Applied Microbiology and Biotechnology

, Volume 97, Issue 10, pp 4235–4241 | Cite as

Alternative splicing in ascomycetes

Mini-Review

Abstract

Alternative splicing is a complex and regulated process, which results in mRNA with different coding capacities from a single gene. Extend and types of alternative splicing vary greatly among eukaryotes. In this review, I focus on alternative splicing in ascomycetes, which in general have significant lower extend of alternative splicing than mammals. Yeast-like species have low numbers of introns and consequently alternative splicing is lower compared to filamentous fungi. Several examples from single studies as well as from genomic scale analysis are presented, including a survey of alternative splicing in Neurospora crassa. Another focus is regulation by riboswitch RNA and alternative splicing in a heterologous system, along with putative protein factors involved in regulation.

Keywords

Regulation Extend and types of alternative splicing Ascomycetes Spliceosome 

Supplementary material

253_2013_4841_MOESM1_ESM.pdf (163 kb)
ESM 1(PDF 162 kb)

References

  1. Ast G (2004) How did alternative splicing evolve? Nat Rev Genet 5:773–782CrossRefGoogle Scholar
  2. Baba Y, Shimonaka A, Koga J, Kubota H, Kono T (2005) Alternative splicing produces two endoglucanases with one or two carbohydrate-binding modules in Mucor circinelloides. J Bacteriol 187:3045–3051CrossRefGoogle Scholar
  3. Barass JD, Beggs JD (2003) Splicing goes global. Trend Genet 19:295–298CrossRefGoogle Scholar
  4. Black DL (2003) Mechanisms of alternative pre-messenger RNA splicing. Ann Rev Biochem 72:291–336CrossRefGoogle Scholar
  5. Blencowe BJ (2006) Alternative splicing: new insights from global analyses. Cell 126:37–47CrossRefGoogle Scholar
  6. Blencowe BJ, Khanna M (2007) RNA in control. Nature 447:391–393CrossRefGoogle Scholar
  7. Boldo JT, Do Amaral KB, Junges A, Pinto PM, Staats CC, Vainstein MH, Schrank A (2010) Evidence of alternative splicing of the chi2 chitinase gene from Metarhizium anisopliae. Gene 462:1–7CrossRefGoogle Scholar
  8. Brunner M, Diernfellner A (2006) How temperature affects the circadian clock of Neurospora crassa. Chronobiol Internat 23:81–90CrossRefGoogle Scholar
  9. Calarco JA, Zhen M, Blencowe BJ (2011) Networking in a global world: establishing functional connections between neural splicing regulators and their target transcripts. RNA 17:775–791CrossRefGoogle Scholar
  10. Chang K-Y, Muddiman DC (2011) Identification of alternative splice variants in Aspergillus flavus through comparison of multiple tandem MS search algorithms. BMC Genomics 12:358CrossRefGoogle Scholar
  11. Chang K-Y, Georgianna DR, Heber S, Payne GA, Muddiman DC (2010) Detection of alternative splice variants at the proteome level in Aspergillus flavus. J Proteome Res 9:1209–1217CrossRefGoogle Scholar
  12. Cheah MT, Wachter A, Sudarsan N, Breaker RR (2007) Control of alternative RNA splicing and gene expression by eukaryotic riboswitches. Nature 447:497–500CrossRefGoogle Scholar
  13. Davis CA, Grate L, Spingola M, Ares M (2000) Test of intron predictions reveals novel splice sites, alternatively spliced mRNAs and new introns in meiotically regulated genes of yeast. Nucl Acids Res 28:1700–1706CrossRefGoogle Scholar
  14. Derr LK, Strathern JN (1993) A role for reverse transcripts in gene conversion. Nature 361:170–173CrossRefGoogle Scholar
