Small RNA pathways and diversity in model legumes: Lessons from genomics

Frontiers in Plant Science

Volumn 4, Issue JUL, 2013, Pages

  Bustos Sanmamed, Pilar ^a   Bazin, Jérémie ^a,b   Hartmann, Caroline ^a,b   Crespi, Martin ^a   Lelandais Brière, Christine ^a,b  

^a CNRS   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Argonaute; Dicer; Model legumes; Small RNA

Indexed keywords

EID: 84900825832     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00236     Document Type: Review

References (117)

1. Allen, E., and Howell, M. C. (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
2. Allen, E., Xie, Z., Gustafson, A. M., Sung, G. H., Spatafora, J. W., and Carrington, J. C. (2004). Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat. Genet. 36, 1282-1290. doi: 10.1038/ng1478
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.
4. Ariel, F., Brault-Hernandez, M., Laffont, C., Huault, E., Brault, M., Plet, J., et al. (2012). Two direct targets of cytokinin signaling regulate symbiotic nodulation in Medicago truncatula. Plant Cell 24, 3838-3852. doi: 10.1105/tpc.112.103267
5. 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
6. Bazin, J., Bustos-Sanmamed, P., Hartmann, C., Lelandais-Brière, C., and Crespi, M. (2012). Complexity of miRNA-dependent regulation in root symbiosis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 367, 1570-1579. doi: 10.1098/rstb.2011.0228
7. Ben Amor, B., Wirth, S., Merchan, F., Laporte, P., d'Aubenton-Carafa, Y., Hirsch, J., et al. (2009). Novel long non-protein coding RNAs involved in Arabidopsis differentiation and stress responses. Genome Res. 19, 57-69. doi: 10.1101/gr.080275.108
8. Boualem, A., Laporte, P., Jovanovic, M., Laffont, C., Plet, J., Combier, J. P., et al. (2008). MicroRNA166 controls root and nodule development in Medicago truncatula. Plant J. 54, 876-887. doi: 10.1111/j.1365-313X.2008.03448.x
9. Bourcy, M., Berrabah, F., Ratet, P., and Gourion, B. (2013). Failure of self-control: defense like reactions during legume/rhizobia symbiosis. Plant Signal. Behav. 8, pii:e23915.
10. Bove, J., Hord, C. L., and Mullen, M. A. (2006). The blossoming of RNA biology: novel insights from plant systems. RNA 12, 2035-2046. doi: 10.1261/rna.303806
11. Branscheid, A., Devers, E. A., May, P., and Krajinski, F. (2011). Distribution pattern of small RNA and degradome reads provides information on miRNA gene structure and regulation. Plant Signal. Behav. 6, 1609-1611. doi: 10.4161/psb.6.10.17305
12. 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
13. Capitão, C., Paiva, J. A., Santos, D. M., and Fevereiro, P. (2011). In Medicago truncatula, water deficit modulates the transcript accumulation of components of small RNA pathways. BMC Plant Biol. 11:79. doi: 10.1186/1471-2229-11-79
14. Carmell, M. A., and Hannon, G. J. (2004). RNase III enzymes and the initiation of gene silencing. Nat. Struct. Mol. Biol. 11, 214-218. doi: 10.1038/nsmb729
15. Cerutti, H., and Casas-Mollano, J. A. (2006). On the origin and functions of RNA-mediated silencing: from protists to man. Curr. Genet. 50, 81-99. doi: 10.1007/s00294-006-0078-x
16. 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
