The Scientific World JournalVolume 2012 (2012), Article ID 298174, 26 pagesdoi:10.1100/2012/298174

Research Article

Conservation of Nucleosome Positions in Duplicated and Orthologous Gene Pairs

Hiromi Nishida

Agricultural Bioinformatics Research Unit, Graduate School of Agriculture and Life Sciences, The University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan

Received 5 October 2011; Accepted 8 December 2011

Academic Editor: David E. Misek

Copyright © 2012 Hiromi Nishida. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract.

Although nucleosome positions tend to be conserved in gene promoters, whether they are conserved in duplicated and orthologous genes is unknown. In order to elucidate how nucleosome positions are conserved between duplicated and orthologous gene pairs, I performed 2 comparative studies. First, I compared the nucleosome position profiles of duplicated genes in the filamentous ascomycete Aspergillus fumigatus. After identifying 63 duplicated gene pairs among 9630 protein-encoding genes, I compared the nucleosome position profiles of the paired genes. Although nucleosome positions are conserved more in gene promoters than in gene bodies, their profiles were diverse, suggesting evolutionary changes after gene duplication. Next, I examined the conservation of nucleosome position profiles in 347 A. fumigatus orthologs of S. cerevisiae genes that showed notably high conservation of nucleosome positions between the parent strain and 2 deletion mutants. In only 11 (3.2%) of the 347 gene pairs, the nucleosome position profile was highly conserved (Spearman’s rank correlation coefficient > 0.7). The absence of nucleosome position conservation in promoters of orthologous genes suggests organismal specificity of nucleosome arrangements.

1. Introduction

Nucleosomes are histone octamers around which DNA is wrapped in 1.65 turns [1]. Neighboring nucleosomes are separated by unwrapped linker DNA. Nucleosome density is lower, and nucleosome position is more conserved in the promoters than in the bodies of genes [2–5]. It is thought that nucleosome positioning in the gene promoter plays an important role in transcriptional regulation.

Although nucleosome positions can be partially simulated using a DNA-sequence-based approach [6], these simulations are limited due to variations between species. The nucleosome positioning mechanism varies between the 2 ascomycetous yeasts, Saccharomyces cerevisiae, and Schizosaccharomyces pombe [7]. Nucleosome positioning differs even among phylogenetically close ascomycetous yeast species [5].

Gene duplication is a driving force behind gene creation, and generating novel functions in newly created genes. Approximately one-half of cellular functions have been gained through gene duplication [8]. The duplicated genes encode similar amino acid sequences and often similar protein functions. It is uncertain, however, whether duplicated genes have similar nucleosome position profiles. In this study, I compared nucleosome positions in the promoter and body regions of duplicated gene pairs in the filamentous ascomycete Aspergillus fumigatus.

Previous analyses have found that nucleosome positions in A. fumigatus are conserved more in gene promoters than in gene bodies, even after treatment with the histone deacetylase inhibitor trichostatin A [4, 9]. In addition, nucleosome positions in S. cerevisiae are more conserved in gene promoters than in gene bodies between the control and the histone acetyltransferase gene ELP3 deletion mutant, and between the control and the histone deacetylase gene HOS2 deletion mutant [10]. The proteins Elp3 and Hos2 show the highest and the third highest evolutionary conservation, respectively, among the fungal histone modification proteins [11].

How well are nucleosome positions conserved in genes of the same origins? If there is a “nucleosome position code” that regulates nucleosome positioning, common nucleosome positions should remain in the promoters of orthologous genes across distinct species. In this study, I compared nucleosome positions in the promoters of duplicated and orthologous genes in A. fumigatus and S. cerevisiae.

2. Materials and Methods

2.1. Identification of Duplicated Gene Pairs in Aspergillus fumigates

Protein-coding gene pairs aligned over more than 80% of query length and more than 70% aminoacid sequence identity were selected by performing a BLAST search of 9630 A. fumigatus proteins at Fungal Genomes Central on NCBI (http://www.ncbi.nlm.nih.gov/projects/genome/guide/fungi/). Pairs in which the lengths differ by more than 25% were not used. Thus, we identified 63 duplicated A. fumigatus gene pairs (Tables 1 and 2).

Table 1: Duplicated gene pairs in Aspergillus fumigatus.

Gene pair
Chromosome
Gene body region
Gene direction
Function

AFUA1G00150
1
25442
27017
+
RING finger protein

AFUA6G09370
6
2245549
2247121
+
RING finger protein

AFUA1G00420
1
135528
137781
+
Carboxypeptidase S1, putative

AFUA8G04120
8
897824
900076
−
Carboxypeptidase S1, putative

AFUA1G00440
1
138359
140093
−
DUF895 domain membrane protein

AFUA8G04110
8
895512
897246
+
DUF895 domain membrane protein

AFUA1G00450
1
143117
144466
+
N-acetylglucosamine-6-phosphate deacetylase(NagA), putative

AFUA8G04100
8
891135
892484
−
N-acetylglucosamine-6-phosphate deacetylase(NagA), putative

AFUA1G00470
1
148615
150219
+
Betaine aldehyde dehydrogenase, putative

AFUA8G04080
8
885376
886980
−
Betaine aldehyde dehydrogenase (BadH), putative

AFUA1G00530
1
164101
164771
−
Thermoresistant gluconokinase family protein

AFUA4G12050
4
3163747
3164530
−
Thermoresistant gluconokinase

AFUA1G00550
1
177114
178593
+
Hypothetical protein

AFUA1G00910
1
328785
330274
+
Hypothetical protein

AFUA1G00580
1
184790
186873
+
Acid phosphatase (PhoG), putative

AFUA8G04050
8
870757
872487
−
Acid phosphatase (PhoG), putative

AFUA1G00650
1
215584
217006
+
Alpha-1,3-glucanase, putative

AFUA7G08510
7
1973398
1974759
+
Alpha-1,3-glucanase, putative

AFUA1G00920
1
331676
332955
−
Hypothetical protein

AFUA3G06425
3
1582748
1584037
−
Hypothetical protein

AFUA1G01050
1
385302
386244
−
Hypothetical protein

AFUA8G06160
8
1465695
1466634
+
Hypothetical protein

AFUA1G02550
1
744583
746335
−
Tubulin alpha-1 subunit

AFUA2G14990
2
3947008
3948834
−
Tubulin alpha-2 subunit

AFUA1G02730
1
788249
789373
−
Mitochondrial phosphate carrier protein (Ptp), putative

AFUA1G15140
1
4070230
4071449
−
Mitochondrial phosphate carrier protein (Mir1), putative

AFUA1G05760
1
1658382
1659697
−
Arsenite efflux transporter

AFUA5G15010
5
3882425
3883746
+
Arsenite permease (ArsB), putative

AFUA1G05760
1
1658382
1659697
−
Arsenite efflux transporter

AFUA1G16100
1
4378898
4380216
+
Arsenite permease (ArsB), putative

AFUA1G10910
1
2848155
2850137
−
Tubulin beta, putative

AFUA7G00250
7
70221
71948
+
Tubulin beta-2 subunit

AFUA1G11260
1
2971529
2971889
−
Conserved hypothetical protein

AFUA6G00270
6
79542
79886
−
Conserved hypothetical protein

AFUA1G11610
1
3060058
3060510
+
3-Dehydroquinate dehydratase, type II

AFUA3G14850
3
3929721
3930173
+
3-Dehydroquinate dehydratase, type II

AFUA1G11890
1
3129447
3131489
+
Serine palmitoyltransferase 2, putative

AFUA6G00300
6
85851
87692
−
Serine palmitoyltransferase 1, putative

AFUA1G12850
1
3398837
3400611
+
Nitrate transporter (nitrate permease)

AFUA1G17470
1
4782320
4783995
+
High-affinity nitrate transporter NrtB

AFUA1G15970
1
4338407
4339712
+
Aldo-keto reductase (AKR13), putative

AFUA8G01560
8
401581
402815
−
Aldo-keto reductase (YakC), putative

AFUA1G16030
1
4358866
4360256
−
Conserved hypothetical protein

AFUA5G14930
5
3863218
3864521
−
Conserved hypothetical protein

AFUA1G16040
1
4363493
4365310
+
Metalloreductase, putative

AFUA5G14940
5
3867797
3869542
+
Cell surface metalloreductase (FreA), putative

AFUA1G16050
1
4366573
4368232
+
Hypothetical protein

AFUA5G14950
5
3870635
3872465
+
Hypothetical protein

AFUA1G16070
1
4370346
4373694
+
Conserved hypothetical protein

AFUA5G14980
5
3874539
3877890
+
Conserved hypothetical protein

AFUA1G16080
1
4374579
4375298
−
Hypothetical protein

AFUA5G14990
5
3878797
3879579
−
Hypothetical protein

AFUA1G16090
1
4377842
4378249
−
Arsenate reductase (ArsC), putative

AFUA5G15000
5
3881386
3881835
−
Arsenate reductase (ArsC), putative

AFUA1G16100
1
4378898
4380216
+
Arsenite permease (ArsB), putative

AFUA5G15010
5
3882425
3883746
+
Arsenite permease (ArsB), putative

AFUA1G16110
1
4380474
4381455
−
Arsenic methyltransferase (Cyt19), putative

AFUA5G15020
5
3883929
3884993
−
Arsenic methyltransferase (Cyt19), putative

AFUA1G16120
1
4385650
4386671
−
Arsenic resistance protein (ArsH), putative

AFUA8G07150
8
1751693
1752688
+
ArsH protein

AFUA1G16120
1
4385650
4386671
−
Arsenic resistance protein (ArsH), putative

AFUA5G15030
5
3887287
3888230
−
Arsenic resistance protein (ArsH), putative

AFUA2G00800
2
178081
179459
−
PelA protein

AFUA5G10380
5
2658656
2659968
+
Pectin lyase, putative

AFUA2G00800
2
178081
179459
−
PelA protein

AFUA7G05030
7
1182104
1183794
−
Pectin lyase B

AFUA2G04010
2
1092973
1094679
−
Alpha, alpha-trehalose-phosphate synthase subunit, putative

AFUA6G12950
6
3268958
3270783
+
Alpha, alpha-trehalose-phosphate Synthase subunitTPS1, putative

