Analysis of the Basidiomycete Reveals Conservation of the Core Meiotic Expression Program over Half a Billion Years of Evolution
Coprinopsis cinerea (also known as Coprinus cinereus) is a multicellular basidiomycete mushroom particularly suited to the study of meiosis due to its synchronous meiotic development and prolonged prophase. We examined the 15-hour meiotic transcriptional program of C. cinerea, encompassing time points prior to haploid nuclear fusion though tetrad formation, using a 70-mer oligonucleotide microarray. As with other organisms, a large proportion (∼20%) of genes are differentially regulated during this developmental process, with successive waves of transcription apparent in nine transcriptional clusters, including one enriched for meiotic functions. C. cinerea and the fungi Saccharomyces cerevisiae and Schizosaccharomyces pombe diverged ∼500–900 million years ago, permitting a comparison of transcriptional programs across a broad evolutionary time scale. Previous studies of S. cerevisiae and S. pombe compared genes that were induced upon entry into meiosis; inclusion of C. cinerea data indicates that meiotic genes are more conserved in their patterns of induction across species than genes not known to be meiotic. In addition, we found that meiotic genes are significantly more conserved in their transcript profiles than genes not known to be meiotic, which indicates a remarkable conservation of the meiotic process across evolutionarily distant organisms. Overall, meiotic function genes are more conserved in both induction and transcript profile than genes not known to be meiotic. However, of 50 meiotic function genes that were co-induced in all three species, 41 transcript profiles were well-correlated in at least two of the three species, but only a single gene (rad50) exhibited coordinated induction and well-correlated transcript profiles in all three species, indicating that co-induction does not necessarily predict correlated expression or vice versa. Differences may reflect differences in meiotic mechanisms or new roles for paralogs. Similarities in induction, transcript profiles, or both, should contribute to gene discovery for orthologs without currently characterized meiotic roles.
Vyšlo v časopise:
Analysis of the Basidiomycete Reveals Conservation of the Core Meiotic Expression Program over Half a Billion Years of Evolution. PLoS Genet 6(9): e32767. doi:10.1371/journal.pgen.1001135
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1001135
Souhrn
Coprinopsis cinerea (also known as Coprinus cinereus) is a multicellular basidiomycete mushroom particularly suited to the study of meiosis due to its synchronous meiotic development and prolonged prophase. We examined the 15-hour meiotic transcriptional program of C. cinerea, encompassing time points prior to haploid nuclear fusion though tetrad formation, using a 70-mer oligonucleotide microarray. As with other organisms, a large proportion (∼20%) of genes are differentially regulated during this developmental process, with successive waves of transcription apparent in nine transcriptional clusters, including one enriched for meiotic functions. C. cinerea and the fungi Saccharomyces cerevisiae and Schizosaccharomyces pombe diverged ∼500–900 million years ago, permitting a comparison of transcriptional programs across a broad evolutionary time scale. Previous studies of S. cerevisiae and S. pombe compared genes that were induced upon entry into meiosis; inclusion of C. cinerea data indicates that meiotic genes are more conserved in their patterns of induction across species than genes not known to be meiotic. In addition, we found that meiotic genes are significantly more conserved in their transcript profiles than genes not known to be meiotic, which indicates a remarkable conservation of the meiotic process across evolutionarily distant organisms. Overall, meiotic function genes are more conserved in both induction and transcript profile than genes not known to be meiotic. However, of 50 meiotic function genes that were co-induced in all three species, 41 transcript profiles were well-correlated in at least two of the three species, but only a single gene (rad50) exhibited coordinated induction and well-correlated transcript profiles in all three species, indicating that co-induction does not necessarily predict correlated expression or vice versa. Differences may reflect differences in meiotic mechanisms or new roles for paralogs. Similarities in induction, transcript profiles, or both, should contribute to gene discovery for orthologs without currently characterized meiotic roles.
