Open Access

The diversity of fungal genome

Biological Procedures Online201517:8

https://doi.org/10.1186/s12575-015-0020-z

Received: 5 December 2014

Accepted: 31 January 2015

Published: 2 April 2015

Abstract

The genome size of an organism varies from species to species. The C-value paradox enigma is a very complex puzzle with regards to vast diversity in genome sizes in eukaryotes. Here we reported the detailed genomic information of 172 fungal species among different fungal genomes and found that fungal genomes are very diverse in nature. In fungi, the diversity of genomes varies from 8.97 Mb to 177.57 Mb. The average genome sizes of Ascomycota and Basidiomycota fungi are 36.91 and 46.48 Mb respectively. But higher genome size is observed in Oomycota (74.85 Mb) species, a lineage of fungus-like eukaryotic microorganisms. The average coding genes of Oomycota species are almost doubled than that of Acomycota and Basidiomycota fungus.

Keywords

AscomycotaBasidiomycotaChytridiomycotaMonoblepharidomycotaNeocallimastigomycotaBlastocladiomycotaGlomeromycotaEntomophthoromycotaStramenopiles and micorsporidia

Introduction

Fungi are the larger group of eukaryotic organisms that ranges from yeast and slime molds to mushrooms. These organisms are majorly classified as monophyletic Eumycota group and their diversity ranges from 500 thousand to 9.9 million spanning over 1 billion years of evolutionary history [1,2]. They are abundant at worldwide scale due to their small size and their cryptic lifestyle in soil, dead and decomposing matter, as symbionts with algae, fungi, bryophyte, pteridophyte, higher plants and animals [3-7]. These organisms dominate earth from polar to temperate and tropical habitats [8-10]. Due to their ecological dominance, they play a central role in human endeavor. The fungus (mushroom and truffle) are directly used as human food and yeasts are used in bread industry. The fungi also carry out nutrient cycling by decomposing organic matter [11-13]. They also produce antibiotics, enzymes, mycotoxins, alkaloids, polyketides and other chemical compounds [14-21].

The kingdom fungi are classified into several major phyla namely Ascomycota, Basidiomycota, Chytridiomycota, Monoblepharidomycota, Neocallimastigomycota, Blastocladiomycota, Glomeromycota, Entomophthoromycota, Stramenopiles and Micorsporidia and sub-phyla namely Kickxellomycotina, mucoromycotina and Zoopagomycotina [22,23]. The diverse ecological dominance of fungus makes them important from an evolutionary point of view. That is why fungi are subjected to intense phylogenetic, ecological and molecular studies. The advancement in high throughput sequencing technology progressed rapidly that led to sequencing of large numbers of fungal genomes. The evolution of biological diversity raises several questions such as how much variation can be expected among closely or related genomes. This can be answered by the comparing closely related genomes. So we carried out a global search of fungal genomes in MycoCosm and JGI database and studied the evolutionary relationships of their genome sizes and reported here [24-26].

Fungal genome size

Recently, the genome sequencing technology has emerged as one of the most efficient tools that can provide whole information of a genome in a small period of time. Since the completion of genome sequencing of the model fungus S. cerevisae in 1996, sequencing of large numbers of fungal genomes are now completed. Sequencing of large numbers of fungal genomes will allow us to understand the diversity of genes encoding enzymes, and pathways that produces several novel compounds [24]. Although the fungi are very diverse in nature, their basic cellular physiology and genetics shares some common components with plants and animal cells. These include multi-cellularity, cytoskeletal structures, cell cycle, circadian rhythm, intercellular signaling, sexual reproduction, development and differentiation [27]. It was previously thought that genomes of all fungi are derived from the genome of the model fungi Saccharomyces cerevisae [27]. However recent explosion in fungal genome sequencing greatly expanded the fungal genomics and molecular diversity of these organisms. Compared to the genome size of animals and plants, the genome sizes of fungi are small [28]. The genome size of model fungi S. cerevisae is bit more than 12 Mb (Table 1). From the studied 172 fungal species, only seven species have genome sizes larger than 100 Mb (Table 1). So, the probability of occurrence of larger genomes in fungi is very small. The genome size of Cenococcum geophilum (177.57 Mb) is the largest and the genome size of Hansenula polymorpha (8.97 Mb) is the smallest from the studied species. Both species belong to Ascomycota. In the group of Basidiomycota species, the genome size of Wallemia sebi (9.82 Mb) is the smallest one and genome of Dendrothele bispora (130.65) is the largest one (Table 1). No single species from Chytridiomycota, Glomeromycota, Oomycota, Stramenopiles, Mucoromycotina have genome size larger than 100 Mb. Although there is large variation in genome size in fungi, the average genome size of fungal species taken during this study is 42. 30 Mb (Table 1). The average genome sizes of fungal species belonging to different phyla are provided in Table 2. From the table we can observe that the average genome size of Ascomycota group of fungi is 36.91 Mb. The average genome size of Basidiomycota group is 46.48 Mb. The average genome size of Oomycota group of fungi is 74.85 Mb which is the highest among all groups (Table 2). If we consider about the coding gene sequence in fungi, in average the Acomycota, Basidiomycota, Oomycota and Mucoromycotina groups encodes for 11129.45, 15431.51, 24173.33, 13306 no. of genes respectively in their genomes (Table 2).
Table 1