AFUA2G11270
2
2897275
2904954
−
Alpha-1,3-glucan synthase, putative

AFUA3G00910
3
210186
217666
+
Alpha-1,3-glucan synthase, putative

AFUA3G00340
3
71186
72734
+
Glycosyl hydrolase, putative

AFUA4G02720
4
751306
752715
−
Glycosyl hydrolase, putative

AFUA3G00680
3
151397
153549
−
Copper amine oxidase

AFUA7G04180
7
943893
946136
+
Amine oxidase

AFUA3G01560
3
393032
394802
−
Aminoacid permease, putative

AFUA5G04260
5
1140953
1142714
+
Arginine transporter, putative

AFUA3G02420
3
597476
598286
+
ThiJ/PfpI family protein

AFUA4G01400
4
369123
369944
−
ThiJ/PfpI family protein

AFUA3G03080
3
824479
825425
+
Endo-1,3(4)-beta-glucanase, putative

AFUA6G14540
6
3702416
3703383
−
Endo-1,3(4)-beta-glucanase, putative

AFUA3G03980
3
1134609
1136404
+
Cytochrome P450 monooxygenase, putative

AFUA5G10050
5
2589301
2591081
−
Cytochrome P450 monooxygenase, putative

AFUA3G08160
3
2094223
2095759
−
Eukaryotic translation initiation Factor eIF4A, putative

AFUA5G02410
5
621886
623486
−
DEAD/DEAH box helicase, putative

AFUA3G14420
3
3831868
3834921
+
Chitin synthase G

AFUA5G00760
5
211013
213795
+
Chitin synthase C

AFUA4G00510
4
133477
135102
−
Hypothetical protein

AFUA7G08600
7
2009436
2011052
+
Hypothetical protein

AFUA4G03110
4
868474
870249
−
Monosaccharide transporter

AFUA5G10690
5
2737348
2739178
−
Monosaccharide transporter

AFUA4G03680
4
1031586
1032539
−
Oxidoreductase, short-chain dehydrogenase/reductase family

AFUA6G03520
6
764308
765294
−
Short-chain dehydrogenase/reductase family protein, putative

AFUA4G09440
4
2462920
2466158
−
Sodium P-type ATPase, putative

AFUA6G03690
6
810027
813362
−
Sodium transport ATPase, putative

AFUA4G14360
4
3774307
3776166
+
Capsular associated protein, putative

AFUA5G07560
5
1889791
1891689
−
Capsular associated protein, putative

AFUA5G00145
5
15749
16327
−
Hypothetical protein

AFUA6G11710
6
2915903
2916483
+
Conserved hypothetical protein

AFUA5G00145
5
15749
16327
−
Hypothetical protein

AFUA7G08440
7
1942319
1942804
+
Hypothetical protein

AFUA5G01030
5
266294
267439
−
Glyceraldehyde 3-phosphate dehydrogenase(Ccg-7), putative

AFUA5G01970
5
503797
505194
+
Glyceraldehyde 3-phosphate dehydrogenase GpdA

AFUA5G06240
5
1494455
1495619
−
Alcohol dehydrogenase, putative

AFUA7G01010
7
270494
271675
−
Alcohol dehydrogenase, putative

AFUA5G07980
5
2019069
2020841
+
Hypothetical protein

AFUA5G14920
5
3857350
3859167
+
Hypothetical protein

AFUA5G09130
5
2345689
2346728
−
Polysaccharide deacetylase family protein

AFUA6G05030
6
1195846
1196956
+
Polysaccharide deacetylase family protein

AFUA5G15030
5
3887287
3888230
−
Arsenic resistance protein (ArsH), putative

AFUA8G07150
8
1751693
1752688
+
ArsH protein

AFUA6G06750
6
1475239
1476209
+
14-3-3 family protein

AFUA2G03290
2
867203
868250
−
14-3-3 family protein ArtA, putative

AFUA6G07070
6
1587643
1589124
+
Cellobiohydrolase D

AFUA6G11610
6
2878078
2879676
−
1,4-beta-D-glucan-cellobiohydrolyase, putative

AFUA6G11430
6
2837140
2839051
+
Aldehyde dehydrogenase, putative

AFUA7G01000
7
267518
269163
−
Aldehyde dehydrogenase, putative

AFUA6G11710
6
2915903
2916483
+
Conserved hypothetical protein

AFUA7G08440
7
1942319
1942804
+
Hypothetical protein

AFUA6G13490
6
3431912
3433612
−
Glutamate decarboxylase

AFUA8G06020
8
1428812
1430515
+
Glutamate decarboxylase

AFUA7G00360
7
102030
103064
−
UDP-galactose 4-epimerase, putative

AFUA8G00860
8
203496
204338
+
UDP-galactose 4-epimerase, putative

AFUA7G07050
7
1725686
1726402
−
Hypothetical protein

AFUA7G08300
7
1870244
1870960
−
Hypothetical protein

AFUA7G07060
7
1728876
1732992
−
Hypothetical protein

AFUA7G08310
7
1873437
1877817
−
Hypothetical protein

Table 2: Spearman's rank correlation coefficients of nucleosome position profiles in the promoter and body regions of 63 duplicated gene pairs in Aspergillus fumigatus.

Gene pair
Gene promoter
Gene body

AFUA1G00150
AFUA6G09370
0.750176913
0.215204254

AFUA1G00420
AFUA8G04120
0.80370974
0.723149072

AFUA1G00440
AFUA8G04110
0.856048561
0.225149091

AFUA1G00450
AFUA8G04100
0.9213602
0.94633912

AFUA1G00470
AFUA8G04080
0.433118045
0.818800395

AFUA1G00530
AFUA4G12050
0.326735006
−0.199291887

AFUA1G00550
AFUA1G00910
0.676910334
0.678763937

AFUA1G00580
AFUA8G04050
0.305291793
0.312927993

AFUA1G00650
AFUA7G08510
0.448171525
0.085599209

AFUA1G00920
AFUA3G06425
0.719748778
−0.340001527

AFUA1G01050
AFUA8G06160
0.635149308
0.176679577

AFUA1G02550
AFUA2G14990
0.139079116
−0.036644732

AFUA1G02730
AFUA1G15140
0.452193259
0.067186644

AFUA1G05760
AFUA5G15010
0.395849711
0.117006666

AFUA1G05760
AFUA1G16100
0.127911436
−0.397363108

AFUA1G10910
AFUA7G00250
0.310718577
0.665906466

AFUA1G11260
AFUA6G00270
0.617303556
−0.02397179

AFUA1G11610
AFUA3G14850
0.636281069
0.869300724

AFUA1G11890
AFUA6G00300
0.254487564
0.429087849

AFUA1G12850
AFUA1G17470
0.644447287
0.008468365

AFUA1G15970
AFUA8G01560
0.373850536
−0.106800689

AFUA1G16030
AFUA5G14930
0.618349765
0.858488283

AFUA1G16040
AFUA5G14940
0.481054005
0.017330056

AFUA1G16050
AFUA5G14950
−0.345037268
−0.392132138

AFUA1G16070
AFUA5G14980
0.930922124
0.902581516

AFUA1G16080
AFUA5G14990
0.559980787
0.136819379

AFUA1G16090
AFUA5G15000
0.773867924
0.338119153

AFUA1G16100
AFUA5G15010
0.681170098
0.70434823

AFUA1G16110
AFUA5G15020
−0.261864905
0.632982505

AFUA1G16120
AFUA8G07150
0.356869915
0.074502754

AFUA1G16120
AFUA5G15030
−0.135442129
−0.239074416

AFUA2G00800
AFUA5G10380
0.352063916
0.460712971

AFUA2G00800
AFUA7G05030
−0.114184443
0.457081245

AFUA2G04010
AFUA6G12950
0.134790545
−0.14813806

AFUA2G11270
AFUA3G00910
−0.004207858
0.192024608

AFUA3G00340
AFUA4G02720
−0.050259987
0.055757479

AFUA3G00680
AFUA7G04180
0.399912713
−0.044615588

AFUA3G01560
AFUA5G04260
0.179395067
0.125177632

AFUA3G02420
AFUA4G01400
0.662712481
0.646400554

AFUA3G03080
AFUA6G14540
0.3401707
−0.021961056

AFUA3G03980
AFUA5G10050
0.486726534
0.318475376

AFUA3G08160
AFUA5G02410
0.309645464
−0.255654021

AFUA3G14420
AFUA5G00760
0.917685134
0.415111431

AFUA4G00510
AFUA7G08600
0.578582743
0.441363777

AFUA4G03110
AFUA5G10690
0.721540193
0.176996881

AFUA4G03680
AFUA6G03520
0.662657833
−0.320417166

AFUA4G09440
AFUA6G03690
0.204159184
0.000609208

AFUA4G14360
AFUA5G07560
0.038083073
0.515103795

AFUA5G00145
AFUA6G11710
0.809402393
−0.741045496

AFUA5G00145
AFUA7G08440
0.019652845
−0.575600966

AFUA5G01030
AFUA5G01970
0.576211178
0.132479521

AFUA5G06240
AFUA7G01010
0.163674862
−0.552899419

AFUA5G07980
AFUA5G14920
0.669562689
−0.265207346

AFUA5G09130
AFUA6G05030
0.092452938
0.729278817

AFUA5G15030
AFUA8G07150
0.337482368
−0.502391454

AFUA6G06750
AFUA2G03290
0.333402926
−0.538389013

AFUA6G07070
AFUA6G11610
−0.048961745
−0.239430043

AFUA6G11430
AFUA7G01000
0.0145492
0.476692417

AFUA6G11710
AFUA7G08440
0.243362623
0.823124582

AFUA6G13490
AFUA8G06020
0.768186533
0.174847009

AFUA7G00360
AFUA8G00860
−0.115050268
0.03815086

AFUA7G07050
AFUA7G08300
0.70756842
0.778653567

AFUA7G07060
AFUA7G08310
0.906852725
0.919839072

2.2. Identification of Orthologous Gene Pairs in Aspergillus fumigates and Saccharomyces cerevisiae

In a comparison of nucleosome positioning between A. fumigatus and S. cerevisiae, I focused on 466 genes (Table 3) that showed notably high conservation of nucleosome positioning in the promoters of the control and the ELP3 and HOS2 deletion mutants from the previous study [10].

