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  • Review Article
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Plant microRNA maturation and function

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Abstract

Since their discovery in 2002, much has been learnt about plant microRNAs (miRNAs), including the genes that encode them and the target genes that they regulate; the microprocessor complex that produces the miRNAs and the effector ARGONAUTE (AGO) proteins with which miRNAs associate; the mechanisms of target-RNA recognition by miRNAs and miRNA modes of action; miRNA subcellular localization; and miRNA mobility between cells and within plants. In this Review, we discuss new mechanistic insights into miRNA maturation and AGO loading, the subcellular locations of miRNA processing and activity and partitioning of miRNAs between the nucleus and cytoplasm, which in turn affects their intercellular mobility. We also discuss intriguing connections between miRNAs and the translation process and present hypotheses to be tested by future studies.

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Fig. 1: An overview of microRNA biogenesis and function in plants.
Fig. 2: Mechanisms and regulation of microRNA processing.
Fig. 3: HYL1 function and regulation in microRNA biogenesis and activity.
Fig. 4: AGO1 loading in the nucleus and cytoplasm.
Fig. 5: Translation repression versus transcript cleavage.

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References

  1. Park, W., Li, J., Song, R., Messing, J. & Chen, X. Carpel factory, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr. Biol. 12, 1484–1495 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Llave, C., Kasschau, K. D., Rector, M. A. & Carrington, J. C. Endogenous and silencing-associated small RNAs in plants. Plant Cell 14, 1605–1619 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Reinhart, B. J., Weinstein, E. G., Rhoades, M. W., Bartel, B. & Bartel, D. P. MicroRNAs in plants. Genes Dev. 16, 1616–1626 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Song, X., Li, Y., Cao, X. & Qi, Y. MicroRNAs and their regulatory roles in plant–environment interactions. Annu. Rev. Plant Biol. 70, 489–525 (2019).

    Article  CAS  PubMed  Google Scholar 

  5. Yu, Y., Zhang, Y., Chen, X. & Chen, Y. Plant noncoding RNAs: hidden players in development and stress responses. Annu. Rev. Cell Dev. Biol. 35, 407–431 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Mencia, R., Gonzalo, L., Tossolini, I. & Manavella, P. A. Keeping up with the miRNAs: current paradigms of the biogenesis pathway. J. Exp. Bot. 74, 2213–2227 (2023).

    Article  CAS  PubMed  Google Scholar 

  7. Zhan, J. & Meyers, B. C. Plant small RNAs: their biogenesis, regulatory roles, and functions. Annu. Rev. Plant Biol. 74, 21–51 (2023).

    Article  CAS  PubMed  Google Scholar 

  8. Xie, Z. et al. Expression of Arabidopsis MIRNA genes. Plant Physiol. 138, 2145–2154 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Han, M. H., Goud, S., Song, L. & Fedoroff, N. The Arabidopsis double-stranded RNA-binding protein HYL1 plays a role in microRNA-mediated gene regulation. Proc. Natl Acad. Sci. USA 101, 1093–1098 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Lobbes, D., Rallapalli, G., Schmidt, D. D., Martin, C. & Clarke, J. SERRATE: a new player on the plant microRNA scene. EMBO Rep. 7, 1052–1058 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Fang, Y. & Spector, D. L. Identification of nuclear dicing bodies containing proteins for microRNA biogenesis in living Arabidopsis plants. Curr. Biol. 17, 818–823 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Song, L., Han, M. H., Lesicka, J. & Fedoroff, N. Arabidopsis primary microRNA processing proteins HYL1 and DCL1 define a nuclear body distinct from the Cajal body. Proc. Natl Acad. Sci. USA 104, 5437–5442 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Dong, Z., Han, M. H. & Fedoroff, N. The RNA-binding proteins HYL1 and SE promote accurate in vitro processing of pri-miRNA by DCL1. Proc. Natl Acad. Sci. USA 105, 9970–9975 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Schwartz, B., Yeung, C. & Meinke, W. Disruption of morphogenesis and transformation of the suspensor in abnormal suspensor mutants of Arabidopsis. Development 120, 3235–3245 (1994).

    Article  CAS  PubMed  Google Scholar 

  15. Ray, A., Lang, J. D., Golden, T. & Ray, S. Short integument (SIN1), a gene required for ovule development in Arabidopsis, also controls flowering time. Development 122, 2631–2638 (1996).

    Article  CAS  PubMed  Google Scholar 

  16. Jacobsen, S. E., Running, M. P. & Meyerowitz, E. M. Disruption of an RNA helicase/RNAse III gene in Arabidopsis causes unregulated cell division in floral meristems. Development 126, 5231–5243 (1999).

    Article  CAS  PubMed  Google Scholar 

  17. Kurihara, Y. & Watanabe, Y. Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions. Proc. Natl Acad. Sci. USA 101, 12753–12758 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Papp, I. et al. Evidence for nuclear processing of plant micro RNA and short interfering RNA precursors. Plant Physiol. 132, 1382–1390 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Park, M. Y., Wu, G., Gonzalez-Sulser, A., Vaucheret, H. & Poethig, R. S. Nuclear processing and export of microRNAs in Arabidopsis. Proc. Natl Acad. Sci. USA 102, 3691–3696 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Margis, R. et al. The evolution and diversification of Dicers in plants. FEBS Lett. 580, 2442–2450 (2006).

