Roche CM, Loros JJ, McCluskey K, Glass NL (2014)
Neurospora crassa: looking back and looking
forward at a model microbe. Am J Bot 101:2022–
2035
Roman E, Cottier F, Ernst JF, Pla J (2009) Msb2 signaling mucin controls activation of Cek1 mitogenactivated protein kinase in Candida albicans.
Eukaryot Cell 8:1235–1249
Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat
Rev Mol Cell Biol 8:519–529
Rose MD, Misra LM, Vogel JP (1989) KAR2, a karyogamy gene, is the yeast homolog of the mammalian
BiP/GRP78 gene. Cell 57:1211–1221
Rubio C, Pincus D, Korennykh A, Schuck S, El-Samad
H, Walter P (2011) Homeostatic adaptation to
endoplasmic reticulum stress depends on Ire1
kinase activity. J Cell Biol 193:171–184
Saloheimo M, Lund M, Penttila ME (1999) The protein
disulphide isomerase gene of the fungus Trichoderma reesei is induced by endoplasmic reticulum
stress and regulated by the carbon source. Mol
Gen Genet 262:35–45
Saloheimo M, Valkonen M, Penttila M (2003) Activation mechanisms of the HAC1-mediated unfolded
protein response in filamentous fungi. Mol Microbiol 47:1149–1161
Samantaray S, Neubauer M, Helmschrott C, Wagener J
(2013) Role of the guanine nucleotide exchange
factor Rom2 in cell wall integrity maintenance of
Aspergillus fumigatus. Eukaryot Cell 12:288–298
Saraswat D, Kumar R, Pande T, Edgerton M, Cullen PJ
(2016) Signalling mucin Msb2 regulates adaptation to thermal stress in Candida albicans. Mol
Microbiol 100:425–441
Scherer M, Heimel K, Starke V, Ka ¨mper J (2006) The
Clp1 protein is required for clamp formation and
pathogenic development of Ustilago maydis. Plant
Cell 18:2388–2401
Schmitz L, Kronstad JW, Heimel K (2019a) Conditional
gene expression reveals stage-specific functions of
the unfolded protein response in the Ustilago maydis-maize pathosystem. Mol Plant Pathol 21
(2):258–271
Schmitz L, Schwier MA, Heimel K (2019b) The
unfolded protein response regulates pathogenic
development of Ustilago maydis by Rok1dependent inhibition of mating-type signaling.
mBio 10e
Schuck S, Gallagher CM, Walter P (2014) ER-phagy
mediates selective degradation of endoplasmic
reticulum independently of the core autophagy
machinery. J Cell Sci 127:4078–4088
Scrimale T, Didone L, de Mesy Bentley KL, Krysan DJ
(2009) The unfolded protein response is induced
by the cell wall integrity mitogen-activated protein
kinase signaling cascade and is required for cell
wall integrity in Saccharomyces cerevisiae. Mol
Biol Cell 20:164–175
Segmuller N, Kokkelink L, Giesbert S, Odinius D, van
Kan J, Tudzynski P (2008) NADPH oxidases are
involved in differentiation and pathogenicity in
Botrytis cinerea. Mol Plant-Microbe Interact
21:808–819
Shimano H, Sato R (2017) SREBP-regulated lipid
metabolism: convergent physiology - divergent
pathophysiology. Nat Rev Endocrinol 13:710–730
Shlezinger N, Irmer H, Dhingra S, Beattie SR, Cramer
RA, Braus GH, Sharon A, Hohl TM (2017) Sterilizing immunity in the lung relies on targeting fungal
apoptosis-like programmed cell death. Science
357:1037–1041
Sidrauski C, Cox JS, Walter P (1996) tRNA ligase is
required for regulated mRNA splicing in the
unfolded protein response. Cell 87:405–413
Sidrauski C, Walter P (1997) The transmembrane
kinase Ire1p is a site-specific endonuclease that
initiates mRNA splicing in the unfolded protein
response. Cell 90:1031–1039
Siegmund U, Heller J, van Kan JA, Tudzynski P (2013)
The NADPH oxidase complexes in Botrytis
cinerea: evidence for a close association with the
ER and the tetraspanin Pls1. PLoS One 8:e55879
