Novel insights from non-conserved microRNAs in plants

Frontiers in Plant Science

Volumn 5, Issue October, 2014, Pages

  Qin, Zhengrui ^a   Li, Chunlian ^b   Mao, Long ^a   Wu, Liang ^a  

^a INSTITUTE OF PLANT PROTECTION   (China)

^b PEKING UNIVERSITY   (China)

Author keywords

Dicots; miRNA; Monocots; Role; Secondary siRNA

Indexed keywords

EID: 84908361215     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00586     Document Type: Review

References (85)

1. Addo-Quaye, C., Eshoo, T. W., Bartel, D. P., and Axtell, M. J. (2008). Endoge¬nous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Curr. Biol. 18, 758-762. doi: 10.1016/j.cub.2008.04.042.
2. Allen, E., and Howell, M. D. (2010). miRNAs in the biogenesis of trans¬acting siRNAs in higher plants. Semin. Cell Dev. Biol. 21, 798-804. doi: 10.1016/j.semcdb.2010.03.008.
3. Allen, E., Xie, Z., Gustafson, A. M., and Carrington, J. C. (2005). microRNA- directed phasing during trans-acting siRNA biogenesis in plants. Cell 121, 207-221. doi: 10.1016/j.cell.2005.04.004.
4. Axtell, M. J. (2013). Classification and comparison of small RNAs from plants. Annu. Rev. Plant Biol. 64, 137-159. doi: 10.1146/annurev-arplant-050312-120043.
5. Axtell, M. J., and Bowman, J. L. (2008). Evolution of plant microRNAs and their targets. Trends Plant Sci. 13, 343-349. doi: 10.1016/j.tplants.2008.03.009.
6. Baumberger, N., and Baulcombe, D. C. (2005). Arabidopsis ARGONAUTE1 is an RNA Slicer that selectively recruits microRNAs and short interfering RNAs. Proc. Natl. Acad. Sci. U.S.A. 102, 11928-11933. doi: 10.1073/pnas.0505461102.
7. Boccara, M., Sarazin, A., Thiebeauld, O., Jay, F., Voinnet, O., Navarro, L., et al. (2014). The Arabidopsis miR472-RDR6 silencing pathway modulates PAMP- and effector-triggered immunity through the post-transcriptional control of disease resistance genes. PLoS Pathog. 10:e1003883. doi: 10.1371/jour-nal.ppat.1003883.
8. Brodersen, P., Sakvarelidze-Achard, L., Bruun-Rasmussen, M., Dunoyer, P., Yamamoto, Y. Y., Sieburth, L., et al. (2008). Widespread translational inhibition by plant miRNAs and siRNAs. Science 320, 1185-1190. doi: 10.1126/science.1159151.
9. Buxdorf, K., Hendelman, A., Stav, R., Lapidot, M., Ori, N., and Arazi, T. (2010). Identification and characterization of a novel miR159 target not related to MYB in tomato. Planta 232, 1009-1022.doi: 10.1007/s00425-010-1231-9.
10. Campo, S., Peris-Peris, C., Sire, C., Moreno, A. B., Donaire, L., Zytnicki, M., et al. (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. doi: 10.1111/nph.12292.
11. Chapman, E. J., and Carrington, J. C. (2007). Specialization and evolution of endogenous small RNA pathways. Nat. Rev. Genet. 8, 884-896. doi: 10.1038/nrg2179.
12. Chellappan, P., Xia, J., Zhou, X., Gao, S., Zhang, X., Coutino, G., et al. (2010). siRNAs from miRNA sites mediate DNA methylation of target genes. Nucleic AcidsRes. 38, 6883-6894. doi: 10.1093/nar/gkq590.
13. Chen, H. M., Chen, L. T., Patel, K., Li, Y. H., Baulcombe, D. C., and Wu, S. H. (2010). 22-Nucleotide RNAs trigger secondarysiRNA biogenesis in plants. Proc. Natl. Acad. Sci. U.S.A. 107, 15269-15274. doi: 10.1073/pnas.1001738107.
14. Chen, H. M., Li, Y. H., and Wu, S. H. (2007). Bioinformatic prediction and experimental validation of a microRNA-directed tandem trans-acting siRNA cascade in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 104, 3318-3323. doi: 10.1073/pnas.0611119104.
15. Chen, X. (2004). A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303, 2022-2025. doi: 10.1126/science.1088060.
16. Chen, X. (2012). Small RNAs in development—insights from plants. Curr. Opin. Genet. Dev. 22, 361-367. doi: 10.1016/j.gde.2012.04.004.
