logenetic conservation of structure and function of
the clock gene frequency. EMBO J 13:2257–2266.
https://doi.org/10.1002/j.1460-2075.1994.tb06507.
x
Merrow MW, Garceau NY, Dunlap JC (1997) Dissection
of a circadian oscillation into discrete domains.
Proc Natl Acad Sci 94:3877–3882. https://doi.org/
10.1073/pnas.94.8.3877
Montenegro-Montero A, Canessa P, Larrondo LF
(2015) Chapter four – Around the fungal clock:
recent advances in the molecular study of circadian clocks in Neurospora and other Fungi. In:
Friedmann T, Dunlap JC, Goodwin SF (eds)
Advances in genetics. Academic Press, Cambridge,
MA, pp 107–184
Morales Y, Olsen KJ, Bulcher JM, Johnson SJ (2018)
Structure of frequency-interacting RNA helicase
from Neurospora crassa reveals high flexibility in
a domain critical for circadian rhythm and RNA
surveillance. PLoS One 13:e0196642
Morgan LW, Greene AV, Bell-Pedersen D (2003) Circadian and light-induced expression of luciferase in
Neurospora crassa. Fungal Genet Biol 38:327–332.
https://doi.org/10.1016/S1087-1845(02)00562-5
Mure LS, Le HD, Benegiamo G et al (2018) Diurnal
transcriptome atlas of a primate across major neural and peripheral tissues. Science 359(80):
eaao0318. https://doi.org/10.1126/science.aao0318
Ode KL, Ukai H, Susaki EA et al (2017) Knockoutrescue embryonic stem cell-derived mouse reveals
circadian-period control by quality and quantity
of CRY1. Mol Cell 65:176–190. https://doi.org/
10.1016/j.molcel.2016.11.022
Olivares-Yan ˜ez C, Emerson J, Kettenbach A et al (2016)
Modulation of circadian gene expression and metabolic compensation by the RCO-1 corepressor of
Neurospora crassa. Genetics 204:163–176. https://
doi.org/10.1534/genetics.116.191064
Ouyang Y, Andersson CR, Kondo T et al (1998) Resonating circadian clocks enhance fitness in cyanobacteria. Proc Natl Acad Sci 95:8660–8664. https://
doi.org/10.1073/pnas.95.15.8660
Padmanabhan K, Robles MS, Westerling T, Weitz CJ
(2012) Feedback regulation of transcriptional termination by the mammalian circadian clock
PERIOD complex. Science 337(80):599–602.
https://doi.org/10.1126/science.1221592
Panda S, Hogenesch JB, Kay SA (2002) Circadian
rhythms from flies to human. Nature 417:329
Pavesi G, Mereghetti P, Mauri G, Pesole G (2004)
Weeder web: discovery of transcription factor
binding sites in a set of sequences from coregulated genes. Nucleic Acids Res 32:W199–
W203. https://doi.org/10.1093/nar/gkh465
Peek CB, Ramsey KM, Marcheva B, Bass J (2012) Nutrient sensing and the circadian clock. Trends Endocrinol Metab 23:312–318. https://doi.org/10.1016/j.
tem.2012.02.003
Pelham JF, Mosier AE, Hurley JM (2018) Characterizing
time-of-day conformational changes in the intrinsically disordered proteins of the circadian clock,
1st edn. Elsevier, Cambridge
Pittendrigh CS, Bruce VG, Rosenweig NS, Rubin ML
(1959) A biological clock in Neurospora. Nature
184:169–170. https://doi.org/10.1038/184169a0
Pregueiro AM, Price-Lloyd N, Bell-Pedersen D et al
(2005) Assignment of an essential role for the
Neurospora frequency gene in circadian entrainment to temperature cycles. Proc Natl Acad Sci U S
A 102:2210
Pregueiro AM, Liu Q, Baker CL et al (2006) The Neurospora checkpoint kinase 2: a regulatory link
between the circadian and cell cycles. Science 313
(80):644–649
Putnam AA, Jankowsky E (2013) DEAD-box helicases
as integrators of RNA, nucleotide and protein
binding. Biochim Biophys Acta 1829:884–893.