List of genome size (Mb), numbers of coding genes, and average numbers of exons present per fungal species from the different phyla of Kingdom Fungi

Sl. No

Name of Fungal Species

Division

Genome Size Mbp

No. Of Contigs

No. Of Scaffolds

No of Gene Models

Average Exons Per Gene

1

Acidomyces richmondensis

Ascomycota

29.88

3164

3164

11202

2.28

2

Acremonium alcalophilum

Ascomycota

54.42

865

15

9491

4.05

3

Agaricus bisporus

Basidiomycota

30.2

254

29

10438

6.05

4

Amanita muscaria Koide

Basidiomycota

40.70

3814

1101

18153

4.54

5

Amorphotheca resinae

Ascomycota

28.63

261

32

9642

2.97

6

Anthostoma avocetta

Ascomycota

56.23

1038

786

15755

2.93

7

Antrodia sinuosa

Basidiomycota

30.17

1482

1387

11327

6.09

8

Apiospora montagnei

Ascomycota

47.67

706

686

16992

2.52

9

Aplanochytrium kerguelense

Stramenopiles

35.77

523

207

11892

2.75

10

Aplosporella prunicola

Ascomycota

32.82

763

334

12579

2.67

11

Ascobolus immersus

Ascomycota

59.53

1225

706

17877

2.67

12

Ascoidea rubescens

Ascomycota

17.50

101

63

6802

1.39

13

Aspergillus acidus

Ascomycota

37.47

318

107

13530

3.10

14

Aspergillus niger

Ascomycota

34.85

24

24

11910

3.38

15

Atractiellales sp.