Zdroje
1. RedheadSA
VilgalysR
MoncalvoJM
JohnsonJ
HoppleJS
2001 Coprinus Pers. and the disposition of Coprinus species sensu lato. Taxon 50 203 241
2. RajuNB
LuBC
1970 Meiosis in Coprinus. 3: Timing of meiotic events in C. lagopus (sensu Buller). Canadian Journal of Botany 48 2183 2186
3. PageSL
HawleyRS
2004 The genetics and molecular biology of the synaptonemal complex. Annual Review of Cell and Developmental Biology 20 525 558
4. HendersonKA
KeeneyS
2005 Synaptonemal complex formation: where does it start? Bioessays 27 995 998
5. LiWX
MaH
2006 Double-stranded DNA breaks and gene functions in recombination and meiosis. Cell Research 16 402 412
6. StajichJE
WilkeSK
AhrenD
AuTCH
BirrenB
2010 Genome evolution in mushrooms: Insights from the genome and assembled chromosomes of Coprinopsis cinerea (Coprinus cinereus). Proc Natl Acad Sci U S A 11889 11894
7. CelerinM
MerinoST
StoneJE
MenzieAM
ZolanME
2000 Multiple roles of Spo11 in meiotic chromosome behavior. Embo Journal 19 2739 2750
8. GereckeEE
ZolanME
2000 An mre11 mutant of Coprinus cinereus has defects in meiotic chromosome pairing, condensation and synapsis. Genetics 154 1125 1139
9. LiLB
GereckeEE
ZolanME
1999 Homolog pairing and meiotic progression in Coprinus cinereus. Chromosoma 108 384 392
10. MerinoST
CummingsWJ
AcharyaSN
ZolanME
2000 Replication-dependent early meiotic requirement for Spo11 and Rad50. Proc Natl Acad Sci U S A 97 10477 10482
11. SeitzLC
TangKL
CummingsWJ
ZolanME
1996 The rad9 gene of Coprinus cinereus encodes a proline-rich protein required for meiotic chromosome condensation and synapsis. Genetics 142 1105 1117
12. StassenNY
LogsdonJM
VoraGJ
OffenbergHH
PalmerJD
1997 Isolation and characterization of rad51 orthologs from Coprinus cinereus and Lycopersicon esculentum, and phylogenetic analysis of eukaryotic recA homologs. Current Genetics 31 144 157
13. Coprinus cinereus Sequencing Project. Broad Institute of MIT and Harvard (www.broad.mit.edu)
14. GathmanAC
LillyWW
Coprinopsis cinerea genome. Available: http://genome.semo.edu/ccin
15. SchlechtU
PrimigM
2003 Mining meiosis and gametogenesis with DNA microarrays. Reproduction 125 447 456
16. ChalmelF
LardenoisA
PrimigM
2007 Toward understanding the core meiotic transcriptome in mammals and its implications for somatic cancer. Testicular Chromosome Structure and Gene Expression 1120 1 15
17. ChuS
DeRisiJ
EisenM
MulhollandJ
BotsteinD
1998 The transcriptional program of sporulation in budding yeast. Science 282 699 705
18. PrimigM
WilliamsRM
WinzelerEA
TevzadzeGG
ConwayAR
2000 The core meiotic transcriptome in budding yeasts. Nature Genetics 26 415 423
19. MataJ
LyneR
BurnsG
BahlerJ
2002 The transcriptional program of meiosis and sporulation in fission yeast. Nature Genetics 32 143 147
20. CnuddeF
HedataleV
de JongH
PiersonES
RaineyDY
2006 Changes in gene expression during male meiosis in Petunia hybrida. Chromosome Research 14 919 932
21. CrismaniW
BaumannU
SuttonT
ShirleyN
WebsterT
