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Small RNAs in Rice: Molecular Species and Their Functions

  • Yutaka Sato
  • Misuzu Nosaka-Takahashi
  • Toshiya Suzuki
  • Sae Shimizu-Sato
Chapter

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.

Keywords

Oryza sativa Rice Small RNA siRNA miRNA DICER AGO 

References

  1. 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 154:1335–1346CrossRefPubMedPubMedCentralGoogle Scholar
  2. Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741CrossRefPubMedPubMedCentralGoogle Scholar
  3. 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 141:1000–1011CrossRefPubMedPubMedCentralGoogle Scholar
  4. Baldrich P, San Segundo B (2016) MicroRNAs in rice innate immunity. Rice (N Y) 9:6CrossRefPubMedCentralGoogle Scholar
  5. 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 12:847–863CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bari R, Pant BD, Stitt M, Scheible WR (2006) PHO2, MicroRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999CrossRefPubMedPubMedCentralGoogle Scholar
  7. Borges F, Martienssen RA (2015) The expanding world of small RNAs in plants. Nat Rev Mol Cell Biol 16:727–741CrossRefPubMedPubMedCentralGoogle Scholar
  8. 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 199:212–227CrossRefPubMedGoogle Scholar
  9. 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 52:971–980CrossRefPubMedGoogle Scholar
  10. 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 8:538–547CrossRefPubMedGoogle Scholar
  11. Chuck G, Cigan AM, Saeteurn K, Hake S (2007) The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat Genet 39:544–549CrossRefPubMedGoogle Scholar
  12. Csorba T, Kontra L, Burgyán J (2015) Viral silencing suppressors: tools forged to fine-tune host-pathogen coexistence. Virology 479–480:85–103CrossRefPubMedGoogle Scholar
  13. 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 80:1108–1117CrossRefPubMedGoogle Scholar
  14. Cuperus JT, Fahlgren N, Carrington JC (2011) Evolution and functional diversification of MIRNA genes. Plant Cell 23:431–442CrossRefPubMedPubMedCentralGoogle Scholar
  15. Ding Y, Ye Y, Jiang Z, Wang Y, Zhu C (2016) MicroRNA390 is involved in cadmium tolerance and accumulation in rice. Front Plant Sci 7:235PubMedPubMedCentralGoogle Scholar
  16. 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:e1002176CrossRefPubMedPubMedCentralGoogle Scholar
  17. 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 2:15203CrossRefPubMedGoogle Scholar
  18. Fang X, Qi Y (2016) RNAi in plants: an Argonaute-centered view. Plant Cell 28:272–285CrossRefPubMedPubMedCentralGoogle Scholar
  19. Fei Q, Xia R, Meyers BC (2013) Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks. Plant Cell 25:2400–2415CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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 2:15196CrossRefPubMedGoogle Scholar
  21. 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 101:1093–1098CrossRefPubMedPubMedCentralGoogle Scholar
  22. 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 22:17–33CrossRefPubMedPubMedCentralGoogle Scholar
  23. 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 143:3407–3416CrossRefPubMedGoogle Scholar
  24. 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:e0137360CrossRefPubMedPubMedCentralGoogle Scholar
  25. 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 5:11324CrossRefPubMedPubMedCentralGoogle Scholar
  26. 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 156:1101–1115CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hunter C, Sun H, Poething RS (2003) The Arabidopsis heterochronic gene ZIPPY is an ARGONAUTE family member. Curr Biol 13:1734–1739CrossRefPubMedGoogle Scholar
  28. Jeong DH, Green PJ (2013) The role of rice microRNAs in abiotic stress responses. J Plant Biol 56:187–197CrossRefGoogle Scholar
  29. 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 23:4185–4207CrossRefPubMedPubMedCentralGoogle Scholar
  30. 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 163:512–519CrossRefPubMedGoogle Scholar
  31. 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 42:541–544CrossRefPubMedGoogle Scholar
  32. 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 9:451CrossRefPubMedPubMedCentralGoogle Scholar
  33. Komiya R (2017) Biogenesis of diverse plant phasiRNAs involves an miRNA-trigger and Dicer-processing. J Plant Res 130:17–23CrossRefPubMedGoogle Scholar
  34. 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 102:9412–9417CrossRefPubMedPubMedCentralGoogle Scholar
  35. 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 5:281–290CrossRefPubMedGoogle Scholar
  36. Li Y et al (2014) Multiple rice microRNAs are involved in immunity against the blast fungus Magnaporthe oryzae. Plant Physiol 164:1077–1092CrossRefPubMedGoogle Scholar