Basidiomycota

51.47

3076

1998

17606

5.30

16

Aulographum hederae

Ascomycota

31.98

613

173

12127

2.66

17

Aurantiochytrium limacinum

Stramenopiles

60.93

1118

181

14859

1.45

18

Aureobasidium pullulans

Ascomycota

29.62

84

75

10809

2.51

19

Auricularia subglabra

Basidiomycota

76.85

2158

761

25459

4.80

20

Babjeviella inositovora

Ascomycota

15.22

210

49

6403

1.27

21

Backusella circina

Mucoromycotina

48.65

2354

1095

17039

4.25

22

Baudoinia compniacensis

Ascomycota

21.88

35

19

10513

2.14

23

Bjerkandera adusta

Basidiomycota

42.73

1263

508

15473

5.59

24

Boletus edulis

Basidiomycota

46.64

4723

1099

16933

4.88

25

Botryobasidium botryosum

Basidiomycota

46.67

1446

334

16526

5.58

26

Calocera cornea

Basidiomycota

33.24

1032

545

13177

4.44

27

Calocera viscosa

Basidiomycota

29.10

487

214

12378

4.59

28

Candida caseinolytica

Ascomycota

9.18

49

6

4657

1.20

29

Catenaria anguillulae

Blastocladiomycota

36.22

2577

801

14188

2.50

30

Cenococcum geophilum

Ascomycota

177.57

2893

268

27529

4.08

31

Cercospora zeae-maydis

Ascomycota

46.61

2555

917

12020

2.32

32

Chalara longipes

Ascomycota

52.43

175

54

19765

3.06

33

Choiromyces venosus

Ascomycota

126.04

3183

1176

17986

2.84

34

Cochliobolus sativus

Ascomycota

34.42

478

157

12250

2.63

35

Coemansia reversa

Kickellomycotina

21.84

1063

346

7347

1.51

36

Conidiobolus coronatus

Entomophthoromycota

39.90

7809

1050

10635

2.78

37

Coniophora puteana

Basdiomycota

42.97

1034

210

13761

6.11

38

Coprinopsis cinerea

Basdiomycota

37.5

---

---

---

---

39

Cortinarius glaucopus

Basidiomycota

63.45

2103

769

20377

5.05

40

Cronartium quercuum

Basidiomycota

76.57

10431

1198

13903

4.35

41

Cryphonectria parasitica

Ascomycota

43.9

33

26

11609

2.91

42

Cryptococcus vishniacii

Basidiomycota

19.69

137

50

7232

6.25

43

Cucurbitaria berberidis

Ascomycota

32.91

184

42

12439

2.71

44

Cyberlindnera jadinii

Ascomycota

13.02

392

76

6038

1.35

45

Cylindrobasidium torrendii

Basidiomycota

31.57

1222

1149

13940

5.17

46

Dacryopinax sp.

Basidiomycota

29.50

878

99

10242

4.83

47

Daedalea quercina

Basidiomycota

32.74

1025

357

12199

5.80

48

Daldinia eschscholzii

Ascomycota

37.55

512

398

11173

2.89

49

Dekkera bruxellensis

Ascomycota

13.37

1374

84

5600

1.44

50

Dendrothele bispora

Basidiomycota

130.65

6351

3942

33645

5.09

51

Dichomitus squalens

Basidiomycota

42.75

2852

542

12290

5.84

52

Didymella exigua

Ascomycota

34.39

1010

176

12394

2.46

53

Dioszegia cryoxerica

Basidiomycota

39.52

1318

865

15948

5.36

54

Dissoconium aciculare

Ascomycota

26.54

232

54

10299

2.17

55

Dothidotthia symphoricarpi

Ascomycota

34.43

268

59

11790

2.71

56

Eurotium rubrum

Ascomycota

26.21

371

110

10076

3.07

57

Exidia glandulosa

Basidiomycota

78.17

4024

1727

26765

4.83

58

Exobasidium vaccinii

Basidiomycota

16.99

246

119

7453

2.79

59

Fibulorhizoctonia sp.

Basidiomycota

95.13

3901

1918

32946

4.63

60

Fomitiporia mediterranea

Basidiomycota

63.35

5766

1412

11333

6.06

61

Fomitopsis pinicola

Basidiomycota

46.30

988

504

13885

5.56

62

Galerina marginata

Basidiomycota

59.42

1272

414

21461

5.30

63

Ganoderma sp.

Basidiomycota

39.52

503

156

12910

5.82

64

Gloeophyllum trabeum

Basidiomycota

37.18

2289

443

11846

6.14

65

Glomerella acutata

Ascomycota

50.04

378

307

15777

2.83

66

Glomerella cingulata

Ascomycota

58.84

774

119

18975

2.79

67

Gonapodya prolifera

Monoblepharidomycetes

48.79

1154

352

13902

5.58

68

Gymnascella aurantiaca

Ascomycota

25.35

356

347

9106

3.12

69

Gymnascella citrina

Ascomycota

25.16

305

272

9779

2.99

70

Gyrodon lividus

Basidiomycota

43.05

1390

369

11779

5.75

71

Hanseniaspora valbyensis

Ascomycota

11.46

1163

646

4800

1.20

72

Hansenula polymorpha

Ascomycota

8.97

9

7

5177

1.20

73

Hebeloma cylindrosporum

Basidiomycota

37.61

222

222

16841

5.05

74

Heterobasidion annosum

Basidiomycota

33.7

18

15

13405

5.54

75

Hydnomerulius pinastri

Basidiomycota

38.28

2315

603

13270

5.84

76

Hypholoma sublateritium

Basidiomycota

48.03

1329

704

17911

5.29

77

Hyphopichia burtonii

Ascomycota

12.40

105

27

6002

1.22

78

Hypoxylon sp.

