Skip to main content

Small RNAs in Rice: Molecular Species and Their Functions

  • Chapter
  • First Online:
Rice Genomics, Genetics and Breeding
  • 2419 Accesses

Abstract

Small RNAs are major components of gene regulatory pathways conserved among eukaryotes. In basic and applied sciences, RNA interference (RNAi) and artificial microRNAs (amiRNAs) are often used to modulate gene expression. The molecular mechanisms of RNAi are mainly studied in nematode or insect cells as models. Functional analyses of endogenous small RNAs, including studies of rice as a model, have greatly contributed to our understanding of plant biology. In plants, small RNA-based gene regulation has unique characteristics not found in animals, and many small RNAs regulate biological phenomena specific to plants. Recently, small RNA profiling using next-generation sequencers became possible, and various small RNA species were identified in plants including rice; their functional analyses are underway. This chapter summarizes the components of small RNA pathways, the molecular species of small RNAs, and the unique function of small RNAs in rice. It also considers the functions of small RNAs in relation to agriculturally important traits.

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 229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 299.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 299.99
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

  • Abe M, Yoshikawa T, Nosaka M, Sakakibara H, Sato Y, Nagato Y, Itoh J (2010) WAVY LEAF1, an ortholog of Arabidopsis HEN1, regulates shoot development by maintaining MicroRNA and trans-acting small interfering RNA accumulation in rice. Plant Physiol 154:1335–1346

    Article  CAS  PubMed  PubMed Central  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  CAS  PubMed  PubMed Central  Google Scholar 

  • Aung K, Lin SI, Wu CC, Huang YT, Su C, Chiou TJ (2006) pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol 141:1000–1011

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baldrich P, San Segundo B (2016) MicroRNAs in rice innate immunity. Rice (N Y) 9:6

    Article  PubMed Central  Google Scholar 

  • Baldrich P, Campo S, Wu MT, Liu TT, Hsing YI, San Segundo B (2015) MicroRNA-mediated regulation of gene expression in the response of rice plants to fungal elicitors. RNA Biol 12:847–863

    Article  PubMed  PubMed Central  Google Scholar 

  • Bari R, Pant BD, Stitt M, Scheible WR (2006) PHO2, MicroRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borges F, Martienssen RA (2015) The expanding world of small RNAs in plants. Nat Rev Mol Cell Biol 16:727–741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campo S, Peris-Peris C, Siré C, Moreno AB, Donaire L, Zytnicki M, Notredame C, Llave C, San Segundo B (2013) Identification of a novel microRNA (miRNA) from rice that targets an alternatively spliced transcript of the Nramp6 (Natural resistance-associated macrophage protein 6) gene involved in pathogen resistance. New Phytol 199:212–227

    Article  CAS  PubMed  Google Scholar 

  • Chen F, He G, He H, Chen W, Zhu X, Liang M, Chen L, Deng XW (2010) Expression analysis of miRNAs and highly-expressed small RNAs in two rice subspecies and their reciprocal hybrids. J Integr Plant Biol 52:971–980

    Article  CAS  PubMed  Google Scholar 

  • Chen CJ, Liu Q, Zhang YC, Qu LH, Chen YQ, Gautheret D (2011) Genome-wide discovery and analysis of microRNAs and other small RNAs from rice embryogenic callus. RNA Biol 8:538–547

    Article  CAS  PubMed  Google Scholar 

  • Chuck G, Cigan AM, Saeteurn K, Hake S (2007) The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat Genet 39:544–549

    Article  CAS  PubMed  Google Scholar 

  • Csorba T, Kontra L, Burgyán J (2015) Viral silencing suppressors: tools forged to fine-tune host-pathogen coexistence. Virology 479–480:85–103

    Article  PubMed  Google Scholar 

  • Cui LG, Shan JX, Shi M, Gao JP, Lin HX (2014) The miR156-SPL9-DFR pathway coordinates the relationship between development and abiotic stress tolerance in plants. Plant J 80:1108–1117

