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Small RNA Pathways and Their Function in the Male Gametophyte

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Non Coding RNAs in Plants

Part of the book series: RNA Technologies ((RNATECHN))

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Abstract

In animals, small RNAs are essential for reproductive development. Without the activity of members of the Piwi class of the Argonaute protein family, and their associated small RNAs, the formation and maintenance of the germline, and gametogenesis, cannot take place correctly. Reproductive development in plants is more complex than in animals; instead of the haploid products of meiosis leading directly to gametes, further mitotic divisions contribute to the formation of a separate haploid generation called the gametophyte. As might be expected, the formation of the gametophyte and gametogenesis also relies on small RNA systems. In plants, almost all of the information so far gathered on the gametophyte has come from studies of the male gametophyte (pollen). Here, recent studies have revealed all the families of small RNAs known from the somatic cells in the diploid sporophyte – microRNAs, trans-acting siRNAs, natural antisense siRNAs and siRNAs to be involved in RNA-dependent DNA methylation. Given the apparent simplicity of the development of the male gametophyte, microRNAs and tasiRNAs are unexpectedly diverse. As in animals, plants use small RNA systems to control transposable element activity in the germline. There is also recent evidence that a specific regulatory module of a natural antisense gene pair, that spawns nat-siRNAs in the sperm cells, has a key role in fertilisation.

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References

  • Allen E, Howell MD (2010) miRNAs in the biogenesis of trans-acting siRNAs in higher plants. Semin Cell Dev Biol. doi:10.1016/j.semcdb.2010.03.008

  • Arkov A, Ramos A (2010) Building RNA-protein granules: insight from the germline. Trends Cell Biol 20:482–  490

    Article  PubMed  CAS  Google Scholar 

  • Batista P, Ruby J, Claycomb J et al (2008) PRG-1 and 21U-RNAs interact to form the piRNA complex required for fertility in C. elegans. Mol Cell 31:67–78

    Article  PubMed  CAS  Google Scholar 

  • Benetti R, Gonzalo S, Jaco I et al (2008) A mammalian microRNA cluster controls DNA methylation and telomere recombination via Rbl2-dependent regulation of DNA methyltransferases. Nat Struct Mol Biol 15:268–279

    Article  PubMed  CAS  Google Scholar 

  • Borg M, Brownfield L, Twell D (2009) Male gametophyte development: a molecular perspective. J Exp Bot 60:1465–1478

    Article  PubMed  CAS  Google Scholar 

  • Borges F, Gomes G, Gardner R et al (2008) Comparative transcriptomics of Arabidopsis sperm cells. Plant Physiol 148:1168–1181

    Article  PubMed  CAS  Google Scholar 

  • Brennecke J, Malone C, Aravin A et al (2008) An epigenetic role for maternally inherited piRNAs in transposon silencing. Science 322:1387–1392

    Article  PubMed  CAS  Google Scholar 

  • Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M et al (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320:1185–1190

    Article  PubMed  CAS  Google Scholar 

  • Cartagena JA, Matsunaga S, Seki M et al (2008) The Arabidopsis SDG4 contributes to the regulation of pollen tube growth by methylation of histone H3 lysines 4 and 36 in mature pollen. Dev Biol 315:355–368

    Article  PubMed  CAS  Google Scholar 

  • Chambers C, Shuai B (2009) Profiling microRNA expression in Arabidopsis pollen using microRNA array and real-time PCR. BMC Plant Biol 9:87

    Article  PubMed  Google Scholar 

  • Chen HM, Chen LT, Patel K et al (2010) 22-nucleotide RNAs trigger secondary siRNA biogenesis in plants. Proc Natl Acad Sci USA 107:15269–15274

    Article  PubMed  CAS  Google Scholar 

  • Cuperus JT, Carbonell A, Fahlgren N et al (2010) Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in Arabidopsis. Nat Struct Mol Biol 17:997–1003

