Skip to main content

Small RNA Inheritance in Hybrids and Allopolyploids

  • Chapter
  • First Online:
Non Coding RNAs in Plants

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

  • 1809 Accesses

Abstract

Small RNAs, including microRNAs (miRNAs), small interfering RNAs (siRNAs), and trans-acting siRNAs (tasiRNAs), control gene expression and epigenetic regulation. Although the physiological and developmental roles of miRNAs and siRNAs have been extensively studied, their roles in morphological diversity among closely related species and in interspecific hybrids and allopolyploids are poorly understood. Here, we discussed recent findings of small RNA regulation with an emphasis on hybrids, interspecific hybrids, and allopolyploids. Divergence between siRNAs and inheritance of these siRNAs through maternal or paternal genome during gametogenesis may exert trans-acting effects on transposable elements and on genes that are important to genomic stability and phenotypic variation. Moreover, expression changes in miRNAs and tasiRNAs between related species or parents may play a role in target gene regulation that is important to growth and development in hybrids and allopolyploids. Inheritance of small RNAs through maternal or paternal genome in interspecific hybrids and allopolyploids are reminiscent of parent-of-origin effects of small RNA regulation on offspring in heterozygous organisms including humans.

Author Information

The authors declare no competing financial interests. Correspondence and requests for any materials should be addressed to ZJC (zjchen@mail.utexas.edu).

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

References

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

    Article  PubMed  CAS  Google Scholar 

  • Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

    Article  Google Scholar 

  • Aravin A, Gaidatzis D, Pfeffer S et al (2006) A novel class of small RNAs bind to MILI protein in mouse testes. Nature 442:203–207

    PubMed  CAS  Google Scholar 

  • Aravin AA, Hannon GJ, Brennecke J (2007) The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318:761–764

    Article  PubMed  CAS  Google Scholar 

  • Arteaga-Vazquez M, Caballero-Perez J, Vielle-Calzada JP (2006) A family of microRNAs present in plants and animals. Plant Cell 18:3355–3369

    Article  PubMed  CAS  Google Scholar 

  • Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741

    Article  PubMed  CAS  Google Scholar 

  • Axtell MJ, Bartel DP (2005) Antiquity of microRNAs and their targets in land plants. Plant Cell 17:1658–1673

    Article  PubMed  CAS  Google Scholar 

  • Axtell MJ, Snyder JA, Bartel DP (2007) Common functions for diverse small RNAs of land plants. Plant Cell 19:1750  –1769

    Article  PubMed  CAS  Google Scholar 

  • Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215–233

    Article  PubMed  CAS  Google Scholar 

  • Bateson W (1909) Heredity and variation in modern lights. In: Seward AC (ed) Darwin and modern science. Cambridge University Press, Cambridge, pp 85–101

    Google Scholar 

  • Baulcombe D (2004) RNA silencing in plants. Nature 431:356–363

    Article  PubMed  CAS  Google Scholar 

  • Bingham PM, Kidwell MG, Rubin GM (1982) The molecular basis of P-M hybrid dysgenesis: the role of the P element, a P-strain-specific transposon family. Cell 29:995–1004

    Article  PubMed  CAS  Google Scholar 

  • Brennecke J, Aravin AA, Stark A et al (2007) Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila. Cell 128:1089–1103

    Article  PubMed  CAS  Google Scholar 

  • Brennecke J, Malone CD, Aravin AA 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 

  • Bucheton A, Paro R, Sang HM et al (1984) The molecular basis of I-R hybrid dysgenesis in Drosophila melanogaster: identification, cloning, and properties of the I factor. Cell 38:153–163

    Article  PubMed  CAS  Google Scholar 

  • Carmell MA, Girard A, van de Kant HJ et al (2007) MIWI2 is essential for spermatogenesis and repression of transposons in the mouse male germline. Dev Cell 12:503–514