Silberstein S, Schlenstedt G, Silver PA, Gilmore R
(1998) A role for the DnaJ homologue Scj1p in
protein folding in the yeast endoplasmic reticulum. J Cell Biol 143:921–933
Steel GJ, Fullerton DM, Tyson JR, Stirling CJ (2004)
Coordinated activation of Hsp70 chaperones. Science 303:98–101
Tam AB, Koong AC, Niwa M (2014) Ire1 has distinct
catalytic mechanisms for XBP1/HAC1 splicing and
RIDD. Cell Rep 9:850–858
Tam JM, Mansour MK, Acharya M, Sokolovska A,
Timmons AK, Lacy-Hulbert A, Vyas JM (2016)
The role of autophagy-related proteins in Candida
albicans infections. Pathogens 5(2):E34
Tanaka Y, Sasaki M, Ito F, Aoyama T, Sato-Okamoto M,
Takahashi-Nakaguchi A, Chibana H, Shibata N
(2018) Cooperation between ER stress and calcineurin signaling contributes to the maintenance of
cell wall integrity in Candida glabrata. Fungal Biol
122:19–33
Tang W, Ru Y, Hong L, Zhu Q, Zuo R, Guo X, Wang J,
Zhang H, Zheng X, Wang P, Zhang Z (2015)
System-wide characterization of bZIP transcription factor proteins involved in infection-related
morphogenesis of Magnaporthe oryzae. Environ
Microbiol 17:1377–1396
Thibault G, Ismail N, Ng DT (2011) The unfolded protein response supports cellular robustness as a
broad-spectrum compensatory pathway. Proc
Natl Acad Sci U S A 108:20597–20602
Thibault G, Ng DT (2012) The endoplasmic reticulumassociated degradation pathways of budding yeast.
Cold Spring Harb Perspect Biol 4(12):a013193
Thomas E, Sircaik S, Roman E, Brunel JM, Johri AK, Pla
J, Panwar SL (2015) The activity of RTA2, a down3 Genetics of the Unfolded Protein Response in Fungi
75
Neurospora crassa: looking back and looking
forward at a model microbe. Am J Bot 101:2022–
2035
Roman E, Cottier F, Ernst JF, Pla J (2009) Msb2 signaling mucin controls activation of Cek1 mitogenactivated protein kinase in Candida albicans.
Eukaryot Cell 8:1235–1249
Ron D, Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat
Rev Mol Cell Biol 8:519–529
Rose MD, Misra LM, Vogel JP (1989) KAR2, a karyogamy gene, is the yeast homolog of the mammalian
BiP/GRP78 gene. Cell 57:1211–1221
Rubio C, Pincus D, Korennykh A, Schuck S, El-Samad
H, Walter P (2011) Homeostatic adaptation to
endoplasmic reticulum stress depends on Ire1
kinase activity. J Cell Biol 193:171–184
Saloheimo M, Lund M, Penttila ME (1999) The protein
disulphide isomerase gene of the fungus Trichoderma reesei is induced by endoplasmic reticulum
stress and regulated by the carbon source. Mol
Gen Genet 262:35–45
Saloheimo M, Valkonen M, Penttila M (2003) Activation mechanisms of the HAC1-mediated unfolded
protein response in filamentous fungi. Mol Microbiol 47:1149–1161
Samantaray S, Neubauer M, Helmschrott C, Wagener J
(2013) Role of the guanine nucleotide exchange
factor Rom2 in cell wall integrity maintenance of
Aspergillus fumigatus. Eukaryot Cell 12:288–298
Saraswat D, Kumar R, Pande T, Edgerton M, Cullen PJ
(2016) Signalling mucin Msb2 regulates adaptation to thermal stress in Candida albicans. Mol
Microbiol 100:425–441
Scherer M, Heimel K, Starke V, Ka ¨mper J (2006) The
Clp1 protein is required for clamp formation and
pathogenic development of Ustilago maydis. Plant
Cell 18:2388–2401
Schmitz L, Kronstad JW, Heimel K (2019a) Conditional
gene expression reveals stage-specific functions of
the unfolded protein response in the Ustilago maydis-maize pathosystem. Mol Plant Pathol 21
(2):258–271
Schmitz L, Schwier MA, Heimel K (2019b) The
unfolded protein response regulates pathogenic
development of Ustilago maydis by Rok1dependent inhibition of mating-type signaling.
