Skip to main content

3 RNAi Function and Diversity in Fungi

  • Chapter
  • First Online:
Biochemistry and Molecular Biology

Part of the book series: The Mycota ((MYCOTA,volume III))

Abstract

The RNA interference (RNAi) phenomenon is taxonomically widely distributed among eukaryotes and has been found in fungi, plants, and animals, suggesting that it was already present very early in eukaryotic evolution. Genes for the three core components Dicer, Argonaute, and RNA-dependent RNA polymerase (RdRP) have been found in most fungal genomes analyzed to date, with a few exceptions. It has been suggested that the ancestral RNAi primarily had a function in defense against viruses and transposons, but a role in gene regulation is a possibility. In this chapter, RNAi functions in three main processes; genome defense, heterochromatin formation, and gene regulation are discussed. Dicer, Argonaute, and RdRP control the biogenesis of the various regulatory small interfering RNAs (siRNAs). The Dicer, an RNase III endonuclease, processes the pre-RNA to form the siRNA. The mature siRNA is then incorporated into a multiprotein complex referred to as the RNA-induced Silencing Complex (RISC) in which Argonaute is the core protein. Argonaute functions as a siRNA-guided endonuclease in the RISC. RISC then recognizes mRNAs with complementary sequence to the engaged siRNA. An RdRP then generates dsRNA from single-stranded transcripts either by de novo, primer-independent second-strand synthesis or by the use of siRNA as primers to synthesize RNA complementary to the target mRNA resulting in the production and amplification of dsRNA as well as silencing of the target gene. However, it seems to be an unlimited number of variation and species-specific differences of the mechanisms, and the more systems that are explored the more mechanisms are revealed of which a few are presented in detail here.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

aRNA:

Aberrant RNA

DdRP:

DNA-dependent RNA polymerase

dsRNA:

Double-stranded DNA

miRNA:

microRNA

milRNAs:

microRNA-like small RNAs

MSUD:

Meiotic Silencing by Unpaired DNA

PTGS:

Posttranscriptional gene silencing

qiRNA:

QDE-2-interacting small RNAs

RdRP:

RNA-dependent RNA polymerase

RISC:

RNA-induced silencing complex

RNAi:

RNA interference

SIS:

Sex-induced silencing

siRNAs:

small interfering RNAs

snRNA:

small nuclear RNA

References

  • Alexander WG, Raju NB, Xiao H, Hammond TM, Predue TD et al (2008) DCL-1 colocalizes with other components of the MSUD machinery and is required for silencing. Fungal Genet Biol 45:719–727

    Article  CAS  PubMed  Google Scholar 

  • Allen E, Howell MD (2010) miRNAs in the biogenesis of trans-acting siRNAs in higher plants. Semin Cell Dev Biol 21:798–804

    Article  CAS  PubMed  Google Scholar 

  • Ambros V (2004) The function of animal microRNAs. Nature 431:350–355

    Article  CAS  PubMed  Google Scholar 

  • Aramayo R, Metzenberg RL (1996) Meiotic transvection in fungi. Cell 86:103–113

    Article  CAS  PubMed  Google Scholar 

  • Archer DB, Mackenzie DA, Jeenes DJ, Roberts IN (1992) Proteolytic degradation of heterologous protein expressed in Aspergillus niger. Biotechnol Lett 14:357–362

    Article  CAS  Google Scholar 

  • Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:203–207

    Article  Google Scholar 

  • Bayne EH, White SA, Kagansky A, Bijos D, Sanchez-Pulido L, Hoe K-L, Kim D-U, Park H-O, Ponting CP, Rappsilber J, Allshire RC (2010) Stc1: A critical link between RNAi and chromatin modification required for heterochromatin integrity. Cell 140:666–677

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Billmyre RB, Calo S, Feretzaki M, Wang X, Heitman J (2013) RNAi function, diversity, and loss in the fungal kingdom. Chromosome Res 21:561–572

    Article  CAS  PubMed  Google Scholar 

  • Catalanotto C, Pallotta M, ReFalo P, Sachs MS, Vayssie L et al (2004) Redundancy of the two Dicer genes in transgene-induced posttranscriptional gene silencing in Neurospora crassa. Mol Biol 24:2536–2545

    CAS  Google Scholar 

  • Chang S, Zhang Z, Liu Y (2012) RNA interference pathways in fungi: mechanisms and function. Annu Rev Microbiol 66:305–323

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cogoni C, Macino G (1997) Conservation of transgene-induced post-transcriptional gene silencing in plants and fungi. Trends Plant Sci 2:205–443

    Article  Google Scholar 

  • Cogoni C, Macino G (1999) Gene silencing in Neurospora crassa requires a protein homologous to RNA-dependent RNA polymerase. Nature 399:166–169