    Article  PubMed  CAS  Google Scholar 

  • Daxinger L, Kanno T, Bucher E et al (2009) A stepwise pathway for biogenesis of 24-nt secondary siRNAs and spreading of DNA methylation. EMBO J 28:48–57

    Article  PubMed  CAS  Google Scholar 

  • Dickinson HG, Grant-Downton R (2009) Bridging the generation gap: flowering plant gametophytes and animal germlines reveal unexpected similarities. Biol Rev Camb Philos Soc 84:589–  615

    Article  PubMed  Google Scholar 

  • Durharcourt S, Lepère G, Meyer E (2009) Developmental genome rearrangements in ciliates: a natural genomic subtraction mediated by non coding transcripts. Trends Genet 25:344–350

    Article  Google Scholar 

  • During HJ (1979) Life strategies of bryophytes: a preliminary review. Lindbergia 5:2–18

    Google Scholar 

  • Ebhardt HA, Fedynak A, Fahlman RP (2010) Naturally occurring variations in sequence length creates microRNA isoforms that differ in Argonaute effector complex specificity. Silence 1:12

    Article  PubMed  Google Scholar 

  • Engel ML, Chaboud A, Dumas C et al (2003) Sperm cells of Zea mays have a complex complement of mRNAs. Plant J 34:697–707

    Article  PubMed  CAS  Google Scholar 

  • Gent J, Schvarzstein M, Villeneuve A et al (2009) A Caenorhabditis elegans RNA-directed RNA polymerase in sperm development and endogenous RNA interference. Genetics 183:1297–1314

    Article  PubMed  CAS  Google Scholar 

  • Grant-Downton RT, Hafidh S, Twell D et al (2009a) Small RNA pathways are present and functional in the angiosperm male gametophyte. Mol Plant 2:500–512

    Article  PubMed  CAS  Google Scholar 

  • Grant-Downton RT, Le Trionnaire G, Schimd R et al (2009b) MicroRNA and ta-siRNA diversity in mature pollen of Arabidopsis thaliana. BMC Genomics 10:643

    Article  PubMed  Google Scholar 

  • Gu W, Shirayama M, Conte D et al (2009) Distinct Argonaute-mediated 22G-RNA pathways direct genome surveillance in the C. elegans germline. Mol Cell 36:231–244

    Article  PubMed  CAS  Google Scholar 

  • Han T, Manoharan A, Harkins T et al (2009) 26G endo-siRNAs regulate spermatogenic and zygotic gene expression in Caenorhabditis elegans. Proc Natl Acad Sci USA 106:18674–18679

    Article  PubMed  CAS  Google Scholar 

  • Iskow RC, McCabe MT, Mills RE et al (2010) Natural mutagenesis of human genomes by endogenous retrotransposons. Cell 141:1253–1261

    Article  PubMed  CAS  Google Scholar 

  • Janousek B, Zluvova J, Vyscot B (2000) Histone H4 acetylation and DNA methylation dynamics during pollen development. Protoplasma 211:116  –122

    Article  CAS  Google Scholar 

  • Kidner CA, Martienssen RA (2005) The role of ARGONAUTE1 (AGO1) in meristem formation and identity. Dev Biol 280:504–517

    Article  PubMed  CAS  Google Scholar 

  • Klattenhoff C, Theurkauf W (2008) Biogenesis and germline functions of piRNAs. Development 135:3–9

    Article  PubMed  CAS  Google Scholar 

  • Kurth H, Mochizuki K (2009) 2′-O-methylation stabilizes Piwi-associated small RNAs and ensures DNA elimination in Tetrahymena. RNA 15:675–  685

    Article  PubMed  CAS  Google Scholar 

  • Lanet E, Delannoy E, Sormani R et al (2009) Biochemical evidence for translational repression by Arabidopsis microRNAs. Plant Cell 21:1762–1768

    Article  PubMed  CAS  Google Scholar 

  • Lau N (2010) Small RNAs in the animal gonad: guarding genomes and guiding development. Int J Biochem Cell Biol 42:1334  –1347