17. Cuperus, J. T., Carbonell, A., Fahlgren, N., Garcia-Ruiz, H., Burke, R. T., Takeda, A., et al. (2010). Unique functionality of 22-nt miRNAs in triggering RDR6- dependent siRNA biogenesis from target transcripts in Arabidopsis. Nat. Struct. Mol. Biol. 17, 997-1003. doi: 10.1038/nsmb.1866.
18. Cuperus, J. T., Fahlgren, N., and Carrington, J. C. (2011). Evolution and functional diversification of MIRNA genes. Plant Cell 23, 431-442. doi: 10.1105/tpc.110.082784.
19. Curaba, J., Singh, M. B., and Bhalla, P. L. (2014). miRNAs in the crosstalk between phytohormone signalling pathways. J. Exp. Bot. 65, 1425-1438. doi: 10.1093/jxb/eru002.
20. Debernardi, J. M., Rodriguez, R. E., Mecchia, M. A., and Palatnik, J. F. (2012). Functional specialization of the plant miR396 regulatory network through dis- tinctmicroRNA-target interactions. PLoS Genet. 8:e1002419. doi: 10.1371/jour-nal.pgen.1002419.
21. Dong, Z., Han, M. H., and Fedoroff, N. (2008). The RNA-binding proteins HYL1 and SE promote accurate in vitro processing ofpri-miRNAbyDCL1. Proc. Natl. Acad. Sci. U.S.A. 105, 9970-9975. doi: 10.1073/pnas.0803356105.
22. Fei, Q., Xia, R., and Meyers, B. C. (2013). Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks. Plant Cell 25,2400-2415. doi: 10.1105/tpc.113.114652.
23. Felippes, F. F., and Weigel, D. (2009). Triggering the formation of tasiRNAs in Arabidopsis thaliana: the role of microRNA miR173. EMBO Rep. 10, 264-270. doi: 10.1038/embor.2008.247.
24. German, M. A., Pillay, M., Jeong, D. H., Hetawal, A., Luo, S., Janardhanan, P., et al. (2008). Global identification of microRNA-target RNA pairs by parallel analysis ofRNAends. Nat. Biotechnol. 26, 941-946. doi: 10.1038/nbt1417.
25. Giacomelli, J. I., Weigel, D., Chan, R. L., and Manavella, P. A. (2012). Role of recently evolved miRNA regulation of sunflower HaWRKY6 in response to temperature damage. New Phytol. 195, 766-773. doi: 10.1111/j.1469-8137.2012.04259.x
26. Guan, X., Pang, M., Nah, G., Shi, X., Ye, W., Stelly, D. M., et al. (2014). miR828 and miR858 regulate homoeologous MYB2 gene functions in Ara-bidopsis trichome and cotton fibre development. Nat. Commun. 5, 3050. doi: 10.1038/ncomms4050.
27. Guo, S., Xu, Y., Liu, H., Mao, Z., Zhang, C., Ma, Y., et al. (2013). The interaction between OsMADS57 and OsTB1 modulates rice tillering via DWARF14. Nat. Commun. 4, 1566. doi: 10.1038/ncomms2542.
28. Gutierrez, L., Mongelard, G., Flokova, K., Pacurar, D. I., Novak, O., Staswick, P., et al. (2012). Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. Plant Cell 24, 2515-2527. doi: 10.1105/tpc.112.099119.
29. Heil, M., and Baldwin, I. T. (2002). Fitness costs of induced resistance: emerging experimental support for a slippery concept. Trends Plant Sci. 7, 61-67. doi: 10.1016/S1360-1385(01)02186-0.
30. Henderson, I. R., Zhang, X., Lu, C., Johnson, L., Meyers, B. C., Green, P. J., et al. (2006). Dissecting Arabidopsis thaliana DICER function in small RNA processing, gene silencing and DNA methylation patterning. Nat. Genet. 38, 721-725. doi: 10.1038/ng1804.
31. Higgins, J. A., Bailey, P. C., and Laurie, D. A. (2010). Comparative genomics of flowering time pathways using Brachypodium distachyon as a model for the temperate grasses. PLoS ONE 5:e10065. doi: 10.1371/journal.pone.0010065.
32. Hu, J. Y., Zhou, Y., He, F., Dong, X., Liu, L. Y., Coupland, G., et al. (2014). miR824-regulated AGAMOUS-LIKE16 contributes to flowering time repression in Arabidopsis. Plant cell 26, 2024-2037. doi: 10.1105/tpc.114.124685.