2006 Microarray expression analysis of meiosis and microsporogenesis in hexaploid bread wheat. BMC Genomics 7 Available: http://www.biomedcentral.com/1471-2164/7/267. Accessed 2008 October 7
22. MaJ
DuncanD
MorrowDJ
FernandesJ
WalbotV
2007 Transcriptome profiling of maize anthers using genetic ablation to analyze pre-meiotic and tapetal cell types. Plant Journal 50 637 648
23. WangZ
LiangY
LiCJ
XuYY
LanLF
2005 Microarray analysis of gene expression involved in anther development in rice (Oryza sativa L.). Plant Molecular Biology 58 721 737
24. XiaQ
ChengD
DuanJ
WangG
ChengT
2007 Microarray-based gene expression profiles in multiple tissues of the domesticated silkworm, Bombyx mori. Genome Biol 8 R162
25. AndrewsJ
BouffardGG
CheadleC
LuJN
BeckerKG
2000 Gene discovery using computational and microarray analysis of transcription in the Drosophila melanogaster testis. Genome Research 10 2030 2043
26. ReinkeV
GilIS
WardS
KazmerK
2004 Genome-wide germline-enriched and sex-biased expression profiles in Caenorhabditis elegans. Development 131 311 323
27. ReinkeV
SmithHE
NanceJ
WangJ
Van DorenC
2000 A global profile of germline gene expression in C. elegans. Molecular Cell 6 605 616
28. SchlechtU
DemouginP
KochR
HermidaL
WiederkehrC
2004 Expression profiling of mammalian male meiosis and gametogenesis identifies novel candidate genes for roles in the regulation of fertility. Molecular Biology of the Cell 15 1031 1043
29. ChalmelF
RollandAD
Niederhauser-WiederkehrC
ChungSSW
DemouginP
2007 The conserved transcriptome in human and rodent male gametogenesis. Proc Natl Acad Sci U S A 104 8346 8351
30. JohnstonDS
WrightWW
DiCandeloroP
WilsonE
KopfGS
2008 Stage-specific gene expression is a fundamental characteristic of rat spermatogenic cells and Sertoli cells. Proc Natl Acad Sci U S A 105 8315 8320
31. PangALY
JohnsonW
RavindranathN
DymM
RennertOM
2006 Expression profiling of purified male germ cells: stage-specific expression patterns related to meiosis and postmeiotic development. Physiological Genomics 24 75 85
32. TaylorJW
BerbeeML
2006 Dating divergences in the Fungal Tree of Life: review and new analyses. Mycologia 98 838 849
33. BlairJE
2009 Fungi.
HedgesSB
KumarS
The Timetree of Life Oxford Oxford University Press 215 219
34. KuesU
2000 Life history and developmental processes in the basidiomycete Coprinus cinereus. Microbiology And Molecular Biology Reviews 64 316 353
35. WrobelG
PrimigM
2005 Mammalian male germ cells are fertile ground for expression profiling of sexual reproduction. Reproduction 129 1 7
36. MitchellAP
1994 Control of meiotic gene expression in Saccharomyces cerevisiae. Microbiological Reviews 58 56 70
37. RameshMA
MalikSB
LogsdonJM
2005 A phylogenomic inventory of meiotic genes: Evidence for sex in Giardia and an early eukaryotic origin of meiosis. Current Biology 15 185 191
38. MalikSB
PightlingAW
StefaniakLM
SchurkoAM
LogsdonJMJr
2008 An expanded inventory of conserved meiotic genes provides evidence for sex in Trichomonas vaginalis. PLoS ONE 3 e2879.