    Article  PubMed  CAS  Google Scholar 

  • Matzke M, Birchler J (2005) RNAi-mediated pathways in the nucleus. Nat Rev Genet 6:24–35

    Article  PubMed  CAS  Google Scholar 

  • McCormick S (2004) Control of male gametophyte development. Plant Cell 16:S142–S153

    Article  PubMed  CAS  Google Scholar 

  • Mogensen HL (1996) The hows and whys of cytoplasmic inheritance in seed plants. Am J Bot 83:383–404

    Article  Google Scholar 

  • Morel JB, Godon C, Mourrrain P et al (2002) Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance. Plant Cell 14:629–  639

    Article  PubMed  CAS  Google Scholar 

  • Nonomura K, Morohoshi A, Nakano M et al (2007) A germ cell specific gene of the ARGONAUTE family is essential for the progression of premeiotic mitosis and meiosis during sporogenesis in rice. Plant Cell 19:2583–2594

    Article  PubMed  CAS  Google Scholar 

  • Oakeley EJ, Podestà A, Jost J-P (1997) Developmental changes in DNA methylation of the two tobacco pollen nuclei during maturation. Proc Natl Acad Sci USA 94:11721–11725

    Article  PubMed  CAS  Google Scholar 

  • Okada T, Endo M, Singh MB et al (2005) Analysis of histone H3 gene family in Arabidopsis and identification of male gamete-specific variant, AtMGH3. Plant J 44:557–568

    Article  PubMed  CAS  Google Scholar 

  • Okada T, Singh MB, Bhalla PL (2006) Histone H3 variants in male gametic cells of lily and H3 methylation in mature pollen. Plant Mol Biol 62:503–512

    Article  PubMed  CAS  Google Scholar 

  • Olmedo-Monfil V, Durán-Figueroa N, Arteaga-Vázquez M et al (2010) Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464:628–  632

    Article  PubMed  CAS  Google Scholar 

  • Onodera Y, Nakagawa K, Haag J et al (2008) Sex-biased lethality or transmission of defective transcription machinery in Arabidopsis. Genetics 180:207–218

    Article  PubMed  CAS  Google Scholar 

  • Palanivelu R, Brass L, Edlund AF et al (2003) Pollen tube growth and guidance is regulated by POP2, an Arabidopsis gene that controls GABA levels. Cell 114:47–59

    Article  PubMed  CAS  Google Scholar 

  • Pina C, Pinto F, Feijó JA et al (2005) Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol 138:744  –756

    Article  PubMed  CAS  Google Scholar 

  • Prado AM, Colaco R, Moreno N et al (2008) Targeting of pollen tubes to ovules is dependent on nitric oxide (NO) signaling. Mol Plant 1:703–714

    Article  PubMed  CAS  Google Scholar 

  • Qin Y, Leydon AR, Manziello A et al (2009) Penetration of the stigma and style elicits a novel transcriptome in pollen tubes identifying genes critical for growth in the pistil. PLoS Genet 5:e1000621

    Article  PubMed  Google Scholar 

  • Rassoulzadegan M, Grandjean V, Gounon P et al (2006) RNA-mediated non-mendelian inheritance of an epigenetic change in the mouse. Nature 441:469–  474

    Article  PubMed  CAS  Google Scholar 

  • Renauld H (1997) Heterochromatin: a meiotic matchmaker? Trends Cell Biol 7:201–205

    Article  PubMed  CAS  Google Scholar 

  • Reynolds S, Ruohola-Baker H (2008) The role of microRNAs in germline differentiation. In: StemBook [Internet]. Harvard Stem Cell Institute, Cambridge

    Google Scholar 

  • Ribeiro T, Viegas W, Morais-Cecílio L (2009) Epigenetic marks in mature pollen of Quercus suber L. (Fagaceae). Sex Plant Reprod 22:1–7