  15. Dong S, Li C, Zenklusen D, Singer RH, Jacobson A, He F (2007) YRA1 autoregulation requires nuclear export and cytoplasmic Edc3p-mediated degradation of its pre-mRNA. Mol Cell 25:559–573CrossRefGoogle Scholar
  16. Eichinger L, Pachebat JA, Glöckner G, Rajandream M-A, Sucgang R, Berriman M, Song J, Olsen R, Szafranski K, Xu Q, Tunggal B, Kummerfeld S, Madera M, Konfortov BA, Rivero F, Bankier AT, Lehmann R, Hamlin N, Davies R, Gaudet P, Fey P, Pilcher K, Chen G, Saunders D, Sodergren E, Davis P, Kerhornou A, Nie X, Hall N, Anjard C, Hemphill L, Bason N, Farbrother P, Desany B, Just E, Morio T, Rost R, Churcher C, Cooper J, Haydock S, van Driessche N, Cronin A, Goodhead I, Muzny MT, Pain A, Lu M, Harper D, Lindsay R, Hauser H, James K, Quiles M, Madan Babu M, Saito T, Buchrieser C, Wardroper A, Felder M, Thangavelu M, Johnson D, Knights A, Loulseged H, Mungall K, Oliver K, Price C, Quail MA, Urushihara H, Hernandez J, Rabbinowitsch E, Steffen D, Sanders M, Ma J, Kohara Y, Sharp S, Simmonds M, Spiegler S, Tivey A, Sugano S, White B, Walker D, Woodward J, Winckler T, Tanaka Y, Shaulsky G, Schleicher M, Weinstock G, Rosenthal A, Cox EC, Chisholm RL, Gibbs R, Loomis WF, Platzer M, Kay RR, Williams J, Dear PH, Noegel AA, Barrell B, Kuspa A (2005) The genome of the social amoeba Dictyostelium discoideum. Nature 435:43–57CrossRefGoogle Scholar
  17. Engebrecht J, Voelkel-Meiman K, Roeder GS (1991) Meiosis-specific RNA splicing in yeast. Cell 66:1257–1268CrossRefGoogle Scholar
  18. Fink GR (1987) Pseudogenes in yeast? Cell 49:5–6CrossRefGoogle Scholar
  19. Freitag J, Ast J, Bölker M (2012) Cryptic peroxisomal targeting via alternative splicing and stop codon read-through in fungi. Nature 485:522–525CrossRefGoogle Scholar
  20. Galagan JE, Henn MR, Ma L-J, Cuomo CA, Birren B (2005) Genomics of the fungal kingdom: insights into eukaryotic biology. Genome Res 15:1620–1631CrossRefGoogle Scholar
  21. Habara Y, Urushiyama S, Tani T, Ohshima Y (1998) The fission yeast prp10(+) gene involved in pre-mRNA splicing encodes a homologue of highly conserved splicing factor, SAP155. Nucl Acids Res 26:5662–5669CrossRefGoogle Scholar
  22. Henscheid KL, Voelker RB, Berglund JA (2008) Alternative modes of binding by U2AF65 at the polypyrimidine tract. Biochem 47:449–459CrossRefGoogle Scholar
  23. Hoppins SC, Go NE, Klein A, Schmitt S, Neupert W, Rapaport D, Nargang FE (2007) Alternative splicing gives rise to different isoforms of the Neurospora crassa Tob55 protein that vary in their ability to insert beta-barrel proteins into the outer mitochondrial membrane. Genetics 177:137–149CrossRefGoogle Scholar
  24. Hoskins AA, Moore MJ (2012) The spliceosome: a flexible, reversible macromolecular machine. Trends Biochem Sci 37:179–188CrossRefGoogle Scholar
  25. Juneau K, Nislow C, Davies RW (2009) Alternative splicing of PTC7 in Saccharomyces cerevisiae determines protein localization. Genetics 183:185–194CrossRefGoogle Scholar
  26. Kabran P, Rossignol T, Gaillardin C, Nicaud J-M, Neuvéglise C (2012) Alternative splicing regulates targeting of malate dehydrogenase in Yarrowia lipolytica. DNA Res 19:231–244CrossRefGoogle Scholar
  27. Kempken F, Kück U (1996) Restless, an active Ac-like transposon from the fungus Tolypocladium inflatum: structure, expression, and alternative RNA splicing. Mol Cell Biol 16:6563–6572Google Scholar
  28. Kempken F, Windhofer F (2004) Alternative splicing of transcripts of transposon Restless is maintained in the foreign host Neurospora crassa and can be modified by introducing mutations at the splice sites. Curr Genet 46:59–65CrossRefGoogle Scholar