17. Chen, H. M., Chen, L. T., Patel, K., Li, Y. H., Baulcombe, D. C., and Wu, S. H. (2010). 22-nucleotide RNAs trigger secondary siRNA biogenesis in plants. Proc. Natl. Acad. Sci. U.S.A. 107, 15269-15274. doi: 10.1073/pnas.1001738107
18. Combier, J. P., Frugier, F., de Billy, F., Boualem, A., El-Yahyaoui, F., Moreau, S., et al. (2006). MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula. Genes Dev. 20, 3084-3088. doi: 10.1101/gad.402806
19. Corradi, N., and Bonfante, P. (2012). The arbuscular mycorrhizal symbiosis: origin and evolution of a beneficial plant infection. PLoS Pathog. 8:e1002600. doi: 10.1371/journal.ppat.1002600
20. 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
21. Curtin, S. J., Kantar, M. B., Yoon, H. W., Whaley, A. M., Schlueter, J. A., and Stupar, R. M. (2012). Co-expression of soybean dicer-like genes in response to stress and development. Funct. Integr. Genomics 12, 671-682. doi: 10.1007/s10142-012-0278-z
22. Czech, B., and Hannon, G. J. (2011). Small RNA sorting: matchmaking for argonautes. Nat. Rev. Genet. 12, 19-31. doi: 10.1038/nrg2916
23. Deinum, E. E., Geurts, R., Bisseling, T., and Mulder, B. M. (2012). Modeling a cortical auxin maximum for nodulation: different signatures of potential strategies. Front. Plant Sci. 3:96. doi: 10.3389/fpls.2012.00096
24. De Luis, A., Markmann, K., Cognat, V., Holt, D. B., Charpentier, M., Parniske, M., et al. (2012). Two microRNAs linked to nodule infection and nitrogen-fixing ability in the legume Lotus japonicus. Plant Physiol. 160, 2137-2154. doi: 10.1104/pp.112.204883
25. Devers, E. A., Branscheid, A., May, P., and Krajinski, F. (2011). Stars and symbiosis: microRNA-and microRNA*-mediated transcript cleavage involved in arbuscular mycorrhizalsymbiosis. Plant Physiol. 156, 1990-2010. doi: 10.1104/pp.111.172627
26. D'Haeseleer, K., Den Herder, G., Laffont, C., Plet, J., Mortier, V., Lelandais-Brière, C., et al. (2011). Transcriptional and post-transcriptional regulation of a NAC1 transcription factor in Medicago truncatula roots. New Phytol. 191, 647-661. doi: 10.1111/j.1469-8137.2011.03719.x
27. Dunoyer, P., Himber, C., Ruiz-Ferrer, V., Alioua, A., and Voinnet, O. (2007). Intra-and intercellular RNA interference in Arabidopsis thaliana requires components of the microRNA and heterochromatic silencing pathways. Nat. Genet. 39, 848-856. doi: 10.1038/ng2081
28. Eamens, A. L., Smith, N. A., Curtin, S. J., Wang, M. B., and Waterhouse, P. M. (2009). The Arabidopsis thalianadouble-stranded RNA binding protein DRB1 directs guide strand selection from microRNA duplexes. RNA 15, 2219-2235. doi: 10.1261/rna.1646909
29. Gasciolli, V., Mallory, A. C., Bartel, D. P., and Vaucheret, H. (2005). Partially redundant functions of Arabidopsisdicer-like enzymes and a role for DCL4 in producing trans-acting siRNAs. Curr. Biol. 15, 1494-1500. doi: 10.1016/j.cub.2005.07.024
30. German, M. A., Luo, S., Schroth, G., Meyers, B. C., and Green, P. J. (2009). Construction of parallel analysis of RNA ends (PARE) libraries for the study of cleaved miRNA targets and the RNA degradome. Nat. Protoc. 4, 356-362. doi: 10.1038/nprot.2009.8
31. Gill, N., Findley, S., Walling, J. G., Hans, C., Ma, J., Doyle, J., et al. (2009). Molecular and chromosomal evidence for allopolyploidy in soybean. Plant Physiol. 151, 1167-1174. doi: 10.1104/pp.109.137935
