How the necrotrophic fungus Alternaria brassicicola kills plant cells remains an Enigma

Eukaryotic Cell

Volumn 14, Issue 4, 2015, Pages 335-344

  Cho, Yangrae ^a  

^a Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ALTERNARIA; ALTERNARIA ALTERNATA; ALTERNARIA BRASSICICOLA; FUNGI;

FUNGAL PROTEIN; MYCOTOXIN; TRANSCRIPTION FACTOR; VIRULENCE FACTOR;

ALTERNARIA; ARABIDOPSIS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; PLANT CELL; PLANT DISEASE; REVERSE GENETICS;

ALTERNARIA; ARABIDOPSIS; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; MYCOTOXINS; PLANT CELLS; PLANT DISEASES; REVERSE GENETICS; TRANSCRIPTION FACTORS; VIRULENCE FACTORS;

EID: 84926353572     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00226-14     Document Type: Article

References (119)

1. Ariyawansa HA, Kang J-C, Alias SA, Chukeatirote E, Hyde KD. 2013. Towards a natural classification of Dothideomycetes: the genera Dermatodothella, Dothideopsella, Grandigallia, Hysteropeltella and Gloeodiscus (Dothideomycetes incertae sedis). Phytotaxa 147:35–47. http://dx.doi.org/10.11646/phytotaxa.147.2.1.
2. Kirk P, Cannon P, Minter D, Stalpers J. 2008. Ainsworth and Bisby’s dictionary of the fungi, 10th ed. CAB International, Wallingford, United Kingdom.
3. Thomma BPHJ. 2003. Alternaria spp.: from general saprophyte to specific parasite. Mol Plant Pathol 4:225–236. http://dx.doi.org/10.1046/j.1364-3703.2003.00173.x.
4. Ohm RA, Feau N, Henrissat B, Schoch CL, Horwitz BA, Barry KW, Condon BJ, Copeland AC, Dhillon B, Glaser F, Hesse CN, Kosti I, LaButti K, Lindquist EA, Lucas S, Salamov AA, Bradshaw RE, Ciuffetti L, Hamelin RC, Kema GH, Lawrence C, Scott JA, Spatafora JW, Turgeon BG, de Wit PJ, Zhong S, Goodwin SB, Grigoriev IV. 2012. Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen Dothideomycetes fungi. PLoS Pathog 8:e1003037. http://dx.doi.org/10.1371/journal.ppat.1003037.
5. Westman A, Kresovich S, Dickson M. 1999. Regional variation in Brassica nigra and other weedy crucifers for disease reaction to Alternaria brassicicola and Xanthomonas campestris pv. campestris. Euphytica 106: 253–259. http://dx.doi.org/10.1023/A:1003544025146.
6. Sigareva M, Earle E. 1999. Camalexin induction in intertribal somatic hybrids between Camelina sativa and rapid cycling Brassica oleracea. Theor Appl Genet 98:164–170. http://dx.doi.org/10.1007/s001220051053.
7. Neergaard P. 1945. Danish species of Alternaria and Stemphylium. Oxford University Press, London, United Kingdom.
8. Warwick SI, Francis A. 1994. Guide to the wild germplasm of Brassica and allied crops. Part 5. Life history and geographical data for wild species in the tribe Brassiceae (Cruciferae). Agric Can Res Branch Tech Bull 1994:2E.
9. Humpherson-Jones FM, Phelps K. 1989. Climatic factors influencing spore production in Alternaria brassicae and Alternaria brassicicola. Ann Appl Biol 114:449–458. http://dx.doi.org/10.1111/j.1744-7348.1989.tb03360.x.
10. Daebeler FD, Riedel A, Riedel V. 1986. Wissenschaftliche Zeitschrift der Wilhelm Pieck-Universitat Rostock naturewissenschaftliche Reiche 35:52.
11. Errakhi R, Meimoun P, Lehner A, Vidal G, Briand J, Corbineau F, Rona JP, Bouteau F. 2008. Anion channel activity is necessary to induce ethylene synthesis and programmed cell death in response to oxalic acid. J Exp Bot 59:3121–3129. http://dx.doi.org/10.1093/jxb/ern166.
12. Friesen TL, Stukenbrock EH, Liu Z, Meinhardt S, Ling H, Faris JD, Rasmussen JB, Solomon PS, McDonald BA, Oliver RP. 2006. Emergence of a new disease as a result of interspecific virulence gene transfer. Nat Genet 38:953–956. http://dx.doi.org/10.1038/ng1839.
13. Kim KS, Min JY, Dickman MB. 2008. Oxalic acid is an elicitor of plant programmed cell death during Sclerotinia sclerotiorum disease development. Mol Plant Microbe Interact 21:605–612. http://dx.doi.org/10.1094/MPMI-21-5-0605.
