Impact of the UPR on the virulence of the plant fungal pathogen A. brassicicola

References

• Salo PM, Arbes SJ Jr., Sever M, Jaramillo R, Cohn RD, London SJ, Zeldin DC. Exposure to Alternaria alternata in US homes is associated with asthma symptoms. J Allergy Clin Immunol 2006; 118:892 - 8; http://dx.doi.org/10.1016/j.jaci.2006.07.037; PMID: 17030243
   PubMed Web of Science ®Google Scholar
• Lawrence CB, Mitchell TK, Craven KD, Cho Y, Cramer RA, Kim K. At Death’s Door: Alternaria Pathogenicity Mechanisms. Plant Pathol J 2008; 24:101 - 11; http://dx.doi.org/10.5423/PPJ.2008.24.2.101
   Web of Science ®Google Scholar
• Divon HH, Fluhr R. Nutrition acquisition strategies during fungal infection of plants. FEMS Microbiol Lett 2007; 266:65 - 74; http://dx.doi.org/10.1111/j.1574-6968.2006.00504.x; PMID: 17083369
   PubMed Web of Science ®Google Scholar
• Cho Y, Cramer RA Jr., Kim KH, Davis J, Mitchell TK, Figuli P, Pryor BM, Lemasters E, Lawrence CB. The Fus3/Kss1 MAP kinase homolog Amk1 regulates the expression of genes encoding hydrolytic enzymes in Alternaria brassicicola. Fungal Genet Biol 2007; 44:543 - 53; http://dx.doi.org/10.1016/j.fgb.2006.11.015; PMID: 17280842
   PubMed Web of Science ®Google Scholar
• Fan C, Köller W. Diversity of cutinases from plant pathogenic fungi: differential and sequential expression of cutinolytic esterases by Alternaria brassicicola. FEMS Microbiol Lett 1998; 158:33 - 8; http://dx.doi.org/10.1111/j.1574-6968.1998.tb12796.x
   Web of Science ®Google Scholar
• Friesen TL, Faris JD, Solomon PS, Oliver RP. Host-specific toxins: effectors of necrotrophic pathogenicity. Cell Microbiol 2008; 10:1421 - 8; http://dx.doi.org/10.1111/j.1462-5822.2008.01153.x; PMID: 18384660
   PubMed Web of Science ®Google Scholar
• Feng X, Krishnan K, Richie DL, Aimanianda V, Hartl L, Grahl N, Powers-Fletcher MV, Zhang M, Fuller KK, Nierman WC, et al. HacA-independent functions of the ER stress sensor IreA synergize with the canonical UPR to influence virulence traits in Aspergillus fumigatus. PLoS Pathog 2011; 7:e1002330; http://dx.doi.org/10.1371/journal.ppat.1002330; PMID: 22028661
   PubMedGoogle Scholar
• Joubert A, Simoneau P, Campion C, Bataillé-Simoneau N, Iacomi-Vasilescu B, Poupard P, François JM, Georgeault S, Sellier E, Guillemette T. Impact of the unfolded protein response on the pathogenicity of the necrotrophic fungus Alternaria brassicicola. Mol Microbiol 2011; 79:1305 - 24; http://dx.doi.org/10.1111/j.1365-2958.2010.07522.x; PMID: 21251090
   PubMed Web of Science ®Google Scholar
• Kaufman RJ, Scheuner D, Schröder M, Shen X, Lee K, Liu CY, Arnold SM. The unfolded protein response in nutrient sensing and differentiation. Nat Rev Mol Cell Biol 2002; 3:411 - 21; http://dx.doi.org/10.1038/nrm829; PMID: 12042763
   PubMed Web of Science ®Google Scholar
• Richie DL, Hartl L, Aimanianda V, Winters MS, Fuller KK, Miley MD, White S, McCarthy JW, Latgé JP, Feldmesser M, et al. A role for the unfolded protein response (UPR) in virulence and antifungal susceptibility in Aspergillus fumigatus. PLoS Pathog 2009; 5:e1000258; http://dx.doi.org/10.1371/journal.ppat.1000258; PMID: 19132084
   PubMed Web of Science ®Google Scholar
• Schröder M, Kaufman RJ. ER stress and the unfolded protein response. Mutat Res 2005; 569:29 - 63; http://dx.doi.org/10.1016/j.mrfmmm.2004.06.056; PMID: 15603751
   PubMed Web of Science ®Google Scholar
• Archer DB, Turner G. Genomics of protein secretion and hyphal growth in Aspergillus. In: Brown A, ed. The Mycota XIII, Fungal Genomics: Springer, 2006:75-96.