32. Griffiths-Jones, S., Grocock, R. J., van Dongen, S., Bateman, A., and Enright, A. J. (2006). miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res. 34, D140-D144. doi: 10.1093/nar/gkj112
33. Gu, M., Xu, K., Chen, A., Zhu, Y., Tang, G., and Xu, G. (2010). Expression analysis suggests potential roles of microRNAs for phosphate and arbuscular mycorrhizal signaling in Solanum lycopersicum. Physiol. Plant. 138, 226-237. doi: 10.1111/j.1399-3054.2009.01320.x
34. Harvey, J. J., Lewsey, M. G., Patel, K., Westwood, J., Heimstädt, S., Carr, J. P., et al. (2011). An antiviral defense role of AGO2 in plants. PLoS ONE 6:e14639. doi: 10.1371/journal.pone.0014639
35. Havecker, E. R., Wallbridge, L. M., Hardcastle, T. J., Bush, M. S., Kelly, K. A., Dunn, R. M., et al. (2010). The Arabidopsis RNA-directed DNA methylation argonautes functionally diverge based on their expression and interaction with target loci. Plant Cell 22, 321-334. doi: 10.1105/tpc.109.072199
36. Henderson, I. R., Zhang, X., Lu, C., Johnson, L., Meyers, B. C., Green, P. J., et al. (2006). Dissecting Arabidopsis thaliana dicerfunction in small RNA processing, gene silencing and DNA methylation patterning. Nat. Genet. 38, 721-725. doi: 10.1038/ng1804
37. Hiraguri, A., Itoh, R., Kondo, N., Nomura, Y., Aizawa, D., Murai, Y., et al. (2005). Specific interactions between dicer-like proteins and HYL1/DRB-family dsRNA-binding proteins in Arabidopsis thaliana. Plant Mol. Biol. 57, 173-188. doi: 10.1007/s11103-004-6853-5
38. Hutvagner, G., and Simard, M. J. (2008). Argonaute proteins: key players in RNA silencing. Nat. Rev. Mol. Cell Biol. 9, 22-32. doi: 10.1038/nrm2321
39. Jagadeeswaran, G., Zheng, Y., Li, Y. F., Shukla, L. I., Matts, J., Hoyt, P., et al. (2009). Cloning and characterization of small RNAs from Medicago truncatula reveals four novel legume-specific microRNA families. New Phytol. 184, 85-98. doi: 10.1111/j.1469-8137.2009.02915.x
40. Ji, L., Liu, X., Yan, J., Wang, W., Yumul, R. E., Kim, Y. J., et al. (2011). ARGONAUTE10 and ARGONAUTE1 regulate the termination of floral stem cells through twomicroRNAs in Arabidopsis. PLoS Genet. 7:e1001358. doi: 10.1371/journal.pgen.1001358
41. Jones, J. D., and Dangl, J. L. (2006). The plant immune system. Nature 444, 323-329. doi: 10.1038/nature05286
42. Jouannet, V., Moreno, A. B., Elmayan, T., Vaucheret, H., Crespi, M. D., and Maizel, A. (2012). Cytoplasmic Arabidopsis AGO7 accumulates in membrane-associated siRNA bodies and is required for ta-siRNA biogenesis. EMBO J. 31, 1704-1713. doi: 10.1038/emboj.2012.20
43. Kapoor, M., Arora, R., Lama, T., Nijhawan, A., Khurana, J. P., Tyagi, A. K., et al. (2008). Genome-wide identification, organization and phylogenetic analysis of dicer-like, argonaute and RNA-dependent RNA polymerase gene families and their expression analysis during reproductive development and stress in rice. BMC Genomics 9:451. doi: 10.1186/1471-2164-9-451
44. Kawashima, C. G., Yoshimoto, N., Maruyama-Nakashita, A., Tsuchiya, Y. N., Saito, K., Takahashi, H., et al. (2009). Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. Plant J. 57, 313-321. doi: 10.1111/j.1365-313X.2008.03690.x