33. Jeong, D. H., Schmidt, S. A., Rymarquis, L. A., Park, S., Ganssmann, M., German, M. A., et al. (2013). Parallel analysis of RNA ends enhances global investigation of microRNAs and target RNAs of Brachypodium distachyon. Genome Biol. 14, R145. doi: 10.1186/gb-2013-14-12-r145.
34. Jia, F., and Rock, C. D. (2013). MIR846 and MIR842 comprise a cistronic MIRNA pair that is regulated by abscisic acid by alternative splicing in roots of Arabidopsis. Plant Mol. Biol. 81,447-460. doi: 10.1007/s11103-013-0015-6.
35. Jiao, Y., Wang, Y., Xue, D., Wang, J., Yan, M., Liu, G., et al. (2010). Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat. Genet. 42, 541-544. doi: 10.1038/ng.591.
36. Jin, D., Wang, Y., Zhao, Y., and Chen, M. (2013). MicroRNAs and their cross-talks in plant development. J. Genet. Genomics 40, 161-170. doi: 10.1016/j.jgg.2013.02.003.
37. Koyama, T., Mitsuda, N., Seki, M., Shinozaki, K., and Ohme-Takagi, M. (2010). TCP transcription factors regulate the activities of ASYMMETRIC LEAVES1 and miR164, as well as the auxin response, during differentiation of leaves in Arabidopsis. Plant Cell 22, 3574-3588. doi: 10.1105/tpc.110.075598.
38. Kutter, C., Schob, H., Stadler, M., Meins, F. Jr., and Si-Ammour, A. (2007). MicroRNA-mediated regulation of stomatal development in Arabidopsis. Plant Cell 19, 2417-2429. doi: 10.1105/tpc.107.050377.
39. Laubinger, S., Sachsenberg, T., Zeller, G., Busch, W., Lohmann, J. U., Ratsch, G., et al. (2008). Dual roles of the nuclear cap-binding complex and SERRATE in pre-mRNA splicing and microRNA processing in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 105, 8795-8800. doi: 10.1073/pnas.0802493105.
40. Law, J. A., and Jacobsen, S. E. (2010). Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat. Rev. Genet. 11, 204-220. doi: 10.1038/nrg2719.
41. Li, F., Pignatta, D., Bendix, C., Brunkard, J. O., Cohn, M. M., Tung, J., et al. (2012). MicroRNA regulation of plant innate immune receptors. Proc. Natl. Acad. Sci. U.S.A. 109, 1790-1795. doi: 10.1073/pnas.1118282109.
42. Li, Y. F., Zheng, Y., Addo-Quaye, C., Zhang, L., Saini, A., Jagadeeswaran, G., et al. (2010). Transcriptome-wide identification of microRNA targets in rice. Plant J. 62, 742-759. doi: 10.1111/j.1365-313X.2010.04187.x
43. Manavella, P. A., Koenig, D., and Weigel, D. (2012). Plant secondary siRNA production determined by microRNA-duplex structure. Proc. Natl. Acad. Sci. U.S.A. 109,2461-2466. doi: 10.1073/pnas.1200169109.
44. Mao, G., Turner, M., Yu, O., and Subramanian, S. (2013). miR393 and miR164 influence indeterminate but not determinate nodule development. Plant Signal. Behav. 8:e26753. doi: 10.4161/psb.26753.
45. Meyers, B. C., Axtell, M. J., Bartel, B., Bartel, D. P., Baulcombe, D., Bowman, J. L., et al. (2008). Criteria for annotation of plant microRNAs. Plant Cell 20, 3186-3190. doi: 10.1105/tpc.108.064311.
46. Miura, K., Ikeda, M., Matsubara, A., Song, X. J., Ito, M., Asano, K., et al. (2010). OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat. Genet. 42, 545-549. doi: 10.1038/ng.592.
47. Molnar, A., Schwach, F., Studholme, D. J., Thuenemann, E. C., and Baulcombe, D. C. (2007). miRNAs control gene expression in the single-cell alga Chlamy- domonas reinhardtii. Nature 447, 1126-1129. doi: 10.1038/nature05903.
48. Montgomery, T. A., Yoo, S. J., Fahlgren, N., Gilbert, S. D., Howell, M. D., Sullivan, C. M., et al. (2008). AGO1-miR173 complex initiates phased siRNA formation in plants. Proc. Natl. Acad. Sci. U.S.A. 105, 20055-20062. doi: 10.1073/pnas.0810241105.
49. Ng, D. W., Zhang, C., Miller, M., Palmer, G., Whiteley, M., Tholl, D., et al. (2011). cis- and trans-Regulation of miR163 and target genes confers natural variation of secondary metabolites in two Arabidopsis species and their allopolyploids. Plant Cell 23, 1729-1740. doi: 10.1105/tpc.111.083915.
