Examining the condition-specific antisense transcription in S. cerevisiae and S. paradoxus

BMC Genomics

Daryi Wang¹  Chuen-Yi Wang¹  Ming-Ren Yen¹  Chih-Hsu Lin¹  Krishna B S Swamy¹ 

[1] Biodiversity Research Center, Academia Sinica, Taipei 115, Taiwan

关键词: Stress;    Budding yeast;    Evolution;    Antisense RNA;   

Others  :  857030
DOI  :  10.1186/1471-2164-15-521

 received in 2013-12-16, accepted in 2014-06-19,  发布年份 2014

【 摘 要 】

Background

Recent studies have demonstrated that antisense transcription is pervasive in budding yeasts and is conserved between Saccharomyces cerevisiae and S. paradoxus. While studies have examined antisense transcripts of S. cerevisiae for inverse expression in stationary phase and stress conditions, there is a lack of comprehensive analysis of the conditional specific evolutionary characteristics of antisense transcription between yeasts. Here we attempt to decipher the evolutionary relationship of antisense transcription of S. cerevisiae and S. paradoxus cultured in mid log, early stationary phase, and heat shock conditions.

Results

Massively parallel sequencing of sequence strand-specific cDNA library was performed from RNA isolated from S. cerevisiae and S. paradoxus cells at mid log, stationary phase and heat shock conditions. We performed this analysis using a stringent set of sense ORF transcripts and non-coding antisense transcripts that were expressed in all the three conditions, as well as in both species. We found the divergence of the condition-specific anti-sense transcription levels is higher than that in condition-specific sense transcription levels, suggesting that antisense transcription played a potential role in adapting to different conditions. Furthermore, 43% of sense-antisense pairs demonstrated inverse expression in either stationary phase or heat shock conditions relative to the mid log conditions. In addition, a large part of sense-antisense pairs (67%), which demonstrated inverse expression, were highly conserved between the two species. Our results were also concordant with known functional analyses from previous studies and with the evidence from mechanistic experiments of role of individual genes.

Conclusions

By performing a genome-scale computational analysis, we have tried to evaluate the role of antisense transcription in mediating sense transcription under different environmental conditions across and in two related yeast species. Our findings suggest that antisense regulation could control expression of the corresponding sense transcript via inverse expression under a range of different circumstances.