45. Khan, G. A., Declerck, M., Sorin, C., Hartmann, C., Crespi, M., and Lelandais-Brière, C. (2011). MicroRNAs as regulators of root development and architecture. Plant Mol. Biol. 77, 47-58. doi: 10.1007/s11103-011-9793-x
46. Khraiwesh, B., Zhu, J. K., and Zhu, J. (2012). Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim. Biophys. Acta 1819, 137-148. doi: 10.1016/j.bbagrm.2011.05.001
47. Kulcheski, F. R., de Oliveira, L. F., Molina, L. G., Almerão, M. P., Rodrigues, F. A., Marcolino, J., et al. (2011). Identification of novel soybean microRNAs involved in abiotic and biotic stresses. BMC Genomics 12:307. doi: 10.1186/1471-2164-12-307
48. Lauressergues, D., Delaux, P. M., Formey, D., Lelandais-Brière, C., Fort, S., Cottaz, S., et al. (2012). The microRNA miR171h modulates arbuscular mycorrhizal colonization of Medicago truncatula by targeting NSP2. Plant J. 72, 512-522. doi: 10.1111/j.1365-313X.2012.05099.x
49. Lelandais-Briere, C., Naya, L., Sallet, E., Calenge, F., Frugier, F., Hartmann, C., et al. (2009). Genome-wide Medicago truncatula small RNA analysis revealed novel microRNAs and isoforms differentially regulated in roots and nodules. Plant Cell 21, 2780-2796. doi: 10.1105/tpc.109.068130
50. Letunic, I., Doerks, T., and Bork, P. (2012). SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res. 40, D302-D305. doi: 10.1093/nar/gkr931
51. 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
52. Li, H., Deng, Y., Wu, T., Subramanian, S., and Yu, O. (2010). Misexpression of miR482, miR1512, and miR1515 increases soybean nodulation. Plant Physiol. 153, 1759-1770. doi: 10.1104/pp.110.156950
53. Li, H., Dong, Y., Yin, H., Wang, N., Yang, J., Liu, X., et al. (2011). Characterization of the stress associated microRNAs in glycine max by deep sequencing. BMC Plant Biol. 11:170. doi: 10.1186/1471-2229-11-170
54. Liang, G., He, H., and Yu, D. (2012). Identification of nitrogen starvation-responsive microRNAs in Arabidopsis thaliana. PLoS ONE 7:e48951. doi:10.1371/journal.pone.0048951
55. Liang, G., Yang, F., and Yu, D. (2010). MicroRNA395 mediates regulation of sulfate accumulation and allocation in Arabidopsis thaliana. Plant J. 62, 1046-1057.
56. Liu, B., Li, P., Li, X., Liu, C., Cao, S., Chu, C., et al. (2005). Loss of function of OsDCL1 affects microRNA accumulation and causes developmental defects in rice. Plant Physiol. 139, 296-305. doi: 10.1104/pp.105.063420
57. Liu, Q., Feng, Y., and Zhu, Z. (2009). Dicer-like (DCL) proteins in plants. Funct. Integr. Genomics 9, 277-286. doi: 10.1007/s10142-009-0111-5
58. López-Gómez, M., Sandal, N., Stougaard, J., and Boller, T. (2012). Interplay of flg22-induced defence responses and nodulation in Lotus japonicus. J. Exp. Bot. 63, 393-401. doi: 10.1093/jxb/err291
59. Lu, C., Kulkarni, K., Souret, F. F., MuthuValliappan, R., Tej, S. S., Poethig, R. S., et al. (2006). MicroRNAs and other small RNAs enriched in the Arabidopsis RNA-dependent RNA polymerase-2 mutant. Genome Res. 16, 1276-1288. doi: 10.1101/gr.5530106
60. Lynn, K., Fernandez, A., Aida, M., Sedbrook, J., Tasaka, M., Masson, P., et al. (1999). The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene. Development 126, 469-481.