50. Nosaka, M., Itoh, J., Nagato, Y., Ono, A., Ishiwata, A., and Sato, Y. (2012). Role of transposon-derived small RNAs in the interplay between genomes and parasitic DNA in rice. PLoS Genet. 8:e1002953. doi: 10.1371/journal.pgen.1002953.
51. Palatnik, J. F., Allen, E., Wu, X., Schommer, C., Schwab, R., Carrington, J. C., et al. (2003). Control ofleafmorphogenesis bymicroRNAs. Nature 425,257-263. doi: 10.1038/nature01958.
52. Park, M. Y., Wu, G., Gonzalez-Sulser, A., Vaucheret, H., and Poethig, R. S. (2005). Nuclear processing and export of microRNAs in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 102,3691-3696. doi: 10.1073/pnas.0405570102.
53. Pesch, M., and Hulskamp, M. (2009). One, two, three...models for tri¬chome patterning in Arabidopsis? Curr. Opin. Plant Biol. 12, 587-592. doi: 10.1016/j.pbi.2009.07.015.
54. Poethig, R. S. (2013). Vegetative phase change and shoot maturation in plants. Curr. Top. Dev. Biol. 105, 125-152. doi: 10.1016/B978-0-12-396968-2.00005-1.
55. Qi, Y., Denli, A. M., and Hannon, G. J. (2005). Biochemical specialization within Arabidopsis RNA silencing pathways. Mol. Cell 19, 421-428. doi: 10.1016/j.molcel.2005.06.014.
56. Rajagopalan, R., Vaucheret, H., Trejo, J., and Bartel, D. P. (2006). A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev. 20, 3407-3425. doi: 10.1101/gad.1476406.
57. Rogers, K., and Chen, X. (2012). microRNA biogenesis and turnover in plants. Cold. SpringHarb. Symp. Quant. Biol. 77, 183-194. doi: 10.1101/sqb.2013.77.014530.
58. Rogers, K., and Chen, X. (2013). Biogenesis, turnover, and mode of action of plant microRNAs. PlantCell 25,2383-2399. doi: 10.1105/tpc.113.113159.
59. Rubio-Somoza, I., and Weigel, D. (2011). MicroRNA networks and developmental plasticity in plants. Trends Plant Sci. 16, 258-264. doi: 10.1016/j.tplants.2011.03.001.
60. Rubio-Somoza, I., and Weigel, D. (2013). Coordination of flower maturation by a regulatory circuit of three microRNAs. PLoS Genet. 9:e1003374. doi: 10.1371/journal.pgen.1003374.
61. Shivaprasad, P. V., Chen, H. M., Patel, K., Bond, D. M., Santos, B. A., and Baulcombe, D. C. (2012). A microRNA superfamily regulates nucleotide bind¬ing site-leucine-rich repeats and other mRNAs. Plant Cell 24, 859-874. doi: 10.1105/tpc.111.095380.
62. Song, X., Li, P., Zhai, J., Zhou, M., Ma, L., Liu, B., et al. (2012). Roles of DCL4 and DCL3b in rice phased small RNA biogenesis. Plant J. 69, 462-474. doi: 10.1111/j.1365-313X.2011.04805.x
63. Spanudakis, E., and Jackson, S. (2014). The role of microRNAs in the control of flowering time. J. Exp. Bot. 65, 365-380. doi: 10.1093/jxb/ert453.
64. Sunkar, R., Girke, T., Jain, P. K., and Zhu, J. K. (2005). Cloning and characterization ofmicroRNAsfrom rice. PlantCell 17, 1397-1411. doi: 10.1105/tpc.105.031682.
65. Tang, G. (2010). Plant microRNAs: an insight into their gene structures and evolution. Semin. Cell Dev. Biol. 21, 782-789. doi: 10.1016/j.semcdb.2010.07.009.
66. Taylor, R. S., Tarver, J. E., Hiscock, S. J., and Donoghue, P. C. (2014). Evolutionary history of plant microRNAs. Trends Plant Sci. 19, 175-182. doi: 10.1016/j.tplants.2013.11.008.
67. Vazquez, F., Blevins, T., Ailhas, J., Boller, T., and Meins, F. Jr. (2008). Evolution of Arabidopsis MIR genes generates novel microRNA classes. NucleicAcidsRes. 36, 6429-6438. doi: 10.1093/nar/gkn670.
68. Voinnet, O. (2009). Origin, biogenesis, and activity of plant microRNAs. Cell 136, 669-687. doi: 10.1016/j.cell.2009.01.046.
