and membrane protein biogenesis and endoplasmic reticulum quality control. J Cell Biol 150:77–88
Ngiam C, Jeenes DJ, Punt PJ, Van Den Hondel CA,
Archer DB (2000) Characterization of a foldase,
protein disulfide isomerase a, in the protein secretory pathway of Aspergillus niger. Appl Environ
Microbiol 66:775–782
Nishikawa SI, Fewell SW, Kato Y, Brodsky JL, Endo T
(2001) Molecular chaperones in the yeast endoplasmic reticulum maintain the solubility of proteins for retrotranslocation and degradation. J Cell
Biol 153:1061–1070
Oikawa D, Kimata Y, Kohno K (2007) Self-association
and BiP dissociation are not sufficient for activation of the ER stress sensor Ire1. J Cell Sci
120:1681–1688
Pakula TM, Laxell M, Huuskonen A, Uusitalo J, Saloheimo M, Penttila M (2003) The effects of drugs
inhibiting protein secretion in the filamentous
fungus Trichoderma reesei. Evidence for downregulation of genes that encode secreted proteins
in the stressed cells. J Biol Chem 278:45011–45020
Pal B, Chan NC, Helfenbaum L, Tan K, Tansey WP,
Gething MJ (2007) SCFCdc4-mediated degradation of the Hac1p transcription factor regulates
the unfolded protein response in Saccharomyces
cerevisiae. Mol Biol Cell 18:426–440
Palmer GE, Askew DS, Williamson PR (2008) The
diverse roles of autophagy in medically important
fungi. Autophagy 4:982–988
Park SH, Bolender N, Eisele F, Kostova Z, Takeuchi J,
Coffino P, Wolf DH (2007) The cytoplasmic Hsp70
chaperone machinery subjects misfolded and
endoplasmic reticulum import-incompetent proteins to degradation via the ubiquitin-proteasome
system. Mol Biol Cell 18:153–165
Patil CK, Li H, Walter P (2004) Gcn4p and novel
upstream activating sequences regulate targets of
the unfolded protein response. PLoS Biol 2:E246
Perez-Martin J, Castillo-Lluva S (2008) Connections
between polar growth and cell cycle arrest during
the induction of the virulence program in the
phytopathogenic fungus Ustilago maydis. Plant
Signal Behav 3:480–481
Pinter N, Hach CA, Hampel M, Rekhter D, Zienkiewicz
K, Feussner I, Poehlein A, Daniel R, Finkernagel F,
Heimel K (2019) Signal peptide peptidase activity
connects the unfolded protein response to plant
defense suppression by Ustilago maydis. PLoS
Pathog 15:e1007734
Pollack JK, Harris SD, Marten MR (2009) Autophagy in
filamentous fungi. Fungal Genet Biol 46:1–8
Promlek T, Ishiwata-Kimata Y, Shido M, Sakuramoto
M, Kohno K, Kimata Y (2011) Membrane aberrancy and unfolded proteins activate the endoplasmic reticulum stress sensor Ire1 in different ways.
Mol Biol Cell 22:3520–3532
Punt PJ, van Gemeren IA, Drint-Kuijvenhoven J, Hessing JG, van Muijlwijk-Harteveld GM, Beijersbergen A, Verrips CT, van den Hondel CA (1998)
Analysis of the role of the gene bipA, encoding
the major endoplasmic reticulum chaperone protein in the secretion of homologous and heterologous proteins in black Aspergilli. Appl Microbiol
Biotechnol 50:447–454
Qi F, Zhang W, Zhang F, Chen G, Liu W (2014) Deciphering the effect of the different N-glycosylation
sites on the secretion, activity, and stability of
cellobiohydrolase I from Trichoderma reesei.
Appl Environ Microbiol 80:3962–3971
Qin L, Wu VW, Glass NL (2017) Deciphering the regulatory network between the SREBP pathway and
protein secretion in Neurospora crassa. MBio 8(2):
e00233–e00217
Raj S, Krishnan K, Askew DS, Helynck O, Suzanne P,
Lesnard A, Rault S, Zeidler U, d’Enfert C, Latge JP,
Munier-Lehmann H, Saveanu C (2015) The toxicity of a novel antifungal compound is modulated
by endoplasmic reticulum-associated protein degradation components. Antimicrob Agents Chemother 60:1438–1449
Reggiori F, Klionsky DJ (2013) Autophagic processes in
yeast: mechanism, machinery and regulation.