    Article  CAS  PubMed  Google Scholar 

  • Cuperus JT, Fahlgren N, Carrington JC (2011) Evolution and functional diversification of MIRNA genes. Plant Cell 23:431–442

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding Y, Ye Y, Jiang Z, Wang Y, Zhu C (2016) MicroRNA390 is involved in cadmium tolerance and accumulation in rice. Front Plant Sci 7:235

    PubMed  PubMed Central  Google Scholar 

  • Du P, Wu J, Zhang J, Zhao S, Zheng H, Gao G, Wei L, Li Y (2011) Viral infection induces expression of novel phased microRNAs from conserved cellular microRNA precursors. PLoS Pathog 7:e1002176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duan P, Ni S, Wang J, Zhang B, Xu R, Wang Y, Chen H, Zhu X, Li Y (2015) Regulation of OsGRF4 by OsmiR396 controls grain size and yield in rice. Nat Plants 2:15203

    Article  PubMed  Google Scholar 

  • Fang X, Qi Y (2016) RNAi in plants: an Argonaute-centered view. Plant Cell 28:272–285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fei Q, Xia R, Meyers BC (2013) Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks. Plant Cell 25:2400–2415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao F, Wang K, Liu Y, Chen Y, Chen P, Shi Z, Luo J, Jiang D, Fan F, Zhu Y, Li S (2015) Blocking miR396 increased rice yield by shaping inflorescence architecture. Nat Plants 2:15196

    Article  PubMed  Google Scholar 

  • Han MH, Goud S, Song L, Fedoroff N (2004) The Arabidopsis double-stranded RNA-binding protein HYL1 plays a role in microRNA-mediated gene regulation. Proc Natl Acad Sci U S A 101:1093–1098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He G, Zhu X, Elling AA, Chen L, Wang X, Guo L, Liang M, He H, Zhang H, Chen F, Qi Y, Chen R, Deng XW (2010) Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell 22:17–33

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hibara K, Isono M, Mimura M, Sentoku N, Kojima M, Sakakibara H, Kitomi Y, Yoshikawa T, Itoh J, Nagato Y (2016) Jasmonate regulates juvenile-to-adult phase transition in rice. Development 143:3407–3416

    Article  CAS  PubMed  Google Scholar 

  • Hong H, Liu Y, Zhang H, Xiao J, Li X, Wang S (2015a) Small RNAs and gene network in a durable disease resistance gene-mediated defense responses in rice. PLoS One 10:e0137360

    Article  PubMed  PubMed Central  Google Scholar 

  • Hong W, Qian D, Sun R, Jiang L, Wang Y, Wei C, Zhang Z, Li Y (2015b) OsRDR6 plays role in host defense against double-stranded RNA virus, Rice Dwarf Phytoreovirus. Sci Rep 5:11324

    Article  PubMed  PubMed Central  Google Scholar 

  • Hu B, Zhu C, Li F, Tang J, Wang Y, Lin A, Liu L, Che R, Chu C (2011) LEAF TIP NECROSIS1 plays a pivotal role in the regulation of multiple phosphate starvation responses in rice. Plant Physiol 156:1101–1115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hunter C, Sun H, Poething RS (2003) The Arabidopsis heterochronic gene ZIPPY is an ARGONAUTE family member. Curr Biol 13:1734–1739

    Article  CAS  PubMed  Google Scholar 

  • Jeong DH, Green PJ (2013) The role of rice microRNAs in abiotic stress responses. J Plant Biol 56:187–197

    Article  CAS  Google Scholar 

  • Jeong DH, Park S, Zhai J, Gurazada SGR, De Paoli E, Meyers BC, Green PJ (2011) Massive analysis of rice small RNAs: mechanistic implications of regulated microRNAs and variants for differential target RNA cleavage. Plant Cell 23:4185–4207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang L, Qian D, Zheng H, Meng LY, Chen J, Le WJ, Zhou T, Zhou YJ, Wei CH, Li Y (2012) RNA-dependent RNA polymerase 6 of rice (Oryza sativa) plays role in host defense against negative-strand RNA virus, Rice stripe virus. Virus Res 163:512–519