14. Lehner A, Meimoun P, Errakhi R, Madiona K, Barakate M, Bouteau F. 2008. Toxic and signaling effects of oxalic acid: oxalic acid—natural born killer or natural born protector? Plant Signal Behav 3:746–748. http://dx.doi.org/10.4161/psb.3.9.6634.
15. Noda J, Brito N, Gonzalez C. 2010. The Botrytis cinerea xylanase Xyn11A contributes to virulence with its necrotizing activity, not with its catalytic activity. BMC Plant Biol 10:38. http://dx.doi.org/10.1186/1471-2229-10-38.
16. Oliver RP, Solomon PS. 2008. Recent fungal diseases of crop plants: is lateral gene transfer a common theme? Mol Plant Microbe Interact 21: 287–293. http://dx.doi.org/10.1094/MPMI-21-3-0287.
17. Pandelova I, Betts MF, Manning VA, Wilhelm LJ, Mockler TC, Ciuffetti LM. 2009. Analysis of transcriptome changes induced by Ptr ToxA in wheat provides insights into the mechanisms of plant susceptibility. Mol Plant 2:1067–1083. http://dx.doi.org/10.1093/mp/ssp045.
18. Lebeda A, Luhová L, Sedláøová M, Jancčová D. 2001. The role of enzymes in plant-fungal pathogens interactions. J Plant Dis Prot 108:89–111.
19. Vidhyasekaran P. 2008. Fungal pathogenesis in plant crops: molecular biology and host defense mechanisms, 2nd ed. CRC Press, New York, NY.
20. Mendgen K, Hahn M, Deising H. 1996. Morphogenesis and mechanisms of penetration by plant pathogenic fungi. Annu Rev Phytopathol 34:367–386. http://dx.doi.org/10.1146/annurev.phyto.34.1.367.
21. Howard RJ, Ferrari MA. 1989. Role of melanin in appressorium function. Exp Mycol 13:403–418. http://dx.doi.org/10.1016/0147-5975(89)90036-4.
22. Osbourn AE. 2001. Tox-boxes, fungal secondary metabolites, and plant disease. Proc Natl Acad Sci U S A 98:14187–14188. http://dx.doi.org/10.1073/pnas.261573598.
23. Voigt CA, Schafer W, Salomon S. 2005. A secreted lipase of Fusarium graminearum is a virulence factor required for infection of cereals. Plant J 42:364–375. http://dx.doi.org/10.1111/j.1365-313X.2005.02377.x.
24. Ball A, Ashby A, Daniels M, Ingram D, Johnstone K. 1991. Evidence for the requirement of extracellular protease in the pathogenic interaction of Pyrenopeziza brassicae with oilseed rape. Physiol Mol Plant Pathol 38:147–161. http://dx.doi.org/10.1016/S0885-5765(05)80132-8.
25. Mukherjee AK, Carp MJ, Zuchman R, Ziv T, Horwitz BA, Gepstein S. 2010. Proteomics of the response of Arabidopsis thaliana to infection with Alternaria brassicicola. J Proteomics 73:709–720. http://dx.doi.org/10.1016/j.jprot.2009.10.005.
26. Narusaka Y, Narusaka M, Seki M, Ishida J, Nakashima M, Kamiya A, Enju A, Sakurai T, Satoh M, Kobayashi M, Tosa Y, Park P, Shinozaki K. 2003. The cDNA microarray analysis using an Arabidopsis pad3 mutant reveals the expression profiles and classification of genes induced by Alternaria brassicicola attack. Plant Cell Physiol 44:377–387. http://dx.doi.org/10.1093/pcp/pcg050.
27. Schenk PM, Thomas-Hall SR, Nguyen AV, Manners JM, Kazan K, Spangenberg G. 2008. Identification of plant defence genes in canola using Arabidopsis cDNA microarrays. Plant Biol (Stuttg) 10:539–547. http://dx.doi.org/10.1111/j.1438-8677.2008.00056.x.
28. Thomma BP, Eggermont K, Penninckx IA, Mauch-Mani B, Vogelsang R, Cammue BP, Broekaert WF. 1998. Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci U S A 95:15107–15111. http://dx.doi.org/10.1073/pnas.95.25.15107.
29. Thomma BP, Nelissen I, Eggermont K, Broekaert WF. 1999. Deficiency in phytoalexin production causes enhanced susceptibility of Arabidopsis thaliana to the fungus Alternaria brassicicola. Plant J 19:163–171. http://dx.doi.org/10.1046/j.1365-313X.1999.00513.x.
