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Reproductive phasiRNAs regulate reprogramming of gene expression and meiotic progression in rice
  1. 1.

    Nelms, B. & Walbot, V. Defining the developmental program leading to meiosis in maize. Science 364, 52–56 (2019).

    ADS  CAS  PubMed  Article  Google Scholar 

  2. 2.

    Nonomura, K. I. Small RNA pathways responsible for non-cell-autonomous regulation of plant reproduction. Plant Reprod. 31, 21–29 (2018).

    CAS  PubMed  Article  Google Scholar 

  3. 3.

    Yu, Y., Zhou, Y., Zhang, Y. & Chen, Y. Grass phasiRNAs and male fertility. Sci. China Life Sci. 61, 148–154 (2018).

    CAS  PubMed  Article  Google Scholar 

  4. 4.

    Komiya, R. et al. Rice germline-specific Argonaute MEL1 protein binds to phasiRNAs generated from more than 700 lincRNAs. Plant J. 78, 385–397 (2014).

    CAS  PubMed  Article  Google Scholar 

  5. 5.

    Fei, Q., Yang, L., Liang, W., Zhang, D. & Meyers, B. C. Dynamic changes of small RNAs in rice spikelet development reveal specialized reproductive phasiRNA pathways. J. Exp. Bot. 67, 6037–6049 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  6. 6.

    Zhai, J. et al. Spatiotemporally dynamic, cell-type-dependent premeiotic and meiotic phasiRNAs in maize anthers. Proc. Natl Acad. Sci. USA 112, 3146–3151 (2015).

    ADS  CAS  PubMed  Article  Google Scholar 

  7. 7.

    Johnson, C. et al. Clusters and superclusters of phased small RNAs in the developing inflorescence of rice. Genome Res. 19, 1429–1440 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  8. 8.

    Dukowic-Schulze, S. et al. Novel meiotic miRNAs and indications for a role of PhasiRNAs in meiosis. Front Plant Sci. 7, 762 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  9. 9.

    Araki, S. et al. miR2118-dependent U-rich phasiRNA production in rice anther wall development. Nat. Commun. 11, 3115 (2020).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  10. 10.

    Fan, Y. et al. PMS1T, producing phased small-interfering RNAs, regulates photoperiod-sensitive male sterility in rice. Proc. Natl Acad. Sci. U.S.A 113, 15144–15149 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  11. 11.

    Ma, Z. & Zhang, X. Actions of plant Argonautes: predictable or unpredictable? Curr. Opin. Plant Biol. 45, 59–67 (2018).

    CAS  PubMed  Article  Google Scholar 

  12. 12.

    Patel, P., Mathioni, S., Kakrana, A., Shatkay, H. & Meyers, B. C. Reproductive phasiRNAs in grasses are compositionally distinct from other classes of small RNAs. N. Phytol. 220, 851–864 (2018).

    CAS  Article  Google Scholar 

  13. 13.

    Tamim, S. et al. Cis-directed cleavage and nonstoichiometric abundances of 21-nucleotide reproductive phased small interfering RNAs in grasses. New Phytol. 220, 865–877 (2018).

    CAS  PubMed  Article  Google Scholar 

  14. 14.

    Nonomura, K. et al. 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 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  15. 15.

    Ono, S. et al. EAT1 transcription factor, a non-cell-autonomous regulator of pollen production, activates meiotic small RNA biogenesis in rice anther tapetum. PLoS Genet. 14, e1007238 (2018).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  16. 16.

    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).

    CAS  PubMed  Article  Google Scholar 

  17. 17.

    Dai, P. et al. A translation-activating function of MIWI/piRNA during mouse spermiogenesis. Cell 179, 1566–1581 e16 (2019).

    CAS  PubMed  Article  Google Scholar 

  18. 18.

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

    ADS  CAS  PubMed  Article  Google Scholar 

  19. 19.

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  20. 20.

    Shiu, S. H. & Bleecker, A. B. Plant receptor-like kinase gene family: diversity, function, and signaling. Sci. STKE 2001, re22 (2001).

    CAS  PubMed  Google Scholar 

  21. 21.

    Nonomura, K. et al. The MSP1 gene is necessary to restrict the number of cells entering into male and female sporogenesis and to initiate anther wall formation in rice. Plant Cell 15, 1728–1739 (2003).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  22. 22.