   Google Scholar
• Conesa A, Punt PJ, van Luijk N, van den Hondel CA. The secretion pathway in filamentous fungi: a biotechnological view. Fungal Genet Biol 2001; 33:155 - 71; http://dx.doi.org/10.1006/fgbi.2001.1276; PMID: 11495573
   PubMed Web of Science ®Google Scholar
• Lubertozzi D, Keasling JD. Developing Aspergillus as a host for heterologous expression. Biotechnol Adv 2009; 27:53 - 75; http://dx.doi.org/10.1016/j.biotechadv.2008.09.001; PMID: 18840517
   PubMed Web of Science ®Google Scholar
• Rüegsegger U, Leber JH, Walter P. Block of HAC1 mRNA translation by long-range base pairing is released by cytoplasmic splicing upon induction of the unfolded protein response. Cell 2001; 107:103 - 14; http://dx.doi.org/10.1016/S0092-8674(01)00505-0; PMID: 11595189
   PubMed Web of Science ®Google Scholar
• Kohno K. Stress-sensing mechanisms in the unfolded protein response: similarities and differences between yeast and mammals. J Biochem 2010; 147:27 - 33; http://dx.doi.org/10.1093/jb/mvp196; PMID: 19942680
   PubMed Web of Science ®Google Scholar
• Miyazaki T, Nakayama H, Nagayoshi Y, Kakeya H, Kohno S. Dissection of Ire1 functions reveals stress response mechanisms uniquely evolved in Candida glabrata. PLoS Pathog 2013; 9:e1003160; http://dx.doi.org/10.1371/journal.ppat.1003160; PMID: 23382685
   PubMedGoogle Scholar
• Kimmig P, Diaz M, Zheng J, Williams CC, Lang A, Aragón T, Li H, Walter P. The unfolded protein response in fission yeast modulates stability of select mRNAs to maintain protein homeostasis. Elife 2012; 1:e00048; http://dx.doi.org/10.7554/eLife.00048; PMID: 23066505
   PubMedGoogle Scholar
• Hoseki J, Ushioda R, Nagata K. Mechanism and components of endoplasmic reticulum-associated degradation. J Biochem 2010; 147:19 - 25; http://dx.doi.org/10.1093/jb/mvp194; PMID: 19923195
   PubMed Web of Science ®Google Scholar
• Richie DL, Feng X, Hartl L, Aimanianda V, Krishnan K, Powers-Fletcher MV, Watson DS, Galande AK, White SM, Willett T, et al. The virulence of the opportunistic fungal pathogen Aspergillus fumigatus requires cooperation between the endoplasmic reticulum-associated degradation pathway (ERAD) and the unfolded protein response (UPR). Virulence 2011; 2:12 - 21; http://dx.doi.org/10.4161/viru.2.1.13345; PMID: 21217201
   PubMed Web of Science ®Google Scholar
• Travers KJ, Patil CK, Wodicka L, Lockhart DJ, Weissman JS, Walter P. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 2000; 101:249 - 58; http://dx.doi.org/10.1016/S0092-8674(00)80835-1; PMID: 10847680
   PubMed Web of Science ®Google Scholar
• Al-Sheikh H, Watson AJ, Lacey GA, Punt PJ, MacKenzie DA, Jeenes DJ, Pakula T, Penttilä M, Alcocer MJ, Archer DB. Endoplasmic reticulum stress leads to the selective transcriptional downregulation of the glucoamylase gene in Aspergillus niger. Mol Microbiol 2004; 53:1731 - 42; http://dx.doi.org/10.1111/j.1365-2958.2004.04236.x; PMID: 15341651
   PubMed Web of Science ®Google Scholar
• Pakula TM, Laxell M, Huuskonen A, Uusitalo J, Saloheimo M, Penttilä M. The effects of drugs inhibiting protein secretion in the filamentous fungus Trichoderma reesei. Evidence for down-regulation of genes that encode secreted proteins in the stressed cells. J Biol Chem 2003; 278:45011 - 20; http://dx.doi.org/10.1074/jbc.M302372200; PMID: 12941955
   PubMed Web of Science ®Google Scholar