39. SaeedAI
SharovV
WhiteJ
LiJ
LiangW
2003 TM4: A free, open-source system for microarray data management and analysis. Biotechniques 34 374 378
40. HosackDA
DennisG
ShermanBT
LaneHC
LempickiRA
2003 Identifying biological themes within lists of genes with EASE. Genome Biology 4 R70
41. KandaT
ArakawaH
YasudaY
TakemaruT
1990 Basidiospore formation in a mutant of incompatibility factors and in mutants that arrest at meta-anaphase-I in Coprinus cinereus. Experimental Mycology 14 218 226
42. DiffleyJFX
LabibK
2002 The chromosome replication cycle. Journal of Cell Science 115 869 872
43. JuneauK
PalmC
MirandaM
DavisRW
2007 High-density yeast-tiling array reveals previously undiscovered introns and extensive regulation of meiotic splicing. Proc Natl Acad Sci U S A 104 1522 1527
44. MoldonA
MalapeiraJ
GabrielliN
GogolM
Gomez-EscodaB
2008 Promoter-driven splicing regulation in fission yeast. Nature 455 997 1001
45. KeeneyS
GirouxCN
KlecknerN
1997 Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88 375 384
46. HeywoodP
MageePT
1976 Meiosis in protists - some structural and physiological aspects of meiosis in algae, fungi, and protozoa. Bacteriological Reviews 40 190 240
47. ThomasG
2000 An encore for ribosome biogenesis in the control of cell proliferation. Nature Cell Biology 2 E71 E72
48. http://www.yeastgenome.org/
49. AshburnerM
BallCA
BlakeJA
BotsteinD
ButlerH
2000 Gene Ontology: tool for the unification of biology. Nature Genetics 25 25 29
50. AdkinsRM
GelkeEL
RoweD
HoneycuttRL
2001 Molecular phylogeny and divergence time estimates for major rodent groups: evidence from multiple genes. Mol Biol Evol 18 777 791
51. KleinF
MahrP
GalovaM
BuonomoSBC
MichaelisC
1999 A central role for cohesions in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 98 91 103
52. WatanabeY
NurseP
1999 Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature 400 461 464
53. YoungJA
HyppaRW
SmithGR
2004 Conserved and nonconserved proteins for meiotic DNA breakage and repair in yeasts. Genetics 167 593 605
54. AcharyaSN
ManyAM
SchroederAP
KennedyFM
SavytskyyOP
2008 Coprinus cinereus Rad50 mutants reveal an essential structural role for Rad50 in axial element and synaptonemal complex formation, homolog pairing and meiotic recombination. Genetics 180 1889 1907
55. LakeCM
TeeterK
PageSL
NielsenR
HawleyRS
2007 A genetic analysis of the Drosophila mcm5 gene defines a domain specifically required for meiotic recombination. Genetics 176 2151 2163
56. GertonJL
HawleyRS
2005 Homologous chromosome interactions in meiosis: Diversity amidst conservation. Nature Reviews Genetics 6 477 487
57. HwangSY
OhB
KnowlesBB
SolterD
LeeJS
2001 Expression of genes involved in mammalian meiosis during the transition from egg to embryo. Molecular Reproduction and Development 59 144 158
58. MataJ
BahlerJ
2003 Correlations between gene expression and gene conservation in fission yeast. Genome Research 13 2686 2690
59. RichardGF
KerrestA
LafontaineI
DujonB
2005 Comparative genomics of hemiascomycete yeasts: Genes involved in DNA replication, repair, and recombination. Molecular Biology and Evolution 22 1011 1023
60. SherwoodRK
BennettRJ
2009 Fungal meiosis and parasexual reproduction–lessons from pathogenic yeast. Current Opinion in Microbiology 12 599 607
61. SchurkoAM
LogsdonJMJr
2008 Using a meiosis detection toolkit to investigate ancient asexual “scandals” and the evolution of sex. Bioessays 30 579 589
62. SakaguchiK
KoshiyamaA
IwabataK
2007 Meiosis and small ubiquitin-related modifier (SUMO)-conjugating enzyme, Ubc9. Febs Journal 274 3519 3531
63. KoshiyamaA
HamadaFN
NamekawaSH
IwabataK
SugawaraH
2006 Sumoylation of a meiosis-specific RecA homolog, Lim15/Dmc1, via interaction with the small ubiquitin-related modifier (SUMO)-conjugating enzyme Ubc9. Febs Journal 273 4003 4012