Ascomycota

46.59

580

505

12256

2.90

79

Jaapia argillacea

Basidiomycota

45.05

1182

295

5.53

5.53

80

Laccaria amethystina

Basidiomycota

52.20

4756

1299

21066

4.49

81

Laccaria bicolor

Basidiomycota

60.71

584

55

23132

5.28

82

Laetiporus sulphureus

Basidiomycota

39.92

1207

403

13774

5.72

83

Lentinus tigrinus

Basidiomycota

39.68

571

286

15581

5.59

84

Leucogyrophana mollusca

Basidiomycota

35.19

1347

1262

14619

5.89

85

Lichtheimia hyalospora

Mucoromycotina

33.28

2294

2222

12062

4.99

86

Lipomyces starkeyi

Ascomycota

21.27

439

117

8192

2.85

87

Lophiostoma macrostomum

Ascomycota

42.58

1294

1282

16160

2.74

88

Macrolepiota fuliginosa

Basidiomycota

46.40

4852

3478

15801

5.39

89

Melampsora laricis-populina

Basidiomycota

101.1

---

462

19694

---

90

Melanconium sp.

Ascomycota

58.52

465

100

16656

2.68

91

Melanomma pulvis-pyrius

Ascomycota

42.09

1771

1754

15881

2.77

92

Meliniomyces bicolor

Basidiomycota

82.38

301

206

18619

2.96

93

Metschnikowia bicuspidata

Ascomycota

16.06

421

48

5851

1.27

94

Mixia osmundae

Basidiomycota

13.63

204

156

6903

4.54

95

Monascus purpureus

Ascomycota

23.44

319

296

8918

3.19

96

Monascus ruber

Ascomycota

24.80

362

320

9650

3.13

97

Mortierella elongata

Mucoromycotina

49.96

3314

473

14964

3.47

98

Mucor circinelloides

Mucoromycotina

36.6

26

26

11719

3.8

99

Myceliophthora thermophila

Ascomycota

38.74

7

7

9110

2.83

100

Mycosphaerella graminicola

Ascomycota

39.7

---

129

10952

---

101

Myriangium duriaei

Ascomycota

25.69

32

16

10685

2.37

102

Nadsonia fulvescens

Ascomycota

13.75

64

20

5657

1.57

103

Neolentinus lepideus

Basidiomycota

35.64

1215

331

13164

5.71

104

Neurospora discreta

Ascomycota

37.3

---

176

9948

---

105

Neurospora tetrasperma

Ascomycota

37.8

542

155

10640

2.72

106

Oidiodendron maius

Ascomycota

46.43

387

100

16703

2.97

107

Pachysolen tannophilus

Ascomycota

12.60

583

198

5675

1.33

108

Patellaria atrata

Ascomycota

28.69

501

127

9794

2.97

109

Paxillus rubicundulus

Basidiomycota

53.01

7170

6945

22065

3.81

110

Penicillium brevicompactum

Ascomycota

32.11

96

35

11536

3.09

111

Penicillium canescens

Ascomycota

33.26

248

62

12374

3.12

112

Penicillium janthinellum

Ascomycota

35.15

273

94

12098

3.07

113

Penicillium raistrickii

Ascomycota

31.44

104

76

11368

3.11

114

Phlebia brevispora

Basidiomycota

49.96

3178

1645

16170

5.66

115

Phlebiopsis gigantea

Basidiomycota

30.14

1195

573

11891

6.00

116

Phycomyces blakesleeanus

Mucoromycotina

53.9

350

80

16528

4.5

117

Phytophthora capsici

Oomycota

64

10760

917

19805

2.20

118

Phytophthora cinnamomi

Oomycota

77.97

9537

1314

26131

2.10

119

Phytophthora sojae

Oomycota

82.60

1643

83

26584

2.39

120

Pichia stipitis

Ascomycota

15.4

---

394

5841

~1

121

Piedraia hortae

Ascomycota

16.95

214

132

7572

1.84

122

Piloderma croceum

Basidiomycota

59.33

4469

715

21583

4.75

123

Piromyces sp.