• Guillemette T, van Peij NN, Goosen T, Lanthaler K, Robson GD, van den Hondel CA, Stam H, Archer DB. Genomic analysis of the secretion stress response in the enzyme-producing cell factory Aspergillus niger. BMC Genomics 2007; 8:158; http://dx.doi.org/10.1186/1471-2164-8-158; PMID: 17561995
   PubMed Web of Science ®Google Scholar
• Leber JH, Bernales S, Walter P. IRE1-independent gain control of the unfolded protein response. PLoS Biol 2004; 2:E235; http://dx.doi.org/10.1371/journal.pbio.0020235; PMID: 15314654
   PubMedGoogle Scholar
• Pochon S, Terrasson E, Guillemette T, Iacomi-Vasilescu B, Georgeault S, Juchaux M, Berruyer R, Debeaujon I, Simoneau P, Campion C. The Arabidopsis thaliana-Alternaria brassicicola pathosystem: A model interaction for investigating seed transmission of necrotrophic fungi. Plant Methods 2012; 8:16; http://dx.doi.org/10.1186/1746-4811-8-16; PMID: 22571391
   PubMed Web of Science ®Google Scholar
• Humpherson-Jones FM. The incidence of Alternaria spp. and Leptosphaeria maculans in commercial brassica seed in the United Kingdom. Plant Pathol 1985; 34:385 - 90; http://dx.doi.org/10.1111/j.1365-3059.1985.tb01377.x
   Web of Science ®Google Scholar
• Kohl J, van Tongeren CAM, Groenenboom-de Haas BH, van Hoof RA, Driessen R, van der Heijden L. Epidemiology of dark leaf spot caused by Alternaria brassicicola and A. brassicae in organic seed production of cauliflower. Plant Pathol 2010; 59:358 - 67; http://dx.doi.org/10.1111/j.1365-3059.2009.02216.x
   Web of Science ®Google Scholar
• Maude RB, Humpherson-Jones FM. Studies on the seed-borne phases of dark leaf spot (Alternaria brassicicola) and grey leaf spot (Alternaria brassicae) of brassicas. Ann Appl Biol 1980; 95:311 - 9; http://dx.doi.org/10.1111/j.1744-7348.1980.tb04752.x
   Web of Science ®Google Scholar
• Bock CH, Thrall PH, Burdon JJ. Genetic structure of populations of Alternaria brassicicola suggests the occurrence of sexual recombination. Mycol Res 2005; 109:227 - 36; http://dx.doi.org/10.1017/S0953756204001674; PMID: 15839106
   PubMedGoogle Scholar
• Iacomi-Vasilescu B, Bataillé-Simoneau N, Campion C, Dongo A, Laurent E, Serandat I, et al. Effect of null mutations in the AbNIK1 gene on saprophytic and parasitic fitness of Alternaria brassicicola isolates highly resistant to dicarboximides fungicides. Plant Pathol 2008; 57:937 - 47; http://dx.doi.org/10.1111/j.1365-3059.2008.01864.x
   Web of Science ®Google Scholar
• Guillemette T, Iacomi-Vasilescu B, Simoneau P. Conventional and real-time PCR-based assay for detecting pathogenic Alternaria brassicae in cruciferous seed. Plant Dis 2004; 88:490 - 6; http://dx.doi.org/10.1094/PDIS.2004.88.5.490
   Web of Science ®Google Scholar
• Martínez IM, Chrispeels MJ. Genomic analysis of the unfolded protein response in Arabidopsis shows its connection to important cellular processes. Plant Cell 2003; 15:561 - 76; http://dx.doi.org/10.1105/tpc.007609; PMID: 12566592
   PubMed Web of Science ®Google Scholar
• Cheon SA, Jung KW, Chen YL, Heitman J, Bahn YS, Kang HA. Unique evolution of the UPR pathway with a novel bZIP transcription factor, Hxl1, for controlling pathogenicity of Cryptococcus neoformans. PLoS Pathog 2011; 7:e1002177; http://dx.doi.org/10.1371/journal.ppat.1002177; PMID: 21852949
   PubMedGoogle Scholar
• Mulder HJ, Nikolaev I. HacA-dependent transcriptional switch releases hacA mRNA from a translational block upon endoplasmic reticulum stress. Eukaryot Cell 2009; 8:665 - 75; http://dx.doi.org/10.1128/EC.00131-08; PMID: 19181870