    Article  CAS  PubMed  Google Scholar 

  • Cogoni C, Irelan JT, Schumacher M, Schmidhauser TJ, Selker EU, Macino G (1996) Transgene silencing of the al-1 gene in vegetative cells of Neurospora is mediated by a cytoplasmic effector and does not depend on DNA-DNA interactions or DNA methylation. EMBO J 15:3153–3163

    PubMed Central  CAS  PubMed  Google Scholar 

  • Dang Y, Yang Q, Xue Z, Liu Y (2011) RNA interference in fungi: pathways, functions, and applications. Eukaryotic Cell 10:1148–1155

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • David L, Huber W, Granovskaia M, Toedling J, Palm CJ, Bofkin L et al (2006) A high-resolution map of transcription in the yeast genome. Proc Natl Acad Sci USA 103:5320–5325

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dean R, Van Kan JAL, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430

    Article  PubMed  Google Scholar 

  • Donaldson ME, Saville BJ (2012) Natural antisense transcripts in fungi. Mol Microbiol 85:405–417

    Article  CAS  PubMed  Google Scholar 

  • Drinnenberg IA, Weinberg DE, Xie KT, Mower JP, Wolf KH, Fink GR, Bartel DP (2009) RNAi in budding yeast. Science 333:544–550

    Article  Google Scholar 

  • Drinnenberg IA, Fink GR, Bartel DP (2011) Compatibility with killer explains the rise of RNAi-deficient fungi. Science 333:1592

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391:806–811

    Article  CAS  PubMed  Google Scholar 

  • Grewal SIS, Jia S (2007) Heterochromatin revisited. Nat Rev Genet 8:35–46

    Article  CAS  PubMed  Google Scholar 

  • Griffiths-Jones S, Grocock RJ, van Dongen S, Bateman A, Enright AJ (2006) miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res 34(Database issue):D140–D144

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gullerova M, Moazed D, Proudfoot NJ (2011) Autoregulation of convergent RNAi genes in fission yeast. Genes Dev 25:556–568

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hammond TM, Xiao H, Boone EC, Predue TD, Pukkila PJ, Shiu PK (2011) SAD-3, a putative helicase required for meiotic silencing by unpaired DNA, interacts with the other components of the silencing machinery. Genes Genomes Genet 1:369–376

    CAS  Google Scholar 

  • Hammond TM, Xiao H, Boone EC, Decker LM, Lee SA, Predue TD, Pukkila PJ, Shiu PK (2013) Novel proteins required for meiotic silencing by unpaired DNA and siRNA generation in Neurospora crassa. Genetics 194:91–100

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • He L, Hannon GJ (2004) MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5:522–531

    Article  CAS  PubMed  Google Scholar 

  • Hu Y, Stenlid J, Elfstrand M, Olson Å (2013) Evolution of RNA interferance proteins dicer and argonaute in Basidiomycota. Mycologia 105:1489–1498

    Article  CAS  PubMed  Google Scholar 

  • Idnurm AYS, Bahn K, Nielsen K, Lin X, Fraser JA et al (2005) Deciphering the model pathogenic fungus Cryptococcus neoformans. Nat Rev Microbiol 3:753–764

    Article  CAS  PubMed  Google Scholar 

  • Janbon G, Maeng S, Yang D-H, Ko Y-J, Jung K-W, Moyrand F, Floyd A, Heitman J, Bahn Y-S (2010) Characterizing the role of RNA silencing components in Cryptococcus neoformans. Fungal Genet Biol 47:1070–1080

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kato H, Goto DB, Martienssen RA, Urano T, Furukawa K, Marakami Y (2005) RNA polymerase II is required for RNAi-dependent heterochromatin assembly. Science 309:467–469

    Article  CAS  PubMed  Google Scholar 

  • Kellis M, Wold B, Snyder MP, Berstein BE, Kundaje A (2014) Defining functional DNA elements in the human genome. PNAS 111:6131–6138

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Kemppainen MJ, Pardo AG (2010) pHg/pSILBAgamma vector system for efficient gene silencing in homobasidiomycetes: optimization of ihpRNA-triggering in mycorrhizal fungus Laccaria bicolor. Microb Biotechnol 3:178–200

    Article  PubMed Central  PubMed  Google Scholar 

  • Kemppainen MJ, Duplessis S, Martin F, Pardo AG (2009) RNA silencing in the model mycorrhizal fungus Laccaria bicolor: gene knock-down of nitrate reductase in inhibition of symbiosis with Populus. Environ Microbiol 11:1878–1896