    Hord, C. L., Chen, C., Deyoung, B. J., Clark, S. E. & Ma, H. The BAM1/BAM2 receptor-like kinases are important regulators of Arabidopsis early anther development. Plant Cell 18, 1667–1680 (2006).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  23. 23.

    Zhao, D. Z., Wang, G. F., Speal, B. & Ma, H. The excess microsporocytes1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev. 16, 2021–2031 (2002).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  24. 24.

    Cui, Y. et al. CIK receptor kinases determine cell fate specification during early anther development in Arabidopsis. Plant Cell 30, 2383–2401 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  25. 25.

    Colcombet, J., Boisson-Dernier, A., Ros-Palau, R., Vera, C. E. & Schroeder, J. I. Arabidopsis somatic embryogenesis receptor kinases 1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17, 3350–3361 (2005).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  26. 26.

    Yokoyama, R., Takahashi, T., Kato, A., Torii, K. U. & Komeda, Y. The Arabidopsis ERECTA gene is expressed in the shoot apical meristem and organ primordia. Plant J. 15, 301–310 (1998).

    CAS  PubMed  Article  Google Scholar 

  27. 27.

    Takasaki, T. et al. The S receptor kinase determines self-incompatibility in Brassica stigma. Nature 403, 913–916 (2000).

    ADS  CAS  PubMed  Article  Google Scholar 

  28. 28.

    Stein, J. C., Howlett, B., Boyes, D. C., Nasrallah, M. E. & Nasrallah, J. B. Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc. Natl Acad. Sci. USA 88, 8816–8820 (1991).

    ADS  CAS  PubMed  Article  Google Scholar 

  29. 29.

    Song, X. et al. Roles of DCL4 and DCL3b in rice phased small RNA biogenesis. Plant J. 69, 462–474 (2012).

    CAS  PubMed  Article  Google Scholar 

  30. 30.

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  31. 31.

    Deng, P., Muhammad, S., Cao, M. & Wu, L. Biogenesis and regulatory hierarchy of phased small interfering RNAs in plants. Plant Biotechnol. J. 16, 965–975 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  32. 32.

    Zhang, Y. C. et al. Genome-wide screening and functional analysis identify a large number of long noncoding RNAs involved in the sexual reproduction of rice. Genome Biol. 15, 512 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  33. 33.

    Reuter, M. et al. Miwi catalysis is required for piRNA amplification-independent LINE1 transposon silencing. Nature 480, 264–267 (2011).

    ADS  CAS  PubMed  Article  Google Scholar 

  34. 34.

    Zhang, P. et al. MIWI and piRNA-mediated cleavage of messenger RNAs in mouse testes. Cell Res. 25, 193–207 (2015).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  35. 35.

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  36. 36.

    Yu, Y., Jia, T. & Chen, X. The ‘how’ and ‘where’ of plant microRNAs. N. Phytol. 216, 1002–1017 (2017).

    CAS  Article  Google Scholar 

  37. 37.

    de Felippes, F. F. Gene regulation mediated by microRNA-triggered secondary small RNAs in plants. Plants 8, 112 (2019).

  38. 38.

    Morgan, M. et al. A programmed wave of uridylation-primed mRNA degradation is essential for meiotic progression and mammalian spermatogenesis. Cell Res. 29, 221–232 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  39. 39.

    Tang, J. & Chu, C. MicroRNAs in crop improvement: fine-tuners for complex traits. Nat. Plants 3, 17077 (2017).

    PubMed  Article  Google Scholar 

  40. 40.

    Kinoshita, A. et al. RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development 137, 3911–3920 (2010).

    CAS  PubMed  Article  Google Scholar 

  41. 41.

    Yamamoto, M., Nishio, T. & Nasrallah, J. B. Activation of self-incompatibility signaling in transgenic Arabidopsis thaliana is independent of AP2-based clathrin-mediated endocytosis. G3 (Bethesda) 8, 2231–2239 (2018).

    CAS  Article  Google Scholar 

  42. 42.

    Fan, Y. & Zhang, Q. Genetic and molecular characterization of photoperiod and thermo-sensitive male sterility in rice. Plant Reprod. 31, 3–14 (2018).

    CAS  PubMed  Article  Google Scholar 

  43. 43.

    Guan, X. et al. miR828 and miR858 regulate homoeologous MYB2 gene functions in Arabidopsis trichome and cotton fibre development. Nat. Commun. 5, 3050 (2014).

    ADS  PubMed  Article  CAS  Google Scholar 

  44. 44.