https://doi.org/10.1016/j.bbagrm.2013.02.002
Querfurth C, Diernfellner ACR, Gin E et al (2011) Circadian conformational change of the Neurospora
clock protein FREQUENCY triggered by clustered
hyperphosphorylation of a basic domain. Mol Cell
43:713–722.
https://doi.org/10.1016/j.molcel.2011.06.033
Raduwan H, Isola AL, Belden WJ (2013) Methylation of
histone H3 on lysine 4 by the lysine methyltransferase SET1 protein is needed for normal clock
gene expression. J Biol Chem 288:8380–8390.
https://doi.org/10.1074/jbc.M112.359935
Ramsdale M, Lakin-Thomas PL (2000) sn-1,2-diacylglycerol levels in the fungus Neurospora crassa
display circadian rhythmicity. J Biol Chem 275
(36):27541–27550
Reinke H, Asher G (2019) Crosstalk between metabolism and circadian clocks. Nat Rev Mol Cell Biol
20:227–241. https://doi.org/10.1038/s41580-0180096-9
Reischl S, Kramer A (2011) Kinases and phosphatases
in the mammalian circadian clock. FEBS Lett
585:1393–1399.
https://doi.org/10.1016/j.febslet.2011.02.038
Salichos L, Rokas A (2010) The diversity and evolution
of circadian clock proteins in fungi. Mycologia
102:269–278
Sancar G, Sancar C, Brunner M, Schafmeier T (2009)
Activity of the circadian transcription factor white
collar complex is modulated by phosphorylation
of SP-motifs. FEBS Lett 583:1833–1840. https://doi.
org/10.1016/j.febslet.2009.04.042
Sancar G, Sancar C, Bru ¨gger B et al (2011) A global
circadian repressor controls antiphasic expression
of metabolic genes in neurospora. Mol Cell 44:687–
697. https://doi.org/10.1016/j.molcel.2011.10.019
Sancar G, Sancar C, Brunner M (2012) Metabolic compensation of the Neurospora clock by a glucosedependent feedback of the circadian repressor
4 From Genetics to Molecular Oscillations: The Circadian Clock in Neurospora crassa
101
the clock gene frequency. EMBO J 13:2257–2266.
https://doi.org/10.1002/j.1460-2075.1994.tb06507.
x
Merrow MW, Garceau NY, Dunlap JC (1997) Dissection
of a circadian oscillation into discrete domains.
Proc Natl Acad Sci 94:3877–3882. https://doi.org/
10.1073/pnas.94.8.3877
Montenegro-Montero A, Canessa P, Larrondo LF
(2015) Chapter four – Around the fungal clock:
recent advances in the molecular study of circadian clocks in Neurospora and other Fungi. In:
Friedmann T, Dunlap JC, Goodwin SF (eds)
Advances in genetics. Academic Press, Cambridge,
MA, pp 107–184
Morales Y, Olsen KJ, Bulcher JM, Johnson SJ (2018)
Structure of frequency-interacting RNA helicase
from Neurospora crassa reveals high flexibility in
a domain critical for circadian rhythm and RNA
surveillance. PLoS One 13:e0196642
Morgan LW, Greene AV, Bell-Pedersen D (2003) Circadian and light-induced expression of luciferase in
Neurospora crassa. Fungal Genet Biol 38:327–332.
https://doi.org/10.1016/S1087-1845(02)00562-5
Mure LS, Le HD, Benegiamo G et al (2018) Diurnal
transcriptome atlas of a primate across major neural and peripheral tissues. Science 359(80):
eaao0318. https://doi.org/10.1126/science.aao0318
Ode KL, Ukai H, Susaki EA et al (2017) Knockoutrescue embryonic stem cell-derived mouse reveals
circadian-period control by quality and quantity
of CRY1. Mol Cell 65:176–190. https://doi.org/
10.1016/j.molcel.2016.11.022
Olivares-Yan ˜ez C, Emerson J, Kettenbach A et al (2016)
Modulation of circadian gene expression and metabolic compensation by the RCO-1 corepressor of
Neurospora crassa. Genetics 204:163–176. https://
doi.org/10.1534/genetics.116.191064
Ouyang Y, Andersson CR, Kondo T et al (1998) Resonating circadian clocks enhance fitness in cyanobacteria. Proc Natl Acad Sci 95:8660–8664. https://
doi.org/10.1073/pnas.95.15.8660
Padmanabhan K, Robles MS, Westerling T, Weitz CJ
(2012) Feedback regulation of transcriptional termination by the mammalian circadian clock
PERIOD complex. Science 337(80):599–602.