    Article  PubMed  CAS  Google Scholar 

  • Ron M, Saez MA, Williams LE et al (2010) Proper regulation of a sperm-specific cis-nat-siRNA is essential for double fertilization in Arabidopsis. Genes Dev 24:1010  –1021

    Article  PubMed  CAS  Google Scholar 

  • Rudall PJ, Bateman RM (2007) Developmental bases for key innovations in the seed plant microgametophyte. Trends Plant Sci 12:317–326

    Article  PubMed  CAS  Google Scholar 

  • Sano Y, Tanaka I (2005) A histone H3.3-like gene specifically expressed in the vegetative cell of developing lily pollen. Plant Cell Physiol 46:1299–1308

    Article  PubMed  CAS  Google Scholar 

  • Schoft V, Chumak N, Mosiolek M et al (2009) Induction of RNA-directed DNA methylation upon decondensation of constitutive heterochromatin. EMBO Rep 10:1015–1021

    Article  PubMed  CAS  Google Scholar 

  • Sieber P, Wellmer F, Gheyselinck J et al (2007) Redundancy and specialization among plant microRNAs: role of the MIR164 family in developmental robustness. Development 134:1051–1060

    Article  PubMed  CAS  Google Scholar 

  • Slotkin RK, Vaughn M, Borges F et al (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:461–  472

    Article  PubMed  CAS  Google Scholar 

  • Tam OH, Aravin AA, Stein P et al (2008) Nature 453:534–  538

    Article  PubMed  CAS  Google Scholar 

  • Tanaka I, Ono K, Fukuda T (1998) The developmental fate of angiosperm pollen is associated with a preferential decrease in the level of histone H1 in the vegetative nucleus. Planta 206:561–569

    Article  CAS  Google Scholar 

  • Thomson T, Lin H (2009) The biogenesis and function of PIWI proteins and piRNAs: progress and prospect. Annu Rev Cell Dev Biol 25:355–376

    Article  PubMed  CAS  Google Scholar 

  • Válóczi A, Várallyay E, Kauppinen S et al (2006) Spatio-temporal accumulation of microRNAs is highly coordinated in developing plant tissues. Plant J 47:140  –151

    Article  PubMed  Google Scholar 

  • van der Heijden G, Bortvin A (2009) Transient relaxation of transposon silencing at the onset of mammalian meiosis. Epigenetics 4:76  –79

    Article  PubMed  Google Scholar 

  • Wagner KD, Wagner N, Ghanbarian H et al (2008) RNA induction and inheritance of epigenetic cardiac hypertrophy in the mouse. Dev Cell 14:962–969

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Zhang WZ, Song LF et al (2008) Transcriptome analyses show changes in gene expression to accompany pollen germination and pollen tube growth in Arabidopsis. Plant Physiol 148:1201–1211

    Article  PubMed  CAS  Google Scholar 

  • Watanabe T, Totoki Y, Kaneda M et al (2008) Endogenous siRNAs from naturally formed dsRNAs regulate transcripts in mouse oocytes. Nature 453:539–543

    Article  PubMed  CAS  Google Scholar 

  • Williams JH (2008) Novelties of the flowering plant pollen tube underlie diversification of a key life history stage. Proc Natl Acad Sci USA 105:11259  –11263

    Article  PubMed  CAS  Google Scholar 

  • Wu HM, Wang H, Cheung AY (1995) A pollen tube growth stimulatory glycoprotein is deglycosylated by pollen tubes and displays a glycosylation gradient in the flower. Cell 82:395–403

    Article  PubMed  CAS  Google Scholar 

  • Yu GH, Sun MX (2007) Deciphering a possible mechanism of GABA in tobacco pollen tube growth and guidance. Plant Signal Behav 2:393–395

    Article  PubMed  Google Scholar 

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Correspondence to Hugh Dickinson .

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Dickinson, H., Grant-Downton, R. (2011). Small RNA Pathways and Their Function in the Male Gametophyte. In: Erdmann, V., Barciszewski, J. (eds) Non Coding RNAs in Plants. RNA Technologies. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-19454-2_11

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