Table 3: Genes of Saccharomyces cerevisiae with highly conserved nucleosome positions in the promoters of the control and histone modification gene deletion mutants.

Chromosome
Gene
Correlation coefficient between the control and the ELP3 deletion
Correlation coefficient between the control and the HOS2 deletion
Translational start site
Transcription direction

chr01
YAL064W-B
0.974719955
0.965814243
12047
+

chr01
YAL056W
0.989801003
0.982157328
39260
+

chr01
YAL047C
0.950243691
0.953129232
56858
−

chr01
YAR019C
0.970115162
0.960628643
175133
−

chr01
YAR033W
0.968807875
0.987221166
188101
+

chr02
YBL111C
0.995802065
0.99455065
5009
−

chr02
YBL108C-A
0.959497013
0.969966542
7733
−

chr02
YBL101C
0.958517125
0.991324096
28299
−

chr02
YBL087C
0.95719187
0.957273203
60735
−

chr02
YBL061C
0.984960212
0.992728731
107408
−

chr02
YBL060W
0.960330289
0.99357258
107934
+

chr02
YBL051C
0.97653734
0.989165943
124762
−

chr02
YBL032W
0.956874854
0.980366627
160187
+

chr02
YBL005W-B
0.950781322
0.952679326
221333
+

chr02
YBL005W-A
0.950781322
0.952679326
221333
+

chr02
YBR023C
0.960238499
0.992906362
287925
−

chr02
YBR029C
0.959231389
0.987222377
297742
−

chr02
YBR047W
0.964564522
0.963289004
331831
+

chr02
YBR060C
0.959229871
0.974718825
362512
−

chr02
YBR084W
0.962172866
0.981530879
411048
+

chr02
YBR090C
0.967658785
0.971792497
427052
−

chr02
YBR091C
0.965037862
0.985960321
427478
−

chr02
YBR131W
0.953323249
0.969685452
497157
+

chr02
YBR136W
0.963546822
0.974854426
505662
+

chr02
YBR173C
0.978518391
0.961438459
582167
−

chr02
YBR179C
0.988489146
0.991754907
589109
−

chr02
YBR180W
0.987132212
0.975974209
589736
+

chr02
YBR204C
0.970958946
0.978433534
633376
−

chr02
YBR243C
0.972253467
0.961252065
706788
−

chr02
YBR244W
0.974202306
0.992702483
707523
+

chr02
YBR249C
0.955742682
0.976101912
717989
−

chr02
YBR250W
0.954149188
0.976352348
719028
+

chr02
YBR251W
0.96273261
0.961120273
721385
+

chr02
YBR258C
0.966601899
0.955155711
730157
−

chr02
YBR260C
0.969346019
0.970918059
734634
−

chr02
YBR279W
0.956081387
0.964626558
761253
+

chr02
YBR290W
0.981586823
0.967935658
782587
+

chr03
YCL064C
0.957150698
0.95270514
16880
−

chr03
YCL058W-A
0.969895345
0.992394829
23584
+

chr03
YCL057C-A
0.990886192
0.987170576
24325
−

chr03
YCL057W
0.963062357
0.961804623
24768
+

chr03
YCL038C
0.978210537
0.957633548
56527
−

chr03
YCL035C
0.981360705
0.973568151
61173
−

chr03
YCL019W
0.953241664
0.978688459
85102
+

chr03
YCR026C
0.96886665
0.97932414
166335
−

chr03
YCR043C
0.951764864
0.966166673
206640
−

chr03
YCR053W
0.989728241
0.992623598
216693
+

chr03
YCR087C-A
0.975398919
0.993232435
264464
−

chr03
YCR090C
0.965637294
0.95018878
272860
−

chr03
YCR108C
0.985803086
0.993860549
316185
−

chr04
YDL248W
0.964701365
0.980217326
1802
+

chr04
YDL247W
0.989686199
0.997997741
5985
+

chr04
YDL233W
0.957672252
0.97857489
36798
+

chr04
YDL232W
0.979592686
0.970413477
38488
+

chr04
YDL225W
0.950053133
0.978441348
52446
+

chr04
YDL208W
0.987264893
0.987894794
87513
+

chr04
YDL189W
0.965815356
0.98561241
122217
+

chr04
YDL174C
0.956215571
0.953787348
147590
−

chr04
YDL147W
0.971755059
0.950911485
190925
+

chr04
YDL116W
0.965936123
0.976379579
251566
+

chr04
YDL110C
0.974238254
0.97295169
264964
−

chr04
YDL102W
0.957786538
0.980122821
276872
+

chr04
YDL085W
0.97887937
0.960150217
303211
+

chr04
YDL035C
0.975573212
0.977145228
392054
−

chr04
YDL025C
0.96134673
0.972526893
407203
−

chr04
YDR019C
0.95269772
0.953635877
485362
−

chr04
YDR028C
0.960937436
0.959981321
500876
−

chr04
YDR034C-C
0.967222636
0.9814374
519353
−

chr04
YDR034C-D
0.967222636
0.981437429
519353
−

chr04
YDR037W
0.951365292
0.956861294
525437
+

chr04
YDR054C
0.955928802
0.982048103
562325
−

chr04
YDR055W
0.950321012
0.952540035
563525
+

chr04
YDR062W
0.974021833
0.967688258
576471
+

chr04
YDR109C
0.954396163
0.952291074
675664
−

chr04
YDR110W
0.986081905
0.974555387
676099
+

chr04
YDR120C
0.960200845
0.969981962
693258
−

chr04
YDR162C
0.967301741
0.984347121
781097
−

chr04
YDR233C
0.967024058
0.967951444
930353
−

chr04
YDR234W
0.967415159
0.980945022
931125
+

chr04
YDR238C
0.97602642
0.973622232
940812
−

chr04
YDR261C-D
0.984848646
0.993722663
992345
−

chr04
YDR261C-C
0.984848646
0.9937227
992345
−

chr04
YDR262W
0.990989397
0.995915841
993130
+

chr04
YDR270W
0.951139826
0.96263534
1005671
+

chr04
YDR281C
0.984619329
0.959392909
1022317
−

chr04
YDR300C
0.975849644
0.971677938
1062787
−

chr04
YDR301W
0.952923341
0.977515222
1063348
+

chr04
YDR307W
0.951918886
0.970033626
1075861
+

chr04
YDR310C
0.951723931
0.969273153
1084312
−

chr04
YDR311W
0.953685357
0.980595738
1085062
+

chr04
YDR317W
0.98969221
0.991598049
1102181
+

chr04
YDR322W
0.954843272
0.97204312
1110586
+

chr04
YDR328C
0.957421993
0.983957835
1126013
−

chr04
YDR334W
0.953030288
0.963155512
1135927
+

chr04
YDR359C
0.977489172
0.969606029
1194877
−

chr04
YDR365C
0.985073544
0.998926611
1206375
−

chr04
YDR367W
0.990041805
0.994689201
1212840
+

chr04
YDR369C
0.957655919
0.96987305
1217572
−

chr04
YDR379W
0.962899057
0.974939821
1230159
+

chr04
YDR397C
0.966298918
0.975133337
1266890
−

chr04
YDR420W
0.971217177
0.991886941
1306259
+

chr04
YDR424C
0.966881808
0.989813233
1319833
−

chr04
YDR432W
0.955728738
0.982171718
1328775
+

chr04
YDR438W
0.971626925
0.98904082
1338266
+

chr04
YDR444W
0.973566433
0.976502447
1350282
+

chr04
YDR453C
0.952661492
0.954481014
1365654
−

chr04
YDR476C
0.969940159
0.964679279
1411119
−

chr04
YDR477W
0.954743343
0.979243738
1412365
+

chr04
YDR479C
0.977460825
0.994501786
1416866
−

chr04
YDR480W
0.967727074
0.986953403
1417391
+

chr04
YDR488C
0.983114512
0.979187155
1430781
−

chr04
YDR497C
0.955855412
0.958236577
1445459
−

chr04
YDR529C
0.966273576
0.971812076
1496540
−

chr05
YEL072W
0.968131913
0.977435534
13720
+

chr05
YEL043W
0.979079858
0.96227706
70478
+

chr05
YEL038W
0.981572221
0.988369151
80462
+

chr05
YEL021W
0.951315475
0.951565922
116167
+

chr05
YER004W
0.956348638
0.987671859
159579
+

chr05
YER026C
0.964952897
0.993875293
208473
−

chr05
YER076C
0.965398244
0.971982059
313494
−

chr05
YER083C
0.953185048
0.981521771
327027
−

chr05
YER094C
0.976027049
0.982595427
349342
−

chr05
YER095W
0.963423619
0.988752501
349976
+

chr05
YER107C
0.982024941
0.98488468
374541
−

chr05
YER109C
0.969371754
0.986034001
377610
−

chr05
YER173W
0.960496827
0.952930419
536295
+

chr05
YER188C-A
0.991489293
0.996538184
569902
−

chr05
YER189W
0.997057108
0.998333831
571150
+

chr06
YFL066C
0.970012372
0.993098415
2615
−

chr06
YFL065C
0.957034943
0.97004682
3338
−

chr06
YFL060C
0.987757312
0.995138274
10969
−

chr06
YFL059W
0.976205235
0.962195117
11363
+

chr06
YFL058W
0.9750941
0.994474768
12929
+

chr06
YFL028C
0.966244522
0.959308346
80211
−

chr06
YFL026W
0.957755207
0.952711873
82578
+

chr06
YFR009W
0.979200258
0.985708335
162482
+

chr06
YFR013W
0.972958971
0.986214291
169914
+

chr06
YFR037C
0.965415915
0.972070667
229173
−

chr07
YGL255W
0.961366208
0.972062316
20978
+

chr07
YGL248W
0.971369747
0.971756841
35653
+

chr07
YGL223C
0.956215218
0.984994924
80364
−

chr07
YGL215W
0.965861339
0.95181154
87980
+

chr07
YGL201C
0.954296336
0.979120204
120911
−

chr07
YGL180W
0.982084299
0.994334205
160071
+

chr07
YGL171W
0.969321982
0.974163208
182396
+

chr07
YGL163C
0.975825825
0.968348392
196409
−

chr07
YGL138C
0.971247145
0.983410766
249536
−

chr07
YGL120C
0.981452639
0.964320425
283943
−

chr07
YGL119W
0.986610225
0.981525372
284448
+

chr07
YGL108C
0.961840326
0.985939242
304074
−

chr07
YGL058W
0.977732494
0.975176081
393992
+

chr07
YGL056C
0.960426378
0.969119302
397624
−

chr07
YGL055W
0.964044825
0.969447792
398631
+

chr07
YGL048C
0.971402915
0.953304338
411289
−

chr07
YGL043W
0.964287661
0.976335397
417487
+

chr07
YGL028C
0.960077919
0.965512687
442914