30. van Wees SC, Chang HS, Zhu T, Glazebrook J. 2003. Characterization of the early response of Arabidopsis to Alternaria brassicicola infection using expression profiling. Plant Physiol 132:606–617. http://dx.doi.org/10.1104/pp.103.022186.
31. Oh IS, Park AR, Bae MS, Kwon SJ, Kim YS, Lee JE, Kang NY, Lee S, Cheong H, Park OK. 2005. Secretome analysis reveals an Arabidopsis lipase involved in defense against Alternaria brassicicola. Plant Cell 17: 2832–2847. http://dx.doi.org/10.1105/tpc.105.034819.
32. Pedras MS, Chumala PB, Jin W, Islam MS, Hauck DW. 2009. The phytopathogenic fungus Alternaria brassicicola: phytotoxin production and phytoalexin elicitation. Phytochemistry 70:394–402. http://dx.doi.org/10.1016/j.phytochem.2009.01.005.
33. Oka K, Akamatsub H, Kodamab M, Nakajimab H, Kawadab T, Otani H. 2005. Host-specific AB-toxin production by germinating spores of Alternaria brassicicola is induced by a host-derived oligosaccharide. Physiol Mol Plant Pathol 66:12–19. http://dx.doi.org/10.1016/j.pmpp.2005.03.005.
34. Pedras MS, Minic Z, Sarma-Mamillapalle VK. 2009. Substrate specificity and inhibition of brassinin hydrolases, detoxifying enzymes from the plant pathogens Leptosphaeria maculans and Alternaria brassicicola. FEBS J 276:7412–7428. http://dx.doi.org/10.1111/j.1742-4658.2009.07457.x.
35. Sellam A, Iacomi-Vasilescu B, Hudhomme P, Simoneau P. 2007. In vitro antifungal activity of brassinin, camalexin and two isothiocyanates against the crucifer pathogens Alternaria brassicicola and Alternaria brassicae. Plant Pathol 56:296–301. http://dx.doi.org/10.1111/j.1365-3059.2006.01497.x.
36. Sellam A, Dongo A, Guillemette T, Hudhomme P, Simoneau P. 2007. Transcriptional responses to exposure to the brassicaceous defence metabolites camalexin and allyl-isothiocyanate in the necrotrophic fungus Alternaria brassicicola. Mol Plant Pathol 8:195–208. http://dx.doi.org/10.1111/j.1364-3703.2007.00387.x.
37. Iacomi-Vasilescu B, Avenot H, Bataillé-Simoneau N, Laurent E, Guénard M, Simoneau P. 2004. In vitro fungicide sensitivity of Alternaria species pathogenic to crucifers and identification of Alternaria brassicicola field isolates highly resistant to both dicarboximides and phenylpyrroles. Crop Prot 23:481–488. http://dx.doi.org/10.1016/j.cropro.2003.10.003.
38. Cramer RA, La Rota CM, Cho Y, Thon M, Craven KD, Knudson DL, Mitchell TK, Lawrence CB. 2006. Bioinformatic analysis of expressed sequence tags derived from a compatible Alternaria brassicicola-Brassica oleracea interaction. Mol Plant Pathol 7:113–124. http://dx.doi.org/10.1111/j.1364-3703.2006.00324.x.
39. Cramer RA, Lawrence CB. 2003. Cloning of a gene encoding an Alt a 1 isoallergen differentially expressed by the necrotrophic fungus Alternaria brassicicola during Arabidopsis infection. Appl Environ Microbiol 69: 2361–2364. http://dx.doi.org/10.1128/AEM.69.4.2361-2364.2003.
40. Cramer RA, Lawrence CB. 2004. Identification of Alternaria brassicicola genes expressed in planta during pathogenesis of Arabidopsis thaliana. Fungal Genet Biol 41:115–128. http://dx.doi.org/10.1016/j.fgb.2003.10.009.
41. Grigoriev IV, Nordberg H, Shabalov I, Aerts A, Cantor M, Goodstein D, Kuo A, Minovitsky S, Nikitin R, Ohm RA, Otillar R, Poliakov A, Ratnere I, Riley R, Smirnova T, Rokhsar D, Dubchak I. 2012. The genome portal of the Department of Energy Joint Genome Institute. Nucleic Acids Res 40:D26–D32. http://dx.doi.org/10.1093/nar/gkr947.
42. Cho Y, Davis JW, Kim KH, Wang J, Sun QH, Cramer RAJ, Lawrence CB. 2006. A high throughput targeted gene disruption method for Alternaria brassicicola functional genomics using linear minimal element (LME) constructs. Mol Plant Microbe Interact 19:7–15. http://dx.doi.org/10.1094/MPMI-19-0007.