    Article  PubMed  CAS  Google Scholar 

  • Castro JP, Carareto CM (2004) Drosophila melanogaster P transposable elements: mechanisms of transposition and regulation. Genetica 121:107–118

    Article  PubMed  CAS  Google Scholar 

  • Chambeyron S, Bucheton A (2005) I elements in Drosophila: in vivo retrotransposition and regulation. Cytogenet Genome Res 110:215–222

    Article  PubMed  CAS  Google Scholar 

  • Chan SW, Zhang X, Bernatavichute YV et al (2006) Two-step recruitment of RNA-directed DNA methylation to tandem repeats. PLoS Biol 4:e363

    Article  PubMed  Google Scholar 

  • Chapman EJ, Carrington JC (2007) Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 8:884–896

    Article  PubMed  CAS  Google Scholar 

  • Chen X (2004) A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303:2022–2025

    Article  PubMed  CAS  Google Scholar 

  • Chen ZJ (2007) Genetic and epigenetic mechanisms for gene expression and phenotypic variation in plant polyploids. Annu Rev Plant Biol 58:377–406

    Article  PubMed  CAS  Google Scholar 

  • Chen X (2009) Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol 25:21–  44

    Article  PubMed  Google Scholar 

  • Chen M, Ha M, Lackey E et al (2008) RNAi of met1 reduces DNA methylation and induces genome-specific changes in gene expression and centromeric small RNA accumulation in Arabidopsis allopolyploids. Genetics 178:1845–1858

    Article  PubMed  CAS  Google Scholar 

  • Comai L (2005) The advantages and disadvantages of being polyploid. Nat Rev Gen 6(11):836–846

    Article  CAS  Google Scholar 

  • Desset S, Meignin C, Dastugue B et al (2003) COM, a heterochromatic locus governing the control of independent endogenous retroviruses from Drosophila melanogaster. Genetics 164:501–509

    PubMed  CAS  Google Scholar 

  • Dobzhansky T (1936) Studies on hybrid sterility. II. Localization of sterility factors in Drosophila Pseudoobscura hybrids. Genetics 21:113–135

    PubMed  CAS  Google Scholar 

  • Engels WR, Preston CR (1979) Hybrid dysgenesis in Drosophila melanogaster: the biology of female and male sterility. Genetics 92:161–174

    PubMed  CAS  Google Scholar 

  • Fabian MR, Sonenberg N, Filipowicz W (2010) Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 79:351–379

    Article  PubMed  CAS  Google Scholar 

  • Fahlgren N, Howell MD, Kasschau KD et al (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of miRNA genes. PLoS ONE 2:e219

    Article  PubMed  Google Scholar 

  • Finigan P, Martienssen RA (2008) Nucleolar dominance and DNA methylation directed by small interfering RNA. Mol Cell 32:753–754

    Article  PubMed  CAS  Google Scholar 

  • Gehring M, Huh JH, Hsieh TF et al (2006) DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation. Cell 124:495–506

    Article  PubMed  CAS  Google Scholar 

  • Ha M, Pang M, Agarwal V et al (2008) Interspecies regulation of microRNAs and their targets. Biochim Biophys Acta 1779:735–742

    Article  PubMed  CAS  Google Scholar 

  • Ha M, Kim ED, Chen ZJ (2009a) Duplicate genes increase expression diversity in closely related species and allopolyploids. Proc Natl Acad Sci USA 106:2295–2300

    Article  PubMed  CAS  Google Scholar 

  • Ha M, Lu J, Tian L et al (2009b) Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids. Proc Natl Acad Sci USA 106(42):17835–17840

    Article  PubMed  CAS  Google Scholar 

  • Hall AE, Kettler GC, Preuss D (2006) Dynamic evolution at pericentromeres. Genome Res 16:355–364

    Article  PubMed  CAS  Google Scholar 

  • Hartig JV, Tomari Y, Forstemann K (2007) piRNAs – the ancient hunters of genome invaders. Genes Dev 21:1707–1713