https://doi.org/10.1126/science.1221592
Panda S, Hogenesch JB, Kay SA (2002) Circadian
rhythms from flies to human. Nature 417:329
Pavesi G, Mereghetti P, Mauri G, Pesole G (2004)
Weeder web: discovery of transcription factor
binding sites in a set of sequences from coregulated genes. Nucleic Acids Res 32:W199–
W203. https://doi.org/10.1093/nar/gkh465
Peek CB, Ramsey KM, Marcheva B, Bass J (2012) Nutrient sensing and the circadian clock. Trends Endocrinol Metab 23:312–318. https://doi.org/10.1016/j.
tem.2012.02.003
Pelham JF, Mosier AE, Hurley JM (2018) Characterizing
time-of-day conformational changes in the intrinsically disordered proteins of the circadian clock,
1st edn. Elsevier, Cambridge
Pittendrigh CS, Bruce VG, Rosenweig NS, Rubin ML
(1959) A biological clock in Neurospora. Nature
184:169–170. https://doi.org/10.1038/184169a0
Pregueiro AM, Price-Lloyd N, Bell-Pedersen D et al
(2005) Assignment of an essential role for the
Neurospora frequency gene in circadian entrainment to temperature cycles. Proc Natl Acad Sci U S
A 102:2210
Pregueiro AM, Liu Q, Baker CL et al (2006) The Neurospora checkpoint kinase 2: a regulatory link
between the circadian and cell cycles. Science 313
(80):644–649
Putnam AA, Jankowsky E (2013) DEAD-box helicases
as integrators of RNA, nucleotide and protein
binding. Biochim Biophys Acta 1829:884–893.
https://doi.org/10.1016/j.bbagrm.2013.02.002
Querfurth C, Diernfellner ACR, Gin E et al (2011) Circadian conformational change of the Neurospora
clock protein FREQUENCY triggered by clustered
hyperphosphorylation of a basic domain. Mol Cell
43:713–722.
https://doi.org/10.1016/j.molcel.2011.06.033
Raduwan H, Isola AL, Belden WJ (2013) Methylation of
histone H3 on lysine 4 by the lysine methyltransferase SET1 protein is needed for normal clock
gene expression. J Biol Chem 288:8380–8390.
https://doi.org/10.1074/jbc.M112.359935
Ramsdale M, Lakin-Thomas PL (2000) sn-1,2-diacylglycerol levels in the fungus Neurospora crassa
display circadian rhythmicity. J Biol Chem 275
(36):27541–27550
Reinke H, Asher G (2019) Crosstalk between metabolism and circadian clocks. Nat Rev Mol Cell Biol
20:227–241. https://doi.org/10.1038/s41580-0180096-9
Reischl S, Kramer A (2011) Kinases and phosphatases
in the mammalian circadian clock. FEBS Lett
585:1393–1399.
https://doi.org/10.1016/j.febslet.2011.02.038
Salichos L, Rokas A (2010) The diversity and evolution
of circadian clock proteins in fungi. Mycologia
102:269–278
Sancar G, Sancar C, Brunner M, Schafmeier T (2009)
Activity of the circadian transcription factor white
collar complex is modulated by phosphorylation
of SP-motifs. FEBS Lett 583:1833–1840. https://doi.
org/10.1016/j.febslet.2009.04.042
Sancar G, Sancar C, Bru ¨gger B et al (2011) A global
circadian repressor controls antiphasic expression
of metabolic genes in neurospora. Mol Cell 44:687–
697. https://doi.org/10.1016/j.molcel.2011.10.019
Sancar G, Sancar C, Brunner M (2012) Metabolic compensation of the Neurospora clock by a glucosedependent feedback of the circadian repressor
4 From Genetics to Molecular Oscillations: The Circadian Clock in Neurospora crassa
101