Widespread natural variation of DNA methylation within angiosperms.
BACKGROUND
DNA methylation is an important feature of plant epigenomes, involved in the formation of heterochromatin and affecting gene expression. Extensive variation of DNA methylation patterns within a species has been uncovered from studies of natural variation. However, the extent to which DNA methylation varies between flowering plant species is still unclear. To understand the variation in genomic patterning of DNA methylation across flowering plant species, we compared single base resolution DNA methylomes of 34 diverse angiosperm species.


RESULTS
By analyzing whole-genome bisulfite sequencing data in a phylogenetic context, it becomes clear that there is extensive variation throughout angiosperms in gene body DNA methylation, euchromatic silencing of transposons and repeats, as well as silencing of heterochromatic transposons. The Brassicaceae have reduced CHG methylation levels and also reduced or loss of CG gene body methylation. The Poaceae are characterized by a lack or reduction of heterochromatic CHH methylation and enrichment of CHH methylation in genic regions. Furthermore, low levels of CHH methylation are observed in a number of species, especially in clonally propagated species.


CONCLUSIONS
These results reveal the extent of variation in DNA methylation in angiosperms and show that DNA methylation patterns are broadly a reflection of the evolutionary and life histories of plant species.
Department of Genetics, University of Georgia, 120 East Green Street, Athens, GA, 30602, USA.
Chad E
CE
Niederhuth
Department of Genetics, University of Georgia, 120 East Green Street, Athens, GA, 30602, USA.
Adam J
AJ
Bewick
Institute of Bioinformatics, University of Georgia, Athens, GA, 30602, USA.
Lexiang
L
Ji
Department of Plant Biology, University of Georgia, Athens, GA, 30602, USA.
Magdy S
MS
Alabady
Center for Applied Genetic Technologies, University of Georgia, Athens, GA, 30602, USA.
Kyung Do
KD
Kim
Department of Plant Biology, Microbial and Plant Genomics Institute, University of Minnesota, Saint Paul, MN, 55108, USA.
Qing
Q
Li
Department of Genetics, University of Georgia, 120 East Green Street, Athens, GA, 30602, USA.
Nicholas A
NA
Rohr
Plant and Wildlife Science Department, Brigham Young University, Provo, UT, 84602, USA.
Aditi
A
Rambani
Department of Plant Biology, University of Georgia, Athens, GA, 30602, USA.
John M
JM
Burke
Department of Plant Biology, Microbial and Plant Genomics Institute, University of Minnesota, Saint Paul, MN, 55108, USA.
Joshua A
JA
Udall
National Root Crops Research Institute (NRCRI), Umudike, Km 8 Ikot Ekpene Road, PMB 7006, Umuahia, 440001, Nigeria.
Chiedozie
C
Egesi
HudsonAlpha Institute for Biotechnology, Huntsville, AL, 35806, USA.|Department of Energy Joint Genome Institute, Walnut Creek, CA, USA.
Jeremy
J
Schmutz
HudsonAlpha Institute for Biotechnology, Huntsville, AL, 35806, USA.
Jane
J
Grimwood
Center for Applied Genetic Technologies, University of Georgia, Athens, GA, 30602, USA.
Scott A
SA
Jackson
Plant and Wildlife Science Department, Brigham Young University, Provo, UT, 84602, USA.
Nathan M
NM
Springer
Department of Genetics, University of Georgia, 120 East Green Street, Athens, GA, 30602, USA. schmitz@uga.edu.