  29. Kornblihtt AR, Schor IE, Alló M, Dujardin G, Petrillo E, Muñoz MJ (2013) Alternative splicing: a pivotal step between eukaryotic transcription and translation. Nature Rev Mol Cell Biol 14:153–165CrossRefGoogle Scholar
  30. Kubodera T, Yamashita N, Nishimura A (2002) Transformation of Aspergillus sp. and Trichoderma reesei using the pyrithiamine resistance gene (ptrA) of Aspergillus oryzae. Biosci Biotechnol Biochem 66:404–406CrossRefGoogle Scholar
  31. Kuldau GA, Raju NB, Glass NL (1998) Repeat-induced point mutations in Pad-1, a putative RNA splicing factor from Neurospora crassa, confer dominant lethal effects on ascus development. Fungal Genet Biol 23:169–180CrossRefGoogle Scholar
  32. Leal J, Squina FM, Freitas JS, Silva EM, Ono CJ, Martinez-Rossi NM, Rossi A (2009) A splice variant of the Neurospora crassa hex-1 transcript, which encodes the major protein of the Woronin body, is modulated by extracellular phosphate and pH changes. FEBS Lett 583:180–184CrossRefGoogle Scholar
  33. Lev-Maor G, Sorek R, Shomron N, Ast G (2003) The birth of an alternatively spliced exon: 3′ splice-site selection in Alu exons. Science 300:1288–1291CrossRefGoogle Scholar
  34. Li S, Breaker RR (2013) Eukaryotic TPP riboswitch regulation of alternative splicing involving long-distance base pairing. Nucl Acids Res. doi:10.1093/nar/gkt057 Google Scholar
  35. Marquez Y, Brown JWS, Simpson C, Barta A, Kalyna M (2012) Transcriptome survey reveals increased complexity of the alternative splicing landscape in Arabidopsis. Genome Res 22:1184–1195CrossRefGoogle Scholar
  36. Mekouar M, Blanc-Lenfle I, Ozanne C, Da Silva C, Cruaud C, Wincker P, Gaillardin C, Neuvéglise C (2010) Detection and analysis of alternative splicing in Yarrowia lipolytica reveal structural constraints facilitating nonsense-mediated decay of intron-retaining transcripts. Genome Biol 11:R65CrossRefGoogle Scholar
  37. Meyer M, Plass M, Pérez-Valle J, Eyras E, Vilardell J (2011) Deciphering 3′ss selection in the yeast genome reveals an RNA thermosensor that mediates alternative splicing. Mol Cell 43:1033–1039CrossRefGoogle Scholar
  38. Mitrovich QM, Tuch BB, Guthrie C, Johnson AD (2007) Computational and experimental approaches double the number of known introns in the pathogenic yeast Candida albicans. Genome Res 17:492–502CrossRefGoogle Scholar
  39. Miura F, Kawaguchi N, Sese J, Toyoda A, Hattori M, Morishita S, Ito T (2006) A large-scale full-length cDNA analysis to explore the budding yeast transcriptome. Proc Natl Acad Sci 103:17846–17851CrossRefGoogle Scholar
  40. Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, Gerstein M, Snyder M (2008) The transcriptional landscape of the yeast genome defined by RNA sequencing. Science 320:1344–1349CrossRefGoogle Scholar
  41. Nakawaga T, Ogawa H (1999) The Saccharomyces cerevisiae MER3 gene, encoding a novel helicase-like protein, is required for crossover control in meiosis. EMBO J 18:5714–5733CrossRefGoogle Scholar
  42. Neuvéglise C, Marck C, Gaillardin C (2011) The intronome of budding yeasts. Comptes Rendus Biologies 334:662–670CrossRefGoogle Scholar
  43. Park G, Servin JA, Turner GE, Altamirano L, Colot HV, Collopy P, Litvinkova L, Li L, Jones CA, Diala F-G, Dunlap JC, Borkovich KA (2011) Global analysis of serine-threonine protein kinase genes in Neurospora crassa. Euk Cell 10:1553–1564CrossRefGoogle Scholar