    Article  PubMed  CAS  Google Scholar 

  • Herr AJ, Jensen MB, Dalmay T et al (2005) RNA polymerase IV directs silencing of endogenous DNA. Science 308:118–120

    Article  PubMed  CAS  Google Scholar 

  • Jia Y, Lisch DR, Ohtsu K et al (2009) Loss of RNA-dependent RNA polymerase 2 (RDR2) function causes widespread and unexpected changes in the expression of transposons, genes, and 24-nt small RNAs. PLoS Genet 5:e1000737

    Article  PubMed  Google Scholar 

  • Josefsson C, Dilkes B, Comai L (2006) Parent-dependent loss of gene silencing during interspecies hybridization. Curr Biol 16:1322–1328

    Article  PubMed  CAS  Google Scholar 

  • Kidwell MG (1977) Reciprocal differences in female recombination associated with hybrid dysgenesis in Drosophila melanogaster. Genet Res 30:77–88

    Article  PubMed  CAS  Google Scholar 

  • Kidwell MG (1981) Hybrid dysgenesis in Drosophila melanogaster: the genetics of cytotype determination in a neutral strain. Genetics 98:275–290

    PubMed  CAS  Google Scholar 

  • Kidwell MG (1983) Hybrid dysgenesis in DROSOPHILA MELANOGASTER: factors affecting chromosomal contamination in the P-M system. Genetics 104:317–341

    PubMed  CAS  Google Scholar 

  • Kim JH, Woo HR, Kim J et al (2009) Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis. Science 323:1053–1057

    Article  PubMed  CAS  Google Scholar 

  • Kinoshita Y, Saze H, Kinoshita T et al (2007) Control of FWA gene silencing in Arabidopsis thaliana by SINE-related direct repeats. Plant J 49:38–45

    Article  PubMed  CAS  Google Scholar 

  • Lau NC, Seto AG, Kim J et al (2006) Characterization of the piRNA complex from rat testes. Science 313:363–367

    Article  PubMed  CAS  Google Scholar 

  • Lee HS, Chen ZJ (2001) Protein-coding genes are epigenetically regulated in Arabidopsis polyploids. Proc Natl Acad Sci USA 98:6753–6758

    Article  PubMed  CAS  Google Scholar 

  • Leitch AR, Leitch IJ (2008) Genomic plasticity and the diversity of polyploid plants. Science 320:481–483

    Article  PubMed  CAS  Google Scholar 

  • Lin H, Spradling AC (1997) A novel group of pumilio mutations affects the asymmetric division of germline stem cells in the Drosophila ovary. Development 124:2463–2476

    PubMed  CAS  Google Scholar 

  • Llave C, Xie Z, Kasschau KD et al (2002) Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297:2053–2056

    Article  PubMed  CAS  Google Scholar 

  • Lockton S, Gaut BS (2009) The contribution of transposable elements to expressed coding sequence in Arabidopsis thaliana. J Mol Evol 68:80  –89

    Article  PubMed  CAS  Google Scholar 

  • Long D, Lee R, Williams P et al (2007) Potent effect of target structure on microRNA function. Nat Struct Mol Biol 14:287–294

    Article  PubMed  CAS  Google Scholar 

  • Ma Z, Coruh C, Axtell MJ (2010) Arabidopsis lyrata small RNAs: transient MIRNA and small interfering RNA loci within the Arabidopsis genus. Plant Cell 22:1090  –1103

    Article  PubMed  CAS  Google Scholar 

  • Mallory AC, Dugas DV, Bartel DP et al (2004a) MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs. Curr Biol 14:1035–1046

    Article  PubMed  CAS  Google Scholar 

  • Mallory AC, Reinhart BJ, Jones-Rhoades MW et al (2004b) MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5′ region. EMBO J 23:3356–3364