43. Oide S, Moeder W, Krasnoff S, Gibson D, Haas H, Yoshioka K, Turgeon BG. 2006. NPS6, encoding a nonribosomal peptide synthetase involved in siderophore-mediated iron metabolism, is a conserved virulence determinant of plant pathogenic ascomycetes. Plant Cell 18:2836–2853. http://dx.doi.org/10.1105/tpc.106.045633.
44. Sweigard JA, Carroll AM, Farrall L, Chumley FG, Valent B. 1997. A series of vectors for fungal transformation. Fungal Genet Newsl 44:52–53.
45. Cho Y, Srivastava A, Ohm RA, Lawrence CB, Wang KH, Grigoriev IV, Marahatta SP. 2012. Transcription factor Amr1 induces melanin biosynthesis and suppresses virulence in Alternaria brassicicola. PLoS Pathog 8:e1002974. http://dx.doi.org/10.1371/journal.ppat.1002974.
46. Cho Y, Kim K-H, La Rota M, Scott D, Santopietro G, Callihan M, Lawrence CB. 2009. Identification of virulence factors by high throughput targeted gene deletion of regulatory genes in Alternaria brassicicola. Mol Microbiol 72:1316–1333. http://dx.doi.org/10.1111/j.1365-2958.2009.06689.x.
47. Cho Y, Srivastava A, Nguyen C. 2013. Improved transformation method for Alternaria brassicicola, p 395–401. In Gupta VK, Tuohy MG, Ayyachamy M, Turner KM, O’Donovan A (ed), Laboratory protocols in fungal biology: current methods in fungal biology. Springer Science:Business Media, LLC, New York, NY. http://dx.doi.org/10.1007/978-1-4614-2356-35.
48. Yang L, Ukil L, Osmani A, Nahm F, Davies J, De Souza CP, Dou X, Perez-Balaguer A, Osmani SA. 2004. Rapid production of gene replacement constructs and generation of a green fluorescent protein-tagged centromeric marker in Aspergillus nidulans. Eukaryot Cell 3:1359–1362. http://dx.doi.org/10.1128/EC.3.5.1359-1362.2004.
49. Yu JH, Hamari Z, Han KH, Seo JA, Reyes-Dominguez Y, Scazzocchio C. 2004. Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet Biol 41:973–981. http://dx.doi.org/10.1016/j.fgb.2004.08.001.
50. Churchill A, Lu S, Turgeon B, Yoder O, Macko V. 1995. Victorindeficient REMI mutants of Cochliobolus victoriae demonstrate a requirement for victorin in pathogenesis. Fungal Genet Newsl 42A:41.
51. Johnson RD, Johnson L, Itoh Y, Kodama M, Otani H, Kohmoto K. 2000. Cloning and characterization of a cyclic peptide synthetase gene from Alternaria alternata apple pathotype whose product is involved in AM-toxin synthesis and pathogenicity. Mol Plant Microbe Interact 13: 742–753. http://dx.doi.org/10.1094/MPMI.2000.13.7.742.
52. Yun S-H, Turgeon B, Yoder O. 1998. REM-induced mutants of Mycosphaerella zeae-maydis lacking the polyketide PM-toxin are deficient in pathogenesis to corn. Physiol Mol Plant Pathol 52:53–66. http://dx.doi.org/10.1006/pmpp.1997.0134.
53. Ciuffetti LM, Tuori RP, Gaventa JM. 1997. A single gene encodes a selective toxin causal to the development of tan spot of wheat. Plant Cell 9:135–144. http://dx.doi.org/10.1105/tpc.9.2.135.
54. Del Sorbo G, Scala F, Parrella G, Lorito M, Comparini C, Ruocco M, Scala A. 2000. Functional expression of the gene cu, encoding the phytotoxic hydrophobin cerato-ulmin, enables Ophiostoma quercus, a nonpathogen on elm, to cause symptoms of Dutch elm disease. Mol Plant Microbe Interact 13:43–53. http://dx.doi.org/10.1094/MPMI.2000.13.1.43.
55. Brandwagt BF, Mesbah LA, Takken FL, Laurent PL, Kneppers TJ, Hille J, Nijkamp HJ. 2000. A longevity assurance gene homolog of tomato mediates resistance to Alternaria alternata f. sp. lycopersici toxins and fumonisin B1. Proc Natl Acad SciUSA97:4961–4966. http://dx.doi.org/10.1073/pnas.97.9.4961.
56. Kohmoto K, Otani H. 1991. Host recognition by toxigenic plant pathogens. Experientia 47:755–764. http://dx.doi.org/10.1007/BF01922454.