    Article  CAS  PubMed  Google Scholar 

  • Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst AO, Landthaler M, Lin C, Socci ND, Hermida L, Fulci V, Chiaretti S, Foà R, Schliwka J, Fuchs U, Novosel A, Müller RU, Schermer B, Bissels U, Inman J, Phan Q, Chien M, Weir DB, Choksi R, De Vita G, Frezzetti D, Trompeter HI, Hornung V, Teng G, Hartmann G, Palkovits M, Di Lauro R, Wernet P, Macino G, Rogler CE, Nagle JW, Ju J, Papavasiliou FN, Benzing T, Lichter P, Tam W, Brownstein MJ, Bosio A, Borkhardt A, Russo JJ, Sander C, Zavolan M, Tuschl T (2007) A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129:1401–1414

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854

    Article  CAS  PubMed  Google Scholar 

  • Lee DW, Pratt RJ, McLaughlin M, Aramayo R (2003) An Argonaute-like protein is required for meiotic silencing. Genetics 164:821–828

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lee HC, Chang SS, Choudhary S, Aalto AP, Maiti M et al (2009) qiRNA is a new type of small interfering RNA induced by DNA damage. Nature 459:274–277

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lee HC, Aalto AP, Yang Q, Chang SS, Huang G et al (2010a) The DNA/RNA-dependent RNA polymerase QDE-1 generates aberrant RNA and dsRNA for RNAi in a process requiring replication protein A and a DNA helicase. PLoS Biol 8:e1000496

    Article  PubMed Central  PubMed  Google Scholar 

  • Lee HC, Li L, Gu W, Xue Z, Crosthwaite SK, Pertsemlidis A, Lewis ZA, Freitag M, Selker EU, Mello CC, Liu Y (2010b) Diverse pathways generate MicroRNA-like RNAs and dicer-independent small interfering RNAs in fungi. Mol Cell 38:803–814

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Llave C, Kasschau KD, Rector MA, Carrington JC (2002) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14:16051619

    Article  Google Scholar 

  • Machida M, Yamada O, Gomi K (2008) Genomics of Aspargillus oryzae: learning from the history of koji mold and exploration of its future. DNA Res 15:173–183

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Maiti M, Lee HC, Liu Y (2007) QIP, a putative exonuclease, interacts with the Neurospora Argonaute protein and facilitates conversion of duplex siRNA into single strands. Genes Dev 21:590–600

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Molnar A, Schwach F, Studholme DJ, Thuenemann EC, Baulcombe DC (2007) miRNAs control gene expression in the single-cell alga Chlamydomonas reinhardtii. Nature 447:1126–1129

    Article  CAS  PubMed  Google Scholar 

  • Motamedi MR, Verdel A, Colmenares SU, Gerber SA, Gygi SP, Moazed D (2004) Two RNAi complexes, RITS and RDRC, physically interact and localize to noncoding centromeric RNAs. Cell 119:789–802

    Article  CAS  PubMed  Google Scholar 

  • Nicolás FE, Torres-Martinez S, Ruiz-Vazquez RM (2003) Two classes of small antisense RNAs in fungal RNA silencing triggered by non-integrative transgenes. EMBO J 22:3983–3991

    Article  PubMed Central  PubMed  Google Scholar 

  • Nolan T, Cecere G, Mancone C, Alonzi T, Tripodi M, Catalanotto C, Cogoni C (2008) The RNA-dependent RNA polymerase essential for post-transcriptional gene silencing in Neurospora crassa interacts with replication protein A. Nucleic Acids Res 36:532–538

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pratt RJ, Lee DW, Aramayo R (2004) DNA methylation affects meiotic trans-sensing, not meiotic silencing, in Neurospora. Genetics 168:1925–1935

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC et al (2000) The 21-nuleotide let-7 RNA regulates development timing in Caenorhabditis elegans. Nature 403:901–906

    Article  CAS  PubMed  Google Scholar 

  • Romano N, Macino G (1992) Quelling: transient inactivation of gene expression in Neurospora crassa by transformation with homologous sequences. Mol Microbiol 6:3343–3353

    Article  CAS  PubMed  Google Scholar 

  • Ruby JG, Jan C, Player C, Axtell MJ, Lee W, Nusbaum C, Ge H, Bartel DP (2006) Large-scale sequencing reveals 21U-RNAs and additional microRNAs and endogenous siRNAs in C. elegans. Cell 127:1193–1207

    Article  CAS  PubMed  Google Scholar 

  • Ruby JG, Stark A, Johnston WK, Kellis M, Bartel DP, Lai EC (2007) Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs. Genome Res 17:1850–1864

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Salame TM, Yarden O, Hadar Y (2010) Pleurotus ostreatus manganese-dependent peroxidase silencing impairs decolourization of Orange II. Microb Biotechnol 3:93–106