   PubMed Web of Science ®Google Scholar
• Wimalasena TT, Enjalbert B, Guillemette T, Plumridge A, Budge S, Yin Z, Brown AJ, Archer DB. Impact of the unfolded protein response upon genome-wide expression patterns, and the role of Hac1 in the polarized growth, of Candida albicans. Fungal Genet Biol 2008; 45:1235 - 47; http://dx.doi.org/10.1016/j.fgb.2008.06.001; PMID: 18602013
   PubMed Web of Science ®Google Scholar
• Bicknell AA, Babour A, Federovitch CM, Niwa M. A novel role in cytokinesis reveals a housekeeping function for the unfolded protein response. J Cell Biol 2007; 177:1017 - 27; http://dx.doi.org/10.1083/jcb.200702101; PMID: 17562790
   PubMed Web of Science ®Google Scholar
• Sellam A, Iacomi-Vasilescu B, Hudhomme P, Simoneau P. In vitro antifungal activity of brassinin, camalexin and two isothiocyanates against the crucifer pathogens Alternaria brassicicola and Alternaria brassicae. Plant Pathol 2007; 56:296 - 301; http://dx.doi.org/10.1111/j.1365-3059.2006.01497.x
   Web of Science ®Google Scholar
• Morrissey JP, Osbourn AE. Fungal resistance to plant antibiotics as a mechanism of pathogenesis. Microbiol Mol Biol Rev 1999; 63:708 - 24; PMID: 10477313
   PubMed Web of Science ®Google Scholar
• Fahey JW, Zalcmann AT, Talalay P. The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 2001; 56:5 - 51; http://dx.doi.org/10.1016/S0031-9422(00)00316-2; PMID: 11198818
   PubMed Web of Science ®Google Scholar
• Pedras MS, Yaya EE, Glawischnig E. The phytoalexins from cultivated and wild crucifers: chemistry and biology. Nat Prod Rep 2011; 28:1381 - 405; http://dx.doi.org/10.1039/c1np00020a; PMID: 21681321
   PubMed Web of Science ®Google Scholar
• Sellam A, Dongo A, Guillemette T, Hudhomme P, Simoneau P. Transcriptional responses to exposure to the brassicaceous defence metabolites camalexin and allyl-isothiocyanate in the necrotrophic fungus Alternaria brassicicola. Mol Plant Pathol 2007; 8:195 - 208; http://dx.doi.org/10.1111/j.1364-3703.2007.00387.x; PMID: 20507491
   PubMed Web of Science ®Google Scholar
• Joubert A, Bataille-Simoneau N, Campion C, Guillemette T, Hudhomme P, Iacomi-Vasilescu B, Leroy T, Pochon S, Poupard P, Simoneau P. 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 2011; 13:62 - 80; http://dx.doi.org/10.1111/j.1462-5822.2010.01520.x; PMID: 20812995
   PubMed Web of Science ®Google Scholar
• Glazebrook J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 2005; 43:205 - 27; http://dx.doi.org/10.1146/annurev.phyto.43.040204.135923; PMID: 16078883
   PubMed Web of Science ®Google Scholar
• Perfect SE, Green JR. Infection structures of biotrophic and hemibiotrophic fungal plant pathogens. Mol Plant Pathol 2001; 2:101 - 8; http://dx.doi.org/10.1046/j.1364-3703.2001.00055.x; PMID: 20572997
   PubMed Web of Science ®Google Scholar
• Yi M, Chi MH, Khang CH, Park SY, Kang S, Valent B, Lee YH. The ER chaperone LHS1 is involved in asexual development and rice infection by the blast fungus Magnaporthe oryzae. Plant Cell 2009; 21:681 - 95; http://dx.doi.org/10.1105/tpc.107.055988; PMID: 19252083
   PubMed Web of Science ®Google Scholar
• Liu J-X, Howell SH. Endoplasmic reticulum protein quality control and its relationship to environmental stress responses in plants. Plant Cell 2010; 22:2930 - 42; http://dx.doi.org/10.1105/tpc.110.078154; PMID: 20876830