61. Mallory, A., and Vaucheret, H. (2010). Form, function, and regulation of ARGONAUTE proteins. Plant Cell 22, 3879-3889. doi: 10.1105/tpc.110.080671
62. 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
63. Manavella, P. A., Weigel, D., and Wu, L. (2011). Argonaute10 as a miRNA locker. Cell 145, 173-174. doi: 10.1016/j.cell.2011.03.045
64. Maunoury, N., and Vaucheret, H. (2011). AGO1 and AGO2 act redundantly in miR408-mediated Plantacyanin regulation. PLoS ONE 6:e28729. doi: 10.1371/journal.pone.0028729
65. Margis, R., Fusaro, A. F., Smith, N. A., Curtin, S. J., Watson, J. M., Finnegan, E. J., et al. (2006). The evolution and diversification of dicers in plants. FEBS Lett. 580, 2442-2450. doi: 10.1016/j.febslet.2006.03.072
66. Marin, E., Jouannet, V., Herz, A., Lokerse, A. S., Weijers, D., Vaucheret, H., et al. (2010). miR390, ArabidopsisTAS3 tasiRNAs, and their auxin response factor targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 22, 1104-1117. doi: 10.1105/tpc.109.072553
67. Marchetti, M., Capela, D., Glew, M., Cruveilles, S., Chane-Woon-Ming, B., Girs, C., et al. (2010). Experimental evolution of a plant pathogen into a legume symbiont. PLoS Biol. 8:e1000280. doi: 10.1371/journal.pbio.1000280
68. Matamoros, M. A., Baird, L. M., Escuredo, P. R., Dalton, D. A., Minchin, F. R., Iturbe-Ormaetxe, I., et al. (1999). Stress-induced legume root nodule senescence. Physiological, biochemical, and structural alterations. Plant Physiol. 121, 97-112. doi: 10.1104/pp.121.1.97
69. Mendoza-Soto, A. B., Sánchez, F., and Hernández, G. (2012). MicroRNAs as regulators in plant metal toxicity response. Front. Plant Sci. 3:105. doi: 10.3389/fpls.2012.00105
70. 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
71. Mi, S., Cai, T., Hu, Y., Chen, Y., Hodges, E., Ni, F., et al. (2008). Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 5′ terminal nucleotide. Cell 133, 116-127. doi: 10.1016/j.cell.2008.02.034
72. Montgomery, T. A., Howell, M. D., Cuperus, J. T., Li, D., Hansen, J. E., Alexander, A. L., et al. (2008). Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133, 128-141. doi: 10.1016/j.cell.2008.02.033
73. Murphy, D., Dancis, B., and Brown, J. R. (2008). The evolution of core proteins involved in microRNA biogenesis. BMC Evol. Biol. 8:92. doi: 10.1186/1471-2148-8-92
74. Naya, L., Khan, G. A., Sorin, C., Hartmann, C., Crespi, M., and Lelandais-Brière, C. (2010). Cleavage of a non-conserved target by a specific miR156 isoform in root apexes of Medicago truncatula. Plant Signal. Behav. 5, 328-331. doi: 10.4161/psb.5.3.11190
75. Nowotny, M., and Yang, W. (2009). Structural and functional modules in RNA interference. Curr. Opin. Struct. Biol. 19, 286-293. doi: 10.1016/j.sbi.2009.04.006
76. Ochman, H., and Moran, M. A. (2001). Gene lost and gene found: evolution of bacterial pathogenesis and symbiosis. Science 292, 1096-1099. doi: 10.1126/science.1058543.