    Article  CAS  PubMed  Google Scholar 

  21. Wei, X. et al. Structural basis of microRNA processing by Dicer-like 1. Nat. Plants 7, 1389–1396 (2021). This paper reported cryo-EM structures of DCL1 complexed with either a pri-miRNA or a pre-miRNA and revealed mechanisms of function of DCL1 in miRNA biogenesis, such as substrate recognition and successive cleavages.

    Article  CAS  PubMed  Google Scholar 

  22. Hiraguri, A. et al. Specific interactions between Dicer-like proteins and HYL1/DRB-family dsRNA-binding proteins in Arabidopsis thaliana. Plant Mol. Biol. 57, 173–188 (2005).

    Article  CAS  PubMed  Google Scholar 

  23. Jin, W., Wang, J., Liu, C. P., Wang, H. W. & Xu, R. M. Structural basis for pri-miRNA recognition by Drosha. Mol. Cell 78, 423–433 (2020).

    Article  CAS  PubMed  Google Scholar 

  24. Partin, A. C. et al. Cryo-EM structures of human Drosha and DGCR8 in complex with primary microRNA. Mol. Cell 78, 411–422 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Lee, Y. Y., Kim, H. & Kim, V. N. Sequence determinant of small RNA production by DICER. Nature 615, 323–330 (2023).

    Article  CAS  PubMed  Google Scholar 

  26. Wang, Q. et al. Mechanism of siRNA production by a plant Dicer–RNA complex in dicing-competent conformation. Science 374, 1152–1157 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Kurihara, Y., Takashi, Y. & Watanabe, Y. The interaction between DCL1 and HYL1 is important for efficient and precise processing of pri-miRNA in plant microRNA biogenesis. RNA 12, 206–212 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Machida, S., Chen, H. Y. & Adam Yuan, Y. Molecular insights into miRNA processing by Arabidopsis thaliana SERRATE. Nucleic Acids Res. 39, 7828–7836 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Wu, F. et al. The N-terminal double-stranded RNA binding domains of Arabidopsis HYPONASTIC LEAVES1 are sufficient for pre-microRNA processing. Plant Cell 19, 914–925 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Reis, R. S., Eamens, A. L., Roberts, T. H. & Waterhouse, P. M. Chimeric DCL1-partnering proteins provide insights into the microRNA pathway. Front. Plant Sci. 6, 1201 (2015).

    PubMed  Google Scholar 

  31. Yang, X. et al. Homodimerization of HYL1 ensures the correct selection of cleavage sites in primary miRNA. Nucleic Acids Res. 42, 12224–12236 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Wieczorek, P., Jarmołowski, A., Szweykowska-Kulińska, Z., Kozak, M. & Taube, M. Solution structure and behaviour of the Arabidopsis thaliana HYL1 protein. Biochim. Biophys. Acta Gen. Subj. 1867, 130376 (2023).

    Article  CAS  PubMed  Google Scholar 

  33. Manavella, P. A. et al. Fast-forward genetics identifies plant CPL phosphatases as regulators of miRNA processing factor HYL1. Cell 151, 859–870 (2012).

    Article  CAS  PubMed  Google Scholar 

  34. Jozwiak, M., Bielewicz, D., Szweykowska-Kulinska, Z., Jarmolowski, A. & Bajczyk, M. SERRATE: a key factor in coordinated RNA processing in plants. Trends Plant Sci. 28, 841–853 (2023).

    Article  CAS  PubMed  Google Scholar 

  35. Xie, D. et al. Phase separation of SERRATE drives dicing body assembly and promotes miRNA processing in Arabidopsis. Nat. Cell Biol. 23, 32–39 (2021). This study found that the phase separation property of SERRATE drives the formation of dicing bodies containing the microprocessor and pri-miRNAs, thereby providing a new perspective for understanding miRNA biosynthesis in plants.

    Article  CAS  PubMed  Google Scholar 

  36. Iwata, Y., Takahashi, M., Fedoroff, N. V. & Hamdan, S. M. Dissecting the interactions of SERRATE with RNA and DICER-LIKE 1 in Arabidopsis microRNA precursor processing. Nucleic Acids Res. 41, 9129–9140 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Song, L., Axtell, M. J. & Fedoroff, N. V. RNA secondary structural determinants of miRNA precursor processing in Arabidopsis. Curr. Biol. 20, 37–41 (2010).

    Article  CAS  PubMed  Google Scholar 

  38. Chorostecki, U. et al. Evolutionary footprints reveal insights into plant microRNA biogenesis. Plant Cell 29, 1248–1261 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Mateos, J. L., Bologna, N. G., Chorostecki, U. & Palatnik, J. F. Identification of microRNA processing determinants by random mutagenesis of Arabidopsis MIR172a precursor. Curr. Biol. 20, 49–54 (2010).

    Article  CAS  PubMed  Google Scholar 

  40. Werner, S., Wollmann, H., Schneeberger, K. & Weigel, D. Structure determinants for accurate processing of miR172a in Arabidopsis thaliana. Curr. Biol. 20, 42–48 (2010).