   PubMed Web of Science ®Google Scholar
• Noh SJ, Kwon CS, Chung WI. Characterization of two homologs of Ire1p, a kinase/endoribonuclease in yeast, in Arabidopsis thaliana. Biochim Biophys Acta 2002; 1575:130 - 4; http://dx.doi.org/10.1016/S0167-4781(02)00237-3; PMID: 12020828
   PubMed Web of Science ®Google Scholar
• Koizumi N, Martinez IM, Kimata Y, Kohno K, Sano H, Chrispeels MJ. Molecular characterization of two Arabidopsis Ire1 homologs, endoplasmic reticulum-located transmembrane protein kinases. Plant Physiol 2001; 127:949 - 62; http://dx.doi.org/10.1104/pp.010636; PMID: 11706177
   PubMed Web of Science ®Google Scholar
• Deng Y, Humbert S, Liu JX, Srivastava R, Rothstein SJ, Howell SH. Heat induces the splicing by IRE1 of a mRNA encoding a transcription factor involved in the unfolded protein response in Arabidopsis. Proc Natl Acad Sci U S A 2011; 108:7247 - 52; http://dx.doi.org/10.1073/pnas.1102117108; PMID: 21482766
   PubMed Web of Science ®Google Scholar
• Nagashima Y, Mishiba K, Suzuki E, Shimada Y, Iwata Y, Koizumi N. Arabidopsis IRE1 catalyses unconventional splicing of bZIP60 mRNA to produce the active transcription factor. Sci Rep 2011; 1:29; http://dx.doi.org/10.1038/srep00029; PMID: 22355548
   PubMed Web of Science ®Google Scholar
• Wiseman RL, Zhang Y, Lee KPK, Harding HP, Haynes CM, Price J, Sicheri F, Ron D. Flavonol activation defines an unanticipated ligand-binding site in the kinase-RNase domain of IRE1. Mol Cell 2010; 38:291 - 304; http://dx.doi.org/10.1016/j.molcel.2010.04.001; PMID: 20417606
   PubMed Web of Science ®Google Scholar
• Iwata Y, Koizumi N. Plant transducers of the endoplasmic reticulum unfolded protein response. Trends Plant Sci 2012; 17:720 - 7; http://dx.doi.org/10.1016/j.tplants.2012.06.014; PMID: 22796463
   PubMed Web of Science ®Google Scholar
• Healy SJ, Gorman AM, Mousavi-Shafaei P, Gupta S, Samali A. Targeting the endoplasmic reticulum-stress response as an anticancer strategy. Eur J Pharmacol 2009; 625:234 - 46; http://dx.doi.org/10.1016/j.ejphar.2009.06.064; PMID: 19835867
   PubMed Web of Science ®Google Scholar
• Woehlbier U, Hetz C. Modulating stress responses by the UPRosome: a matter of life and death. Trends Biochem Sci 2011; 36:329 - 37; http://dx.doi.org/10.1016/j.tibs.2011.03.001; PMID: 21482118
   PubMed Web of Science ®Google Scholar
• Cross BC, Bond PJ, Sadowski PG, Jha BK, Zak J, Goodman JM, Silverman RH, Neubert TA, Baxendale IR, Ron D, et al. The molecular basis for selective inhibition of unconventional mRNA splicing by an IRE1-binding small molecule. Proc Natl Acad Sci U S A 2012; 109:E869 - 78; http://dx.doi.org/10.1073/pnas.1115623109; PMID: 22315414
   PubMed Web of Science ®Google Scholar
• Papandreou I, Denko NC, Olson M, Van Melckebeke H, Lust S, Tam A, Solow-Cordero DE, Bouley DM, Offner F, Niwa M, et al. Identification of an Ire1alpha endonuclease specific inhibitor with cytotoxic activity against human multiple myeloma. Blood 2011; 117:1311 - 4; http://dx.doi.org/10.1182/blood-2010-08-303099; PMID: 21081713
   PubMed Web of Science ®Google Scholar
• Volkmann K, Lucas JL, Vuga D, Wang X, Brumm D, Stiles C, Kriebel D, Der-Sarkissian A, Krishnan K, Schweitzer C, et al. Potent and selective inhibitors of the inositol-requiring enzyme 1 endoribonuclease. J Biol Chem 2011; 286:12743 - 55; http://dx.doi.org/10.1074/jbc.M110.199737; PMID: 21303903
   PubMed Web of Science ®Google Scholar