    Article  CAS  PubMed  Google Scholar 

  • Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X, Qian Q, Li J (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42:541–544

    Article  CAS  PubMed  Google Scholar 

  • Kapoor M, Arora R, Lama T, Nijhawan A, Khurana JP, Tyagi AK, Kapoor S (2008) Genome-wide identification, organization and phylogenetic analysis of Dicer-like, Argonaute and RNA-dependent RNA polymerase gene families and their expression analysis during reproductive development and stress in rice. BMC Genomics 9:451

    Article  PubMed  PubMed Central  Google Scholar 

  • Komiya R (2017) Biogenesis of diverse plant phasiRNAs involves an miRNA-trigger and Dicer-processing. J Plant Res 130:17–23

    Article  CAS  PubMed  Google Scholar 

  • Lauter N, Kampani A, Carison S, Gobel M, Moose SP (2005) microRNA172 down-regulates glossy15 to promote vegetative phase change in maize. Proc Natl Acad Sci U S A 102:9412–9417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li HJ, Li XH, Xiao JH, Wing RA, Wang SP (2012) Ortholog alleles at Xa3/Xa26 locus confer conserved race-specific resistance against Xanthomonas oryzae in rice. Mol Plant 5:281–290

    Article  CAS  PubMed  Google Scholar 

  • Li Y et al (2014) Multiple rice microRNAs are involved in immunity against the blast fungus Magnaporthe oryzae. Plant Physiol 164:1077–1092

    Article  CAS  PubMed  Google Scholar 

  • Lin SI, Santi C, Jobet E, Lacut E, Kholti NE, Karlowski WM, Verdeil JL, Breitler JC, Périn C, Ko SS, Guiderdoni E, Chiou TJ, Echeverria M (2010) Complex regulation of two target genes encoding SPX-MFS proteins by rice miR827 in response to phosphate starvation. Plant Cell Physiol 51:2119–2131

    Article  CAS  PubMed  Google Scholar 

  • Liu B, Li P, Li X, Liu C, Cao S, Chu C, Cao X (2005) Loss of function of OsDCL1 affects microRNA accumulation and causes developmental defects in rice. Plant Physiol 139:296–305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu B, Chen Z, Song X, Liu C, Cui X, Zhao X, Fang J, Xu W, Zhang H, Wang X, Chu C, Deng X, Xue Y, Cao X (2007) Oryza sativa dicer-like4 reveals a key role for small interfering RNA silencing in plant development. Plant Cell 19:2705–2718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Margis R, Fusaro AF, Smith NA, Curtin SJ, Watson JM, Finnegan EJ, Waterhouse PM (2006) The evolution and diversification of Dicers in plants. FEBS Lett 580:2442–2450

    Article  CAS  PubMed  Google Scholar 

  • Miura K, Ikeda M, Matsubara A, Song XJ, Ito M, Asano K, Matsuoka M, Kitano H, Ashikari M (2010) OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet 42:545–549

    Article  CAS  PubMed  Google Scholar 

  • Mourrain P, Béclin C, Elmayan T, Feuerbach F, Godon C, Morel JB, Jouette D, Lacombe AM, Nikic S, Picault N, Rémoué K, Sanial M, Vo TA, Vaucheret H (2000) Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101:533–542

    Article  CAS  PubMed  Google Scholar 

  • Nagasaki H, Itoh J, Hayashi K, Hibara K, Satoh-Nagasawa N, Nosaka M, Mukouhata M, Ashikari M, Kitano H, Matsuoka M, Nagato Y, Sato Y (2007) The small interfering RNA production pathway is required for shoot meristem initiation in rice. Proc Natl Acad Sci U S A 104:14867–14871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nobuta K et al (2007) An expression atlas of rice mRNAs and small RNAs. Nat Biotechnol 25:473–477