−

chr07
YGL006W
0.950151816
0.968357705
485925
+

chr07
YGR001C
0.958621356
0.990717019
498038
−

chr07
YGR006W
0.980877592
0.97721459
506074
+

chr07
YGR027W-B
0.973585999
0.969942324
536061
+

chr07
YGR027W-A
0.973585999
0.969942324
536061
+

chr07
YGR054W
0.964434273
0.980689617
596697
+

chr07
YGR076C
0.981588154
0.958402031
637581
−

chr07
YGR082W
0.986433799
0.977608093
644048
+

chr07
YGR084C
0.952879595
0.959716787
648146
−

chr07
YGR109C
0.967037071
0.989224447
706505
−

chr07
YGR109W-B
0.964433838
0.990506548
707614
+

chr07
YGR109W-A
0.964433838
0.990506548
707614
+

chr07
YGR149W
0.957244122
0.960107682
789036
+

chr07
YGR161W-B
0.958455297
0.972873884
811743
+

chr07
YGR161W-A
0.958455297
0.9728739
811743
+

chr07
YGR161C-D
0.9711882
0.974318881
823020
−

chr07
YGR161C-C
0.9711882
0.9743189
823020
−

chr07
YGR162W
0.967152562
0.972476532
824064
+

chr07
YGR165W
0.959888658
0.951709091
829121
+

chr07
YGR166W
0.978481923
0.950610672
830520
+

chr07
YGR173W
0.978946749
0.974220242
843859
+

chr07
YGR178C
0.97338186
0.951056442
853220
−

chr07
YGR193C
0.977703185
0.9816188
885746
−

chr07
YGR198W
0.954889766
0.972754857
894698
+

chr07
YGR239C
0.968888325
0.989258725
970058
−

chr07
YGR240C
0.966313371
0.971843468
973739
−

chr07
YGR255C
0.966583058
0.991666026
1003967
−

chr07
YGR267C
0.960278778
0.969707488
1025741
−

chr07
YGR280C
0.961084505
0.952670993
1051732
−

chr07
YGR295C
0.967286944
0.964457386
1082736
−

chr07
YGR296W
0.971130914
0.991185295
1084871
+

chr08
YHL044W
0.958725508
0.965538017
13563
+

chr08
YHL029C
0.988947037
0.966760586
47966
−

chr08
YHL028W
0.983034685
0.977043411
48761
+

chr08
YHL024W
0.961645582
0.966633627
56647
+

chr08
YHL020C
0.978013871
0.986901259
67453
−

chr08
YHL016C
0.976082816
0.988408432
74241
−

chr08
YHL007C
0.973847748
0.981293306
97933
−

chr08
YHL004W
0.97418766
0.993677693
99215
+

chr08
YHL001W
0.959021584
0.965334128
104272
+

chr08
YHR001W-A
0.991644256
0.988918444
107821
+

chr08
YHR056C
0.972836967
0.982728846
217836
−

chr08
YHR081W
0.961720079
0.960688905
267540
+

chr08
YHR091C
0.955695121
0.987437891
286772
−

chr08
YHR101C
0.984820398
0.996893941
315971
−

chr08
YHR102W
0.96127201
0.995534701
316575
+

chr08
YHR107C
0.950250496
0.982165489
328039
−

chr08
YHR118C
0.973725305
0.961118169
345631
−

chr08
YHR127W
0.95014104
0.981438554
360916
+

chr08
YHR136C
0.953476026
0.965665058
375103
−

chr08
YHR148W
0.978585198
0.950179497
393537
+

chr08
YHR153C
0.959414518
0.982780385
402685
−

chr08
YHR165C
0.958747068
0.984253541
436950
−

chr08
YHR214C-D
0.987951207
0.966688891
550941
−

chr08
YHR215W
0.987951207
0.966688891
552099
+

chr08
YHR216W
0.972948554
0.975124764
554396
+

chr09
YIL158W
0.961579117
0.957386446
46201
+

chr09
YIL154C
0.954401073
0.971892535
55021
−

chr09
YIL137C
0.976010283
0.976810775
92788
−

chr09
YIL135C
0.976089791
0.979613921
96375
−

chr09
YIL134W
0.974541094
0.979148771
97395
+

chr09
YIL129C
0.958227819
0.99048832
113237
−

chr09
YIL125W
0.963070211
0.960333013
122689
+

chr09
YIL063C
0.970956253
0.957414461
243741
−

chr09
YIL061C
0.95394965
0.989156182
245556
−

chr09
YIL046W
0.967209958
0.952996831
268650
+

chr09
YIL033C
0.989017477
0.989306501
291668
−

chr09
YIL031W
0.985799922
0.98683422
292632
+

chr09
YIL030C
0.957449018
0.97109633
300008
−

chr09
YIR022W
0.960636707
0.971998311
398730
+

chr09
YIR024C
0.961569219
0.970038905
403488
−

chr09
YIR038C
0.973108358
0.975735046
424510
−

chr10
YJL221C
0.992889333
0.995409763
18536
−

chr10
YJL219W
0.992889333
0.995409763
19497
+

chr10
YJL197W
0.963017116
0.967339021
63804
+

chr10
YJL181W
0.971567753
0.971225117
85658
+

chr10
YJL176C
0.979890865
0.967535459
94528
−

chr10
YJL174W
0.983474082
0.9822043
95090
+

chr10
YJL173C
0.986867668
0.989398406
96527
−

chr10
YJL151C
0.952976229
0.987631587
136770
−

chr10
YJL149W
0.975756648
0.990848833
137376
+

chr10
YJL118W
0.953268112
0.959468203
191638
+

chr10
YJL113W
0.982940363
0.963188993
197913
+

chr10
YJL114W
0.982940363
0.963188993
197913
+

chr10
YJL093C
0.967675882
0.964352732
256807
−

chr10
YJL092W
0.963240719
0.958166876
257418
+

chr10
YJL066C
0.953982678
0.974252054
314867
−

chr10
YJL050W
0.950677364
0.95235067
342517
+

chr10
YJL048C
0.96132641
0.958967756
348632
−

chr10
YJL039C
0.950918953
0.970557445
373794
−

chr10
YJL034W
0.963347804
0.980266739
381322
+

chr10
YJR010W
0.971667854
0.97428271
456232
+

chr10
YJR021C
0.956762721
0.994264722
469572
−

chr10
YJR029W
0.958070547
0.974229894
478337
+

chr10
YJR028W
0.958070547
0.9742299
478337
+

chr10
YJR041C
0.976618081
0.981063923
513756
−

chr10
YJR048W
0.960606245
0.975055837
526328
+

chr10
YJR049C
0.954983464
0.986149168
528469
−

chr10
YJR055W
0.976932113
0.992763445
538765
+

chr10
YJR065C
0.975569729
0.987649101
559151
−

chr10
YJR095W
0.97047495
0.971814385
609769
+

chr10
YJR113C
0.969228269
0.954716018
638969
−

chr10
YJR115W
0.952485858
0.960980837
639936
+

chr10
YJR141W
0.957349189
0.956946497
695900
+

chr10
YJR160C
0.978268521
0.997490962
739810
−

chr10
YJR161C
0.965251269
0.976575544
743993
−

chr11
YKL191W
0.950933251
0.978993764
81040
+

chr11
YKL179C
0.975707433
0.967918905
112508
−

chr11
YKL167C
0.956085616
0.955561088
134139
−

chr11
YKL165C
0.960609423
0.966621061
140696
−

chr11
YKL157W
0.95635277
0.9813363
154996
+

chr11
YKL127W
0.955985661
0.982208081
203185
+

chr11
YKL125W
0.976449752
0.960074911
207891
+

chr11
YKL113C
0.971544612
0.954413703
225519
−

chr11
YKL065C
0.96005541
0.969818928
316701
−

chr11
YKL064W
0.974644257
0.972632809
317408
+

chr11
YKL059C
0.957153957
0.961241915
329087
−

chr11
YKL020C
0.955860253
0.977812511
401723
−

chr11
YKL013C
0.972958978
0.953444609
417666
−

chr11
YKR007W
0.981387104
0.972277081
451077
+

chr11
YKR024C
0.971944038
0.981215773
487015
−

chr11
YKR031C
0.952123552
0.969614994
506037
−

chr11
YKR036C
0.959340192
0.988104612
510275
−

chr11
YKR041W
0.982786597
0.957524998
517840
+

chr11
YKR052C
0.954392373
0.96688713
533106
−

chr11
YKR082W
0.962931616
0.991018501
592467
+

chr11
YKR084C
0.953228662
0.976903834
598532
−

chr11
YKR086W
0.952006608
0.976533657
599499
+

chr12
YLL050C
0.976179673
0.990695339
40413
−

chr12
YLL002W
0.972688874
0.981122544
146290
+

chr12
YLR001C
0.966206724
0.98012374
153976
−

chr12
YLR012C
0.956516633
0.962463803
170280
−

chr12
YLR013W
0.978873849
0.985557204
171338
+

chr12
YLR024C
0.953442868
0.956160837
193282
−

chr12
YLR025W
0.971468039
0.96202948
194453
+

chr12
YLR029C
0.961637928
0.991619508
202591
−

chr12
YLR059C
0.963450626
0.974770886
260548
−

chr12
YLR085C
0.9560163
0.984640913
301990
−

chr12
YLR087C
0.953704478
0.990085627
315732
−

chr12
YLR096W
0.977966477
0.979318401
332591
+

chr12
YLR104W
0.966174553
0.97921157
346586
+

chr12
YLR133W
0.961307333
0.951823465
408446
+

chr12
YLR135W
0.977560494
0.977991425
413282
+

chr12
YLR137W
0.967174193
0.983596278
417007
+

chr12
YLR162W-A
0.968123219
0.962766706
490407
+

chr12
YLR208W
0.96802684
0.969296393
559553
+

chr12
YLR223C
0.966783974
0.974989936
585492
−

chr12
YLR224W
0.974582795
0.978003757
586466
+

chr12
YLR286C
0.972231318
0.978358686
710138
−

chr12
YLR299W
0.962625418
0.970226227
726071
+

chr12
YLR307W
0.962710223
0.990591743
745622
+

chr12
YLR323C
0.953205594
0.975247431
778952
−

chr12
YLR326W
0.979769576
0.991583861
782174
+

chr12
YLR355C
0.967858474
0.973834311
839252
−

chr12
YLR356W
0.968277882
0.974767083
840320
+

chr12
YLR378C
0.974122358
0.977246394
877177
−

chr12
YLR380W
0.973258508
0.97821865
878282
+

chr12
YLR410W-A
0.951545011
0.9529714
941481
+

chr12
YLR410W-B
0.951545011
0.952971407
941481
+

chr12
YLR426W
0.9668981
0.990317101
987059
+

chr12
YLR427W
0.968631588
0.972538491
988425
+

chr12
YLR429W
0.950464544
0.951528134
990774
+

chr12
YLR443W
0.964525656
0.991440098
1022622
+

chr13
YML121W
0.974659011
0.985969584