    Article  CAS  PubMed  Google Scholar 

  41. Bologna, N. G., Mateos, J. L., Bresso, E. G. & Palatnik, J. F. A loop-to-base processing mechanism underlies the biogenesis of plant microRNAs miR319 and miR159. EMBO J. 28, 3646–3656 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Zhu, H. et al. Bidirectional processing of pri-miRNAs with branched terminal loops by Arabidopsis Dicer-like 1. Nat. Struct. Mol. Biol. 20, 1106–1115 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Yan, X. et al. Parallel degradome-seq and DMS-MaPseq substantially revise the miRNA biogenesis atlas in Arabidopsis. Nat. Plants 10, 1126–1143 (2024). This study mapped the initial DCL1-mediated cleavage sites of pri-miRNAs, profiled the secondary structures of pri-miRNAs genome wide and provided an atlas of pri-miRNA processing patterns.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Narjala, A., Nair, A., Tirumalai, V., Hari Sundar, G. V. & Shivaprasad, P. V. A conserved sequence signature is essential for robust plant miRNA biogenesis. Nucleic Acids Res. 48, 3103–3118 (2020). This study showed that the presence of specific GC-rich sequence signatures within the miRNA–miRNA* region is required for precise miRNA biogenesis.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Yang, S. W. et al. Structure of Arabidopsis HYPONASTIC LEAVES1 and its molecular implications for miRNA processing. Structure 18, 594–605 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Rojas, A. M. L. et al. Identification of key sequence features required for microRNA biogenesis in plants. Nat. Commun. 11, 5320 (2020). This study identified the key sequence features required for the biosynthesis of plant miRNAs.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Hirata, R. et al. Unpaired nucleotides on the stem of microRNA precursor are important for precise cleavage by DICER-LIKE 1 in Arabidopsis. Genes Cell 27, 280–292 (2022).

    Article  CAS  Google Scholar 

  48. Song, J. et al. Prevalent cytidylation and uridylation of precursor miRNAs in Arabidopsis. Nat. Plants 5, 1260–1272 (2019).

    Article  CAS  PubMed  Google Scholar 

  49. Bhat, S. S. et al. mRNA adenosine methylase (MTA) deposits m(6)A on pri-miRNAs to modulate miRNA biogenesis in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 117, 21785–21795 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Gonzalo, L., Giudicatti, A. J. & Manavella, P. A. HYL1’s multiverse: a journey through miRNA biogenesis and beyond canonical and non-canonical functions of HYL1. Curr. Opin. Plant Biol. 80, 102546 (2024).

    Article  CAS  PubMed  Google Scholar 

  51. Achkar, N. P. et al. A quick HYL1-dependent reactivation of microRNA production is required for a proper developmental response after extended periods of light deprivation. Dev. Cell 46, 236–247 (2018).

    Article  CAS  PubMed  Google Scholar 

  52. Jung, H. J. et al. HYL1-CLEAVAGE SUBTILASE 1 (HCS1) suppresses miRNA biogenesis in response to light-to-dark transition. Proc. Natl Acad. Sci. USA 119, e2116757119 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Zhang, Z. et al. KETCH1 imports HYL1 to nucleus for miRNA biogenesis in Arabidopsis. Proc. Natl Acad. Sci. USA 114, 4011–4016 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Su, C. et al. The PROTEIN PHOSPHATASE 4 and SMEK1 complex dephosphorylates HYL1 to promote miRNA biogenesis by antagonizing the MAPK cascade in Arabidopsis. Dev. Cell 41, 527–539 (2017).

    Article  CAS  PubMed  Google Scholar 

  55. Wang, S. et al. The PROTEIN PHOSPHATASE4 complex promotes transcription and processing of primary microRNAs in Arabidopsis. Plant Cell 31, 486–501 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Raghuram, B., Sheikh, A. H., Rustagi, Y. & Sinha, A. K. MicroRNA biogenesis factor DRB1 is a phosphorylation target of mitogen activated protein kinase MPK3 in both rice and Arabidopsis. FEBS J. 282, 521–536 (2015).

    Article  CAS  PubMed  Google Scholar 

  57. Yan, J. et al. The SnRK2 kinases modulate miRNA accumulation in Arabidopsis. PLoS Genet. 13, e1006753 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  58. Bajczyk, M. et al. SERRATE interacts with the nuclear exosome targeting (NEXT) complex to degrade primary miRNA precursors in Arabidopsis. Nucleic Acids Res. 48, 6839–6854 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Wang, L. et al. PRP4KA phosphorylates SERRATE for degradation via 20S proteasome to fine-tune miRNA production in Arabidopsis. Sci. Adv. 8, eabm8435 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Liu, C., Axtell, M. J. & Fedoroff, N. V. The helicase and RNaseIIIa domains of Arabidopsis Dicer-Like1 modulate catalytic parameters during microRNA biogenesis. Plant Physiol. 159, 748–758 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Sang, Q. et al. MicroRNA156 conditions auxin sensitivity to enable growth plasticity in response to environmental changes in Arabidopsis. Nat. Commun. 14, 1449 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Ma, E., MacRae, I. J., Kirsch, J. F. & Doudna, J. A. Autoinhibition of human dicer by its internal helicase domain. J. Mol. Biol. 380, 237–243 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Lee, Y. Y., Lee, H., Kim, H., Kim, V. N. & Roh, S. H. Structure of the human DICER–pre-miRNA complex in a dicing state. Nature 615, 331–338 (2023).