Neocallimastigomycota

71.02

17217

1656

14648

3.09

124

Pisolithus microcarpus

Basidiomycota

53.03

5476

1064

21064

4.04

125

Pleomassaria siparia

Ascomycota

43.18

1023

193

13486

2.81

126

Pleurotus ostreatus

Basidiomycota

35.6

3272

572

11603

6.1

127

Polychaeton citri

Ascomycota

27.21

451

416

10582

2.12

128

Polyporus arcularius

Basidiomycota

43.45

2601

2540

17525

5.27

129

Punctularia strigosozonata

Basidiomycota

34.17

1327

195

11538

6.23

130

Pycnoporus sanguineus

Basidiomycota

36.04

2046

657

14165

5.59

131

Ramaria rubella

Basidiomycota

105.46

5927

1553

19287

5.53

132

Rhizophagus irregularis

Glomeromycota

91.08

28405

28371

30282

3.46

133

Rhizopus microsporus

Mucoromycotina

25.97

823

131

10905

4.03

134

Rhodotorula graminis

Basidiomycota

21.01

620

26

7283

6.24

135

Rickenella mellea

Basidiomycota

46.03

1236

1092

18952

4.98

136

Saccharata proteae

Ascomycota

31.43

727

245

9234

3.08

137

Saccharomyces cerevisiae

Ascomycota

12.07

16

16

6575

1.04

138

Saitoella complicata

Ascomycota

14.14

35

35

7034

2.23

139

Schizophyllum commune Loenen D

Basidiomycota

35.88

1822

1774

13827

5.55

140

Schizophyllum commune Tattone D

Basidiomycota

36.46

1757

1707

15199

5.27

141

Schizopora paradoxa

Basidiomycota

44.41

1342

1291

17098

5.78

142

Scleroderma citrinum

Basidiomycota

56.14

3919

938

21012

4.33

143

Sebacina vermifera

Basidiomycota

38.09

2457

546

15312

4.94

144

Septoria musiva

Ascomycota

29.35

706

72

10233

2.44

145

Serpula lacrymans

Basidiomycota

42.73

375

36

12789

5.73

146

Sistotremastrum niveocremeum

Basidiomycota

35.36

699

179

13080

5.95

147

Sodiomyces alkalinus

Ascomycota

43.45

290

25

9411

3.32

148

Spathaspora passalidarum

Ascomycota

13.2

26

8

5983

1.2

149

Sporobolomyces roseus

Basidiomycota

21.2

---

76

5536

---

150

Sporormia fimetaria

Ascomycota

25.89

293

140

10783

2.70

151

Stereum hirsutum

Basidiomycota

46.51

995

159

14072

6.52

152

Suillus brevipes

Basidiomycota

51.71

4139

1550

22453

4.54

153

Talaromyces aculeatus

Ascomycota

37.27

165

49

13793

3.16

154

Terfezia boudieri

Ascomycota

63.23

2078

516

10200

3.61

155

Thermoascus aurantiacus

Ascomycota

28.49

196

48

8798

3.33

156

Thielavia appendiculata

Ascomycota

32.74

501

109

11942

2.77

157

Thielavia arenaria

Ascomycota

30.99

354

69

10954

2.80

158

Thielavia hyrcaniae

Ascomycota

31.18

972

251

11338

2.73

159

Trametes versicolor

Basidiomycota

44.79

1443

283

14296

5.81

160

Trichaptum abietinum

Basiodiomycota

40.61

1345

492

14978

5.65

161

Trichoderma citrinoviride

Ascomycota

33.48

699

533

9737

3.10

162

Trypethelium eluteriae

Ascomycota

32.16

747

730

11858

2.83

163

Tulasnella calospora

Basidiomycota

62.39

6848

1335

19659

4.65

164

Umbelopsis ramanniana

Mucoromycotina

23.08

239

198

9931

4.75

165

Wallemia sebi

Basidiomycota

9.82

114

56

5284

4.03

166

Wickerhamomyces anomalus

Ascomycota

14.15

207

46

6423

1.42

167

Wilcoxina mikolae

Ascomycota

117.29

5591

1604

13093

3.24

168

Wolfiporia cocos

Basidiomycota

50.48

2228

348

12746

6.31

169

Xanthoria parietina

Ascomycota

31.90

302

39

10818

2.98

170

Xylona heveae

Ascomycota

24.34

56

27

8205

3.41

171

Zasmidium cellare

Ascomycota

38.25

365

267

16015

2.50

172

Zopfia rhizophila

Ascomycota

152.78

1349

864

21730

2.77

 

Average

 

42.300

  

13437.21

3.79

The fungal classifications (phyla/sub-phyla) are based on reports of Humber (2012) and Hibbet et al. (2007) [22,23].