Genetics 194:341–361
Reilly MC, Qin L, Craig JP, Starr TL, Glass NL (2015)
Deletion of homologs of the SREBP pathway
results in hyper-production of cellulases in Neurospora crassa and Trichoderma reesei. Biotechnol
Biofuels 8:121
Richie DL, Feng X, Hartl L, Aimanianda V, Krishnan K,
Powers-Fletcher MV, Watson DS, Galande AK,
White SM, Willett T, Latge JP, Rhodes JC, Askew
DS (2011b) The virulence of the opportunistic
fungal pathogen Aspergillus fumigatus requires
cooperation between the endoplasmic reticulumassociated degradation pathway (ERAD) and
the unfolded protein response (UPR). Virulence
2:12–21
Richie DL, Feng X, Krishnan K, Askew DS (2011a)
Secretion stress and antifungal resistance: an
Achilles’ heel of Aspergillus fumigatus? Med
Mycol 49(Suppl 1):S101–S106
Richie DL, Hartl L, Aimanianda V, Winters MS, Fuller
KK, Miley MD, White S, McCarthy JW, Latge JP,
Feldmesser M, Rhodes JC, Askew DS (2009) A role
for the unfolded protein response (UPR) in virulence and antifungal susceptibility in Aspergillus
fumigatus. PLoS Pathog 5:e1000258
Robichon C, Dugail I (2007) De novo cholesterol synthesis at the crossroads of adaptive response to
extracellular stress through SREBP. Biochimie
89:260–264
Roca MG, Weichert M, Siegmund U, Tudzynski P,
Fleissner A (2012) Germling fusion via conidial
anastomosis tubes in the grey mould Botrytis
cinerea requires NADPH oxidase activity. Fungal
Biol 116:379–387
74
R. Harting and K. Heimel
Ngiam C, Jeenes DJ, Punt PJ, Van Den Hondel CA,
Archer DB (2000) Characterization of a foldase,
protein disulfide isomerase a, in the protein secretory pathway of Aspergillus niger. Appl Environ
Microbiol 66:775–782
Nishikawa SI, Fewell SW, Kato Y, Brodsky JL, Endo T
(2001) Molecular chaperones in the yeast endoplasmic reticulum maintain the solubility of proteins for retrotranslocation and degradation. J Cell
Biol 153:1061–1070
Oikawa D, Kimata Y, Kohno K (2007) Self-association
and BiP dissociation are not sufficient for activation of the ER stress sensor Ire1. J Cell Sci
120:1681–1688
Pakula TM, Laxell M, Huuskonen A, Uusitalo J, Saloheimo M, Penttila M (2003) The effects of drugs
inhibiting protein secretion in the filamentous
fungus Trichoderma reesei. Evidence for downregulation of genes that encode secreted proteins
in the stressed cells. J Biol Chem 278:45011–45020
Pal B, Chan NC, Helfenbaum L, Tan K, Tansey WP,
Gething MJ (2007) SCFCdc4-mediated degradation of the Hac1p transcription factor regulates
the unfolded protein response in Saccharomyces
cerevisiae. Mol Biol Cell 18:426–440
Palmer GE, Askew DS, Williamson PR (2008) The
diverse roles of autophagy in medically important
fungi. Autophagy 4:982–988
Park SH, Bolender N, Eisele F, Kostova Z, Takeuchi J,
Coffino P, Wolf DH (2007) The cytoplasmic Hsp70
chaperone machinery subjects misfolded and
endoplasmic reticulum import-incompetent proteins to degradation via the ubiquitin-proteasome
system. Mol Biol Cell 18:153–165
Patil CK, Li H, Walter P (2004) Gcn4p and novel
upstream activating sequences regulate targets of
the unfolded protein response. PLoS Biol 2:E246
Perez-Martin J, Castillo-Lluva S (2008) Connections
between polar growth and cell cycle arrest during
the induction of the virulence program in the
phytopathogenic fungus Ustilago maydis. Plant
Signal Behav 3:480–481
Pinter N, Hach CA, Hampel M, Rekhter D, Zienkiewicz
K, Feussner I, Poehlein A, Daniel R, Finkernagel F,
Heimel K (2019) Signal peptide peptidase activity
connects the unfolded protein response to plant
defense suppression by Ustilago maydis. PLoS
Pathog 15:e1007734
Pollack JK, Harris SD, Marten MR (2009) Autophagy in
filamentous fungi. Fungal Genet Biol 46:1–8
Promlek T, Ishiwata-Kimata Y, Shido M, Sakuramoto
M, Kohno K, Kimata Y (2011) Membrane aberrancy and unfolded proteins activate the endoplasmic reticulum stress sensor Ire1 in different ways.