    Article  CAS  PubMed  Google Scholar 

  64. Jia, T. et al. The Arabidopsis MOS4-associated complex promotes microRNA biogenesis and precursor messenger RNA splicing. Plant Cell 29, 2626–2643 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Zhang, B. et al. Linking key steps of microRNA biogenesis by TREX-2 and the nuclear pore complex in Arabidopsis. Nat. Plants 6, 957–969 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Liang, C. et al. Arabidopsis RBV is a conserved WD40 repeat protein that promotes microRNA biogenesis and ARGONAUTE1 loading. Nat. Commun. 13, 1217 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Li, Q. et al. DEAD-box helicases modulate dicing body formation in Arabidopsis. Sci. Adv. 7, eabc6266 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Qiao, Y., Shi, J., Zhai, Y., Hou, Y. & Ma, W. Phytophthora effector targets a novel component of small RNA pathway in plants to promote infection. Proc. Natl Acad. Sci. USA 112, 5850–5855 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Gonzalo, L. et al. R-loops at microRNA encoding loci promote co-transcriptional processing of pri-miRNAs in plants. Nat. Plants 8, 402–418 (2022). This study demonstrated that most Arabidopsis pri-miRNAs are processed both co-transcriptionally and post-transcriptionally and that R-loops near TSSs promote co-transcriptional processing.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Fang, X., Cui, Y., Li, Y. & Qi, Y. Transcription and processing of primary microRNAs are coupled by Elongator complex in Arabidopsis. Nat. Plants 1, 15075 (2015).

    Article  CAS  PubMed  Google Scholar 

  71. Wang, L. et al. NOT2 proteins promote polymerase II-dependent transcription and interact with multiple microRNA biogenesis factors in Arabidopsis. Plant Cell 25, 715–727 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Cambiagno, D. A. et al. HASTY modulates miRNA biogenesis by linking pri-miRNA transcription and processing. Mol. Plant 14, 426–439 (2021).

    Article  CAS  PubMed  Google Scholar 

  73. Stepien, A. et al. Chromatin-associated microprocessor assembly is regulated by the U1 snRNP auxiliary protein PRP40. Plant Cell 34, 4920–4935 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  74. Bielewicz, D. et al. Hyponastic leaves 1 interacts with RNA Pol II to ensure proper transcription of microRNA genes. Plant Cell Physiol. 64, 571–582 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Park, J. et al. The high expression of osmotically responsive GENE15-HISTONE DEACETYLASE9 complex associates with HYPONASTIC LEAVES 1 to modulate microRNA expression in response to abscisic acid signaling. Plant Cell 35, 2910–2928 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Hudzik, C., Maguire, S., Guan, S., Held, J. & Axtell, M. J. Trans-species microRNA loci in the parasitic plant Cuscuta campestris have a U6-like snRNA promoter. Plant Cell 35, 1834–1847 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Yu, B. et al. Methylation as a crucial step in plant microRNA biogenesis. Science 307, 932–935 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Baumberger, N. & Baulcombe, D. C. Arabidopsis ARGONAUTE1 is an RNA slicer that selectively recruits microRNAs and short interfering RNAs. Proc. Natl Acad. Sci. USA 102, 11928–11933 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Qi, Y., Denli, A. M. & Hannon, G. J. Biochemical specialization within Arabidopsis RNA silencing pathways. Mol. Cell 19, 421–428 (2005).

    Article  CAS  PubMed  Google Scholar 

  80. Mi, S. et al. Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5′ terminal nucleotide. Cell 133, 116–127 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Zhang, X. et al. Arabidopsis argonaute 2 regulates innate immunity via miRNA393(*)-mediated silencing of a Golgi-localized SNARE gene. MEMB12. Mol. Cell 42, 356–366 (2011).

    Article  CAS  PubMed  Google Scholar 

  82. Niu, D. et al. Bacillus cereus AR156 primes induced systemic resistance by suppressing miR825/825* and activating defense-related genes in Arabidopsis. J. Integr. Plant Biol. 58, 426–439 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Bohmert, K. et al. AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J. 17, 170–180 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Li, Z. et al. Origin, evolution and diversification of plant ARGONAUTE proteins. Plant J. 109, 1086–1097 (2022).

    Article  CAS  PubMed  Google Scholar 

  85. Lingel, A., Simon, B., Izaurralde, E. & Sattler, M. Nucleic acid 3′-end recognition by the Argonaute2 PAZ domain. Nat. Struct. Mol. Biol. 11, 576–577 (2004).

    Article  CAS  PubMed  Google Scholar 

  86. Ma, J. B., Ye, K. & Patel, D. J. Structural basis for overhang-specific small interfering RNA recognition by the PAZ domain. Nature 429, 318–322 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Song, J. J., Smith, S. K., Hannon, G. J. & Joshua-Tor, L. Crystal structure of Argonaute and its implications for RISC slicer activity. Science 305, 1434–1437 (2004).