Table 2

Average genome size, and average number of coding genes and exons present in the different phyla/sub-phyla of the Kingdom Fungi

Fungal division

Average Genome Size (Mb)

Average No. Of Genes

Average No. Of Exons

Ascomycota

36.91

11129.45

2.58

Basidiomycota

46.48

15431.51

5.28

Oomycota

74.85

24173.33

2.23

Mucoromycotina

38.777

13306.85

4.25

The comparative analysis of fungal genomes show fungi are very divergent [27]. It was earlier thought that genomes of Magnaporthe grisea and Neurospora crassa share a common ancestor. But, comparative genomes analyses revealed only 47% amino acid sequence identity and absence of conserved synteny [27]. Only few genes are identified to be in conserved co-linearity. This shows that even members of the same genus can show remarkable divergence at the genomic level. A genomic comparison between Aspergillus nidulans, Aspergillus fumigatus and Aspergillus oryzae shows only 68% of amino acid sequence identity [27]. The genome duplication and translocation have major impact in evolution in yeast (Figure 1) [29,30]. The whole genome duplication in yeast followed by massive gene loss is confirmed by comparative experimental analysis [31,32]. This indicates that fungal genomes are very dynamic in nature. Lavergne et al. [33] reported that genome size reduction can trigger rapid phenotypic evolution in invasive plants. Their report suggests that the invasive genotypes had smaller genomes. Smaller genome sizes have phenotypic effects that increased the invasive potential [33]. But in exception, for example, the duckweeds which are smallest, fast-growing and simplest flowering plants are invasive in nature and contains increased DNA content in their genomes [34].
Figure 1

Role of different forces affecting the evolution of genome size. The major important factors are transposable elements (TEs), short sequence repeats, microsatellites, genome duplication and others. The mutational and selection pressure plays a significant role in this process. The negligible selective effects governed by genetic drift also contribute for the evolution of genome size. Overall all the forces play a role towards the increase in genome size at different levels. The photograph is adapted according to the report of Petrov [37].

Evolution in genome size

Genomes are aggregates of genes and this concept nicely fits with the prokaryotic organisms and viruses [35]. This concept is very inappropriate for eukaryotic organisms as most of the eukaryotic genomes are studded with nongenic and unconstrained repetitive DNA. This can lead to approximately 200,000 fold variation in genome size [36]. The genome size of an organism depends on the particular developmental and ecological need of the organism [37]. The genes are made up of DNA and it is a general assumption that more complex organisms requires more genes and thus contain more DNA in its genomes. The simple organisms probably contain fewer essential genes compared to more complex organisms and thus contain less DNA in its genomes. However this observation is not true. Some very simple organisms could have more DNA content than complex multi-cellular organisms. For example, some amoeba species have 200 times more DNA than humans [38]. Similarly, lilies have 200 times more DNA than that of rice [39]. But in many organisms much of the DNA content is noncoding and repetitive. But it is very important to understand which evolutionary forces produces enormous amount of noncoding DNA? What are the adaptive functions of these nongenic DNA? If these nongenic DNA don’t have any essential adaptive roles, than why natural selection favors the burden of synthesis of extra DNA? Several hypotheses are postulated since long days to address these questions. But still there is debate over it. Some of the hypotheses are discussed later. From the studied fungal genomes, the average genome sizes of Oomycota species (74.85 Mb) are higher than other. The Ascomycota and Mucoromycotina species shares more or less than same average genome size i.e. 36.91 and 37.02 Mb, respectively. In contrary, the average genome sizes of Basidiomycota species is 46.48 Mbs. The increase in genome size in Oomycota species is also directly correlated with the increase in the numbers of average coding gene sequences. The average numbers of coding genes present in Oomycota species are 24173.33 genes per genome which is almost the double number present in Ascomycota and Basidiomycota species.

The adaptive theories of genome evolution

If certain numbers of genes are responsible for the phenotype and genotypic characters of an organism, why there are extra amounts of DNA in its genome? The adaptive theory explains that this extra DNA abundance is for adaptive function and its content don’t have any significant effects in phenotype of the organism [40]. A large genome directly increases the nuclear and cellular volumes [41]. This largely helps to buffer the fluctuation in the concentration of regulatory proteins or protect coding DNA from spontaneous mutation [42]. So the variation in the genome size is due to adaptive needs or due to natural selection in different organisms [37].