    Article  PubMed  CAS  Google Scholar 

  • Martienssen RA (2010) Heterochromatin, small RNA and post-fertilization dysgenesis in allopolyploid and interploid hybrids of Arabidopsis. New Phytol 186:46  –53

    Article  PubMed  CAS  Google Scholar 

  • McClintock B (1984) The significance of responses of the genome to challenge. Science 226:792–801

    Article  PubMed  CAS  Google Scholar 

  • McConnell JR, Emery J, Eshed Y et al (2001) Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots. Nature 411:709  –713

    Article  PubMed  CAS  Google Scholar 

  • Messing J, Bharti AK, Karlowski WM et al (2004) Sequence composition and genome organization of maize. Proc Natl Acad Sci USA 101:14349–14354

    Article  PubMed  CAS  Google Scholar 

  • Mosher RA, Melnyk CW, Kelly KA et al (2009) Uniparental expression of PolIV-dependent siRNAs in developing endosperm of Arabidopsis. Nature 460:283–286

    Article  PubMed  CAS  Google Scholar 

  • Muller HJ (1942) Isolating mechanisms, evolution and temperature. Biol Symp 6:71–125

    Google Scholar 

  • Niwa R, Slack FJ (2007) The evolution of animal microRNA function. Curr Opin Genet Dev 17:145–150

    Article  PubMed  CAS  Google Scholar 

  • Obbard DJ, Jiggins FM, Halligan DL et al (2006) Natural selection drives extremely rapid evolution in antiviral RNAi genes. Curr Biol 16:580  –585

    Article  PubMed  CAS  Google Scholar 

  • Onodera Y, Haag JR, Ream T et al (2005) Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell 120:613–  622

    Article  PubMed  CAS  Google Scholar 

  • Osborn TC, Pires JC, Birchler JA et al (2003) Understanding mechanisms of novel gene ­expression in polyploids. Trends Genet 19:141–147

    Article  PubMed  CAS  Google Scholar 

  • Otto SP (2007) The evolutionary consequences of polyploidy. Cell 131:452–  462

    Article  PubMed  CAS  Google Scholar 

  • Palatnik JF, Allen E, Wu X et al (2003) Control of leaf morphogenesis by microRNAs. Nature 425:257–263

    Article  PubMed  CAS  Google Scholar 

  • Pelisson A (1981) The I–R system of hybrid dysgenesis in Drosophila melanogaster: are I factor insertions responsible for the mutator effect of the I–R interaction? Mol Gen Genet 183:123–129

    Article  PubMed  CAS  Google Scholar 

  • Picard G (1976) Non-mendelian female sterility in Drosophila melanogaster: hereditary transmission of I factor. Genetics 83:107–123

    PubMed  CAS  Google Scholar 

  • Pikaard CS (2000) The epigenetics of nucleolar dominance. Trends Genet 16:495–500

    Article  PubMed  CAS  Google Scholar 

  • Preuss SB, Costa-Nunes P, Tucker S et al (2008) Multimegabase silencing in nucleolar dominance involves siRNA-directed DNA methylation and specific methylcytosine-binding proteins. Mol Cell 32:673–684

    Article  PubMed  CAS  Google Scholar 

  • Rajagopalan R, Vaucheret H, Trejo J et al (2006) A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 20:3407–3425

    Article  PubMed  CAS  Google Scholar 

  • Reeder RH (1985) Mechanisms of nucleolar dominance in animals and plants. J Cell Biol 101:2013–2016

    Article  PubMed  CAS  Google Scholar 

  • Reinhart BJ, Weinstein EG, Rhoades MW et al (2002) MicroRNAs in plants. Genes Dev 16:1616–1626

    Article  PubMed  CAS  Google Scholar 

  • Rhoades MW, Reinhart BJ, Lim LP et al (2002) Prediction of plant microRNA targets. Cell 110:513–520