69. Wang, Y., Itaya, A., Zhong, X., Wu, Y., Zhang, J., van der Knaap, E., et al. (2011). Function and evolution of a MicroRNA that regulates a Ca2+-ATPase and triggers the formation of phased small interfering RNAs in tomato reproductive growth. PlantCell 23, 3185-3203. doi: 10.1105/tpc.111.088013.
70. Wei, B., Cai, T., Zhang, R., Li, A., Huo, N., Li, S., et al. (2009). Novel microRNAs uncovered by deep sequencing of small RNA transcriptomes in bread wheat (Triticum aestivum L.) and Brachypodium distachyon (L.) Beauv. Funct. Integr. Genomics 9, 499-511. doi: 10.1007/s10142-009-0128-9.
71. Winter, J., and Diederichs, S. (2011). Argonaute proteins regulate microRNA stability: increased microRNA abundance by Argonaute proteins is due to microRNAstabilization. RNABiol. 8, 1149-1157. doi: 10.4161/rna.8.6.17665.
72. Wu, G. (2013). PlantmicroRNAs and development. J. Genet. Genomics 40,217-230. doi: 10.1016/j.jgg.2013.04.002.
73. Wu, G., Park, M. Y., Conway, S. R., Wang, J. W., Weigel, D., and Poethig, R. S. (2009a). The sequential action ofmiR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138, 750-759. doi: 10.1016/j.cell.2009.06.031.
74. Wu, L., Zhang, Q., Zhou, H., Ni, F., Wu, X., and Qi, Y. (2009b). Rice microRNA effector complexes and targets. Plant Cell 21, 3421-3435. doi: 10.1105/tpc.109.070938.
75. Wu, L., Liu, D., Wu, J., Zhang, R., Qin, Z., Li, A., et al. (2013). Regulation of FLOWERING LOCUS T byamicroRNA in Brachypodium distachyon. PlantCell 25, 4363-4377. doi: 10.1105/tpc.113.118620.
76. Wu, L., Mao, L., and Qi, Y. (2012). Roles of DICER-LIKE and ARGONAUTE proteins in TAS-derived small interfering RNA-triggered DNA methylation. PlantPhysiol. 160,990-999. doi: 10.1104/pp.112.200279.
77. Wu, L., Zhou, H., Zhang, Q., Zhang, J., Ni, F., Liu, C., et al. (2010). DNA methylation mediated by a microRNA pathway. Mol. Cell 38, 465-475. doi: 10.1016/j.molcel.2010.03.008.
78. Yan, K., Liu, P., Wu, C. A., Yang, G. D., Xu, R., Guo, Q. H., et al. (2012). Stress-induced alternative splicing provides a mechanism for the regulation of microRNA processing in Arabidopsis thaliana. Mol. Cell 48, 521-531. doi: 10.1016/j.molcel.2012.08.032.
79. Yan, Y., Wang, H., Hamera, S., Chen, X., and Fang, R. (2014). miR444a has multiple functions in the rice nitrate-signaling pathway. Plant J. 78, 44-55. doi: 10.1111/tpj.12446.
80. Yoshikawa, M., Iki, T., Tsutsui, Y., Miyashita, K., Poethig, R. S., Habu, Y., et al. (2013). 3'fragment of miR173-programmed RISC-cleaved RNA is protected from degradation inacomplexwith RISC and SGS3. Proc. Natl. Acad. Sci. U.S.A. 110,4117-4122. doi: 10.1073/pnas.1217050110.
81. Yu, B., Yang, Z., Li, J., Minakhina, S., Yang, M., Padgett, R. W., et al. (2005). Methylation as a crucial step in plant microRNA biogenesis. Science 307, 932-935. doi: 10.1126/science.1107130.
82. Zhai, J., Jeong, D. H., De Paoli, E., Park, S., Rosen, B. D., Li, Y., et al. (2011). MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev. 25, 2540-2553. doi: 10.1101/gad.177527.111.
83. Zhang, J., Xu, Y., Huan, Q., and Chong, K. (2009). Deep sequencing of Brachypodium small RNAs at the global genome level identifies microRNAs involved in cold stress response. BMC Genomics 10:449. doi: 10.1186/1471-2164-10-449.
84. Zhang, Y. C., Yu, Y., Wang, C. Y., Li, Z. Y., Liu, Q., Xu, J., et al. (2013). Overexpression of microRNA OsmiR397 improves rice yield by increasing grain size and promoting panicle branching. Nat. Biotechnol. 31, 848-852. doi: 10.1038/nbt.2646.
85. Zhao, T., Li, G., Mi, S., Li, S., Hannon, G. J., Wang, X. J., et al. (2007). A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii. GenesDev. 21, 1190-1203. doi: 10.1101/gad.1543507