    Article  CAS  PubMed  Google Scholar 

  88. Frank, F., Sonenberg, N. & Nagar, B. Structural basis for 5′-nucleotide base-specific recognition of guide RNA by human AGO2. Nature 465, 818–822 (2010).

    Article  CAS  PubMed  Google Scholar 

  89. Kwak, P. B. & Tomari, Y. The N domain of Argonaute drives duplex unwinding during RISC assembly. Nat. Struct. Mol. Biol. 19, 145–151 (2012).

    Article  CAS  PubMed  Google Scholar 

  90. Wang, Y., Sheng, G., Juranek, S., Tuschl, T. & Patel, D. J. Structure of the guide-strand-containing argonaute silencing complex. Nature 456, 209–213 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Nakanishi, K., Weinberg, D. E., Bartel, D. P. & Patel, D. J. Structure of yeast Argonaute with guide RNA. Nature 486, 368–374 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Schirle, N. T. & MacRae, I. J. The crystal structure of human Argonaute2. Science 336, 1037–1040 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Xiao, Y. & MacRae, I. J. The molecular mechanism of microRNA duplex selectivity of Arabidopsis ARGONAUTE10. Nucleic Acids Res. 50, 10041–10052 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Frank, F., Hauver, J., Sonenberg, N. & Nagar, B. Arabidopsis argonaute MID domains use their nucleotide specificity loop to sort small RNAs. EMBO J. 31, 3588–3595 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Zhu, H. et al. Arabidopsis argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 145, 242–256 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Endo, Y., Iwakawa, H. O. & Tomari, Y. Arabidopsis ARGONAUTE7 selects miR390 through multiple checkpoints during RISC assembly. EMBO Rep. 14, 652–658 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Li, H. et al. A spontaneous thermo-sensitive female sterility mutation in rice enables fully mechanized hybrid breeding. Cell Res. 32, 931–945 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Zhang, X. et al. ARGONAUTE PIWI domain and microRNA duplex structure regulate small RNA sorting in Arabidopsis. Nat. Commun. 5, 5468 (2014).

    Article  PubMed  Google Scholar 

  99. Bortolamiol, D., Pazhouhandeh, M., Marrocco, K., Genschik, P. & Ziegler-Graff, V. The Polerovirus F box protein P0 targets ARGONAUTE1 to suppress RNA silencing. Curr. Biol. 17, 1615–1621 (2007).

    Article  CAS  PubMed  Google Scholar 

  100. Csorba, T., Lózsa, R., Hutvágner, G. & Burgyán, J. Polerovirus protein P0 prevents the assembly of small RNA-containing RISC complexes and leads to degradation of ARGONAUTE1. Plant J. 62, 463–472 (2010).

    Article  CAS  PubMed  Google Scholar 

  101. Michaeli, S. et al. The viral F-box protein P0 induces an ER-derived autophagy degradation pathway for the clearance of membrane-bound AGO1. Proc. Natl Acad. Sci. USA 116, 22872–22883 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Chiu, M. H., Chen, I. H., Baulcombe, D. C. & Tsai, C. H. The silencing suppressor P25 of Potato virus X interacts with Argonaute1 and mediates its degradation through the proteasome pathway. Mol. Plant Pathol. 11, 641–649 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Várallyay, E., Válóczi, A., Agyi, A., Burgyán, J. & Havelda, Z. Plant virus-mediated induction of miR168 is associated with repression of ARGONAUTE1 accumulation. EMBO J. 29, 3507–3519 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  104. Blagojevic, A. et al. Heat stress promotes Arabidopsis AGO1 phase separation and association with stress granule components. iScience 27, 109151 (2024).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Hacquard, T. et al. The Arabidopsis F-box protein FBW2 targets AGO1 for degradation to prevent spurious loading of illegitimate small RNA. Cell Rep. 39, 110671 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Bologna, N. G. et al. Nucleo-cytosolic shuttling of ARGONAUTE1 prompts a revised model of the plant microRNA pathway. Mol. Cell 69, 709–719.e5 (2018).

    Article  CAS  PubMed  Google Scholar 

  107. Xu, Y. et al. The N-terminal extension of Arabidopsis ARGONAUTE 1 is essential for microRNA activities. PLoS Genet. 19, e1010450 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Fan, L. et al. Microtubules promote the non-cell autonomous action of microRNAs by inhibiting their cytoplasmic loading onto ARGONAUTE1 in Arabidopsis. Dev. Cell 57, 995–1008 (2022). This study found that microtubules promote the non-cell-autonomous function of miRNAs by inhibiting their loading onto AGO1 in the cytoplasm.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Dalmadi, Á., Gyula, P., Bálint, J., Szittya, G. & Havelda, Z. AGO-unbound cytosolic pool of mature miRNAs in plant cells reveals a novel regulatory step at AGO1 loading. Nucleic Acids Res. 47, 9803–9817 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Eamens, A. L., Smith, N. A., Curtin, S. J., Wang, M. B. & Waterhouse, P. M. The Arabidopsis thaliana double-stranded RNA binding protein DRB1 directs guide strand selection from microRNA duplexes. RNA 15, 2219–2235 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Tomassi, A. H. et al. The intrinsically disordered protein CARP9 bridges HYL1 to AGO1 in the nucleus to promote microRNA activity. Plant Physiol. 184, 316–329 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Iki, T. et al. In vitro assembly of plant RNA-induced silencing complexes facilitated by molecular chaperone HSP90. Mol. Cell 39, 282–291 (2010).