Robert J
RJ
Schmitz
Science. 2013 Dec 20;342(6165):1241089
24357323
Nature. 2007 Sep 27;449(7161):463-7
17721507
Mol Biol Evol. 2000 Apr;17(4):540-52
10742046
Nature. 2000 Dec 14;408(6814):796-815
11130711
Mob DNA. 2015 Jun 02;6:11
26045719
Bioinformatics. 2012 Aug 1;28(15):2059-61
22628521
Genome Biol. 2014 Jun 10;15(6):R77
24916971
Nature. 2011 Nov 16;480(7378):520-4
22089132
Nat Rev Mol Cell Biol. 2015 Sep;16(9):519-32
26296162
Nat Genet. 2013 Jul;45(7):831-5
23749190
Mol Cell. 2014 Aug 7;55(3):495-504
25018018
Nat Rev Genet. 2010 Mar;11(3):204-20
20142834
Nature. 1999 Sep 9;401(6749):157-61
10490023
Nat Methods. 2012 Jul 30;9(8):772
22847109
Mol Biol Evol. 2000 Jan;17(1):32-43
10666704
Proc Natl Acad Sci U S A. 2012 Oct 2;109(40):16240-5
22988127
Science. 2009 Nov 20;326(5956):1112-5
19965430
Curr Protoc Bioinformatics. 2010 Dec;Chapter 11:Unit 11.7
21154709
Nature. 2010 Jan 14;463(7278):178-83
20075913
Nucleic Acids Res. 2007 Jan;35(Database issue):D883-7
17145706
Mol Biol Evol. 2012 Jan;29(1):219-27
21813466
Genome Biol. 2013 Jun 03;14(6):r53
23731509
Bioinformatics. 2008 Jul 1;24(13):1530-1
18467344
Nature. 2009 Jan 29;457(7229):551-6
19189423
Ann Bot. 2005 Jan;95(1):127-32
15596462
J Comput Biol. 2015 May;22(5):377-86
25549288
Plant Cell. 2013 Aug;25(8):2783-97
23922207
Nature. 2015 Jul 9;523(7559):212-6
26030523
Mol Plant. 2014 Mar;7(3):472-80
24270503
Nat Biotechnol. 2014 Jul;32(7):656-62
24908277
PLoS Genet. 2015 Mar 31;11(3):e1005142
25826366
Curr Biol. 2012 Feb 21;22(4):326-31
22285031
BMC Bioinformatics. 2005 Feb 15;6:31
15713233
Plant Cell. 2014 Dec;26(12):4602-16
25527708
Nat Protoc. 2012 Mar 01;7(3):562-78
22383036
Bioinformatics. 2007 Nov 15;23(22):3024-31
17848398
Plant Physiol. 1999 Jun;120(2):383-90
10364389
Proc Natl Acad Sci U S A. 2012 Jul 24;109(30):12040-5
22778444
Plant Physiol. 2005 Jul;138(3):1723-33
15951485
Cell. 2008 May 2;133(3):523-36
18423832
Trop Plant Biol. 2012 Mar;5(1):88-94
22523606
Nature. 2010 Feb 11;463(7282):763-8
20148030
Curr Biol. 2005 Jan 26;15(2):154-9
15668172
Nat Biotechnol. 2010 Sep;28(9):951-6
20729833
Biochem Genet. 1974 Oct;12(4):257-69
4441361
Annu Rev Genet. 2014;48:49-70
25149370
Cell. 2012 Sep 28;151(1):167-80
23021223
Nat Genet. 2011 May;43(5):476-81
21478890
Nat Plants. 2016 Jan 25;2:15222
27249194
Cell. 2013 Mar 28;153(1):193-205
23540698
Elife. 2015 May 05;4:e05255
25939354
Nature. 2013 Mar 14;495(7440):193-8
23467092
Nat Struct Mol Biol. 2014 Jan;21(1):64-72
24336224
PLoS Biol. 2007 Jul;5(7):e174
17579518
Proc Natl Acad Sci U S A. 2010 May 11;107(19):8689-94
20395551
Genome Biol. 2017 May 1;18(1):65
28457232
Front Plant Sci. 2013 Mar 21;4:46
23518688
Genome Res. 2013 Oct;23(10):1663-74
23739894
PLoS Comput Biol. 2014 Apr 10;10(4):e1003537
24722319
Nature. 2014 Jan 23;505(7484):546-9
24352233
Annu Rev Plant Physiol Plant Mol Biol. 1998 Jun;49:223-247
15012234
Proc Natl Acad Sci U S A. 2015 Nov 24;112(47):14728-33
26553984
PLoS One. 2012;7(2):e30100
22319559
Genome Biol. 2011;12(1):R10
21251332
Cell. 2013 Jan 17;152(1-2):352-64
23313553
Nat Genet. 2007 Jan;39(1):61-9
17128275
Genes Dev. 2015 Oct 15;29(20):2183-202
26494791
Genome Res. 2009 Jun;19(6):959-66