26930
+

chr13
YML115C
0.97337994
0.996063492
41794
−

chr13
YML080W
0.989302036
0.986381735
108806
+

chr13
YML078W
0.975873108
0.974136336
111002
+

chr13
YML045W
0.993016416
0.993250991
184461
+

chr13
YML045W-A
0.993016416
0.993251
184461
+

chr13
YML041C
0.969801821
0.979224272
195755
−

chr13
YML020W
0.975260683
0.95439232
231149
+

chr13
YML004C
0.966616377
0.98388072
262685
−

chr13
YML003W
0.968338912
0.981828638
263483
+

chr13
YMR010W
0.985774326
0.979191015
285099
+

chr13
YMR011W
0.963732981
0.981283867
288078
+

chr13
YMR027W
0.961041993
0.957831173
325876
+

chr13
YMR036C
0.969260192
0.963784402
343519
−

chr13
YMR060C
0.990018805
0.990517987
392514
−

chr13
YMR066W
0.98321165
0.95995151
401540
+

chr13
YMR078C
0.969392941
0.976546196
424727
−

chr13
YMR081C
0.981254312
0.956294421
431094
−

chr13
YMR110C
0.961424621
0.983151943
491991
−

chr13
YMR116C
0.977129849
0.989254306
500687
−

chr13
YMR137C
0.971971845
0.978526214
544962
−

chr13
YMR138W
0.978634859
0.963362392
545154
+

chr13
YMR152W
0.958913422
0.961601086
563095
+

chr13
YMR197C
0.960464224
0.981756931
659197
−

chr13
YMR210W
0.974579381
0.983178959
687515
+

chr13
YMR214W
0.977906077
0.988639434
695349
+

chr13
YMR219W
0.964555974
0.962486321
707132
+

chr13
YMR224C
0.975063127
0.950620617
720652
−

chr13
YMR229C
0.960514554
0.957025636
731122
−

chr13
YMR241W
0.956225901
0.967912184
751960
+

chr13
YMR319C
0.950340769
0.968043162
914536
−

chr14
YNL339C
0.975221324
0.997373072
6098
−

chr14
YNL334C
0.968865734
0.991228175
12876
−

chr14
YNL322C
0.954706246
0.977799203
34234
−

chr14
YNL311C
0.986814003
0.993782307
51687
−

chr14
YNL310C
0.956852702
0.980516471
52430
−

chr14
YNL309W
0.988062215
0.993825499
52661
+

chr14
YNL301C
0.968107997
0.966680876
64562
−

chr14
YNL295W
0.952849161
0.964836983
76946
+

chr14
YNL261W
0.950477134
0.976226949
155101
+

chr14
YNL260C
0.968893453
0.965562883
157456
−

chr14
YNL255C
0.959418743
0.961868386
167791
−

chr14
YNL248C
0.959305496
0.962132738
182609
−

chr14
YNL241C
0.952591706
0.968306617
197944
−

chr14
YNL234W
0.975005906
0.964281927
210234
+

chr14
YNL224C
0.973438019
0.985601741
227100
−

chr14
YNL212W
0.967303893
0.964441355
247462
+

chr14
YNL166C
0.973079673
0.979903307
323567
−

chr14
YNL156C
0.961076874
0.96913283
341970
−

chr14
YNL112W
0.953769466
0.987266001
413641
+

chr14
YNL099C
0.959678116
0.95727388
439285
−

chr14
YNL097C
0.978605808
0.986440434
442360
−

chr14
YNL082W
0.955790378
0.980457797
473392
+

chr14
YNL055C
0.982685169
0.981068004
518846
−

chr14
YNL042W-B
0.956836355
0.979900708
547114
+

chr14
YNL029C
0.976101029
0.988675718
578774
−

chr14
YNL027W
0.96462873
0.978413199
579581
+

chr14
YNR012W
0.958400399
0.977490746
647434
+

chr14
YNR015W
0.967843094
0.979265652
653389
+

chr14
YNR023W
0.975180387
0.972628935
670420
+

chr14
YNR026C
0.966267575
0.984095961
674691
−

chr14
YNR036C
0.955455936
0.956914254
694824
−

chr14
YNR039C
0.97056523
0.9708253
699433
−

chr14
YNR075W
0.950188074
0.953766447
779916
+

chr14
YNR075C-A
0.986389631
0.991000914
781603
−

chr15
YOL166W-A
0.969218719
0.964760148
585
+

chr15
YOL157C
0.977029388
0.98945557
24293
−

chr15
YOL156W
0.979765672
0.992685071
25272
+

chr15
YOL148C
0.957761501
0.971157209
47573
−

chr15
YOL104C
0.976917372
0.981386975
117454
−

chr15
YOL100W
0.961328138
0.959394148
129237
+

chr15
YOL089C
0.971692903
0.984860678
153490
−

chr15
YOL086C
0.976082094
0.966862518
160594
−

chr15
YOL077C
0.956963602
0.983941333
186723
−

chr15
YOL068C
0.959180595
0.953847182
201879
−

chr15
YOL062C
0.954102242
0.967526899
211995
−

chr15
YOL058W
0.969401099
0.978364009
219210
+

chr15
YOL045W
0.966108727
0.955785397
243496
+

chr15
YOL031C
0.971563515
0.959211572
267530
−

chr15
YOL026C
0.954115513
0.976281121
274354
−

chr15
YOL023W
0.960879668
0.960550998
278057
+

chr15
YOL006C
0.971429281
0.978082289
315388
−

chr15
YOR043W
0.970409112
0.977199399
410870
+

chr15
YOR048C
0.95240535
0.972598244
421651
−

chr15
YOR056C
0.95552512
0.980531823
431628
−

chr15
YOR058C
0.977288174
0.978577416
436347
−

chr15
YOR071C
0.980341941
0.989920087
461278
−

chr15
YOR075W
0.983591979
0.981471486
468214
+

chr15
YOR089C
0.978934603
0.984066065
490830
−

chr15
YOR104W
0.965107091
0.973591736
517643
+

chr15
YOR124C
0.97179062
0.983946384
558643
−

chr15
YOR129C
0.979558976
0.983142651
569559
−

chr15
YOR132W
0.955282168
0.965555781
573176
+

chr15
YOR148C
0.987044445
0.98569999
609198
−

chr15
YOR192C-C
0.980704362
0.966062169
704225
−

chr15
YOR193W
0.973179583
0.992657727
710447
+

chr15
YOR204W
0.985619071
0.960639074
722912
+

chr15
YOR216C
0.971045967
0.970515948
748980
−

chr15
YOR247W
0.959336754
0.957210052
797677
+

chr15
YOR294W
0.972999786
0.97236413
868339
+

chr15
YOR336W
0.973501735
0.969442343
949770
+

chr15
YOR365C
0.981766719
0.98630012
1025570
−

chr15
YOR372C
0.955936893
0.971693401
1036469
−

chr15
YOR389W
0.964833697
0.976852438
1074211
+

chr15
YOR390W
0.98673199
0.997343789
1076782
+

chr15
YOR391C
0.952090431
0.990889663
1079256
−

chr15
YOR393W
0.952090431
0.990889663
1080274
+

chr16
YPL283C
0.990485958
0.9953985
6007
−

chr16
YPL281C
0.961921468
0.977623026
10870
−

chr16
YPL280W
0.961921468
0.977623026
11887
+

chr16
YPL278C
0.965633274
0.959753752
15355
−

chr16
YPL257W-B
0.976897418
0.976806903
56748
+

chr16
YPL257W-A
0.976897418
0.976807
56748
+

chr16
YPL255W
0.96664841
0.970266728
67725
+

chr16
YPL254W
0.95123182
0.962107221
69485
+

chr16
YPL206C
0.975807996
0.972912432
163596
−

chr16
YPL196W
0.978338347
0.984467392
175042
+

chr16
YPL180W
0.976152618
0.987674239
205247
+

chr16
YPL171C
0.96524809
0.961521166
227370
−

chr16
YPL158C
0.980225654
0.985491741
254309
−

chr16
YPL157W
0.98638216
0.988124386
254813
+

chr16
YPL146C
0.98509812
0.956540524
277528
−

chr16
YPL139C
0.981115598
0.987215069
291050
−

chr16
YPL126W
0.988937478
0.982334739
310209
+

chr16
YPL082C
0.980458525
0.992300343
404080
−

chr16
YPL078C
0.957476311
0.95576197
408741
−

chr16
YPL038W
0.953416137
0.966495031
480532
+

chr16
YPL030W
0.973101156
0.975002429
493541
+

chr16
YPL007C
0.954338314
0.983931954
543845
−

chr16
YPR010C
0.983770387
0.983449754
581193
−

chr16
YPR017C
0.986325514
0.989002388
593914
−

chr16
YPR018W
0.981145288
0.96510122
594473
+

chr16
YPR020W
0.950323294
0.983815562
599867
+

chr16
YPR048W
0.980910651
0.976100682
659179
+

chr16
YPR060C
0.960902075
0.969265445
675628
−

chr16
YPR062W
0.96911875
0.967204709
677162
+

chr16
YPR088C
0.957617837
0.976321629
713026
−

chr16
YPR141C
0.978516693
0.973377917
817919
−

chr16
YPR145C-A
0.961127516
0.965220022
824922
−

chr16
YPR156C
0.966866802
0.956230015
839773
−

chr16
YPR158C-D
0.981640164
0.971311933
856253
−

chr16
YPR158C-C
0.981640164
0.971311933
856253
−

chr16
YPR161C
0.969622155
0.984283791
866418
−

chr16
YPR165W
0.959239007
0.967322323
875364
+

chr16
YPR176C
0.986542093
0.977514778
892074
−

chr16
YPR187W
0.964480751
0.98804279
911253
+

chr16
YPR203W
0.968955474
0.985644074
943876
+

A total of 3339 ortholog clusters were identified (See table 1 in Supplementary Material available at doi: 10.1100/2012/298174) between A. fumigatus and S. cerevisiae by ortholog cluster analysis in the Microbial Genome Database for Comparative Analysis (MBGD, http://mbgd.nibb.ac.jp/) [12]. Of these orthologous gene pairs, 347 (Table 4) are yeast genes that showed a high level of nucleosome positioning conservation in the control and deletion mutants. I focused on these 347 orthologous pairs to compare nucleosome positioning between species. The same number of pairs of A. fumigatus and S. cerevisiae genes chosen at random were used as a control.

Table 4: Spearman's rank correlation coefficients between nucleosome position profiles in the promoters of 347 orthologous gene pairs between Aspergillus fumigatus and Saccharomyces cerevisiae.