    Article  CAS  PubMed  Google Scholar 

  113. Iwasaki, S. et al. Hsc70/Hsp90 chaperone machinery mediates ATP-dependent RISC loading of small RNA duplexes. Mol. Cell 39, 292–299 (2010).

    Article  CAS  PubMed  Google Scholar 

  114. Iki, T., Yoshikawa, M., Meshi, T. & Ishikawa, M. Cyclophilin 40 facilitates HSP90-mediated RISC assembly in plants. EMBO J. 31, 267–278 (2012).

    Article  CAS  PubMed  Google Scholar 

  115. Miyoshi, T., Takeuchi, A., Siomi, H. & Siomi, M. C. A direct role for Hsp90 in pre-RISC formation in Drosophila. Nat. Struct. Mol. Biol. 17, 1024–1026 (2010).

    Article  CAS  PubMed  Google Scholar 

  116. Naruse, K., Matsuura-Suzuki, E., Watanabe, M., Iwasaki, S. & Tomari, Y. In vitro reconstitution of chaperone-mediated human RISC assembly. RNA 24, 6–11 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Tsuboyama, K., Tadakuma, H. & Tomari, Y. Conformational activation of Argonaute by distinct yet coordinated actions of the Hsp70 and Hsp90 chaperone systems. Mol. Cell 70, 722–729.e4 (2018).

    Article  CAS  PubMed  Google Scholar 

  118. Iki, T., Takami, M. & Kai, T. Modulation of Ago2 loading by cyclophilin 40 endows a unique repertoire of functional miRNAs during sperm maturation in Drosophila. Cell Rep. 33, 108380 (2020).

    Article  CAS  PubMed  Google Scholar 

  119. Martinez, N. J. & Gregory, R. I. Argonaute2 expression is post-transcriptionally coupled to microRNA abundance. RNA 19, 605–612 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Pare, J. M., LaPointe, P. & Hobman, T. C. Hsp90 cochaperones p23 and FKBP4 physically interact with hAgo2 and activate RNA interference-mediated silencing in mammalian cells. Mol. Biol. Cell 24, 2303–2310 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Wang, W. et al. An importin β protein negatively regulates microRNA activity in Arabidopsis. Plant Cell 23, 3565–3576 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Cui, Y., Fang, X. & Qi, Y. TRANSPORTIN1 promotes the association of microRNA with ARGONAUTE1 in Arabidopsis. Plant Cell 28, 2576–2585 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. You, C. et al. FIERY1 promotes microRNA accumulation by suppressing rRNA-derived small interfering RNAs in Arabidopsis. Nat. Commun. 10, 4424 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  124. Hang, R. et al. Arabidopsis HOT3/eIF5B1 constrains rRNA RNAi by facilitating 18S rRNA maturation. Proc. Natl Acad. Sci. USA 120, e2301081120 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Gonzalo, L. et al. The nuclear pore complex acts as a hub for pri-miRNA transcription and processing in plants. Preprint at bioRxiv 2024.2010.2024.620027 (2024).

  126. Brioudes, F. et al. HASTY, the Arabidopsis EXPORTIN5 ortholog, regulates cell-to-cell and vascular microRNA movement. EMBO J. 40, e107455 (2021). This study revealed a requirement for HASTY in the intercellular and vascular transport of plant microRNAs.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Devers, E. A. et al. Movement and differential consumption of short interfering RNA duplexes underlie mobile RNA interference. Nat. Plants 6, 789–799 (2020).

    Article  CAS  PubMed  Google Scholar 

  128. Shi, C. et al. Temperature-sensitive male sterility in rice determined by the roles of AGO1d in reproductive phasiRNA biogenesis and function. N. Phytol. 236, 1529–1544 (2022).

    Article  CAS  Google Scholar 

  129. Si, F. et al. Mobile ARGONAUTE 1d binds 22-nt miRNAs to generate phasiRNAs important for low-temperature male fertility in rice. Sci. China Life Sci. 66, 197–208 (2023). This study revealed that mobile AGO1d binds 22-nt miRNAs to generate phased siRNAs, which are crucial for male fertility in rice in low temperatures, thereby providing insights into the environmental functions of plant miRNAs.

    Article  CAS  PubMed  Google Scholar 

  130. Tamotsu, H., Koizumi, K., Briones, A. V. & Komiya, R. Spatial distribution of three ARGONAUTEs regulates the anther phasiRNA pathway. Nat. Commun. 14, 3333 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Erokhina, T. N., Ryazantsev, D. Y., Zavriev, S. K. & Morozov, S. Y. Regulatory miPEP open reading frames contained in the primary transcripts of microRNAs. Int. J. Mol. Sci. 24, 2114 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Li, S. et al. Biogenesis of phased siRNAs on membrane-bound polysomes in Arabidopsis. eLife 5, e22750 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  135. Li, S. et al. MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell 153, 562–574 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Brodersen, P. et al. Widespread translational inhibition by plant miRNAs and siRNAs. Science 320, 1185–1190 (2008).