    Zhang, Y. C. et al. Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching. Nat. Biotechnol. 31, 848–852 (2013).

    CAS  PubMed  Article  Google Scholar 

  45. 45.

    Ma, X. et al. A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol. Plant 8, 1274–1284 (2015).

    CAS  PubMed  Article  Google Scholar 

  46. 46.

    He, F., Zhang, F., Sun, W., Ning, Y. & Wang, G. L. A versatile vector toolkit for functional analysis of rice genes. Rice 11, 27 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  47. 47.

    Liu, B. et al. Loss of function of OsDCL1 affects microRNA accumulation and causes developmental defects in rice. Plant Physiol. 139, 296–305 (2005).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  48. 48.

    Tang, G. et al. Construction of short tandem target mimic (STTM) to block the functions of plant and animal microRNAs. Methods 58, 118–125 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  49. 49.

    Trapnell, C. et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511–515 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  50. 50.

    Trapnell, C. et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562–578 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  51. 51.

    Ouyang, S. et al. The TIGR rice genome annotation resource: improvements and new features. Nucleic Acids Res. 35, D883–D887 (2007).

    CAS  PubMed  Article  Google Scholar 

  52. 52.

    Meng, Y. J., Shao, C. G., Wang, H. Z., Ma, X. X. & Chen, M. Construction of gene regulatory networks mediated by vegetative and reproductive stage-specific small RNAs in rice (Oryza sativa). N. Phytologist 197, 441–453 (2013).

    CAS  Article  Google Scholar 

  53. 53.

    Kakrana, A., Hammond, R., Patel, P., Nakano, M. & Meyers, B. C. sPARTA: a parallelized pipeline for integrated analysis of plant miRNA and cleaved mRNA data sets, including new miRNA target-identification software. Nucleic Acids Res. 42, e139 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  54. 54.

    Mustroph, A., Juntawong, P. & Bailey-Serres, J. Isolation of plant polysomal mRNA by differential centrifugation and ribosome immunopurification methods. Methods Mol. Biol. 553, 109–126 (2009).

    CAS  PubMed  Article  Google Scholar 

Original Text (This is the original text for your reference.)

  1. 1.

    Nelms, B. & Walbot, V. Defining the developmental program leading to meiosis in maize. Science 364, 52–56 (2019).

    ADS  CAS  PubMed  Article  Google Scholar 

  2. 2.

    Nonomura, K. I. Small RNA pathways responsible for non-cell-autonomous regulation of plant reproduction. Plant Reprod. 31, 21–29 (2018).

    CAS  PubMed  Article  Google Scholar 

  3. 3.

    Yu, Y., Zhou, Y., Zhang, Y. & Chen, Y. Grass phasiRNAs and male fertility. Sci. China Life Sci. 61, 148–154 (2018).

    CAS  PubMed  Article  Google Scholar 

  4. 4.

    Komiya, R. et al. Rice germline-specific Argonaute MEL1 protein binds to phasiRNAs generated from more than 700 lincRNAs. Plant J. 78, 385–397 (2014).

    CAS  PubMed  Article  Google Scholar 

  5. 5.

    Fei, Q., Yang, L., Liang, W., Zhang, D. & Meyers, B. C. Dynamic changes of small RNAs in rice spikelet development reveal specialized reproductive phasiRNA pathways. J. Exp. Bot. 67, 6037–6049 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  6. 6.

    Zhai, J. et al. Spatiotemporally dynamic, cell-type-dependent premeiotic and meiotic phasiRNAs in maize anthers. Proc. Natl Acad. Sci. USA 112, 3146–3151 (2015).

    ADS  CAS  PubMed  Article  Google Scholar 

  7. 7.

    Johnson, C. et al. Clusters and superclusters of phased small RNAs in the developing inflorescence of rice. Genome Res. 19, 1429–1440 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  8. 8.

    Dukowic-Schulze, S. et al. Novel meiotic miRNAs and indications for a role of PhasiRNAs in meiosis. Front Plant Sci. 7, 762 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  9. 9.

    Araki, S. et al. miR2118-dependent U-rich phasiRNA production in rice anther wall development. Nat. Commun. 11, 3115 (2020).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  10. 10.

    Fan, Y. et al. PMS1T, producing phased small-interfering RNAs, regulates photoperiod-sensitive male sterility in rice. Proc. Natl Acad. Sci. U.S.A 113, 15144–15149 (2016).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  11. 11.

