questions and serve as an important model for
the fungal kingdom due to its rich history in the
field, a diversity of chromatin-based mechanisms shared among many fungi, and the availability of powerful molecular genetic tools to
drive future studies. Important goals for future
work include developing a more complete
understanding of promoter structure and how
it contributes to gene regulation, defining
unknown mechanisms that control assembly
and maintenance of both facultative and constitutive heterochromatin, defining the genes
and mechanisms that govern threedimensional chromosome organization in the
nucleus and how organization might change
under different conditions, and, lastly, defining
the complete complement of histone modifications in N. crassa and resolving additional subtypes of chromatin within euchromatin and
heterochromatin based on co-occurrence of
histone modifications and histone binding proteins.
References
Adhvaryu KK, Berge E, Tamaru H et al (2011) Substitutions in the amino-terminal tail of Neurospora
histone H3 have varied effects on DNA methylation. PLoS Genet 7:e1002423
Adhvaryu KK, Gessaman JD, Honda S et al (2015) The
cullin-4 complex DCDC does not require E3 ubiquitin ligase elements to control heterochromatin
in Neurospora crassa. Eukaryot Cell 14:25–28
Adhvaryu KK, Morris SA, Strahl BD, Selker EU (2005)
Methylation of histone H3 lysine 36 is required for
normal development in Neurospora crassa. Eukaryot Cell 4:1455–1464
Adhvaryu KK, Selker EU (2008) Protein phosphatase
PP1 is required for normal DNA methylation in
Neurospora. Genes Dev 22:3391–3396
Allis CD, Berger SL, Cote J et al (2007) New nomenclature for chromatin-modifying enzymes. Cell
131:633–636
Allis CD, Jenuwein T (2016) The molecular hallmarks of
epigenetic control. Nat Rev Genet 17:487–500
Anderson DC, Green GR, Smith K, Selker EU (2010)
Extensive and varied modifications in histone H2B
of wild-type and histone Deacetylase 1 mutant of
Neurospora crassa. Biochemistry 49:5244–5257
Basenko EY, Sasaki T, Ji L et al (2015) Genome-wide
redistribution of H3K27me3 is linked to genotoxic
stress and defective growth. Proc Natl Acad Sci U S
A 112:E6339–E6348
Belden WJ, Lewis ZA, Selker EU et al (2011) CHD1
remodels chromatin and influences transient
DNA methylation at the clock gene frequency.
PLoS Genet 7:e1002166
Belden WJ, Loros JJ, Dunlap JC (2007) Execution of the
circadian negative feedback loop in Neurospora
requires
the
ATP-dependent
chromatinremodeling enzyme CLOCKSWITCH. Mol Cell
25:587–600
Bicocca VT, Ormsby T, Adhvaryu KK et al (2018)
ASH1-catalyzed H3K36 methylation drives gene
repression and marks H3K27me2/3-competent
chromatin. elife 7:e41497. https://doi.org/10.7554/
eLife.41497
Borkovich KA, Alex LA, Yarden O et al (2004) Lessons
from the genome sequence of Neurospora crassa:
tracing the path from genomic blueprint to multicellular organism. Microbiol Mol Biol Rev 68:1–108
Brenna A, Grimaldi B, Filetici P, Ballario P (2012)
Physical association of the WC-1 photoreceptor
and the histone acetyltransferase NGF-1 is
required for blue light signal transduction in Neurospora crassa. Mol Biol Cell 23:3863–3872
Buenrostro JD, Giresi PG, Zaba LC et al (2013) Transposition of native chromatin for fast and sensitive
epigenomic profiling of open chromatin, DNAbinding proteins and nucleosome position. Nat
Methods 10:1213–1218
Carrozza MJ, Li B, Florens L et al (2005) Histone H3
methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123:581–592
Cha J, Zhou M, Liu Y (2013) CATP is a critical component of the Neurospora circadian clock by regulating the nucleosome occupancy rhythm at the
frequency locus. EMBO Rep 14:923–930
Cha J, Zhou M, Liu Y (2015) Mechanism of the Neurospora circadian clock, a FREQUENCY-centric view.
Biochemistry 54:150–156
Chambers AL, Downs JA (2007) The contribution of the
budding yeast histone H2A C-terminal tail to
DNA-damage responses. Biochem Soc Trans
35:1519–1524
Chicas A, Forrest EC, Sepich S et al (2005) Small interfering RNAs that trigger posttranscriptional gene
silencing are not required for the histone H3 Lys9
methylation necessary for transgenic tandem
repeat stabilization in Neurospora crassa. Mol
Cell Biol 25:3793–3801
Clapier CR, Cairns BR (2009) The biology of chromatin
remodeling complexes. Annu Rev Biochem
78:273–304
Clapier CR, Iwasa J, Cairns BR, Peterson CL (2017)
Mechanisms of action and regulation of ATPdependent chromatin-remodelling complexes.