    Article  CAS  PubMed  Google Scholar 

  137. Lauressergues, D. et al. Primary transcripts of microRNAs encode regulatory peptides. Nature 520, 90–93 (2015).

    Article  CAS  PubMed  Google Scholar 

  138. Sharma, A., Badola, P. K., Bhatia, C., Sharma, D. & Trivedi, P. K. Primary transcript of miR858 encodes regulatory peptide and controls flavonoid biosynthesis and development in Arabidopsis. Nat. Plants 6, 1262–1274 (2020).

    Article  CAS  PubMed  Google Scholar 

  139. Lauressergues, D. et al. Characterization of plant microRNA-encoded peptides (miPEPs) reveals molecular mechanisms from the translation to activity and specificity. Cell Rep. 38, 110339 (2022).

    Article  CAS  PubMed  Google Scholar 

  140. Lu, L. et al. MicroRNA-encoded regulatory peptides modulate cadmium tolerance and accumulation in rice. Plant Cell Environ. 47, 1452–1470 (2024).

    Article  CAS  PubMed  Google Scholar 

  141. Couzigou, J. M., André, O., Guillotin, B., Alexandre, M. & Combier, J. P. Use of microRNA-encoded peptide miPEP172c to stimulate nodulation in soybean. N. Phytol. 211, 379–381 (2016).

    Article  CAS  Google Scholar 

  142. Chen, Q. J. et al. A miRNA-encoded small peptide, vvi-miPEP171d1, regulates adventitious root formation. Plant Physiol. 183, 656–670 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Wu, H. L. et al. Improved super-resolution ribosome profiling reveals prevalent translation of upstream ORFs and small ORFs in Arabidopsis. Plant Cell 36, 510–539 (2024).

    Article  CAS  PubMed  Google Scholar 

  144. Fei, Q., Xia, R. & Meyers, B. C. Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks. Plant Cell 25, 2400–2415 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Xia, R. et al. 24-nt reproductive phasiRNAs are broadly present in angiosperms. Nat. Commun. 10, 627 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Teng, C. et al. Dicer-like 5 deficiency confers temperature-sensitive male sterility in maize. Nat. Commun. 11, 2912 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Hou, C. Y. et al. Global analysis of truncated RNA ends reveals new insights into ribosome stalling in plants. Plant Cell 28, 2398–2416 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Bazin, J. et al. Global analysis of ribosome-associated noncoding RNAs unveils new modes of translational regulation. Proc. Natl Acad. Sci. USA 114, e10018–e10027 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Yoshikawa, M. et al. A short open reading frame encompassing the microRNA173 target site plays a role in trans-acting small interfering RNA biogenesis. Plant. Physiol. 171, 359–368 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Zhang, C., Ng, D. W., Lu, J. & Chen, Z. J. Roles of target site location and sequence complementarity in trans-acting siRNA formation in Arabidopsis. Plant. J. 69, 217–226 (2012).

    Article  CAS  PubMed  Google Scholar 

  151. Iwakawa, H. O. et al. Ribosome stalling caused by the Argonaute–microRNA–SGS3 complex regulates the production of secondary siRNAs in plants. Cell Rep. 35, 109300 (2021).

    Article  CAS  PubMed  Google Scholar 

  152. Yang, X. et al. Comparative ribosome profiling reveals distinct translational landscapes of salt-sensitive and -tolerant rice. BMC Genomics 22, 612 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Ren, G. et al. Methylation protects microRNAs from an AGO1-associated activity that uridylates 5′ RNA fragments generated by AGO1 cleavage. Proc. Natl Acad. Sci. USA 111, 6365–6370 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Zuber, H., Scheer, H., Joly, A. C. & Gagliardi, D. Respective contributions of URT1 and HESO1 to the uridylation of 5′ fragments produced from RISC-cleaved mRNAs. Front. Plant Sci. 9, 1438 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  155. Souret, F. F., Kastenmayer, J. P. & Green, P. J. AtXRN4 degrades mRNA in Arabidopsis and its substrates include selected miRNA targets. Mol. Cell 15, 173–183 (2004).

    Article  CAS  PubMed  Google Scholar 

  156. Branscheid, A. et al. SKI2 mediates degradation of RISC 5′-cleavage fragments and prevents secondary siRNA production from miRNA targets in Arabidopsis. Nucleic Acids Res. 43, 10975–10988 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Vigh, M. L., Bressendorff, S., Thieffry, A., Arribas-Hernández, L. & Brodersen, P. Nuclear and cytoplasmic RNA exosomes and PELOTA1 prevent miRNA-induced secondary siRNA production in Arabidopsis. Nucleic Acids Res. 50, 1396–1415 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  158. Lanet, E. et al. Biochemical evidence for translational repression by Arabidopsis microRNAs. Plant Cell 21, 1762–1768 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Yang, X. et al. Widespread occurrence of microRNA-mediated target cleavage on membrane-bound polysomes. Genome Biol. 22, 15 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Iwakawa, H. O. & Tomari, Y. Molecular insights into microRNA-mediated translational repression in plants. Mol. Cell 52, 591–601 (2013).