    Article  PubMed  CAS  Google Scholar 

  • Rieseberg LH, Raymond O, Rosenthal DM et al (2003) Major ecological transitions in wild sunflowers facilitated by hybridization. Science 301:1211–1216

    Article  PubMed  CAS  Google Scholar 

  • Rubin GM, Kidwell MG, Bingham PM (1982) The molecular basis of P-M hybrid dysgenesis: the nature of induced mutations. Cell 29:987–994

    Article  PubMed  CAS  Google Scholar 

  • Ruvkun G (2001) Glimpses of a tiny RNA world. Science 294:797–799

    Article  PubMed  CAS  Google Scholar 

  • Saito K, Nishida KM, Mori T et al (2006) Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome. Genes Dev 20:2214  –2222

    Article  PubMed  CAS  Google Scholar 

  • Salmon A, Ainouche ML, Wendel JF (2005) Genetic and epigenetic consequences of recent hybridization and polyploidy in Spartina (Poaceae). Mol Ecol 14:1163–1175

    Article  PubMed  CAS  Google Scholar 

  • SanMiguel P, Tikhonov A, Jin Y-K et al (1996) Nested retrotransposons in the intergenic regions of the maize genome. Science 274:765–768

    Article  PubMed  CAS  Google Scholar 

  • Siomi H, Siomi MC (2010) Posttranscriptional regulation of microRNA biogenesis in animals. Mol Cell 38:323–332

    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 

  • Soltis PS, Soltis DE (2009) The role of hybridization in plant speciation. Annu Rev Plant Biol 60:561–588

    Article  PubMed  CAS  Google Scholar 

  • Tsukahara S, Kobayashi A, Kawabe A et al (2009) Bursts of retrotransposition reproduced in Arabidopsis. Nature 461:423–  426

    Article  PubMed  CAS  Google Scholar 

  • Ungerer MC, Strakosh SC, Zhen Y (2006) Genome expansion in three hybrid sunflower species is associated with retrotransposon proliferation. Curr Biol 16:R872–R873

    Article  PubMed  CAS  Google Scholar 

  • Vagin VV, Sigova A, Li C et al (2006) A distinct small RNA pathway silences selfish genetic elements in the germline. Science 313:320  –324

    Article  PubMed  CAS  Google Scholar 

  • Vaucheret H (2006) Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Dev 20:759–771

    Article  PubMed  CAS  Google Scholar 

  • Vazquez F (2006) Arabidopsis endogenous small RNAs: highways and byways. Trends Plant Sci 11:460  –  468

    Article  PubMed  CAS  Google Scholar 

  • Villar CB, Erilova A, Makarevich G et al (2009) Control of PHERES1 imprinting in Arabidopsis by direct tandem repeats. Mol Plant 2:654  –660

    Article  PubMed  CAS  Google Scholar 

  • Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687

    Article  PubMed  CAS  Google Scholar 

  • Wang J, Tian L, Lee HS et al (2006) Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. Genetics 172:507–517

    Article  PubMed  CAS  Google Scholar 

  • Wendel JF (2000) Genome evolution in polyploids. Plant Mol Biol 42:225–249

    Article  PubMed  CAS  Google Scholar 

  • Wu G, Park MY, Conway SR et al (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138:750  –759

    Article  PubMed  CAS  Google Scholar 

  • Yoshikawa M, Peragine A, Park MY et al (2005) A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev 19:2164  –2175

    Article  PubMed  CAS  Google Scholar 

  • Zhang X, Henderson IR, Lu C et al (2007) Role of RNA polymerase IV in plant small RNA metabolism. Proc Natl Acad Sci USA 104:4536  –  4541

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

The work is supported by the grants from the National Science Foundation Plant Genome Research Program (DBI0733857) and National Institutes of Health (GM067015), USA to ZJC.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Z. Jeffrey Chen .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Lu, J., Chen, Z.J. (2011). Small RNA Inheritance in Hybrids and Allopolyploids. 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_7

Download citation

Publish with us

Policies and ethics