mBio 10e
Schuck S, Gallagher CM, Walter P (2014) ER-phagy
mediates selective degradation of endoplasmic
reticulum independently of the core autophagy
machinery. J Cell Sci 127:4078–4088
Scrimale T, Didone L, de Mesy Bentley KL, Krysan DJ
(2009) The unfolded protein response is induced
by the cell wall integrity mitogen-activated protein
kinase signaling cascade and is required for cell
wall integrity in Saccharomyces cerevisiae. Mol
Biol Cell 20:164–175
Segmuller N, Kokkelink L, Giesbert S, Odinius D, van
Kan J, Tudzynski P (2008) NADPH oxidases are
involved in differentiation and pathogenicity in
Botrytis cinerea. Mol Plant-Microbe Interact
21:808–819
Shimano H, Sato R (2017) SREBP-regulated lipid
metabolism: convergent physiology - divergent
pathophysiology. Nat Rev Endocrinol 13:710–730
Shlezinger N, Irmer H, Dhingra S, Beattie SR, Cramer
RA, Braus GH, Sharon A, Hohl TM (2017) Sterilizing immunity in the lung relies on targeting fungal
apoptosis-like programmed cell death. Science
357:1037–1041
Sidrauski C, Cox JS, Walter P (1996) tRNA ligase is
required for regulated mRNA splicing in the
unfolded protein response. Cell 87:405–413
Sidrauski C, Walter P (1997) The transmembrane
kinase Ire1p is a site-specific endonuclease that
initiates mRNA splicing in the unfolded protein
response. Cell 90:1031–1039
Siegmund U, Heller J, van Kan JA, Tudzynski P (2013)
The NADPH oxidase complexes in Botrytis
cinerea: evidence for a close association with the
ER and the tetraspanin Pls1. PLoS One 8:e55879
Silberstein S, Schlenstedt G, Silver PA, Gilmore R
(1998) A role for the DnaJ homologue Scj1p in
protein folding in the yeast endoplasmic reticulum. J Cell Biol 143:921–933
Steel GJ, Fullerton DM, Tyson JR, Stirling CJ (2004)
Coordinated activation of Hsp70 chaperones. Science 303:98–101
Tam AB, Koong AC, Niwa M (2014) Ire1 has distinct
catalytic mechanisms for XBP1/HAC1 splicing and
RIDD. Cell Rep 9:850–858
Tam JM, Mansour MK, Acharya M, Sokolovska A,
Timmons AK, Lacy-Hulbert A, Vyas JM (2016)
The role of autophagy-related proteins in Candida
albicans infections. Pathogens 5(2):E34
Tanaka Y, Sasaki M, Ito F, Aoyama T, Sato-Okamoto M,
Takahashi-Nakaguchi A, Chibana H, Shibata N
(2018) Cooperation between ER stress and calcineurin signaling contributes to the maintenance of
cell wall integrity in Candida glabrata. Fungal Biol
122:19–33
Tang W, Ru Y, Hong L, Zhu Q, Zuo R, Guo X, Wang J,
Zhang H, Zheng X, Wang P, Zhang Z (2015)
System-wide characterization of bZIP transcription factor proteins involved in infection-related
morphogenesis of Magnaporthe oryzae. Environ
Microbiol 17:1377–1396
Thibault G, Ismail N, Ng DT (2011) The unfolded protein response supports cellular robustness as a
broad-spectrum compensatory pathway. Proc
Natl Acad Sci U S A 108:20597–20602
Thibault G, Ng DT (2012) The endoplasmic reticulumassociated degradation pathways of budding yeast.
Cold Spring Harb Perspect Biol 4(12):a013193
Thomas E, Sircaik S, Roman E, Brunel JM, Johri AK, Pla
J, Panwar SL (2015) The activity of RTA2, a down3 Genetics of the Unfolded Protein Response in Fungi
75