Science, 208(4447): 990-1000. doi:110.1126/science.208.4447.990. PMID: 17779010.
46. Kolattukudy, P.E. 1985. Enzymatic penetration of the plant cuticle by fungal pathogens. Annu. Rev. Phytopathol. 23: 223-250. doi:110.1146/annurev.py.23. 090185.001255.
47. Kolattukudy, P.E., and Agrawal, V.P. 1974. Structure and composition of aliphatic constituents of potato tuber skin (suberin). Lipids, 9(9): 682-691. doi:1 10.1007/BF02532176.
48. Kolattukudy, P.E., Rogers, L.M., Li, D., Hwang, C.S., and Flaishman, M.A. 1995. Surface signaling in pathogenesis. Proc. Natl. Acad. Sci. U.S.A., 92(10): 4080-4087. doi:110.1073/pnas.92.10.4080. PMID:7753774.
49. Köller, W., and Parker, D.M. 1989. Purification and characterization of cutinase from Venturia inaequalis. Phytopathology, 79(3): 278-283. doi:110.1094/Phyto-79-278.
50. Köller, W., Parker, D.M., and Becker, C.M. 1991. Role of cutinase in the penetration of apple leaves by Venturia inaequalis. Phytopatholology, 81(11): 1375-1379. doi:110.1094/Phyto-81-1375.
51. Köller, W., Yao, C.L., Trail, F., and Parker, D.M. 1995. Role of cutinase in the invasion of plants. Can. J. Bot. 73(S1): 1109-1118. doi:110.1139/b95-366.
52. Kontkanen, H., Westerholm-Parvinen, A., Saloheimo, M., Bailey, M., Rättö, M., Mattila, I., Mohsina, M., Kalkkinen, N., Nakari-Setälä, T., and Buchert, J. 2009. Novel Coprinopsis cinerea polyesterase that hydrolyzes cutin and suberin. Appl. Environ. Microbiol. 75(7): 2148-2157. doi:110.1128/AEM.02103-08. PMID:19201950.
53. Lambert, D.H., and Loria, R. 1989a. Streptomyces scabies sp. nov., nom. rev. Int. J. Syst. Bacteriol. 39(4): 387-392. doi:110.1099/00207713-39-4-387.
54. Lambert, D.H., and Loria, R. 1989b. Streptomyces acidiscabies sp. nov. Int. J. Syst. Bacteriol. 39(4): 393-396. doi:110.1099/00207713-39-4-393.
55. Lauzier, A., Goyer, C., Brzezinski, R., Crawford, D.L., and Beaulieu, C. 2002. Effect of amino acids on thaxtomin A biosynthesis in Streptomyces scabies. Can. J. Microbiol. 48(4): 359-364. doi:110.1139/w02-031. PMID:1203709.
56. Lerat, S., Simao-Beaunoir, A.-M., Wu, R., Beaudoin, N., and Beaulieu, C. 2010. Involvement of the plant polymer suberin and the disaccharide cellobiose in triggering thaxtomin A biosynthesis, a phytotoxin produced by the pathogenic agent Streptomyces scabies. Phytopathology, 100(1): 91-96. doi:110.1094/PHYTO-100-1-0091. PMID:19968554.
57. Li, D., Ashby, A.M., and 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(6): 545-552. doi:110.1094/MPMI. 2003.16.6.545. PMID:12795380.
58. Lin, T.S., and Kolattukudy, P.E. 1978. Induction of a biopolyester hydrolase (cutinase) by low levels of cutin monomers in Fusarium solani f. sp. pisi. J. Bacteriol. 133(2): 942-951. PMID:415052.
59. Loria, R., Coombs, J., Yoshida, M., Kers, J., and Bukhalid, R.A. 2003. A paucity of bacterial root diseases: Streptomyces succeeds where others fail. Physiol. Mol. Plant Pathol. 62(2): 65-72. doi:110.1016/S0885-5765(03)00041-9.
60. Loria, R., Kers, J., and Joshi, M. 2006. Evolution of plant pathogenicity in Streptomyces. Annu. Rev. Phytopathol. 44: 469-487. doi:110.1146/annurev.phyto.44. 032905.091147. PMID:16719719.
61. Martinez, C., Nicolas, A., van Tilbeurgh, H., Egloff, M.P., Cudrey, C., Verger, R., and Cambillau, C. 1994. Cutinase, a lipolytic enzyme with a preformed oxyanion hole. Biochemistry, 33(1): 83-89. doi:110.1021/bi00167a011. PMID:8286366.
62. McQueen, D.A.R., and Schottel, J.L. 1987. Purification and characterization of a novel extracellular esterase from pathogenic Streptomyces scabies that is inducible by zinc. J. Bacteriol. 169(5): 1967-1971. PMID:3571156.
63. Miller, C.D., Hall, K., Liang, Y.N., Nieman, K., Sorensen, D., Issa, B., Anderson, A.J., and Sims, R.C. 2004. Isolation and characterization of polycyclic aromatic hydrocarbon-degrading Mycobacterium isolates from soil. Microb. Ecol. 48(2): 230-238. doi:110.1007/s00248-003-1044-5. PMID:15107954.
64. Miyajima, K., Tanaka, F., Takeuchi, T., and Kuninaga, S. 1998. Streptomyces turgidiscabies sp. nov. Int. J. Syst. Bacteriol. 48(2): 495-502. doi:110.1099/00207713- 48-2-495. PMID:9731290.