Junk DNA theory of genome evolution

The junk DNA hypothesis suggests that these extra DNAs are useless, maladaptive DNAs and fixed by random drift [43]. These DNAs are carried in chromosome and don’t have any significant role in the phenotype of an organism [43]. These junk DNAs are known as parasitic DNA or transposable elements (TEs) [44]. The mutational mechanisms of DNA gain or loss can lead to minor changes in the genome of an organism, but changes in genome size may occur by the involvement of different evolutionary forces [37]. An increase in transposition rate certainly can lead to an increase in genome size [37]. Instead of thinking in genome size evolution by adaptive evolution theory or by junk DNA theory, it is very important to understand which evolutionary force is responsible for changes in genome size. The mutational and selective forces might have vast potential to affect the change in genome sizes (Figure 1) [37]. If we can get the specific clue, we can try to estimate the strength of individual force and whether the magnitude of individual force may produce changes in genome sizes. This approach can explain the quantitative sense about genetic mechanism and the selective forces that affect the genome size.

The activities of transposable elements are very fast and can able to amplify the a transposable copy number into 20-100 copies (~0.1-1 Mbp) in a single generation [45,46]. The changes in genome size through spontaneous deletion or insertion are relatively slow [47]. For example, the Drosophila melanogaster genome losses less than a single base pair per generation [47]. If there is strong selection in increasing in gnome sizes, strong mutational pressure also can not affect the evolution of genome size [37]. However, strong selection for increase in genome size can substantially slow down the impact of mutation rate. If we can get the information of time scale of genome size divergence, then we can infer the genome-size changes between two closely related organisms. If we will consider the evolutionary development of fungus, Ascomycota has higher evolutionary rate than Basidiomycota [48]. But when we compared the average genome size of Ascomycota, Basidiomycota and Mucoromycotina, we found that the genome size of Basidiomycota is larger than the genome size of Ascomycota and Mucoromycotina. This may suggests that the evolution of fungal genome size is due to addition of nucleotides/DNA contents rather than deletion of nucleotides.

Some forces act on the traits correlated with total genome size of an organism [37]. In this case, natural selection forces affect only to few genomic components. For example, the increase in rate of heterochromatin shrinkage through heterochromatic DNA should not affect the size of euchromatin [37]. Similarly, the expansion in satellite DNA should not hamper the size of satellite free sequences. Another important question is that, whether different genomic components are varying together in a correlated fashion during evolution of genome size? Although there are no significant current evidences regarding this question, there are certain cytogenetic and molecular studies available. The cytogenetic study revealed that genome size differences are scattered throughout the euchromatic portion of the genome [49-52]. Comparison of orthologous introns revealed correlation between average size of intron and genome size [53]. The changes in the intron length do not account for the changes in the genome size. Although transposable elements are largely associated with the increase in genome size, presence of increased simple repeated sequences, pseudogenes, increased size of inter-enhancer spacers and microsatellites are also associated with increase in genome size (Figure 1) [54-56]. When there are changes in genome size, they do it across all the genomic components. This suggests that a global force acts as the direct agent for change in genome size. So, from our study we can speculate that Oomycota species might harbors high densities of TEs, simple repeat sequences, microsatellites and pseudogenes. Similarly, the Basidiomycota species might have more densities of TEs, simple repeat sequences, microsatellites and pseudogenes compared to Ascomycota and other groups. Whitney et al. [57] reported about the nonadaptive process in plant genome size evolution. They hypothesized that genome expansion is maladaptive and lineages with small effective population size evolve larger genomes than those with large population size. In addition, mating systems are likely to affect genome size evolution via population size and spread of transposable elements [57].

Conclusion

The question of genome size (C-value paradox) is very puzzling. Most probably we can better understand about the evolution of fungal genome size by completely understanding the roles of noncoding DNAs. It is also equally important to understand whether the addition and deletion of additional DNA content varies between species to species and at organism level too. Although experimental approach like cytogenetic study of euchromatic region can give some lime light about this issue, still high fidelity experimental approaches are lacking till to date.

Declarations

Acknowledgement

This work was carried out with the support of the Next-Generation Biogreen 21 Program (PJ011113), Rural Development Administration, Republic of Korea.

Authors’ Affiliations

(1)
Department of Biotechnology, Yeungnam University

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