77. Olmedo-Monfil, V., Durán-Figueroa, N., Arteaga-Vázquez, M., Demesa-Arévalo, E., Autran, D., Grimanelli, D., et al. (2010). Control of female gamete formation by a small RNA pathway in Arabidopsis. Nature 464, 628-632. doi: 10.1038/nature08828
78. Onodera, Y., Haag, J. R., Ream, T., Costa Nunes, P., Pontes, O., and Pikaard, C. S. (2005). Plant nuclear RNA polymerase IV mediates siRNA and DNA methylation-dependent heterochromatin formation. Cell 120, 613-622. doi: 10.1016/j.cell.2005.02.007
79. Parent, J. S., Martínez de Alba, A. E., and Vaucheret, H. (2012). The origin and effect of small RNA signaling in plants. Front. Plant Sci. 3:179. doi: 10.3389/fpls.2012.00179
80. Parker, J. S. (2010). How to slice: snapshots of Argonaute in action. Silence 1:3. doi: 10.1186/1758-907X-1-3
81. Peleg-Grossman, S., Melamed-Book, N., and Levine, A. (2013). ROS production during symbiotic infection suppresses pathogenesis-related gene expression. Plant Signal. Behav. 7, 409-415. doi: 10.4161/psb.19217
82. Peragine, A., Yoshikawa, M., Wu, G., Albrecht, H. L., and Poethig, R. S. (2004). SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. Genes Dev. 18, 2368-2379. doi: 10.1101/gad.1231804
83. Qi, Y., He, X., Wang, X. J., Kohany, O., Jurka, J., and Hannon, G. J. (2006). Distinct catalytic and non-catalytic roles of ARGONAUTE4 in RNA-directed DNA methylation. Nature 443, 1008-1012. doi: 10.1038/nature05198
84. Qian, Y., Cheng, Y., Cheng, X., Jiang, H., Zhu, S., and Cheng, B. (2011). Identification and characterization of dicer-like, Argonaute and RNA-dependent RNA polymerase gene families in maize. Plant Cell Rep. 30, 1347-1363. doi: 10.1007/s00299-011-1046-6
85. Radwan, O., Liu, Y., and Clough, S. J. (2011). Transcriptional analysis of soybean root response to Fusarium virguliforme, the causal agent of sudden death syndrome. Mol. Plant Microbe Interact. 24, 958-972. doi: 10.1094/MPMI-11-10-0271
86. 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
87. Rubio, M. C., Becana, M., Sato, S., James, E. K., Tabata, S., and Spaink, H. P. (2007). Characterization of genomic clones and expression analysis of the three types of superoxide dismutases during nodule development in Lotus japonicus. Mol. Plant Microbe Interact. 20, 262-275. doi: 10.1094/MPMI-20-3-0262
88. Sato, S., Nakamura, Y., Kaneko, T., Asamizu, E., Kato, T., Nakao, M., et al. (2008). Genome structure of the legume, Lotus japonicus. DNA Res. 15, 227-239. doi: 10.1093/dnares/dsn008
89. Schmutz, J., Cannon, S. B., Schlueter, J., Ma, J., Mitros, T., Nelson, W., et al. (2010). Genome sequence of the palaeopolyploid soybean. Nature 463, 178-183. doi: 10.1038/nature08670
90. Shivaprasad, P. V., Chen, H. M., Patel, K., Bond, D. M., Santos, B. A., and Baulcombe, D. C. (2012). A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. Plant Cell 24, 859-874. doi: 10.1105/tpc.111.095380
91. Simon, S. A., Meyers, B. C., and Sherrier, D. J. (2009). MicroRNAs in the rhizobia legume symbiosis. Plant Physiol. 151, 1002-1008. doi: 10.1104/pp.109.144345
92. Song, Q. X., Liu, Y. F., Hu, X. Y., Zhang, W. K., Ma, B., Chen, S. Y., et al. (2011). Identification of miRNAs and their target genes in developing soybean seeds by deep sequencing. BMC Plant Biol. 11:5. doi: 10.1186/1471-2229-11-5