57. Spassieva SD, Markham JE, Hille J. 2002. The plant disease resistance gene Asc-1 prevents disruption of sphingolipid metabolism during AALtoxin- induced programmed cell death. Plant J 32:561–572. http://dx.doi.org/10.1046/j.1365-313X.2002.01444.x.
58. Tanaka A, Shiotani H, Yamamoto M, Tsuge T. 1999. Insertional mutagenesis and cloning of the genes required for biosynthesis of the host-specific AK-toxin in the Japanese pear pathotype of Alternaria alternata. Mol Plant Microbe Interact 12:691–702. http://dx.doi.org/10.1094/MPMI.1999.12.8.691.
59. Tanaka A, Tsuge T. 2000. Structural and functional complexity of the genomic region controlling AK-toxin biosynthesis and pathogenicity in the Japanese pear pathotype of Alternaria alternata. Mol Plant Microbe Interact 13:975–986. http://dx.doi.org/10.1094/MPMI.2000.13.9.975.
60. Ito K, Tanaka T, Hatta R, Yamamoto M, Akimitsu K, Tsuge T. 2004. Dissection of the host range of the fungal plant pathogen Alternaria alternate by modification of secondary metabolism. Mol Microbiol 52: 399–411. http://dx.doi.org/10.1111/j.1365-2958.2004.04004.x.
61. Tsuge T, Harimoto Y, Akimitsu K, Ohtani K, Kodama M, Akagi Y, Egusa M, Yamamoto M, Otani H. 2013. Host-selective toxins produced by the plant pathogenic fungus Alternaria alternata. FEMS Microbiol Rev 37:44–66. http://dx.doi.org/10.1111/j.1574-6976.2012.00350.x.
62. Johnson LJ, Johnson RD, Akamatsu H, Salamiah A, Otani H, Kohmoto K, Kodama M. 2001. Spontaneous loss of a conditionally dispensable chromosome from the Alternaria alternata apple pathotype leads to loss of toxin production and pathogenicity. Curr Genet 40:65–72. http://dx.doi.org/10.1007/s002940100233.
63. Hatta R, Ito K, Hosaki Y, Tanaka T, Tanaka A, Yamamoto M, Akimitsu K, Tsuge T. 2002. A conditionally dispensable chromosome controls host-specific pathogenicity in the fungal plant pathogen Alternaria alternata. Genetics 161:59–70.
64. Akagi Y, Akamatsu H, Otani H, Kodama M. 2009. Horizontal chromosome transfer, a mechanism for the evolution and differentiation of a plant-pathogenic fungus. Eukaryot Cell 8:1732–1738. http://dx.doi.org/10.1128/EC.00135-09.
65. Salamiah AH, Fukumasa-Nakai YHO, Kodama M. 2001. Construction and genetic analysis of hybrid strains between apple and tomato pathotypes of Alternaria alternata by protoplast fusion. J Gen Plant Pathol 67:97–105. http://dx.doi.org/10.1007/PL00013006.
66. Wight WD, Kim KH, Lawrence CB, Walton JD. 2009. Biosynthesis and role in virulence of the histone deacetylase inhibitor depudecin from Alternaria brassicicola. Mol Plant Microbe Interact 22:1258–1267. http: //dx.doi.org/10.1094/MPMI-22-10-1258.
67. Hashimoto M, Higuchi Y, Takahashi S, Osada H, Sakaki T, Toyomasu T, Sassa T, Kato N, Dairi T. 2009. Functional analyses of cytochrome P450 genes responsible for the early steps of brassicicene C biosynthesis. Bioorg Med Chem Lett 19:5640–5643. http://dx.doi.org/10.1016/j.bmcl.2009.08.026.
68. Otani H, Kohnobe A, Kodama M, Kohmoto K. 1998. Production of a host-specific toxin by germinating spores of Alternaria brassicicola. Physiol Mol Plant Pathol 52:285–295. http://dx.doi.org/10.1006/pmpp.1998.0147.
69. Kim K-H, Cho Y, La Rota M, Cramer R, Lawrence C. 2007. Functional analysis of the Alternaria brassicicola nonribosomal peptide synthetase gene AbNPS2 reveals a role in conidial cell wall construction. Mol Plant Pathol 8:23–39. http://dx.doi.org/10.1111/j.1364-3703.2006.00366.x.
70. Köllera W, Allana C, Kolattukudy P. 1982. Role of cutinase and cell wall degrading enzymes in infection of Pisum sativum by Fusarium solani f. sp. pisi. Physiol Plant Pathol 20:47–52. http://dx.doi.org/10.1016/0048-4059(82)90023-6.
71. Soliday C, Flurkey W, Okita T, Kolattukudy P. 1984. Cloning and structure determination of cDNA for cutinase, an enzyme involved in fungal penetration of plants. Proc Natl Acad Sci U S A 81:3939–3943. http://dx.doi.org/10.1073/pnas.81.13.3939.