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Salame TM, Ziv C, Hadar Y, Yarden O (2011) RNAi as a potential tool for biotechnological applications in fungi. Appl Microbiol Biotechnol 89:501–512

    Article  CAS  PubMed  Google Scholar 

  • Shabalina SA, Koonin EV (2008) Origins and evolution of eukaryotic RNA interference. Trends Ecol Evol 23:578–587

    Article  PubMed Central  PubMed  Google Scholar 

  • Shiu PK, Glass NL (2000) Cell and nuclear recognition mechanisms mediated by mating type in filamentous ascomycetes. Curr Opin Microbiol 3:183–188

    Article  CAS  PubMed  Google Scholar 

  • Shiu PK, Metzenberg RL (2002) Meiotic silencing by unpaired DNA: properties, regulation and suppression. Genetics 161:1483–1495

    PubMed Central  CAS  PubMed  Google Scholar 

  • Shiu PK, Zickler D, Raju NB, Ruprich-Robert G, Metzenberg RL (2006) SAD-2 is required for meiotic silencing by unpaired DNA and perinuclear localization of SAD-1 RNA-directed RNA polymerase. Proc Natl Acad Sci USA 103:2243–2248

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Takeno S, Sakuradani E, Tomi A, Inohara-Ochiai M, Kawashima H, Ashikari T, Shimizu S (2005) Improvement of the fatty acid composition of an oil-producing filamentous fungus, Mortierella alpina 1S-4, through RNA interference with delta 12-desaturase gene expression. Appl Environ Microbiol 71:5124–5128

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ulitsky I, Bartel DP (2013) lincRNAs: genomics, evolution, and mechanisms. Cell 154:26–46

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Verdel A, Jia S, Gerber S, Sugiyama T, Gygi S et al (2004) RNAi-mediated targeting of heterochromatin by the RITS complex. Science 303:672–676

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Volpe TA, Kidner C, Hall IM, Teng G, Grewal SIS, Martienssen RA (2002) Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297:1833–1837

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Hsueh Y-P, Li W, Floyd A, Skalsky R, Heitman J (2010) Sex-induced silencing defends the genome of Cryptococcus neoformans via RNAi. Genes Dev 24:2566–2582

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang X, Wang P, Sun S, Darwiche S, Idnurm A, Heitman J (2012) Transgen induced co-suppression during vegetative growth in Cryptococcus neoformans. PLos Genet 8:e1002885

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang X, Darwiche S, Heitman J (2013) Sex-induced silencing operates during opposite-sex and unisexual reproduction in Cryptococcus neoformans. Genetics 193:1163–1174

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Weiberg A, Wang M, Lin F-M, Zhao H, Zhang Z, Kaloshian I, Huang H-D, Jin H (2013) Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342:118–123

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wianny F, Zernicka-Goetz M (2000) Specific interference with gene function by double-stranded RNA in early mouse development. Nat Cell Biol 2:70–75

    Article  CAS  PubMed  Google Scholar 

  • Wilhelm BT, Marguerat S, Watt S, Schubert F, Wood V, Goodhead I et al (2008) Dynamic repertoire of a eukaryotic transcriptome surveyed at single-nucleotide resolution. Nature 453:1239–1243

    Article  CAS  PubMed  Google Scholar 

  • Woolcock KJ, Gaidatzis D, Punga T, Bühler M (2011) Dicer associates with chromatin to repress genome activity in Schizosaccharomyces pombe. Nat Struct Mol Biol 18:94–99

    Article  CAS  PubMed  Google Scholar 

  • Woolcock KJ et al (2012) RNAi keeps Atf1-bound stress response genes in check at nuclear pores. Genes Dev 26:683–692

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Xiao H, Alexander WG, Hammond TM, Boone EC, Perdue TD et al (2010) QIP, a protein that converts duplex siRNA into single strands, is required for meiotic silencing by unpaired DNA. Genetics 186:119–126

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhao T, Li G, Mi S, Li S, Hannon GJ, Wang XJ, Qi Y (2007) A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii. Genes Dev 21:1190–1203

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zheng XF, Kobayashi Y, Takeuchi M (1998) Construction of a low-serine-type-carboxypeptidase-producing mutant of Aspargillus oryzae by the expression of antisense RNA and its use a host for heterologous protein secretion. Appl Microbiol Biotechnol 49:39–44

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgment

The author would like to thank The Swedish Foundation for Strategic Research for financial support. Dr M. Lind is acknowledged for his constructive comments on this chapter.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Åke Olson .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Olson, Å. (2016). 3 RNAi Function and Diversity in Fungi. In: Hoffmeister, D. (eds) Biochemistry and Molecular Biology. The Mycota, vol III. Springer, Cham. https://doi.org/10.1007/978-3-319-27790-5_3

Download citation

Publish with us

Policies and ethics