    Ma, Z. & Zhang, X. Actions of plant Argonautes: predictable or unpredictable? Curr. Opin. Plant Biol. 45, 59–67 (2018).

    CAS  PubMed  Article  Google Scholar 

  12. 12.

    Patel, P., Mathioni, S., Kakrana, A., Shatkay, H. & Meyers, B. C. Reproductive phasiRNAs in grasses are compositionally distinct from other classes of small RNAs. N. Phytol. 220, 851–864 (2018).

    CAS  Article  Google Scholar 

  13. 13.

    Tamim, S. et al. Cis-directed cleavage and nonstoichiometric abundances of 21-nucleotide reproductive phased small interfering RNAs in grasses. New Phytol. 220, 865–877 (2018).

    CAS  PubMed  Article  Google Scholar 

  14. 14.

    Nonomura, K. et al. 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 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  15. 15.

    Ono, S. et al. EAT1 transcription factor, a non-cell-autonomous regulator of pollen production, activates meiotic small RNA biogenesis in rice anther tapetum. PLoS Genet. 14, e1007238 (2018).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  16. 16.

    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).

    CAS  PubMed  Article  Google Scholar 

  17. 17.

    Dai, P. et al. A translation-activating function of MIWI/piRNA during mouse spermiogenesis. Cell 179, 1566–1581 e16 (2019).

    CAS  PubMed  Article  Google Scholar 

  18. 18.

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

    ADS  CAS  PubMed  Article  Google Scholar 

  19. 19.

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  20. 20.

    Shiu, S. H. & Bleecker, A. B. Plant receptor-like kinase gene family: diversity, function, and signaling. Sci. STKE 2001, re22 (2001).

    CAS  PubMed  Google Scholar 

  21. 21.

    Nonomura, K. et al. The MSP1 gene is necessary to restrict the number of cells entering into male and female sporogenesis and to initiate anther wall formation in rice. Plant Cell 15, 1728–1739 (2003).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  22. 22.

    Hord, C. L., Chen, C., Deyoung, B. J., Clark, S. E. & Ma, H. The BAM1/BAM2 receptor-like kinases are important regulators of Arabidopsis early anther development. Plant Cell 18, 1667–1680 (2006).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  23. 23.

    Zhao, D. Z., Wang, G. F., Speal, B. & Ma, H. The excess microsporocytes1 gene encodes a putative leucine-rich repeat receptor protein kinase that controls somatic and reproductive cell fates in the Arabidopsis anther. Genes Dev. 16, 2021–2031 (2002).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  24. 24.

    Cui, Y. et al. CIK receptor kinases determine cell fate specification during early anther development in Arabidopsis. Plant Cell 30, 2383–2401 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  25. 25.

    Colcombet, J., Boisson-Dernier, A., Ros-Palau, R., Vera, C. E. & Schroeder, J. I. Arabidopsis somatic embryogenesis receptor kinases 1 and 2 are essential for tapetum development and microspore maturation. Plant Cell 17, 3350–3361 (2005).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  26. 26.

    Yokoyama, R., Takahashi, T., Kato, A., Torii, K. U. & Komeda, Y. The Arabidopsis ERECTA gene is expressed in the shoot apical meristem and organ primordia. Plant J. 15, 301–310 (1998).

    CAS  PubMed  Article  Google Scholar 

  27. 27.

    Takasaki, T. et al. The S receptor kinase determines self-incompatibility in Brassica stigma. Nature 403, 913–916 (2000).

    ADS  CAS  PubMed  Article  Google Scholar 

  28. 28.

    Stein, J. C., Howlett, B., Boyes, D. C., Nasrallah, M. E. & Nasrallah, J. B. Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc. Natl Acad. Sci. USA 88, 8816–8820 (1991).

    ADS  CAS  PubMed  Article  Google Scholar 

  29. 29.

    Song, X. et al. Roles of DCL4 and DCL3b in rice phased small RNA biogenesis. Plant J. 69, 462–474 (2012).

    CAS  PubMed  Article  Google Scholar 

  30. 30.

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  31. 31.

    Deng, P., Muhammad, S., Cao, M. & Wu, L. Biogenesis and regulatory hierarchy of phased small interfering RNAs in plants. Plant Biotechnol. J. 16, 965–975 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  32. 32.

    Zhang, Y. C. et al. Genome-wide screening and functional analysis identify a large number of long noncoding RNAs involved in the sexual reproduction of rice. Genome Biol. 15, 512 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  33. 33.