    Article  CAS  PubMed  Google Scholar 

  161. Grant-Downton, R. et al. Artificial microRNAs reveal cell-specific differences in small RNA activity in pollen. Curr. Biol. 23, R599–R601 (2013).

    Article  CAS  PubMed  Google Scholar 

  162. Rong, F. et al. Switching action modes of miR408-5p mediates auxin signaling in rice. Nat. Commun. 15, 2525 (2024). This study found that miR408-5p mediates auxin signalling in rice by switching its modes of action between transcript cleavage and translation inhibition.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Ding, N. & Zhang, B. microRNA production in Arabidopsis. Front. Plant Sci. 14, 1096772 (2023).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  164. Cai, Q. et al. The disease resistance protein SNC1 represses the biogenesis of microRNAs and phased siRNAs. Nat. Commun. 9, 5080 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  165. Sun, Z., Guo, T., Liu, Y., Liu, Q. & Fang, Y. The roles of Arabidopsis CDF2 in transcriptional and posttranscriptional regulation of primary microRNAs. PLoS Genet. 11, e1005598 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  166. Wang, J. et al. Spliceosome disassembly factors ILP1 and NTR1 promote miRNA biogenesis in Arabidopsis thaliana. Nucleic Acids Res. 47, 7886–7900 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  167. Hajheidari, M., Farrona, S., Huettel, B., Koncz, Z. & Koncz, C. CDKF;1 and CDKD protein kinases regulate phosphorylation of serine residues in the C-terminal domain of Arabidopsis RNA polymerase II. Plant Cell 24, 1626–1642 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Xu, M., Leichty, A. R., Hu, T. & Poethig, R. S. H2A.Z promotes the transcription of MIR156A and MIR156C in Arabidopsis by facilitating the deposition of H3K4me3. Development 145, dev152868 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  169. Kim, W. et al. Histone acetyltransferase GCN5 interferes with the miRNA pathway in Arabidopsis. Cell Res. 19, 899–909 (2009).

    Article  CAS  PubMed  Google Scholar 

  170. Xu, M., Hu, T., Smith, M. R. & Poethig, R. S. Epigenetic regulation of vegetative phase change in Arabidopsis. Plant Cell 28, 28–41 (2016).

    Article  CAS  PubMed  Google Scholar 

  171. Grigorova, B. et al. LEUNIG and SEUSS co-repressors regulate miR172 expression in Arabidopsis flowers. Development 138, 2451–2456 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  172. Xie, Y. et al. Phytochrome-interacting factors directly suppress MIR156 expression to enhance shade-avoidance syndrome in Arabidopsis. Nat. Commun. 8, 348 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  173. Wang, F. & Perry, S. E. Identification of direct targets of FUSCA3, a key regulator of Arabidopsis seed development. Plant Physiol. 161, 1251–1264 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Yumul, R. E. et al. POWERDRESS and diversified expression of the MIR172 gene family bolster the floral stem cell network. PLoS Genet. 9, e1003218 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

Research on small RNAs in the Chen laboratory is funded by the National Natural Science Foundation of China (32488102 and 32070614), Ministry of Science and Technology of the People’s Republic of China (Chinese Ministry of Science and Technology, 2023YFC3402200), Qidong-SLS Innovation Fund and the National Center for Protein Sciences at Peking University.

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Glossary

Elongator

A highly conserved protein complex in eukaryotes that has crucial roles in diverse molecular processes, including transcription elongation, tRNA modification and protein acetylation.

Mediator

A large protein complex that recruits RNA polymerase II to genes for transcription initiation of both protein-coding genes and non-coding RNA genes.

miRNA*

Refers to the passenger strand of a mature miRNA duplex, which is typically degraded; however, some miRNA* may be incorporated into the RNA-induced silencing complex and mediate gene silencing.

Processing bodies

(P-bodies). Cytoplasmic membrane-less organelles that increase in size and number in stress conditions. P-bodies consist of RNA and proteins associated with mRNA decay and function in both mRNA degradation and translation repression.

Ribo-seq

A high-throughput sequencing technique used for translatome profiling, which enables the identification of ribosome-protected regions in RNAs as well as their translational status, such as ribosome pausing and ribosome collisions.

Secondary phased small interfering RNAs

siRNAs that are processed from double-stranded RNA in a phased manner. They are ‘secondary’ because their biogenesis is triggered by a ‘primary’ small RNA (miRNA or siRNA).

siRNA bodies

Cytoplasmic foci that are formed by AGO7, SGS3 and RDR6 and are responsible for tasiRNA production.

Stress granules

Stress-induced cytoplasmic membrane-less granules, which comprise RNA and translation-related proteins and act as mRNA storage sites to help the cell cope with and recover from stress.

Trans-acting siRNAs

Often abbreviated as ‘tasiRNAs’, a subset of secondary phased siRNAs with a demonstrated role in the regulation of gene expression in trans (similar to miRNAs).

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Yu, Y., Wang, H., You, C. et al. Plant microRNA maturation and function. Nat Rev Mol Cell Biol 27, 55–70 (2026). https://doi.org/10.1038/s41580-025-00871-y

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