【 授权许可】

   
2014 Swamy et al.; licensee BioMed Central Ltd.

【 图 表 】

【 参考文献 】

• [1]Lasa I, Toledo-Arana A, Dobin A, Villanueva M, de los Mozos IR, Vergara-Irigaray M, Segura V, Fagegaltier D, Penades JR, Valle J, Solano C, Gingeras TR: Genome-wide antisense transcription drives mRNA processing in bacteria. Proc Natl Acad Sci U S A 2011, 108(50):20172-20177.
• [2]Lasa I, Toledo-Arana A, Gingeras TR: An effort to make sense of antisense transcription in bacteria. RNA Biol 2012, 9(8):1039-1044.
• [3]Raghavan R, Sloan DB, Ochman H: Antisense transcription is pervasive but rarely conserved in enteric bacteria. mBio 2012, 3(4):e00156-12.
• [4]Munroe SH, Zhu J: Overlapping transcripts, double-stranded RNA and antisense regulation: a genomic perspective. Cell Mol Life Sci 2006, 63(18):2102-2118.
• [5]Dinger ME, Amaral PP, Mercer TR, Mattick JS: Pervasive transcription of the eukaryotic genome: functional indices and conceptual implications. Brief Funct Genomic Proteomic 2009, 8(6):407-423.
• [6]Faghihi MA, Wahlestedt C: Regulatory roles of natural antisense transcripts. Nat Rev Mol Cell Biol 2009, 10(9):637-643.
• [7]Nishizawa M, Okumura T, Ikeya Y, Kimura T: Regulation of inducible gene expression by natural antisense transcripts. Front Biosci 2012, 17:938-958.
• [8]Yassour M, Pfiffner J, Levin JZ, Adiconis X, Gnirke A, Nusbaum C, Thompson DA, Friedman N, Regev A: Strand-specific RNA sequencing reveals extensive regulated long antisense transcripts that are conserved across yeast species. Genome Biol 2010, 11(8):R87.
• [9]Numata K, Kiyosawa H: Genome-wide impact of endogenous antisense transcripts in eukaryotes. Front Biosci 2012, 17:300-315.
• [10]Sun M, Hurst LD, Carmichael GG, Chen J: Evidence for variation in abundance of antisense transcripts between multicellular animals but no relationship between antisense transcriptionand organismic complexity. Genome Res 2006, 16(7):922-933.
• [11]Zubko E, Kunova A, Meyer P: Sense and antisense transcripts of convergent gene pairs in Arabidopsis thaliana can share a common polyadenylation region. PLoS One 2011, 6(2):e16769.
• [12]Dahary D, Elroy-Stein O, Sorek R: Naturally occurring antisense: transcriptional leakage or real overlap? Genome Res 2005, 15(3):364-368.
• [13]David L, Huber W, Granovskaia M, Toedling J, Palm CJ, Bofkin L, Jones T, Davis RW, Steinmetz LM: A high-resolution map of transcription in the yeast genome. Proc Natl Acad Sci U S A 2006, 103(14):5320-5325.
• [14]Hongay CF, Grisafi PL, Galitski T, Fink GR: Antisense transcription controls cell fate in Saccharomyces cerevisiae. Cell 2006, 127(4):735-745.
• [15]Camblong J, Iglesias N, Fickentscher C, Dieppois G, Stutz F: Antisense RNA stabilization induces transcriptional gene silencing via histone deacetylation in S. cerevisiae. Cell 2007, 131(4):706-717.
• [16]Bodi Z, Button JD, Grierson D, Fray RG: Yeast targets for mRNA methylation. Nucleic Acids Res 2010, 38(16):5327-5335.
• [17]Houseley J, Rubbi L, Grunstein M, Tollervey D, Vogelauer M: A ncRNA modulates histone modification and mRNA induction in the yeast GAL gene cluster. Mol Cell 2008, 32(5):685-695.
• [18]Goodman AJ, Daugharthy ER, Kim J: Pervasive antisense transcription is evolutionarily conserved in budding yeast. Mol Biol Evol 2013, 30(2):409-421.
• [19]Chen J, Sun M, Hurst LD, Carmichael GG, Rowley JD: Genome-wide analysis of coordinate expression and evolution of human cis-encoded sense-antisense transcripts. Trends Genet 2005, 21(6):326-329.
• [20]Lin CH, Tsai ZT, Wang D: Role of antisense RNAs in evolution of yeast regulatory complexity. Genomics 2013, 102(5–6):484-490.
