Epigenetic Control of Phenotypic Plasticity in the Filamentous Fungus Neurospora crassa.
Phenotypic plasticity is the ability of a genotype to produce different phenotypes under different environmental or developmental conditions. Phenotypic plasticity is a ubiquitous feature of living organisms, and is typically based on variable patterns of gene expression. However, the mechanisms by which gene expression is influenced and regulated during plastic responses are poorly understood in most organisms. While modifications to DNA and histone proteins have been implicated as likely candidates for generating and regulating phenotypic plasticity, specific details of each modification and its mode of operation have remained largely unknown. In this study, we investigated how epigenetic mechanisms affect phenotypic plasticity in the filamentous fungus Neurospora crassa By measuring reaction norms of strains that are deficient in one of several key physiological processes, we show that epigenetic mechanisms play a role in homeostasis and phenotypic plasticity of the fungus across a range of controlled environments. In general, effects on plasticity are specific to an environment and mechanism, indicating that epigenetic regulation is context dependent and is not governed by general plasticity genes. Specifically, we found that, in Neurospora, histone methylation at H3K36 affected plastic response to high temperatures, H3K4 methylation affected plastic response to pH, but H3K27 methylation had no effect. Similarly, DNA methylation had only a small effect in response to sucrose. Histone deacetylation mainly decreased reaction norm elevation, as did genes involved in histone demethylation and acetylation. In contrast, the RNA interference pathway was involved in plastic responses to multiple environments.
Centre of Excellence in Biological Interactions, Department of Biological and Environmental Sciences, University of Jyväskylä, FI-40014, Finland ilkka.kronholm@jyu.fi.
Ilkka
0000-0002-4126-0250
I
Kronholm
Department of Organismal Biology, University of Uppsala, 752 36, Sweden.
Hanna
H
Johannesson
Centre of Excellence in Biological Interactions, Department of Biological and Environmental Sciences, University of Jyväskylä, FI-40014, Finland.
Tarmo
T
Ketola
D000107:Acetylation; D000465:Algorithms; D000704:Analysis of Variance; D003433:Crosses, Genetic; D019175:DNA Methylation; D044127:Epigenesis, Genetic; D015966:Gene Expression Regulation, Fungal; D055786:Gene Knockout Techniques; D056726:Genetic Association Studies; D005838:Genotype; D006657:Histones / Q000378:metabolism; D008745:Methylation; D008954:Models, Biological; D015233:Models, Statistical; D009154:Mutation; D009492:Neurospora crassa / Q000235:genetics* / Q000378:metabolism*; D010641:Phenotype; D034622:RNA Interference
D006657:Histones
DNA methylation; RNA interference; fungi; histone deacetylation; histone methylation; reaction norm
Mycologia. 2009 Nov-Dec;101(6):823-32
19927747
Nat Rev Genet. 2014 Jun;15(6):394-408
24805120
Mycologia. 2006 Jul-Aug;98(4):550-9
17139848
Nature. 2009 May 14;459(7244):274-7
19444217
Eukaryot Cell. 2005 Aug;4(8):1446-54
16087749
Annu Rev Biochem. 2004;73:417-35
15189148
PLoS One. 2012;7(9):e41143
22984395
Mol Cell Biol. 2006 Oct;26(19):7077-85
16980612
Mol Ecol. 2016 Apr;25(8):1856-68
26139359
Cell. 2005 Aug 26;122(4):517-27
16122420
Cell. 2014 Dec 4;159(6):1352-64
25480298
Nature. 2012 Sep 20;489(7416):452-5
22914091
New Phytol. 2015 Nov;208(3):684-94
26037337
Science. 2004 Jun 25;304(5679):1939
15218142
Trends Plant Sci. 2010 Dec;15(12):684-92
20970368
Proc Natl Acad Sci U S A. 2006 Jul 5;103(27):10352-7
16801547
Bioessays. 2013 Jun;35(6):571-8
23580343
Nat Commun. 2013;4:1349
23322037
Cell. 2003 May 16;113(4):429-32
12757703
Science. 2015 Nov 6;350(6261):aab2006
26449473
Science. 2014 Mar 7;343(6175):1145-8
24505129
Plant Cell. 2006 Apr;18(4):805-14
16531498
Mol Cell. 2010 Jun 25;38(6):803-14
20417140
Evolution. 2014 Mar;68(3):656-72
24410266
J Evol Biol. 2009 Jul;22(7):1435-46
19467134
J Biosci. 2010 Mar;35(1):119-26
20413916
PLoS Genet. 2013;9(9):e1003761
24039604
Proc Natl Acad Sci U S A. 2013 Apr 9;110(15):6027-32
23530226
Sci Rep. 2014 May 30;4:5135
24875794
Nature. 2006 May 25;441(7092):469-74
16724059
Cell. 2008 Oct 17;135(2):272-83
18957202
Genetics. 2010 Dec;186(4):1207-16
20876559
PLoS Biol. 2010 Apr 27;8(4):e1000357
20463950
Mol Ecol. 2012 Jun;21(11):2602-16
22171717
Mol Cell. 2007 Apr 13;26(1):89-101
17434129
New Phytol. 2010 Mar;185(4):1108-18
20003072
Cell. 2011 Dec 9;147(6):1248-56
22119442
Genes Dev. 2007 Mar 1;21(5):590-600
17311884
Nat Rev Genet. 2012 Apr 03;13(5):343-57
22473383
Plant Mol Biol. 2015 Jul;88(4-5):387-400
25944663
Plant Physiol. 2012 Feb;158(2):854-63
22209873
Proc Natl Acad Sci U S A. 2010 May 4;107(18):8310-5
20404183
PLoS One. 2012;7(6):e38605
22723869
Proc Biol Sci. 2015 Oct 7;282(1816):20151651
26423845
Mol Ecol. 2015 Feb;24(4):710-25
25604587
Genes Dev. 2010 Mar 1;24(5):443-54
20139222
Nat Genet. 2003 May;34(1):75-9
12679815
Nature. 2014 Sep 25;513(7519):555-8
25079329
Am Nat. 2011 Aug;178(2):E18-36
21750377
Mol Cell Biol. 2004 Mar;24(6):2536-45
14993290
Nat Rev Genet. 2013 Jul;14(7):447-59
23732335
Cell. 2012 Jul 6;150(1):88-99
22738725
Nat Struct Mol Biol. 2012 Apr 15;19(5):471-7, S1
22504884
Biochim Biophys Acta. 2014 Aug;1839(8):627-43
24631868
Eukaryot Cell. 2005 Aug;4(8):1455-64
16087750
Mol Cell. 1999 Jul;4(1):123-8
10445034
Nature. 2001 Nov 15;414(6861):277-83
11713521
Plant Signal Behav. 2012 Jun;7(6):615-8
22580690
J Biol Chem. 2013 Mar 22;288(12):8380-90
23319591
Mol Biol Cell. 2012 Oct;23(19):3863-72
22875992
PLoS Genet. 2010 Nov 04;6(11):e1001196
21079689
EMBO J. 2011 Jun 21;30(14):2817-28
21694722
PLoS Biol. 2008 Apr 15;6(4):e83
18416601
Plant Cell. 2015 Feb;27(2):337-48
25670769
Mol Ecol. 2016 Apr;25(8):1785-800
25958780
Cell. 1992 Jun 12;69(6):915-26
1606615
Evolution. 2012 Sep;66(9):2891-902
22946810
Proc Biol Sci. 2014 Oct 22;281(1793):null
25209938
Plant Physiol. 2012 Feb;158(2):844-53
22147520
Nat Rev Genet. 2008 Aug;9(8):575-81
18574472