64. MedinaPMB
2003 Isolation of genes required for meiotic synapsis in the basidiomycete Coprinus cinereus. Ph.D Thesis. Chapel Hill, University of North Carolina
65. BozdechZ
ZhuJC
JoachimiakMP
CohenFE
PulliamB
2003 Expression profiling of the schizont and trophozoite stages of Plasmodium falciparum with a long-oligonucleotide microarray. Genome Biology 4 Available: http://genomebiology.com/2003/4/2/R9. Accessed 2006 January 8
66. PearsonWR
LipmanDJ
1988 Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A 85 2444 2448
67. AltschulSF
GishW
MillerW
MyersEW
LipmanDJ
1990 Basic local alignment search tool. Journal of Molecular Biology 215 403 410
68. HeZL
WuLY
LiXY
FieldsMW
ZhouJZ
2005 Empirical establishment of oligonucleotide probe design criteria. Applied and Environmental Microbiology 71 3753 3760
69. MoreyJS
RyanJC
Van DolahFM
2006 Microarray validation: factors influencing correlation between oligonucleotide microarrays and real-time PCR. Biological Procedures Online 175 193
70. IwabataK
KoshiyamaA
YamaguchiT
SugawaraH
HamadaFN
2005 DNA topoisomerase II interacts with Lim15/Dmc1 in meiosis. Nucleic Acids Research 33 5809 5818
71. NamekawaS
IchijimaY
HamadaF
KasaiN
IwabataK
2003 DNA ligase IV from a basidiomycete, Coprinus cinereus, and its expression during meiosis. Microbiology-Sgm 149 2119 2128
72. NaraT
SakaT
SawadoT
TakaseH
ItoY
1999 Isolation of a Lim15/Dmc1 homolog from the basidiomycete Coprinus cinereus and its expression in relation to meiotic chromosome pairing. Molecular and General Genetics 262 781 789
73. YamaguchiT
NamekawaSH
HamadaFN
KasaiN
NaraT
2004 Expression of flap endonuclease-1 during meiosis in a basidiomycete, Coprinus cinereus. Fungal Genetics And Biology 41 493 500
74. ValentineG
WallaceYJ
TurnerFR
ZolanME
1995 Pathway analysis of radiation-sensitive meiotic mutants of Coprinus cinereus. Molecular & General Genetics 247 169 179
75. ZolanME
TremelCJ
PukkilaPJ
1988 Production and characterization of radiation-sensitive meiotic mutants of Coprinus cinereus. Genetics 120 379 387
76. GentlemanRC
CareyVJ
BatesDM
BolstadB
DettlingM
2004 Bioconductor: open software development for computational biology and bioinformatics. Genome Biology 5 Available http://genomebiology.com/2004/5/10/R80. Accessed 2007 June 23
77. FutschikME
CromptonT
2005 OLIN: optimized normalization, visualization and quality testing of two-channel microarray data. Bioinformatics 21 1724 1726
78. TusherVG
TibshiraniR
ChuG
2001 Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98 5116 5121
79. SoukasA
CohenP
SocciND
FriedmanJM
2000 Leptin-specific patterns of gene expression in white adipose tissue. Genes & Development 14 963 980
80. ErnstJ
VainasO
HarbisonCT
SimonI
Bar-JosephZ
2007 Reconstructing dynamic regulatory maps. Molecular Systems Biology 3 74
81. LiL
StoeckertCJJr
RoosDS
2003 OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Research 13 2178 2189
82. EnrightAJ
Van DongenS
OuzounisCA
2002 An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 30 1575 1584
83. van DongenS
2005 Graph clustering by flow simulation. Ph.D. Thesis. University of Utrecht, Netherlands
84. ChenF
MackeyAJ
VermuntJK
RoosDS
2007 Assessing performance of orthology detection strategies applied to eukaryotic genomes. PLoS ONE 2 e383.
85. PadmoreR
CaoL
KlecknerN
1991 Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell 66 1239 1256
86. HunterN
KlecknerN
2001 The single-end invasion: An asymmetric intermediate at the double-strand break to double-Holliday junction transition of meiotic recombination. Cell 106 59 70
87. BahlerJ
SchuchertP
GrimmC
KohliJ
1991 Synchronized meiosis and recombination in fission yeast - Observations with Pat1-114 diploid cells. Current Genetics 19 445 451
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