• [21]Rhind N, Chen Z, Yassour M, Thompson DA, Haas BJ, Habib N, Wapinski I, Roy S, Lin MF, Heiman DI, Young SK, Furuya K, Guo Y, Pidoux A, Chen HM, Robbertse B, Goldberg JM, Aoki K, Bayne EH, Berlin AM, Desjardins CA, Dobbs E, Dukaj L, Fan L, FitzGerald MG, French C, Gujja S, Hansen K, Keifenheim D, Levin JZ, et al.: Comparative functional genomics of the fission yeasts. Science 2011, 332(6032):930-936.
• [22]Lapidot M, Pilpel Y: Genome-wide natural antisense transcription: coupling its regulation to its different regulatory mechanisms. EMBO Rep 2006, 7(12):1216-1222.
• [23]Parkhomchuk D, Borodina T, Amstislavskiy V, Banaru M, Hallen L, Krobitsch S, Lehrach H, Soldatov A: Transcriptome analysis by strand-specific sequencing of complementary DNA. Nucleic Acids Res 2009, 37(18):e123.
• [24]Levin JZ, Yassour M, Adiconis X, Nusbaum C, Thompson DA, Friedman N, Gnirke A, Regev A: Comprehensive comparative analysis of strand-specific RNA sequencing methods. Nat Methods 2010, 7(9):709-715.
• [25]Langmead B, Trapnell C, Pop M, Salzberg SL: Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009, 10(3):R25.
• [26]Trapnell C, Pachter L, Salzberg SL: TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009, 25(9):1105-1111.
• [27]Liti G, Carter DM, Moses AM, Warringer J, Parts L, James SA, Davey RP, Roberts IN, Burt A, Koufopanou V, Tsai IJ, Bergman CM, Bensasson D, O’Kelly MJ, van Oudenaarden A, Barton DB, Bailes E, Nguyen AN, Jones M, Quail MA, Goodhead I, Sims S, Smith F, Blomberg A, Durbin R, Louis EJ: Population genomics of domestic and wild yeasts. Nature 2009, 458(7236):337-341.
• [28]Yang L, Duff MO, Graveley BR, Carmichael GG, Chen LL: Genomewide characterization of non-polyadenylated RNAs. Genome Biol 2011, 12(2):R16.
• [29]Grate L, Ares M Jr: Searching yeast intron data at Ares lab Web site. Methods Enzymol 2002, 350:380-392.
• [30]Murray SC, Serra Barros A, Brown DA, Dudek P, Ayling J, Mellor J: A pre-initiation complex at the 3′-end of genes drives antisense transcription independent of divergent sense transcription. Nucleic Acids Res 2012, 40(6):2432-2444.
• [31]Katayama S, Tomaru Y, Kasukawa T, Waki K, Nakanishi M, Nakamura M, Nishida H, Yap CC, Suzuki M, Kawai J, Suzuki H, Carninci P, Hayashizaki Y, Wells C, Frith M, Ravasi T, Pang KC, Hallinan J, Mattick J, Hume DA, Lipovich L, Batalov S, Engström PG, Mizuno Y, Faghihi MA, Sandelin A, Chalk AM, Mottagui-Tabar S, Liang Z, Lenhard B: Antisense transcription in the mammalian transcriptome. Science 2005, 309(5740):1564-1566.
• [32]Kiyosawa H, Yamanaka I, Osato N, Kondo S, Hayashizaki Y: Antisense transcripts with FANTOM2 clone set and their implications for gene regulation. Genome Res 2003, 13(6B):1324-1334.
• [33]Chen J, Sun M, Kent WJ, Huang X, Xie H, Wang W, Zhou G, Shi RZ, Rowley JD: Over 20% of human transcripts might form sense-antisense pairs. Nucleic Acids Res 2004, 32(16):4812-4820.
• [34]Sun M, Hurst LD, Carmichael GG, Chen J: Evidence for a preferential targeting of 3′-UTRs by cis-encoded natural antisense transcripts. Nucleic Acids Res 2005, 33(17):5533-5543.
• [35]Chechik G, Oh E, Rando O, Weissman J, Regev A, Koller D: Activity motifs reveal principles of timing in transcriptional control of the yeast metabolic network. Nat Biotechnol 2008, 26(11):1251-1259.
• [36]Xu Z, Wei W, Gagneur J, Perocchi F, Clauder-Munster S, Camblong J, Guffanti E, Stutz F, Huber W, Steinmetz LM: Bidirectional promoters generate pervasive transcription in yeast. Nature 2009, 457(7232):1033-1037.
• [37]Xu Z, Wei W, Gagneur J, Clauder-Munster S, Smolik M, Huber W, Steinmetz LM: Antisense expression increases gene expression variability and locus interdependency. Mol Syst Biol 2011, 7:468.