65. Normand, P., and Lalonde, M. 1982. Evaluation of Frankia strains isolated from provenances of two Alnus species. Can. J. Microbiol. 28(10): 1133-1142. doi:110. 1139/m82-168.
66. Ofong, A.U., and Pearce, R.B. 1994. Suberin degrading by Rosellinia desmazieresii. Eur. J. For. Pathol. 24(6-7): 316-322. doi:110.1111/j.1439-0329.1994.tb00825.x.
67. Ospina-Giraldo, M.D., McWalters, J., and Seyer, L. 2010. Structural and functional profile of the carbohydrate esterase gene complement in Phytophthora infestans. Curr. Genet. 56(6): 495-506. doi:110.1007/s00294-010-0317-z. PMID: 20725833.
68. Parker, S.K., Curtin, K.M., and Vasil, M.L. 2007. Purification and characterization of mycobacterial phospholipase A: an activity associated with mycobacterial cutinase. J. Bacteriol. 189(11): 4153-4160. doi:110.1128/JB.01909-06. PMID: 17416658.
69. Pfaffl, M.W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29(9): 2002-2007. doi:110.1093/nar/29.9. e45. PMID:11328886.
70. Pollard, M., Beisson, F., Li, Y., and Ohlrogge, J.B. 2008. Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci. 13(5): 236-246. doi:110. 1016/j.tplants.2008.03.003. PMID:18440267.
71. Sambrook, J., and Russell, D.W. 2001. Molecular cloning: a laboratory manual. 3rd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y., USA.
72. Schué, M., Maurin, D., Dhouib, R., BakalaN'Goma, J.C., Delorme, V., Lambeau, G., Carrière, F., and Canaan, S. 2010. Two cutinase-like proteins secreted by Mycobacterium tuberculosis show very different lipolytic activities reflecting their physiological function. FASEB J. 24(6): 1893-1903. doi:110.1096/fj.09-144766. PMID:20103719.
73. Shirling, E.B., and Gottlieb, D. 1972. Cooperative description of type strain of Streptomyces V. Additional descriptions. Int. J. Syst. Bacteriol. 22(4): 265-394. doi:110.1099/00207713-22-4-265.
74. Skamnioti, P., and Gurr, S.J. 2007. Magnaporthe grisea cutinase2 mediates appressorium differentiation and host penetration and is required for full virulence. Plant Cell, 19(8): 2674-2689. doi:110.1105/tpc.107.051219. PMID:17704215.
75. St-Onge, R., Goyer, C., Coffin, R., and Filion, M. 2008. Genetic diversity of treptomyces spp. causing common scab of potato in eastern Canada. Syst. Appl. Microbiol. 31(6-8): 474-484. doi:110.1016/j.syapm.2008.09.002. PMID:18947953.
76. Takeuchi, T., Sawada, H., Tanaka, F., and Matsuda, I. 1996. Phylogenetic analysis of Streptomyces spp. causing potato scab based on 16s rRNA sequences. Int. J. Syst. Bacteriol. 46(2): 476-479. doi:110.1099/ijs.0.02624-0. PMID:8934906.
77. Tanabe, K., Nishimura, S. and Kohmoto, K. 1988. Pathogenicity of cutinase- and pectic enzymes-deficient mutants of Alternaria alternata Japanese pear pathotype. Ann. Phytopathol. Soc. Japan, 54(4): 552-555. Available from http://pdfcast.org/download/pathogenicity-of-cutinase-and-pectic-enzymesdeficient-mutants-of-alternar-a-alternata-japanese-pear-pathotype.pdf. doi:110.3186/jjphytopath.54.552.
78. Tesch, C., Nikoleit, K., Gnau, V., Götz, F., and Bormann, C. 1996. Biochemical and molecular characterization of the extracellular esterase from Streptomyces diastatochromogenes. J. Bacteriol. 178(7): 1858-1865. PMID:8606158.
79. van Kan, J.A., van't Klooster, J.W., Wagemakers, C.A., Dees, D.C., and van der Vlugt-Bergmans, C.J. 1997. Cutinase A of Botrytis cinerea is expressed, but not essential, during penetration of gerbera and tomato. Mol. Plant- Microbe Interact. 10(1): 30-38. doi:110.1094/MPMI. 1997.10.1.30. PMID:9002270.
80. van Wezel, G.P., Vijgenboom, E., and Bosch, L. 1991. A comparative study of the ribosomal RNA operons of Streptomyces coelicolor A3(2) and sequence analysis of rrnA. Nucleic Acids Res. 19(16): 4399-4403. doi:110.1093/nar/19.16.4399.PMID:1715981.
81. West, N.P., Chow, F.M., Randall, E.J., Wu, J., Chen, J., Ribeiro, J.M., and Britton, W.J. 2009. Cutinase-like proteins of Mycobacterium tuberculosis: characterization of their variable enzymatic functions and active site identification. FASEB J. 23(6): 1694-1704. doi:110.1096/fj.08-114421. PMID:19225166.
82. Yao, C., and Köller, W. 1995. Diversity of cutinases from plant pathogenic fungi: different cutinases are expressed during saprophytic and pathogenic stages of Alternaria brassicicola. Mol. Plant-Microbe Interact. 8(1): 122-130. doi:110.1094/MPMI-8-0122.
83. Zimmerman, W., and Seemüller, E. 1984. Degradation of raspberry suberin by Fusarium solani f. sp. pisi and Armillaria mellea. J. Phytopathol. 110(3): 192-199. doi:110.1111/j.1439-0434.1984.tb00747.x.