19273618
Epigenetics Chromatin. 2015 Jul 31;8:26
26229551
Proc Natl Acad Sci U S A. 2013 Nov 26;110(48):19478-82
24225854
Nat Commun. 2014 Apr 23;5:3722
24759728
Plant Cell. 2005 May;17(5):1549-58
15805479
Nat Genet. 2010 Oct;42(10):833-9
20802477
Nature. 2008 Mar 13;452(7184):215-9
18278030
Curr Opin Genet Dev. 2008 Dec;18(6):565-70
19131240
Nat Protoc. 2015 Mar;10(3):475-83
25692984
Syst Biol. 2003 Oct;52(5):696-704
14530136
Elife. 2013 Mar 19;2:e00354
23539454
PLoS Genet. 2014 Nov 13;10(11):e1004785
25393550
Proc Natl Acad Sci U S A. 2002 Dec 10;99 Suppl 4:16491-8
12151602
Science. 2001 Jun 15;292(5524):2077-80
11349138
PLoS One. 2014 Aug 14;9(8):e105267
25122127
Trends Genet. 2012 Dec;28(12):583-5
23131467
Front Plant Sci. 2013 Jul 02;4:170
23874343
Nat Genet. 2013 Aug;45(8):891-8
23817568
Cell. 2009 Feb 6;136(3):461-72
19203581
PLoS Genet. 2013 Apr;9(4):e1003437
23593031
Science. 2010 May 14;328(5980):916-9
20395474
Cell. 2012 Sep 28;151(1):194-205
23000270
Cell. 2006 Sep 22;126(6):1189-201
16949657
Comput Appl Biosci. 1997 Oct;13(5):555-6
9367129
Front Genet. 2015 Jan 29;6:4
25688257
Nature. 2012 May 30;485(7400):635-41
22660326
Nat Genet. 2013 May;45(5):487-94
23525075
Science. 2006 Sep 15;313(5793):1596-604
16973872
Nat Biotechnol. 2013 Feb;31(2):154-9
23354102
Cell. 2016 May 19;165(5):1280-1292
27203113
Proc Natl Acad Sci U S A. 1996 Aug 6;93(16):8449-54
8710891
Proc Natl Acad Sci U S A. 2013 Jan 29;110(5):1797-802
23319627
Proc Natl Acad Sci U S A. 2003 Jul 22;100(15):8828-33
12817081
New Phytol. 2010 Apr;186(2):318-32
20202131
Nature. 2012 Dec 20;492(7429):423-7
23257886
DNA Res. 2015 Aug;22(4):279-91
26070980
Nat Genet. 2014 Jul;46(7):707-13
24908249
Cell. 1995 Dec 1;83(5):725-34
8521489
PLoS Genet. 2011 Nov;7(11):e1002372
22125494
Science. 2011 Oct 21;334(6054):369-73
21921155
Genome Biol. 2013 Apr 25;14(4):R36
23618408
Curr Biol. 2002 Jul 9;12(13):1138-44
12121623
Proc Natl Acad Sci U S A. 2016 Aug 9;113(32):9111-6
27457936
Nucleic Acids Res. 2012 Jan;40(Database issue):D1178-86
22110026
BMC Evol Biol. 2010 Feb 24;10:61
20181251
Nature. 2015 Sep 24;525(7570):533-7
26352475
DNA Res. 2008 Aug;15(4):227-39
18511435
Cytogenet Genome Res. 2010 Jul;129(1-3):17-23
20628248
Genome Res. 2013 Apr;23(4):628-37
23269663
Nat Rev Genet. 2012 May 29;13(7):484-92
22641018
Plant Cell Rep. 2009 Sep;28(9):1373-84
19565244
Genome Biol. 2011 Oct 20;12(10):R102
22014239
Nature. 2014 Jun 19;510(7505):356-62
24919147
Science. 2007 Sep 21;317(5845):1760-4
17673620
Nature. 2011 Sep 20;480(7376):245-9
22057020
Bioinformatics. 2004 Jan 22;20(2):289-90
14734327
Front Plant Sci. 2015 Aug 13;6:590
26322052
Nat Genet. 2006 Aug;38(8):948-52
16832354
Bioinformatics. 2010 Mar 15;26(6):841-2
20110278
Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
15034147
Genome Res. 2013 Oct;23(10):1651-62
23739895
New Phytol. 2015 Sep;207(4):1181-97
25919642
Nat Genet. 2011 Feb;43(2):109-16
21186353
Nat Plants. 2015 Feb 02;1:14023
27246759
Nature. 2009 Oct 22;461(7267):1135-8
19847267
Cell. 2016 Jul 14;166(2):492-505
27419873
Proc Natl Acad Sci U S A. 2015 Mar 17;112(11):3553-7
25733903
BMC Genomics. 2012 Nov 22;13:660
23173562