• [38]Tirosh I, Weinberger A, Carmi M, Barkai N: A genetic signature of interspecies variations in gene expression. Nat Genet 2006, 38(7):830-834.
• [39]Nishizawa M, Komai T, Katou Y, Shirahige K, Ito T, Toh EA: Nutrient-regulated antisense and intragenic RNAs modulate a signal transduction pathway in yeast. PLoS Biol 2008, 6(12):2817-2830.
• [40]Wapinski I, Pfeffer A, Friedman N, Regev A: Automatic genome-wide reconstruction of phylogenetic gene trees. Bioinformatics 2007, 23(13):i549-i558.
• [41]Hunter S, Jones P, Mitchell A, Apweiler R, Attwood TK, Bateman A, Bernard T, Binns D, Bork P, Burge S, de Castro E, Coggill P, Corbett M, Das U, Daugherty L, Duquenne L, Finn RD, Fraser M, Gough J, Haft D, Hulo N, Kahn D, Kelly E, Letunic I, Lonsdale D, Lopez R, Madera M, Maslen J, McAnulla C, McDowall J, et al.: InterPro in 2011: new developments in the family and domain prediction database. Nucleic Acids Res 2012, 40(Database issue):D306-D312.
• [42]Iwase M, Toh-e A: Nis1 encoded by YNL078W: a new neck protein of Saccharomyces cerevisiae. Genes Genet Syst 2001, 76(5):335-343.
• [43]Makhnevych T, Lusk CP, Anderson AM, Aitchison JD, Wozniak RW: Cell cycle regulated transport controlled by alterations in the nuclear pore complex. Cell 2003, 115(7):813-823.
• [44]Matsufuji Y, Fujimura S, Ito T, Nishizawa M, Miyaji T, Nakagawa J, Ohyama T, Tomizuka N, Nakagawa T: Acetaldehyde tolerance in Saccharomyces cerevisiae involves the pentose phosphate pathway and oleic acid biosynthesis. Yeast 2008, 25(11):825-833.
• [45]Suzuki T, Sugiyama M, Wakazono K, Kaneko Y, Harashima S: Lactic-acid stress causes vacuolar fragmentation and impairs intracellular amino-acid homeostasis in Saccharomyces cerevisiae. J Biosci Bioeng 2012, 113(4):421-430.
• [46]Tkach JM, Yimit A, Lee AY, Riffle M, Costanzo M, Jaschob D, Hendry JA, Ou J, Moffat J, Boone C, Davis TN, Nislow C, Brown GW: Dissecting DNA damage response pathways by analysing protein localization and abundance changes during DNA replication stress. Nat Cell Biol 2012, 14(9):966-976.
• [47]Ashrafi K, Farazi TA, Gordon JI: A role for Saccharomyces cerevisiae fatty acid activation protein 4 in regulating protein N-myristoylation during entry into stationary phase. J Biol Chem 1998, 273(40):25864-25874.
• [48]Hirata Y, Andoh T, Asahara T, Kikuchi A: Yeast glycogen synthase kinase-3 activates Msn2p-dependent transcription of stress responsive genes. Mol Biol Cell 2003, 14(1):302-312.
• [49]Martin DE, Soulard A, Hall MN: TOR regulates ribosomal protein gene expression via PKA and the Forkhead transcription factor FHL1. Cell 2004, 119(7):969-979.
• [50]Daignan-Fornier B, Nguyen CC, Reisdorf P, Lemeignan B, Bolotin-Fukuhara M: MBR1 and MBR3, two related yeast genes that can suppress the growth defect of hap2, hap3 and hap4 mutants. Mol Gen Genet 1994, 243(5):575-583.
• [51]Werner-Washburne M, Braun E, Johnston GC, Singer RA: Stationary phase in the yeast Saccharomyces cerevisiae. Microbiol Rev 1993, 57(2):383-401.
• [52]Barnes CA, Johnston GC, Singer RA: Thermotolerance is independent of induction of the full spectrum of heat shock proteins and of cell cycle blockage in the yeast Saccharomyces cerevisiae. J Bacteriol 1990, 172(8):4352-4358.
• [53]Finkelstein DB, Strausberg S, McAlister L: Alterations of transcription during heat shock of Saccharomyces cerevisiae. J Biol Chem 1982, 257(14):8405-8411.
• [54]Lavorgna G, Dahary D, Lehner B, Sorek R, Sanderson CM, Casari G: In search of antisense. Trends Biochem Sci 2004, 29(2):88-94.