  44. Patel AA, Steitz JA (2003) Splicing double: insights from the second spliceosome. Nature Rev Mol Cell Biol 4:960–970CrossRefGoogle Scholar
  45. Plass M, Codony-Servat C, Ferreira PG, Vilardell J, Eyras E (2012) RNA secondary structure mediates alternative 3′ss selection in Saccharomyces cerevisiae. RNA 18:1103–1115CrossRefGoogle Scholar
  46. Preker PJ, Guthrie C (2012) Autoregulation of the mRNA export factor Yra1p requires inefficient splicing of its pre-mRNA. RNA 12:994–1006CrossRefGoogle Scholar
  47. Ramani AK, Calarco JA, Pan Q, Mavandadi S, Wang Y, Nelson AC, Lee LJ, Morris Q, Blencowe BJ, Zhen M, Fraser AG (2011) Genome-wide analysis of alternative splicing in Caenorhabditis elegans. Genome Res 21:342–348CrossRefGoogle Scholar
  48. Rep M, Duyvesteijn RGE, Gale L, Usgaard T, Cornelissen BJC, Ma L-J, Ward TJ (2006) The presence of GC-AG introns in Neurospora crassa and other euascomycetes determined from analyses of complete genomes: implications for automated gene prediction. Genomics 87:338–347CrossRefGoogle Scholar
  49. Sugnet CW, Kent WJ, Ares M, Haussler D (2004) Transcriptome and genome conservation of alternative splicing events in humans and mice. Pacific Symp Biocomp 66–77Google Scholar
  50. Tenney K, Hunt I, Sweigard J, Pounder JI, McClain C, Bowman EJ, Bowman BJ (2000) Hex-1, a gene unique to filamentous fungi, encodes the major protein of the Woronin body and functions as a plug for septal pores. Fungal Genet Biol 31:205–217CrossRefGoogle Scholar
  51. Tey WK, North AJ, Reyes JL, Lu Y, Jedd G (2005) Polarized gene expression determines Woronin body formation at the leading edge of the fungal colony. Mol Biol Cell 16:2651–2659CrossRefGoogle Scholar
  52. Trevisan GL, Oliveira EHD, Peres NTA, Cruz AHS, Martinez-Rossi NM, Rossi A (2011) Transcription of Aspergillus nidulans pacC is modulated by alternative RNA splicing of palB. FEBS Lett 585:3442–3445CrossRefGoogle Scholar
  53. Vilardell J, Chartrand P, Singer RH, Warner JR (2000) The odyssey of a regulated transcript. RNA 6:1773–1780CrossRefGoogle Scholar
  54. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB (2008) Alternative isoform regulation in human tissue transcriptomes. Nature 456:470–476CrossRefGoogle Scholar
  55. Will CL, Lührmann R (2005) Splicing of a rare class of introns by the U12-dependent spliceosome. Biol Chem 386:713–724CrossRefGoogle Scholar
  56. Windhofer F, Catcheside DEA, Kempken F (2000) Methylation of the foreign transposon Restless in vegetative mycelia of Neurospora crassa. Curr Genet 37:194–199CrossRefGoogle Scholar
  57. Yu B, Fey P, Kestin-Pilcher KE, Fedorov A, Prakash A, Chisholm RL, Wu JY (2011) Spliceosomal genes in the D. discoideum genome: a comparison with those in H. sapiens, D. melanogaster, A. thaliana and S. cerevisiae. Protein Cell 2:395–409CrossRefGoogle Scholar
  58. Zhang M-Y, Miyake T (2009) Development and media regulate alternative splicing of a methyltransferase pre-mRNA in Monascus pilosus. J Agricult Food Chem 57:4162–4167CrossRefGoogle Scholar
  59. Zhao C, Waalwijk C, de Wit PJGM, Tang D, van der Lee T (2013) RNA-Seq analysis reveals new gene models and alternative splicing in the fungal pathogen Fusarium graminearum. BMC Genomics 14:21CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  1. 1.Abteilung für Botanische Genetik und Molekularbiologie, Botanisches Institut und Botanischer GartenChristian-Albrechts-Universität zu KielKielGermany

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