Mol Biol Cell 22:3520–3532
Punt PJ, van Gemeren IA, Drint-Kuijvenhoven J, Hessing JG, van Muijlwijk-Harteveld GM, Beijersbergen A, Verrips CT, van den Hondel CA (1998)
Analysis of the role of the gene bipA, encoding
the major endoplasmic reticulum chaperone protein in the secretion of homologous and heterologous proteins in black Aspergilli. Appl Microbiol
Biotechnol 50:447–454
Qi F, Zhang W, Zhang F, Chen G, Liu W (2014) Deciphering the effect of the different N-glycosylation
sites on the secretion, activity, and stability of
cellobiohydrolase I from Trichoderma reesei.
Appl Environ Microbiol 80:3962–3971
Qin L, Wu VW, Glass NL (2017) Deciphering the regulatory network between the SREBP pathway and
protein secretion in Neurospora crassa. MBio 8(2):
e00233–e00217
Raj S, Krishnan K, Askew DS, Helynck O, Suzanne P,
Lesnard A, Rault S, Zeidler U, d’Enfert C, Latge JP,
Munier-Lehmann H, Saveanu C (2015) The toxicity of a novel antifungal compound is modulated
by endoplasmic reticulum-associated protein degradation components. Antimicrob Agents Chemother 60:1438–1449
Reggiori F, Klionsky DJ (2013) Autophagic processes in
yeast: mechanism, machinery and regulation.
Genetics 194:341–361
Reilly MC, Qin L, Craig JP, Starr TL, Glass NL (2015)
Deletion of homologs of the SREBP pathway
results in hyper-production of cellulases in Neurospora crassa and Trichoderma reesei. Biotechnol
Biofuels 8:121
Richie DL, Feng X, Hartl L, Aimanianda V, Krishnan K,
Powers-Fletcher MV, Watson DS, Galande AK,
White SM, Willett T, Latge JP, Rhodes JC, Askew
DS (2011b) The virulence of the opportunistic
fungal pathogen Aspergillus fumigatus requires
cooperation between the endoplasmic reticulumassociated degradation pathway (ERAD) and
the unfolded protein response (UPR). Virulence
2:12–21
Richie DL, Feng X, Krishnan K, Askew DS (2011a)
Secretion stress and antifungal resistance: an
Achilles’ heel of Aspergillus fumigatus? Med
Mycol 49(Suppl 1):S101–S106
Richie DL, Hartl L, Aimanianda V, Winters MS, Fuller
KK, Miley MD, White S, McCarthy JW, Latge JP,
Feldmesser M, Rhodes JC, Askew DS (2009) A role
for the unfolded protein response (UPR) in virulence and antifungal susceptibility in Aspergillus
fumigatus. PLoS Pathog 5:e1000258
Robichon C, Dugail I (2007) De novo cholesterol synthesis at the crossroads of adaptive response to
extracellular stress through SREBP. Biochimie
89:260–264
Roca MG, Weichert M, Siegmund U, Tudzynski P,
Fleissner A (2012) Germling fusion via conidial
anastomosis tubes in the grey mould Botrytis
cinerea requires NADPH oxidase activity. Fungal
Biol 116:379–387
74
R. Harting and K. Heimel