S. cerevisiae gene
A. fumigatus gene
Correlation coefficient

YCR053W
AFUA_3G08980
0.851750303

YOL006C
AFUA_1G03500
0.814728478

YLR208W
AFUA_4G06090
0.810778356

YJR160C
AFUA_8G07240
0.807607644

YKL064W
AFUA_2G08070
0.771984405

YDL208W
AFUA_1G13570
0.763687527

YDL247W
AFUA_8G07240
0.751799318

YJL034W
AFUA_2G04620
0.751475734

YJL174W
AFUA_2G07590
0.731359519

YGL006W
AFUA_1G10880
0.706118907

YLR307W
AFUA_6G10430
0.701428537

YOR056C
AFUA_5G04000
0.693624039

YJR049C
AFUA_5G12870
0.6873278

YOR132W
AFUA_5G07150
0.684358232

YDR028C
AFUA_8G02720
0.681519128

YKL059C
AFUA_2G06220
0.677236775

YDR019C
AFUA_1G10780
0.673590566

YDR262W
AFUA_8G05360
0.668577442

YJR160C
AFUA_3G01700
0.655149877

YBL087C
AFUA_2G03380
0.654275917

YDR120C
AFUA_3G04200
0.653965099

YMR110C
AFUA_4G13500
0.649573592

YDR479C
AFUA_2G01510
0.649340576

YLR307W
AFUA_4G09940
0.641152119

YLL050C
AFUA_5G10570
0.636927762

YMR011W
AFUA_2G11520
0.631877767

YGR149W
AFUA_3G08240
0.627253467

YKL125W
AFUA_1G02590
0.626251676

YDL247W
AFUA_3G01700
0.621782331

YHR165C
AFUA_2G03030
0.616638486

YLR355C
AFUA_3G14490
0.615946987

YLR307W
AFUA_3G07210
0.615345397

YNL156C
AFUA_4G07680
0.605449075

YOL157C
AFUA_8G07070
0.600254438

YPL196W
AFUA_3G08740
0.596649007

YOL156W
AFUA_2G11520
0.589475104

YGL055W
AFUA_7G05920
0.583471232

YER094C
AFUA_4G07420
0.580111415

YER026C
AFUA_4G13680
0.579632053

YKR031C
AFUA_3G05630
0.578947614

YJR041C
AFUA_1G13200
0.577042969

YCL057C-A
AFUA_1G13195
0.56703028

YKL167C
AFUA_6G12620
0.566497151

YDR334W
AFUA_7G02370
0.556810391

YDL085W
AFUA_1G11960
0.555058025

YIR038C
AFUA_8G02500
0.553657653

YGL056C
AFUA_1G06660
0.550891198

YLR133W
AFUA_1G15930
0.547961885

YLR137W
AFUA_2G09930
0.542448721

YER095W
AFUA_1G10410
0.540102076

YCR090C
AFUA_2G15510
0.540015424

YIR022W
AFUA_3G12840
0.539096148

YJR048W
AFUA_2G13110
0.537701308

YDL247W
AFUA_8G01340
0.536753536

YGL119W
AFUA_6G04380
0.528264148

YDR054C
AFUA_5G09200
0.520282879

YNR036C
AFUA_5G10750
0.51817226

YJL050W
AFUA_4G07160
0.517374235

YKR036C
AFUA_5G13140
0.515007541

YML041C
AFUA_2G05030
0.514819597

YML080W
AFUA_1G16550
0.512494533

YJL093C
AFUA_1G14250
0.5107227

YDR238C
AFUA_1G10970
0.509749906

YJL197W
AFUA_2G14130
0.501902821

YER173W
AFUA_8G02820
0.501581347

YJR160C
AFUA_8G01340
0.499250408

YOL058W
AFUA_2G04310
0.497155736

YGR006W
AFUA_1G16990
0.496383573

YPR161C
AFUA_5G05510
0.495551014

YBR136W
AFUA_4G04760
0.49434371

YJR049C
AFUA_2G01350
0.493221085

YPR060C
AFUA_5G13130
0.490832735

YDR055W
AFUA_4G06820
0.482973721

YLR104W
AFUA_5G04040
0.47610876

YIL129C
AFUA_6G11010
0.473123981

YDR300C
AFUA_2G07570
0.469287567

YOL156W
AFUA_7G00950
0.46726022

YGL201C
AFUA_5G10890
0.462753539

YKR086W
AFUA_1G03820
0.461061937

YPL157W
AFUA_6G08610
0.460257721

YIL046W
AFUA_2G14110
0.45798838

YGL048C
AFUA_4G04660
0.457664607

YHR216W
AFUA_2G03610
0.456902272

YDR424C
AFUA_1G04850
0.455530713

YPR141C
AFUA_2G14280
0.452133975

YLR427W
AFUA_1G07150
0.444534443

YHL004W
AFUA_1G06570
0.439699159

YLL002W
AFUA_5G09540
0.431520497

YKR052C
AFUA_6G12550
0.429429023

YNL260C
AFUA_1G09000
0.425937756

YNL112W
AFUA_2G10750
0.423331447

YFL026W
AFUA_3G14330
0.422540136

YCL038C
AFUA_2G15370
0.420548714

YPR156C
AFUA_4G01140
0.419838437

YHL024W
AFUA_3G06230
0.417835282

YBR173C
AFUA_5G10740
0.414366599

YGR178C
AFUA_1G09630
0.410618083

YMR036C
AFUA_6G08200
0.408252022

YDL147W
AFUA_3G06610
0.40670988

YJR095W
AFUA_2G16930
0.405617695

YPL171C
AFUA_2G17960
0.40043227

YBL061C
AFUA_8G05620
0.398124519

YHL001W
AFUA_6G03830
0.397471165

YNL255C
AFUA_1G07630
0.390527675

YGL006W
AFUA_3G10690
0.389206341

YIL125W
AFUA_4G11650
0.387564721

YMR011W
AFUA_5G01160
0.381368332

YMR010W
AFUA_5G03510
0.378223656

YMR319C
AFUA_4G14640
0.376638524

YDL110C
AFUA_1G09160
0.376540694

YOL086C
AFUA_5G06240
0.376281416

YGR076C
AFUA_4G09000
0.373900773

YOR204W
AFUA_4G07660
0.368301524

YMR229C
AFUA_2G16040
0.367246087

YLR025W
AFUA_1G06420
0.363738278

YPL281C
AFUA_6G06770
0.363265962

YOR294W
AFUA_7G04430
0.363077313

YLR299W
AFUA_7G04760
0.36169498

YCL038C
AFUA_2G06170
0.359699115

YKL113C
AFUA_3G06060
0.351986208

YHL020C
AFUA_5G09420
0.350312962

YMR224C
AFUA_6G11410
0.348946198

YDR444W
AFUA_3G04240
0.345942811

YER107C
AFUA_1G09020
0.34238252

YDR162C
AFUA_2G03680
0.342381673

YNL212W
AFUA_3G08750
0.341561675

YNL097C
AFUA_3G11940
0.339603963

YKL191W
AFUA_6G07100
0.337319743

YPL030W
AFUA_6G02570
0.336821966

YNL224C
AFUA_3G05330
0.336636223

YKR024C
AFUA_5G11050
0.328747023

YPR020W
AFUA_1G16280
0.323479927

YPL171C
AFUA_2G04060
0.322952534

YOR393W
AFUA_6G06770
0.321210691

YPR088C
AFUA_5G03880
0.31284654

YGL058W
AFUA_6G14210
0.312000165

YFL059W
AFUA_5G08090
0.309971957

YBR243C
AFUA_2G11240
0.307271969

YJL048C
AFUA_3G06360
0.306215007

YNL055C
AFUA_4G06910
0.305279025

YOR058C
AFUA_2G16260
0.305221634

YGR240C
AFUA_4G00960
0.304340045

YBR279W
AFUA_2G11000
0.303224

YPL078C
AFUA_8G05440
0.300712891

YLR059C
AFUA_3G11820
0.296403753

YLR380W
AFUA_6G12690
0.295562758

YDL174C
AFUA_1G17520
0.29517154

YCL057W
AFUA_7G05930
0.293762978

YDR234W
AFUA_5G08890
0.293096856

YDR438W
AFUA_5G12140
0.287954196

YGL028C
AFUA_8G05610
0.287899385

YML004C
AFUA_6G07940
0.285261452

YOL045W
AFUA_2G02850
0.284622252

YLR429W
AFUA_2G14270
0.283845667

YDR397C
AFUA_3G02340
0.283499213

YBR260C
AFUA_3G06280
0.282196097

YCR087C-A
AFUA_7G04700
0.281322207

YMR011W
AFUA_7G00950
0.280854319

YOL148C
AFUA_1G16580
0.274850272

YDR379W
AFUA_1G12680
0.273041289

YJL151C
AFUA_5G10590
0.272979399

YML020W
AFUA_5G12090
0.266526854

YGR082W
AFUA_6G11380
0.265129767

YJR113C
AFUA_1G04280
0.262789584

YIL031W
AFUA_5G03200
0.256820972

YDR432W
AFUA_3G10100
0.255963453

YDR359C
AFUA_4G07560
0.255317292

YDR233C
AFUA_6G13670
0.253861938

YGR255C
AFUA_4G12930
0.252312468

YFR009W
AFUA_4G06070
0.245534257

YPL280W
AFUA_3G08490
0.243781447

YOR075W
AFUA_2G09670
0.239487119

YJL219W
AFUA_7G00950
0.239124986

YCR026C
AFUA_2G14770
0.234276623

YOR391C
AFUA_3G08490
0.233098887

YGL180W
AFUA_4G09050
0.231299038

YLR323C
AFUA_5G07720
0.231114462

YGL006W
AFUA_7G01030
0.222088168

YBR179C
AFUA_5G13392
0.219453048

YKR082W
AFUA_4G05840
0.214144582

YLR087C
AFUA_2G13520
0.209434557

YCL064C
AFUA_4G07810
0.204494803

YOL156W
AFUA_5G01160
0.203744073

YBR249C
AFUA_7G04070
0.202306902

YJL093C
AFUA_3G07540
0.201465401

YOL077C