72. Dickman M, Patil S. 1986. Cutinase deficient mutants of Colletotrichum gloeosporioides are non-pathogenic to papaya fruit. Physiol Mol Plant Pathol 28:235–242. http://dx.doi.org/10.1016/S0048-4059(86)80067-4.
73. Woloshuk C, Kolattukudy P. 1986. Mechanism by which contact with plant cuticle triggers cutinase gene expression in the spores of Fusarium solani f. sp. pisi. Proc Natl Acad Sci U S A 83:1704–1708. http://dx.doi.org/10.1073/pnas.83.6.1704.
74. Dickman M, Podila G, Kolattukudy P. 1989. Insertion of cutinase gene into a wound pathogen enables it to infect intact host. Nature 342:446–448. http://dx.doi.org/10.1038/342446a0.
75. Soliday C, Dickman B, Kolattukudy P. 1989. Structure of cutinase gene and detection of promoter activity in the 5=-flanking region by fungal transformation. J Bacteriol 171:1942–1951.
76. Li D, Ashby A, 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. http://dx.doi.org/10.1094/MPMI.2003.16.6.545.
77. Yao C, 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 8:122–130. http://dx.doi.org/10.1094/MPMI-8-0122.
78. Srivastava A, Ohm RA, Oxiles L, Brooks F, Lawrence CB, Grigoriev IV, Cho Y. 2012. A zinc-finger-family transcription factor, AbVf19, is required for the induction of a gene subset important for virulence in Alternaria brassicicola. Mol Plant Microbe Interact 25:443–452. http://dx.doi.org/10.1094/MPMI-10-11-0275.
79. Stahl D, Schafer W. 1992. Cutinase is not required for fungal pathogenicity on pea. Plant Cell 4:621–629. http://dx.doi.org/10.1105/tpc.4.6.621.
80. Sweigard J, Chumley F, Valent V. 1992. Disruption of a Magnaporthe grisea cutinase gene. Mol Gen Genet 232:183–190.
81. van Kan J, van’t Klooster J, Wagemakers C, Dees D, van der Vlugt-Berfmans C. 1997. Cutinase A of Botrytis cinerea is expressed, but not essential during penetration of gerbera and tomato. Mol Plant Microbe Interact 10:30–38. http://dx.doi.org/10.1094/MPMI.1997.10.1.30.
82. Lawrence CB, Mitchell TK, Craven KD, Cho Y, Cramer RA, Kim KH. 2008. At death’s door: alternaria pathogenicity mechanisms. Plant Pathol J 24:101–111. http://dx.doi.org/10.5423/PPJ.2008.24.2.101.
83. Beg QK, Kapoor MLM, GS H. 2001. Microbial xylanases and their industrial applications: a review. Appl Microbiol Biotechnol 56:326– 338. http://dx.doi.org/10.1007/s002530100704.
84. Carpita NC, Gibeaut DM. 1993. Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30. http://dx.doi.org/10.1111/j.1365-313X.1993.tb00007.x.
85. Annis S, Goodwin P. 1997. Recent advances in the molecular genetics of plant cell wall-degrading enzymes in plant pathogenic fungi. Eur J Plant Pathol 103:1–14. http://dx.doi.org/10.1023/A:1008656013255.
86. Shieh MT, Brown RL, Whitehead MP, Cary JW, Cotty PJ, Cleveland TE, Dean RA. 1997. Molecular genetic evidence for the involvement of a specific polygalacturonase, P2c, in the invasion and spread of Aspergillus flavus in cotton bolls. Appl Environ Microbiol 63:3548–3552.
87. ten Have A, Mulder W, Visser J, van Kan JA. 1998. The endopolygalacturonase gene Bcpg1 is required for full virulence of Botrytis cinerea. Mol Plant Microbe Interact 11:1009–1016. http://dx.doi.org/10.1094/MPMI.1998.11.10.1009.
88. Oeser B, Heidrich PM, Muller U, Tudzynski P, Tenberge KB. 2002. Polygalacturonase is a pathogenicity factor in the Claviceps purpurea/rye interaction. Fungal Genet Biol 36:176–186. http://dx.doi.org/10.1016/S1087-1845(02)00020-8.
89. Updegraff DM. 1969. Semimicro determination of cellulose in biological materials. Anal Biochem 32:420–424. http://dx.doi.org/10.1016/S0003-2697(69)80009-6.
90. Lev S, Horwitz BA. 2003. A mitogen-activated protein kinase pathway modulates the expression of two cellulase genes in Cochliobolus heterostrophus during plant infection. Plant Cell 15:835–844. http://dx.doi.org/10.1105/tpc.010546.