Nat Rev Mol Cell Biol 18:407–422
Collins RE, Tachibana M, Tamaru H et al (2005) In vitro
and in vivo analyses of a Phe/Tyr switch
controlling product specificity of histone lysine
methyltransferases. J Biol Chem 280:5563–5570
20
A. J. Courtney et al.
the fungal kingdom due to its rich history in the
field, a diversity of chromatin-based mechanisms shared among many fungi, and the availability of powerful molecular genetic tools to
drive future studies. Important goals for future
work include developing a more complete
understanding of promoter structure and how
it contributes to gene regulation, defining
unknown mechanisms that control assembly
and maintenance of both facultative and constitutive heterochromatin, defining the genes
and mechanisms that govern threedimensional chromosome organization in the
nucleus and how organization might change
under different conditions, and, lastly, defining
the complete complement of histone modifications in N. crassa and resolving additional subtypes of chromatin within euchromatin and
heterochromatin based on co-occurrence of
histone modifications and histone binding proteins.
References
Adhvaryu KK, Berge E, Tamaru H et al (2011) Substitutions in the amino-terminal tail of Neurospora
histone H3 have varied effects on DNA methylation. PLoS Genet 7:e1002423
Adhvaryu KK, Gessaman JD, Honda S et al (2015) The
cullin-4 complex DCDC does not require E3 ubiquitin ligase elements to control heterochromatin
in Neurospora crassa. Eukaryot Cell 14:25–28
Adhvaryu KK, Morris SA, Strahl BD, Selker EU (2005)
Methylation of histone H3 lysine 36 is required for
normal development in Neurospora crassa. Eukaryot Cell 4:1455–1464
Adhvaryu KK, Selker EU (2008) Protein phosphatase
PP1 is required for normal DNA methylation in
Neurospora. Genes Dev 22:3391–3396
Allis CD, Berger SL, Cote J et al (2007) New nomenclature for chromatin-modifying enzymes. Cell
131:633–636
Allis CD, Jenuwein T (2016) The molecular hallmarks of
epigenetic control. Nat Rev Genet 17:487–500
Anderson DC, Green GR, Smith K, Selker EU (2010)
Extensive and varied modifications in histone H2B
of wild-type and histone Deacetylase 1 mutant of
Neurospora crassa. Biochemistry 49:5244–5257
Basenko EY, Sasaki T, Ji L et al (2015) Genome-wide
redistribution of H3K27me3 is linked to genotoxic
stress and defective growth. Proc Natl Acad Sci U S
A 112:E6339–E6348
Belden WJ, Lewis ZA, Selker EU et al (2011) CHD1
remodels chromatin and influences transient
DNA methylation at the clock gene frequency.
PLoS Genet 7:e1002166
Belden WJ, Loros JJ, Dunlap JC (2007) Execution of the
circadian negative feedback loop in Neurospora
requires
the
ATP-dependent
chromatinremodeling enzyme CLOCKSWITCH. Mol Cell
25:587–600
Bicocca VT, Ormsby T, Adhvaryu KK et al (2018)
ASH1-catalyzed H3K36 methylation drives gene
repression and marks H3K27me2/3-competent
chromatin. elife 7:e41497. https://doi.org/10.7554/
eLife.41497
Borkovich KA, Alex LA, Yarden O et al (2004) Lessons
from the genome sequence of Neurospora crassa:
tracing the path from genomic blueprint to multicellular organism. Microbiol Mol Biol Rev 68:1–108
Brenna A, Grimaldi B, Filetici P, Ballario P (2012)
Physical association of the WC-1 photoreceptor
and the histone acetyltransferase NGF-1 is
required for blue light signal transduction in Neurospora crassa. Mol Biol Cell 23:3863–3872
Buenrostro JD, Giresi PG, Zaba LC et al (2013) Transposition of native chromatin for fast and sensitive
epigenomic profiling of open chromatin, DNAbinding proteins and nucleosome position. Nat
Methods 10:1213–1218
Carrozza MJ, Li B, Florens L et al (2005) Histone H3
methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription. Cell 123:581–592
Cha J, Zhou M, Liu Y (2013) CATP is a critical component of the Neurospora circadian clock by regulating the nucleosome occupancy rhythm at the
frequency locus. EMBO Rep 14:923–930
Cha J, Zhou M, Liu Y (2015) Mechanism of the Neurospora circadian clock, a FREQUENCY-centric view.
Biochemistry 54:150–156
Chambers AL, Downs JA (2007) The contribution of the
budding yeast histone H2A C-terminal tail to
DNA-damage responses. Biochem Soc Trans
35:1519–1524
Chicas A, Forrest EC, Sepich S et al (2005) Small interfering RNAs that trigger posttranscriptional gene
silencing are not required for the histone H3 Lys9
methylation necessary for transgenic tandem
repeat stabilization in Neurospora crassa. Mol
Cell Biol 25:3793–3801
Clapier CR, Cairns BR (2009) The biology of chromatin
remodeling complexes. Annu Rev Biochem
78:273–304
Clapier CR, Iwasa J, Cairns BR, Peterson CL (2017)
Mechanisms of action and regulation of ATPdependent chromatin-remodelling complexes.
Nat Rev Mol Cell Biol 18:407–422
Collins RE, Tachibana M, Tamaru H et al (2005) In vitro
and in vivo analyses of a Phe/Tyr switch
controlling product specificity of histone lysine
methyltransferases. J Biol Chem 280:5563–5570
20
A. J. Courtney et al.