AFUA_1G02210
0.196710807

YLR426W
AFUA_1G06280
0.196041865

YMR060C
AFUA_2G03840
0.194299595

YOR048C
AFUA_1G13730
0.193994391

YDL174C
AFUA_7G02560
0.193117882

YJL221C
AFUA_8G07070
0.187015236

YGR054W
AFUA_3G05970
0.181434929

YPR176C
AFUA_7G04460
0.180215936

YML003W
AFUA_1G09870
0.173517378

YKR084C
AFUA_2G04630
0.171646807

YDR270W
AFUA_4G12620
0.171601357

YOR336W
AFUA_2G02360
0.164107564

YFL058W
AFUA_5G02470
0.160695353

YNL301C
AFUA_2G07380
0.151927636

YJL221C
AFUA_7G06380
0.150927464

YGR280C
AFUA_7G03690
0.150422383

YOL089C
AFUA_6G01960
0.149731857

YGR193C
AFUA_3G08270
0.14875632

YDR328C
AFUA_5G06060
0.143711765

YPL254W
AFUA_2G06060
0.143220591

YPL206C
AFUA_2G00990
0.138505935

YEL021W
AFUA_2G08360
0.13720587

YOL068C
AFUA_4G12120
0.134069861

YJR160C
AFUA_7G06390
0.131179873

YNL310C
AFUA_6G08230
0.130305791

YIL061C
AFUA_5G13480
0.126828721

YGL163C
AFUA_6G12910
0.12597657

YGR173W
AFUA_5G06770
0.123606414

YJL092W
AFUA_2G03910
0.122708164

YJR065C
AFUA_5G11560
0.121854722

YBR023C
AFUA_8G05630
0.120791924

YBR084W
AFUA_3G08650
0.118154138

YMR197C
AFUA_4G10710
0.114428905

YMR241W
AFUA_5G04220
0.114113659

YNL097C
AFUA_7G01870
0.109316946

YGL171W
AFUA_1G16290
0.103112508

YOR365C
AFUA_4G13340
0.094260129

YHR215W
AFUA_6G11330
0.092128581

YKL013C
AFUA_6G02370
0.088958318

YOR043W
AFUA_4G06130
0.087990985

YPR062W
AFUA_1G05050
0.087018417

YDR497C
AFUA_2G07910
0.078863767

YDR477W
AFUA_2G01700
0.074801159

YLR378C
AFUA_5G08130
0.074624328

YBR060C
AFUA_5G08110
0.073589072

YGL120C
AFUA_5G11620
0.069009268

YIL063C
AFUA_2G10810
0.06328373

YOL157C
AFUA_7G06380
0.06047767

YGL043W
AFUA_3G07670
0.059398891

YMR027W
AFUA_5G06710
0.058232831

YHR215W
AFUA_8G01910
0.05787337

YDL247W
AFUA_7G05190
0.05184022

YPR048W
AFUA_5G07290
0.049809159

YBL051C
AFUA_5G01940
0.048514144

YHR148W
AFUA_2G08320
0.047441878

YJR160C
AFUA_7G05190
0.045923723

YJL039C
AFUA_5G12670
0.042943521

YNL029C
AFUA_5G12160
0.031203315

YGR267C
AFUA_5G03140
0.029526621

YNL027W
AFUA_1G06900
0.02747405

YDL247W
AFUA_7G06390
0.023887472

YHR107C
AFUA_5G03080
0.020068991

YKL165C
AFUA_4G03970
0.01938034

YNR012W
AFUA_2G05430
0.019075112

YLR085C
AFUA_4G04420
0.018617278

YPL082C
AFUA_1G05830
0.017285628

YCL064C
AFUA_1G06150
0.014476469

YNR039C
AFUA_1G12090
0.011820922

YOR216C
AFUA_1G08830
0.008439713

YOR148C
AFUA_4G07550
0.006702846

YDR420W
AFUA_4G00500
0.006566287

YPR018W
AFUA_5G03720
−0.000683184

YDR322W
AFUA_5G12810
−0.002517201

YNR015W
AFUA_3G08390
−0.013154917

YBR251W
AFUA_5G11540
−0.01637247

YHL028W
AFUA_5G09020
−0.020657813

YPL146C
AFUA_2G05550
−0.023787247

YKL127W
AFUA_3G11830
−0.026619404

YJR160C
AFUA_2G10910
−0.029508087

YIR038C
AFUA_1G17010
−0.030714781

YDL247W
AFUA_2G10910
−0.033905332

YBR204C
AFUA_1G03540
−0.038361835

YJR010W
AFUA_3G06530
−0.038908707

YMR210W
AFUA_6G04640
−0.046477426

YPR187W
AFUA_1G05160
−0.048502572

YDR037W
AFUA_6G07640
−0.052027721

YIL134W
AFUA_6G05170
−0.053118026

YLR286C
AFUA_5G03760
−0.062116003

YKL179C
AFUA_1G14240
−0.062203351

YDR109C
AFUA_4G04680
−0.063717983

YOL157C
AFUA_3G07380
−0.064624439

YIR038C
AFUA_2G17300
−0.068756542

YDL102W
AFUA_2G16600
−0.088010728

YOR389W
AFUA_2G01940
−0.09375584

YBR244W
AFUA_3G12270
−0.097477745

YJL219W
AFUA_2G11520
−0.098366126

YPL126W
AFUA_7G02610
−0.101632712

YDL189W
AFUA_1G09400
−0.104331651

YHL016C
AFUA_1G04870
−0.106608293

YLR380W
AFUA_4G13930
−0.111437921

YPR165W
AFUA_6G06900
−0.117573203

YOL062C
AFUA_5G07930
−0.122120003

YGL248W
AFUA_1G14890
−0.124318908

YLR029C
AFUA_1G04660
−0.129375946

YMR214W
AFUA_2G08300
−0.130867913

YOR124C
AFUA_6G12270
−0.136050424

YOL023W
AFUA_1G06520
−0.136914472

YPL280W
AFUA_3G01210
−0.13706189

YLR380W
AFUA_7G06760
−0.141209958

YNL241C
AFUA_3G08470
−0.153108798

YOR391C
AFUA_3G01210
−0.154014157

YOL089C
AFUA_6G02330
−0.161608796

YGL215W
AFUA_3G10040
−0.170171082

YMR137C
AFUA_2G15220
−0.174259735

YER004W
AFUA_6G08930
−0.179730339

YDR365C
AFUA_2G05420
−0.181946191

YDR529C
AFUA_4G06790
−0.185927497

YDR062W
AFUA_6G00300
−0.189190157

YOL086C
AFUA_7G01010
−0.190813468

YOL026C
AFUA_5G03630
−0.19138562

YIL033C
AFUA_3G10000
−0.195925157

YBR290W
AFUA_4G13740
−0.19955841

YAR019C
AFUA_4G06750
−0.204744755

YHL007C
AFUA_2G04680
−0.20737573

YMR078C
AFUA_7G05480
−0.222707833

YDR311W
AFUA_4G11690
−0.22686955

YOL100W
AFUA_3G12670
−0.230714484

YGR162W
AFUA_2G09490
−0.232235851

YGL255W
AFUA_1G01550
−0.248116851

YPL038W
AFUA_6G01910
−0.252388553

YCL035C
AFUA_1G06100
−0.255759517

YNL082W
AFUA_2G13410
−0.259394819

YDR062W
AFUA_1G11890
−0.263523207

YOR390W
AFUA_2G16210
−0.269616243

YJR141W
AFUA_3G07970
−0.2738444

YOR365C
AFUA_2G17650
−0.274036262

YDL116W
AFUA_1G10860
−0.278315121

YKL020C
AFUA_1G12550
−0.278379939

YDL174C
AFUA_3G06820
−0.286419799

YBR029C
AFUA_1G07010
−0.296926336

YLR096W
AFUA_1G11080
−0.297540349

YFL028C
AFUA_6G05080
−0.303502181

YOR089C
AFUA_3G10740
−0.30892361

YPR010C
AFUA_2G13000
−0.309890067

YJL219W
AFUA_5G01160
−0.321415181

YNL097C
AFUA_4G11660
−0.329160424

YMR116C
AFUA_4G13170
−0.329415498

YPL280W
AFUA_5G01430
−0.331554435

YHR091C
AFUA_2G14030
−0.337931682

YIL030C
AFUA_2G08650
−0.350942099

YFR037C
AFUA_7G05510
−0.356342064

YOR391C
AFUA_5G01430
−0.356843862

YDL174C
AFUA_1G00510
−0.402217656

YML121W
AFUA_5G09650
−0.410825283

YFL060C
AFUA_2G08580
−0.411505108

YDR301W
AFUA_8G04040
−0.413112754

YJL221C
AFUA_3G07380
−0.413321446

YLR326W
AFUA_5G12410
−0.458648708

YBL108C-A
AFUA_4G03360
−0.487139446

YGR165W
AFUA_5G08380
−0.519339895

YKL157W
AFUA_4G09030
−0.604021491

YNL334C
AFUA_2G08580
−0.720610634

2.3. Nucleosome Position Profile

Nucleosome mapping numbers at each genomic position were determined [13] based on genome-wide nucleosome mapping data for A. fumigatus [9] and S. cerevisiae [10]. In this analysis, a 1-kb region upstream of the translational start site was defined as a gene promoter. When the length of the gene body region is more than 1 kb, a 1-kb region downstream of the translational start site was defined as the gene body. When the length of the gene body is less than 1 kb, the region between the translational start and end sites was defined as the gene body. Analyses of nucleosome position data including calculation of Spearman’s rank correlation coefficient were performed using the statistics software R (http://www.r-project.org/).