91. Apel-Birkhold PC, Walton JD. 1996. Cloning, disruption, and expression of two endo-beta 1, 4-xylanase genes, XYL2 and XYL3, from Cochliobolus carbonum. Appl Environ Microbiol 62:4129–4135.
92. Scott-Craig JS, Panaccione DG, Cervone F, Walton JD. 1990. Endopolygalacturonase is not required for pathogenicity of Cochliobolus car- bonum on maize. Plant Cell 2:1191–1200. http://dx.doi.org/10.1105/tpc.2.12.1191.
93. Wegener S, Ransom RF, Walton JD. 1999. A unique eukaryotic betaxylosidase gene from the phytopathogenic fungus Cochliobolus carbonum. Microbiology 145(Part 5):1089–1095. http://dx.doi.org/10.1099/13500872-145-5-1089.
94. Rogers LM, Kim YK, Guo W, Gonzalez-Candelas L, Li D, Kolattukudy PE. 2000. Requirement for either a host- or pectin-induced pectate lyase for infection of Pisum sativum by Nectria hematococca. Proc Natl Acad Sci U S A 97:9813–9818. http://dx.doi.org/10.1073/pnas.160271497.
95. Akimitsu K, Isshiki A, Ohtani K, Yamamoto H, Eshel D, Prusky D. 2004. Sugars and pH: a clue to the regulation of fungal cell walldegrading enzymes in plants. Physiol Mol Plant Pathol 65:271–275. http: //dx.doi.org/10.1016/j.pmpp.2005.03.001.
96. Brito N, Espino JJ, Gonzalez C. 2006. The endo-beta-1,4-xylanase xyn11A is required for virulence in Botrytis cinerea. Mol Plant Microbe Interact 19:25–32. http://dx.doi.org/10.1094/MPMI-19-0025.
97. Kars I, Krooshof GH, Wagemakers L, Joosten R, Benen JA, van Kan JA. 2005. Necrotizing activity of five Botrytis cinerea endopolygalacturonases produced in Pichia pastoris. Plant J 43:213–225. http://dx.doi.org/10.1111/j.1365-313X.2005.02436.x.
98. Kim KH, Willger SD, Park SW, Puttikamonkul S, Grahl N, Cho Y, Mukhopadhyay B, Cramer RA, Jr, Lawrence CB. 2009. TmpL, a transmembrane protein required for intracellular redox homeostasis and virulence in a plant and an animal fungal pathogen. PLoS Pathog 5:e1000653. http://dx.doi.org/10.1371/journal.ppat.1000653.
99. Ron D, Walter P. 2007. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8:519–529. http://dx.doi.org/10.1038/nrm2199.
100. Joubert A, Simoneau P, Campion C, Bataille-Simoneau N, Iacomi- Vasilescu B, Poupard P, Francois JM, Georgeault S, Sellier E, Guillemette T. 2011. Impact of the unfolded protein response on the pathogenicity of the necrotrophic fungus Alternaria brassicicola. Mol Microbiol 79:1305–1324. http://dx.doi.org/10.1111/j.1365-2958.2010.07522.x.
101. Joubert A, Bataille-Simoneau N, Campion C, Guillemette T, Hudhomme P, Iacomi-Vasilescu B, Leroy T, Pochon S, Poupard P, Simoneau P. 2011. Cell wall integrity and high osmolarity glycerol pathways are required for adaptation of Alternaria brassicicola to cell wall stress caused by brassicaceous indolic phytoalexins. Cell Microbiol 13:62–80. http://dx.doi.org/10.1111/j.1462-5822.2010.01520.x.
102. Zhao X, Mehrabi R, Xu JR. 2007. Mitogen-activated protein kinase pathways and fungal pathogenesis. Eukaryot Cell 6:1701–1714. http://dx.doi.org/10.1128/EC.00216-07.
103. Cho Y, Cramer RA, Jr, Kim KH, Davis J, Mitchell TK, Figuli P, Pryor BM, Lemasters E, Lawrence CB. 2007. The Fus3/Kss1 MAP kinase homolog Amk1 regulates the expression of genes encoding hydrolytic enzymes in Alternaria brassicicola. Fungal Genet Biol 44:543–553. http: //dx.doi.org/10.1016/j.fgb.2006.11.015.
104. Craven KD, Velez H, Cho Y, Lawrence CB, Mitchell TK. 2008. Anastomosis is required for virulence of the fungal necrotroph Alternaria brassicicola. Eukaryot Cell 7:675–683. http://dx.doi.org/10.1128/EC.00423-07.