    Article  CAS  PubMed  Google Scholar 

  • Nonomura K, Morohoshi A, Nakano M, Eiguchi M, Miyao A, Hirochika H, Kurata N (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  CAS  PubMed  PubMed Central  Google Scholar 

  • Nosaka M, Itoh J, Nagato Y, Ono A, Ishiwata A, Sato Y (2012) Role of transposon-derived small RNAs in the interplay between genomes and parasitic DNA in rice. PLoS Genet 8:e1002953

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng M, Hannam C, Gu H, Bi YM, Rothstein SJ (2007) A mutation in NLA, which encodes a RING-type ubiquitin ligase, disrupts the adaptability of Arabidopsis to nitrogen limitation. Plant J 50:320–337

    Article  CAS  PubMed  Google Scholar 

  • Peng T, Lv Q, Zhang J, Li J, Du Y, Zhao Q (2011) Differential expression of the microRNAs in superior and inferior spikelets in rice (Oryza sariva). J Exp Bot 62:4943–4954

    Article  CAS  PubMed  Google Scholar 

  • Peng T, Du Y, Zhang J, Li J, Liu Y, Zhao Y, Sun H, Zhao Q (2013) Genome-wide analysis of 24-nt siRNAs dynamic variations during rice superior and inferior grain filling. PLoS One 8:e61029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peragine A, Ypshikawa M, Wu G, Albrecht HL, Poethig RS (2004) SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev 18:2368–2379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Secco D, Jabnoune M, Walker H, Shou H, Wu P, Poirier Y, Whelan J (2013) Spatio-temporal transcript profiling of rice roots and shoots in response to phosphate starvation and recovery. Plant Cell 25:4285–4304

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seo JK, Wu J, Lii Y, Li Y, Jin H (2013) Contribution of small RNA pathway components in plant immunity. Mol Plant-Microbe Interact 26:617–625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith MR, Willmann MR, Wu G, Berardini TZ, Moller B, Weijers D, Poethig RS (2009) Cyclophilin 40 is required for microRNA activity in Arabidopsis. Proc Natl Acad Sci U S A 106:5424–5429

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song X, Li P, Zhai J, Zhou M, Ma L, Liu B, Jeong DH, Nakano M, Cao S, Liu C, Chu C, Wang XJ, Green PJ, Meyers BC, Cao X (2012) Roles of DCL4 and DCL3b in rice phased small RNA biogenesis. Plant J 69:462–474

    Article  CAS  PubMed  Google Scholar 

  • Sun X, Cao Y, Yang Z, Xu C, Li X, Wang S, Zhang Q (2004) Xa26, a gene conferring resistance to Xanthomonas oryzae pv. oryzae in rice, encodes an LRR receptor kinase-like protein. Plant J 37:517–527

    Article  CAS  PubMed  Google Scholar 

  • Takeda A, Iwasaki S, Watanabe T, Utsumi M, Watanabe Y (2008) The mechanism selecting the guide strand from small RNA duplexes is different among argonaute proteins. Plant Cell Physiol 49:493–500

    Article  CAS  PubMed  Google Scholar 

  • Tanaka N, Itoh H, Sentoku N, Kojima M, Sakakibara H, Izawa T, Itoh J, Nagato Y (2011) The COP1 ortholog PPS regulates the juvenile–adult and vegetative–reproductive phase changes in rice. Plant Cell 23:2143–2154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Toriba T, Suzaki T, Yamaguchi T, Ohmori Y, Tsukaya H, Hirano HY (2010) Distinct regulation of adaxial-abaxial polarity in anther patterning in rice. Plant Cell 22:1452–1462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Sun X, Hoshino Y, Yu Y, Jia B, Sun Z, Sun M, Duan X, Zhu Y (2014) MicroRNA319 positively regulates cold tolerance by targeting OsPCF6 and OsTCP21 in rice (Oryza sativa L.) PLoS One 9:e91357