3. Results and Discussion

3.1. Nucleosome Position Profiles of Duplicated Genes in Aspergillus fumigates

I compared nucleosome position profiles in each of the 63 duplicated gene pairs. Nucleosome positioning was conserved more in gene promoters than in gene bodies (Figure 1), as observed in the comparison of nucleosome positioning between trichostatin A-treated and -untreated A. fumigatus [4]. This result suggests that nucleosome positioning in the gene promoter plays an important role in transcriptional regulation [14].

Figure 1: Boxplots of Spearman’s rank correlation coefficients of nucleosome position profiles in the promoter and body regions of 63 duplicated gene pairs. Circles represent the correlation coefficients and values of the same genes are connected by lines.

Single-gene duplications and gene cluster duplications consisting of multiple genes were identified. One cluster of 4 genes (AFUA_1G00420 to AFUA_1G00470) is a duplication of another 4-gene cluster (AFUA_8G04120 to AFUA_8G04080) (Table 2). Among these gene pairs, the nucleosome position profile was poorly conserved in the gene promoter between AFUA_1G00470 and AFUA_8G04080 and in the gene body between AFUA_1G00440 and AFUA_8G04110 (Spearman’s rank correlation coefficients were 0.43 and 0.23, resp.) (Table 2). With the exception of these 2 cases, the nucleosome position profile was highly conserved (correlation coefficients were higher than 0.7) (Table 2).

We analyzed another pair of duplicated clusters (9 genes) (AFUA_1G16030 to AFUA_1G16120 and AFUA_5G14930 to AFUA_5G15030). The genes in each cluster have evolved for the same period after the duplication (Table 2). At present, conservation of the nucleosome position profiles varies among the 9 genes (Table 2). For example, the nucleosome position profile is poorly conserved in the gene promoters of 3 gene pairs (AFUA_1G16050 and AFUA_5G14950, AFUA_16110 and AFUA_15020, AFUA_1G16120 and AFUA_15030) (Spearman’s rank correlation coefficients are −0.35, −0.26, and −0.14, resp.). On the other hand, the nucleosome position profile is highly conserved in the promoters of AFUA_16070 and AFUA_5G14980 and was strongly correlated (correlation coefficient = 0.93). These results suggest that transcriptional regulation of duplicated genes is associated with nucleosome positions in the gene promoters.

3.2. Nucleosome Position Profiles of Orthologous Gene Promoters in Aspergillus fumigates and Saccharomyces cerevisiae

I compared the nucleosome position profiles in the promoters of 347 orthologous pairs of yeast genes that showed notably high conservation in the control and mutant strains. In the 63 duplicated A. fumigatus gene pairs, 13 (20.6%) gene promoter profiles and 11 (17.5%) gene body profiles were highly correlated (Spearman’s rank correlation coefficient > 0.7) (Table 1, Figure 1). On the other hand, of the 347 orthologous gene pairs, only 11 (3.2%) nucleosome position profiles were highly correlated (Spearman’s rank correlation coefficient > 0.7) (Table 4, Figure 2). The distribution of correlation coefficients of the 347 orthologous gene promoters did not significantly differ from that of the control (gene pairs chosen at random) (-value = 0.28 Kolmogorov-Smirnov test). One potential cause of this low conservation is the large evolutionary distance between the 2 fungi. A. fumigatus and S. cerevisiae belong to the subphyla Pezizomycotina and Saccharomycotina, respectively. Alternatively, this low conservation may represent a difference in mechanisms regulating the nucleosome arrangement, since the nucleosomal (nucleosome-bound) DNA lengths differ between the 2 fungi [9, 10].

Figure 2: Boxplots of Spearman’s rank correlation coefficients between nucleosome position profiles in the promoters of 347 orthologous gene pairs between Aspergillus fumigatus and Saccharomyces cerevisiae. The same number of gene pairs was chosen at random to serve as a control. Dots indicate correlation coefficients. The distributions of correlation coefficients did not significantly differ (-value = 0.28 in Kolmogorov-Smirnov test) between the orthologous gene promoters and the controls.

Nucleosome position profiles in gene promoters are thought to be related to gene function. For example, YIR038C of S. cerevisiae encodes an amino acid sequence protein (glutathione S-transferase) similar to 3 genes (AFUA_1G17010, AFUA_2G17300, and AFUA_8G02500) in A. fumigatus (Table 4). Although the nucleosome position profiles show some conservation between YIR038C and AFUA_8G02500 (Spearman’s rank correlation coefficient = 0.55, except for one nucleosome position loss in A. fumigatus), they are poorly conserved between YIR038C and AFUA_1G17010 (Spearman’s rank correlation coefficient = −0.03) and between YIR038C and AFUA_2G17300 (Spearman’s rank correlation coefficient = −0.07) (Table 4, Figure 3).

(a)

(b)

(c)

(d)

(e)

(f)

(g)

(h)

Figure 3: Mapping numbers of nucleosomes and transcription start sites in the promoter regions of YIR038C, AFUA_8G02500, AFUA_1G17010, and AFUA_2G17300. Position 0 indicates the translational start site.

Interestingly, although the nucleosome position profile of AFUA_8G02500 is completely different from that of AFUA_2G17300, the transcription start site patterns are very similar between these genes (Figure 3), suggesting that the relationship between transcription start site and nucleosome position in the gene promoter varies.

Acknowledgments

The author thanks Dr. Shinji Kondo for helpful comments and critical review of the paper. This study was supported in part by a grant from the Institute for Fermentation, Osaka (IFO), Japan.

References

K. Luger, A. W. Mäder, R. K. Richmond, D. F. Sargent, and T. J. Richmond, “Crystal structure of the nucleosome core particle at 2.8 Å resolution,” Nature, vol. 389, no. 6648, pp. 251–260, 1997.

C. K. Lee, Y. Shibata, B. Rao, B. D. Strahl, and J. D. Lieb, “Evidence for nucleosome depletion at active regulatory regions genome-wide,” Nature Genetics, vol. 36, no. 8, pp. 900–905, 2004.

G. C. Yuan, Y. J. Liu, M. F. Dion et al., “Molecular biology: genome-scale identification of nucleosome positions in S. cerevisiae,” Science, vol. 309, no. 5734, pp. 626–630, 2005.

H. Nishida, T. Motoyama, Y. Suzuki, S. Yamamoto, H. Aburatani, and H. Osada, “Genome-wide maps of mononucleosomes and dinucleosomes containing hyperacetylated histOnes of Aspergillus fumigatus,” PloS One, vol. 5, no. 3, article e9916, 2010.

A. M. Tsankov, D. A. Thompson, A. Socha, A. Regev, and O. J. Rando, “The role of nucleosome positioning in the evolution of gene regulation,” PLoS Biology, vol. 8, no. 7, article e1000414, 2010.

E. Segal, Y. Fondufe-Mittendorf, L. Chen et al., “A genomic code for nucleosome positioning,” Nature, vol. 442, no. 7104, pp. 772–778, 2006.

A. B. Lantermann, T. Straub, A. Strålfors, G. C. Yuan, K. Ekwall, and P. Korber, “Schizosaccharomyces pombe genome-wide nucleosome mapping reveals positioning mechanisms distinct from those of Saccharomyces cerevisiae,” Nature Structural and Molecular Biology, vol. 17, no. 2, pp. 251–257, 2010.

S. A. Teichmann and M. M. Babu, “Gene regulatory network growth by duplication,” Nature Genetics, vol. 36, no. 5, pp. 492–496, 2004.

H. Nishida, T. Motoyama, S. Yamamoto, H. Aburatani, and H. Osada, “Genome-wide maps of mono- and di-nucleosomes of Aspergillus fumigatus,” Bioinformatics, vol. 25, no. 18, pp. 2295–2297, 2009.

T. Matsumoto, C.-S. Yun, H. Yoshikawa, and H. Nishida, “Comparative studies of genome-wide maps of nucleosomes between deletion mutants of elp3 and hos2 genes of Saccharomyces cerevisiae,” PLoS One, vol. 6, no. 1, article e16372, 2011.

H. Nishida, “Evolutionary conservation levels of subunits of histOne-modifying protein complexes in fungi,” Comparative and Functional Genomics, vol. 2009, Article ID 379317, 6 pages, 2009.

I. Uchiyama, T. Higuchi, and M. Kawai, “MBGD update 2010: toward a comprehensive resource for exploring microbial genome diversity,” Nucleic Acids Research, vol. 38, no. 1, pp. D361–D365, 2009.

H. Nishida, “Calculation of the ratio of the mononucleosome mapping number to the dinucleosome mapping number for each nucleotide position in the Aspergillus fumigatus genome,” Open Access Bioinformatics, vol. 1, pp. 1–6, 2009.

D. E. SchOnes, K. Cui, S. Cuddapah et al., “Dynamic regulation of nucleosome positioning in the human genome,” Cell, vol. 132, no. 5, pp. 887–898, 2008.