105. Van Vu B, Itoh K, Nguyen QB, Tosa Y, Nakayashiki H. 2012. Cellulases belonging to glycoside hydrolase families 6 and 7 contribute to the virulence of Magnaporthe oryzae. Mol Plant Microbe Interact 25:1135–1141. http://dx.doi.org/10.1094/MPMI-02-12-0043-R.
106. Tonukari NJ, Scott-Craig JS, Walton JD. 2000. The Cochliobolus carbonum SNF1 gene is required for cell wall-degrading enzyme expression and virulence on maize. Plant Cell 12:237–248. http://dx.doi.org/10.1105/tpc.12.2.237.
107. Palecek SP, Parikh AS, Huh JH, Kron SJ. 2002. Depression of Saccharomyces cerevisiae invasive growth on non-glucose carbon sources requires the Snf1 kinase. Mol Microbiol 45:453–469. http://dx.doi.org/10.1046/j.1365-2958.2002.03024.x.
108. Ospina-Giraldo MD, Mullins E, Kang S. 2003. Loss of function of the Fusarium oxysporum SNF1 gene reduces virulence on cabbage and Arabidopsis. Curr Genet 44:49–57. http://dx.doi.org/10.1007/s00294-003-0419-y.
109. Takasugi M, Katsui N, Shirata A. 1986. Isolation of three novel sulphurcontaining phytoalexins from the chinese cabbage Brassica campestris L. ssp. pekinensis(cruciferae). J Chem Soc Chem Commun (Camb) 1986: 1077–1078. http://dx.doi.org/10.1039/C39860001077.
110. Pedras MS, Yaya EE, Glawischnig E. 2011. The phytoalexins from cultivated and wild crucifers: chemistry and biology. Nat Prod Rep 28: 1381–1405. http://dx.doi.org/10.1039/c1np00020a.
111. Srivastava A, Cho IK, Cho Y. 2013. The Bdtf1 gene in Alternaria brassicicola is important in detoxifying brassinin and maintaining virulence on Brassica species. Mol Plant Microbe Interact 26:1429–1440. http://dx.doi.org/10.1094/MPMI-07-13-0186-R.
112. Cho Y, Ohm RA, Devappa R, Lee HB, Grigoriev IV, Kim BY, Ahn JS. 2014. Transcriptional responses of the Bdtf1-deletion mutant to the phytoalexin brassinin in the necrotrophic fungus Alternaria brassicicola. Molecules 19:10717–10732. http://dx.doi.org/10.3390/molecules190810717.
113. Cho Y, Ohm RA, Grigoriev IV, Srivastava A. 2013. Fungal-specific transcription factor AbPf2 activates pathogenicity in Alternaria brassicicola. Plant J 75:498–514. http://dx.doi.org/10.1111/tpj.12217.
114. Nakayashiki H, Nguyen QB. 2008. RNA interference: roles in fungal biology. Curr Opin Microbiol 11:494–502. http://dx.doi.org/10.1016/j.mib.2008.10.001.
115. Kale SD, Gu B, Capelluto DG, Dou D, Feldman E, Rumore A, Arredondo FD, Hanlon R, Fudal I, Rouxel T, Lawrence CB, Shan W, Tyler BM. 2010. External lipid PI3P mediates entry of eukaryotic pathogen effectors into plant and animal host cells. Cell 142:284–295. http://dx.doi.org/10.1016/j.cell.2010.06.008.
116. Kale SD, Tyler BM. 2011. Entry of oomycete and fungal effectors into plant and animal host cells. Cell Microbiol 13:1839–1848. http://dx.doi.org/10.1111/j.1462-5822.2011.01659.x.
117. Djamei A, Schipper K, Rabe F, Ghosh A, Vincon V, Kahnt J, Osorio S, Tohge T, Fernie AR, Feussner I, Feussner K, Meinicke P, Stierhof YD, Schwarz H, Macek B, Mann M, Kahmann R. 2011. Metabolic priming by a secreted fungal effector. Nature 478:395–398. http://dx.doi.org/10.1038/nature10454.
118. Doehlemann G, van der Linde K, Assmann D, Schwammbach D, Hof A, Mohanty A, Jackson D, Kahmann R. 2009. Pep1, a secreted effector protein of Ustilago maydis, is required for successful invasion of plant cells. PLoS Pathog 5:e1000290. http://dx.doi.org/10.1371/journal.ppat.1000290.
119. Ciuffetti LM, Manning VA, Pandelova I, Betts MF, Martinez JP. 2010. Host-selective toxins, Ptr ToxA and Ptr ToxB, as necrotrophic effectors in the Pyrenophora tritici-repentis–wheat interaction. New Phytol 187: 911–919. http://dx.doi.org/10.1111/j.1469-8137.2010.03362.x