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang L, Sun S, Jin J, Fu D, Yang X, Weng X, Xu C, Li X, Xiao J, Zhang Q (2015) Coordinated regulation of vegetative and reproductive branching in rice. Proc Natl Acad Sci U S A 112:15504–15509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang H, Jiao X, Kong X, Hamera S, Wu Y, Chen X, Fang R, Yan Y (2016) A signaling cascade from miR444 to RDR1 in rice antiviral RNA silencing pathway. Plant Physiol 170:2365–2377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei L, Gu L, Song X, Cui X, Lu Z, Zhou M, Wang L, Hu F, Zhai J, Meyers BC, Cao X (2014) Dicer-like 3 produces transposable element-associated 24-nt siRNAs that control agricultural traits in rice. Proc Natl Acad Sci U S A 111:3877–3882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133:3539–3547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu L, Zhou H, Zhang Q, Zhang J, Ni F, Liu C, Qi Y (2010) DNA methylation mediated by a microRNA pathway. Mol Cell 38:465–475

    Article  CAS  PubMed  Google Scholar 

  • Wu J et al (2017) ROS accumulation and antiviral defence control by microRNA528 in rice. Nat Plants 3:16203

    Article  CAS  PubMed  Google Scholar 

  • Xia K, Wang R, Ou X, Fang Z, Tian C, Duan J, Wang Y, Zhang M (2012) OsTIR1 and OsAFB2 downregulation via OsmiR393 overexpression leads to more tillers, early flowering and less tolerance to salt and drought in rice. PLoS One 7:e30039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie K, Wu C, Xiong L (2006) Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol 142:280–293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xue LJ, Zhang JJ, Xue HW (2009) Characterization and expression profiles of miRNAs in rice seeds. Nucleic Acids Res 37:916–930

    Article  CAS  PubMed  Google Scholar 

  • Yan Y, Wang H, Hamera S, Chen X, Fang R (2014) miR444a has multiple functions in the rice nitrate-signaling pathway. Plant J 78:44–55

    Article  CAS  PubMed  Google Scholar 

  • Yoshikawa T, Ozawa S, Sentoku N, Itoh J-I, Nagato Y, Yokoi S (2013) Change of shoot architecture during juvenile-to-adult phase transition in soybean. Planta 238:229–237

    Article  CAS  PubMed  Google Scholar 

  • Yue E, Liu Z, Li C, Li Y, Liu Q, Xu JH (2017) Overexpression of miR529a confers enhanced resistance to oxidative stress in rice (Oryza sativa L.) Plant Cell Rep 36:1171–1182

    Article  CAS  PubMed  Google Scholar 

  • Zhang YC, Yu Y, Wang CY, Li ZY, Liu Q, Xu J, Liao JY, Wang XJ, Qu LH, Chen F, Xin P, Yan C, Chu J, Li HQ, Chen YQ (2013) Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching. Nat Biotechnol 31:848–852

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Peng Y, Wei X, Dai Y, Yuan D, Lu Y, Pan Y, Zhu Z (2014) Small RNAs as important regulators for the hybrid vigour of super-hybrid rice. J Exp Bot 65:5989–6002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Zhang J, Yan J, Gou F, Mao Y, Tang G, Botella JR, Zhu JK (2017) Short tandem target mimic rice lines uncover functions of miRNAs in regulating important agronomic traits. Proc Natl Acad Sci U S A 114:5277–5282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao B, Liang R, Ge L, Li W, Xiao H, Lin H, Ruan K, Jin Y (2007) Identification of drought-induced microRNAs in rice. BBRC 354:585–590

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yutaka Sato .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Sato, Y., Nosaka-Takahashi, M., Suzuki, T., Shimizu-Sato, S. (2018). Small RNAs in Rice: Molecular Species and Their Functions. In: Sasaki, T., Ashikari, M. (eds) Rice Genomics, Genetics and Breeding. Springer, Singapore. https://doi.org/10.1007/978-981-10-7461-5_2

Download citation

Publish with us

Policies and ethics