  37. 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 51:2119–2131CrossRefPubMedGoogle Scholar
  38. 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 139:296–305CrossRefPubMedPubMedCentralGoogle Scholar
  39. 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 19:2705–2718CrossRefPubMedPubMedCentralGoogle Scholar
  40. 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 580:2442–2450CrossRefPubMedGoogle Scholar
  41. 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 42:545–549CrossRefPubMedGoogle Scholar
  42. 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 101:533–542CrossRefPubMedGoogle Scholar
  43. 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 104:14867–14871CrossRefPubMedPubMedCentralGoogle Scholar
  44. Nobuta K et al (2007) An expression atlas of rice mRNAs and small RNAs. Nat Biotechnol 25:473–477CrossRefPubMedGoogle Scholar
  45. 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 19:2583–2594CrossRefPubMedPubMedCentralGoogle Scholar
  46. 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:e1002953CrossRefPubMedPubMedCentralGoogle Scholar
  47. 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 50:320–337CrossRefPubMedGoogle Scholar
  48. 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 62:4943–4954CrossRefPubMedGoogle Scholar
  49. 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:e61029CrossRefPubMedPubMedCentralGoogle Scholar
  50. 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 18:2368–2379CrossRefPubMedPubMedCentralGoogle Scholar
  51. 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 25:4285–4304CrossRefPubMedPubMedCentralGoogle Scholar
  52. Seo JK, Wu J, Lii Y, Li Y, Jin H (2013) Contribution of small RNA pathway components in plant immunity. Mol Plant-Microbe Interact 26:617–625CrossRefPubMedPubMedCentralGoogle Scholar
  53. 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 106:5424–5429CrossRefPubMedPubMedCentralGoogle Scholar
  54. 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 69:462–474CrossRefPubMedGoogle Scholar
  55. 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 37:517–527CrossRefPubMedGoogle Scholar
  56. 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 49:493–500CrossRefPubMedGoogle Scholar
  57. 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 23:2143–2154CrossRefPubMedPubMedCentralGoogle Scholar
  58. 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 22:1452–1462CrossRefPubMedPubMedCentralGoogle Scholar
  59. Vaucheret H (2006) Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Dev 20:759–771CrossRefPubMedGoogle Scholar
  60. 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:e91357CrossRefPubMedPubMedCentralGoogle Scholar
  61. 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 112:15504–15509CrossRefPubMedPubMedCentralGoogle Scholar
  62. 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 170:2365–2377CrossRefPubMedPubMedCentralGoogle Scholar
  63. 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 111:3877–3882CrossRefPubMedPubMedCentralGoogle Scholar
  64. Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133:3539–3547CrossRefPubMedPubMedCentralGoogle Scholar
  65. Wu L, Zhou H, Zhang Q, Zhang J, Ni F, Liu C, Qi Y (2010) DNA methylation mediated by a microRNA pathway. Mol Cell 38:465–475CrossRefPubMedGoogle Scholar
  66. Wu J et al (2017) ROS accumulation and antiviral defence control by microRNA528 in rice. Nat Plants 3:16203CrossRefPubMedGoogle Scholar
  67. 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:e30039CrossRefPubMedPubMedCentralGoogle Scholar
  68. 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 142:280–293CrossRefPubMedPubMedCentralGoogle Scholar
  69. Xue LJ, Zhang JJ, Xue HW (2009) Characterization and expression profiles of miRNAs in rice seeds. Nucleic Acids Res 37:916–930CrossRefPubMedGoogle Scholar
  70. Yan Y, Wang H, Hamera S, Chen X, Fang R (2014) miR444a has multiple functions in the rice nitrate-signaling pathway. Plant J 78:44–55CrossRefPubMedGoogle Scholar
  71. 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 238:229–237CrossRefPubMedGoogle Scholar
  72. 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 36:1171–1182CrossRefPubMedGoogle Scholar
  73. 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 31:848–852CrossRefPubMedGoogle Scholar
  74. 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 65:5989–6002CrossRefPubMedPubMedCentralGoogle Scholar
  75. 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 114:5277–5282CrossRefPubMedPubMedCentralGoogle Scholar
  76. 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 354:585–590PubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Yutaka Sato
    • 1
  • Misuzu Nosaka-Takahashi
    • 1
  • Toshiya Suzuki
    • 1
  • Sae Shimizu-Sato
    • 1
  1. 1.National Institute of GeneticsMishimaJapan

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