    Reuter, M. et al. Miwi catalysis is required for piRNA amplification-independent LINE1 transposon silencing. Nature 480, 264–267 (2011).

    ADS  CAS  PubMed  Article  Google Scholar 

  34. 34.

    Zhang, P. et al. MIWI and piRNA-mediated cleavage of messenger RNAs in mouse testes. Cell Res. 25, 193–207 (2015).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  35. 35.

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  36. 36.

    Yu, Y., Jia, T. & Chen, X. The ‘how’ and ‘where’ of plant microRNAs. N. Phytol. 216, 1002–1017 (2017).

    CAS  Article  Google Scholar 

  37. 37.

    de Felippes, F. F. Gene regulation mediated by microRNA-triggered secondary small RNAs in plants. Plants 8, 112 (2019).

  38. 38.

    Morgan, M. et al. A programmed wave of uridylation-primed mRNA degradation is essential for meiotic progression and mammalian spermatogenesis. Cell Res. 29, 221–232 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  39. 39.

    Tang, J. & Chu, C. MicroRNAs in crop improvement: fine-tuners for complex traits. Nat. Plants 3, 17077 (2017).

    PubMed  Article  Google Scholar 

  40. 40.

    Kinoshita, A. et al. RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development 137, 3911–3920 (2010).

    CAS  PubMed  Article  Google Scholar 

  41. 41.

    Yamamoto, M., Nishio, T. & Nasrallah, J. B. Activation of self-incompatibility signaling in transgenic Arabidopsis thaliana is independent of AP2-based clathrin-mediated endocytosis. G3 (Bethesda) 8, 2231–2239 (2018).

    CAS  Article  Google Scholar 

  42. 42.

    Fan, Y. & Zhang, Q. Genetic and molecular characterization of photoperiod and thermo-sensitive male sterility in rice. Plant Reprod. 31, 3–14 (2018).

    CAS  PubMed  Article  Google Scholar 

  43. 43.

    Guan, X. et al. miR828 and miR858 regulate homoeologous MYB2 gene functions in Arabidopsis trichome and cotton fibre development. Nat. Commun. 5, 3050 (2014).

    ADS  PubMed  Article  CAS  Google Scholar 

  44. 44.

    Zhang, Y. C. et al. Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching. Nat. Biotechnol. 31, 848–852 (2013).

    CAS  PubMed  Article  Google Scholar 

  45. 45.

    Ma, X. et al. A robust CRISPR/Cas9 system for convenient, high-efficiency multiplex genome editing in monocot and dicot plants. Mol. Plant 8, 1274–1284 (2015).

    CAS  PubMed  Article  Google Scholar 

  46. 46.

    He, F., Zhang, F., Sun, W., Ning, Y. & Wang, G. L. A versatile vector toolkit for functional analysis of rice genes. Rice 11, 27 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  47. 47.

    Liu, B. et al. Loss of function of OsDCL1 affects microRNA accumulation and causes developmental defects in rice. Plant Physiol. 139, 296–305 (2005).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  48. 48.

    Tang, G. et al. Construction of short tandem target mimic (STTM) to block the functions of plant and animal microRNAs. Methods 58, 118–125 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  49. 49.

    Trapnell, C. et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511–515 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  50. 50.

    Trapnell, C. et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562–578 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  51. 51.

    Ouyang, S. et al. The TIGR rice genome annotation resource: improvements and new features. Nucleic Acids Res. 35, D883–D887 (2007).

    CAS  PubMed  Article  Google Scholar 

  52. 52.

    Meng, Y. J., Shao, C. G., Wang, H. Z., Ma, X. X. & Chen, M. Construction of gene regulatory networks mediated by vegetative and reproductive stage-specific small RNAs in rice (Oryza sativa). N. Phytologist 197, 441–453 (2013).

    CAS  Article  Google Scholar 

  53. 53.

    Kakrana, A., Hammond, R., Patel, P., Nakano, M. & Meyers, B. C. sPARTA: a parallelized pipeline for integrated analysis of plant miRNA and cleaved mRNA data sets, including new miRNA target-identification software. Nucleic Acids Res. 42, e139 (2014).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  54. 54.

    Mustroph, A., Juntawong, P. & Bailey-Serres, J. Isolation of plant polysomal mRNA by differential centrifugation and ribosome immunopurification methods. Methods Mol. Biol. 553, 109–126 (2009).

    CAS  PubMed  Article  Google Scholar 

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