93. 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
94. Soto, M. J., Domínguez-Ferreras, A., Pérez-Mendoza, D., Sanjuán, J., and Olivares, J. (2009). Mutualism versus pathogenesis: the give-and-take in plant-bacteria interactions. Cell. Microbiol. 11, 381-388. doi: 10.1111/j.1462-5822.2009.01282.x
95. Subramanian, S., Fu, Y., Sunkar, R., Barbazuk, W. B., Zhu, J. K., and Yu, O. (2008). Novel and nodulation-regulated microRNAs in soybean roots. BMC Genomics 9:160. doi: 10.1186/1471-2164-9-160
96. Subramanian, S., Stacey, G., and Yu, O. (2007). Distinct, crucial roles of flavonoids during legume nodulation. Trends Plant Sci. 12, 282-285. doi: 10.1016/j.tplants.2007.06.006
97. Sunkar, R., and Jagadeeswaran, G. (2008). In silico identification of conserved microRNAs in large number of diverse plant species. BMC Plant Biol. 8:37. doi: 10.1186/1471-2229-8-37
98. Szittya, G., Moxon, S., Santos, D. M., Jing, R., Fevereiro, M. P., Moulton, V. T., et al. (2008). High-throughput sequencing of Medicago truncatula short RNAs identifies eight new miRNA families. BMC Genomics 9:593. doi: 10.1186/1471-2164-9-593
99. Takeda, A., Iwasaki, S., Watanabe, T., Utsumi, M., and Watanabe, Y. (2008). The mechanism selecting the guide strand from small RNA duplexes is different among argonaute proteins. Plant Cell Physiol. 49, 493-500. doi: 10.1093/pcp/pcn043
100. Turner, M., Yu, O., and Subramanian, S. (2012). Genome organization and characteristics of soybean microRNAs. BMC Genomics 13:169. doi: 10.1186/1471-2164-13-169
101. Tuskan, G. A., Difazio, S., Jansson, S., Bohlmann, J., Grigoriev, I., Hellsten, U., et al. (2006). The genome of black cottonwood, Populus trichocarpa (Torr. andamp; Gray). Science 313, 1596-1604. doi: 10.1126/science.1128691
102. Van de Velde, W., Zehirov, G., Szatmari, A., Debreczeny, M., Ishihara, H., Kevei, Z., et al. (2010). Plant peptides govern terminal differentiation of bacteria in symbiosis. Science 327, 1122-1126. doi: 10.1126/science.1184057
103. Vaucheret, H. (2005). MicroRNA-dependent trans-acting siRNA production. Sci. STKE 300, pe43.
104. Vaucheret, H. (2008). Plant ARGONAUTES. Trends Plant Sci. 13, 350-358. doi: 10.1016/j.tplants.2008.04.007
105. Vazquez, F. (2006). Arabidopsis endogenous small RNAs: highways and byways. Trends Plant Sci. 11, 460-468. doi: 10.1016/j.tplants.2006.07.006
106. Vazquez, F., Legrand, S., and Windels, D. (2010). The biosynthetic pathways and biological scopes of plant small RNAs. Trends Plant Sci. 15, 337-345. doi: 10.1016/j.tplants.2010.04.001
107. Voinnet, O. (2009). Origin, biogenesis, and activity of plant microRNAs. Cell 136, 669-687. doi: 10.1016/j.cell.2009.01.046
108. Wang, H. W., Noland, C., Siridechadilok, B., Taylor, D. W., Ma, E., Felderer, K., et al. (2009). Structural insights into RNA processing by the human RISC-loading complex. Nat. Struct. Mol. Biol. 16, 1148-1153. doi: 10.1038/nsmb.1673
109. Wang, X. B., Jovel, J., Udomporn, P., Wang, Y., Wu, Q., Li, W. X., et al. (2011). The 21-nucleotide, but not 22-nucleotide, viral secondary small interfering RNAs direct potent antiviral defense by two cooperative argonautes in Arabidopsis thaliana. Plant Cell 23, 1625-1638. doi: 10.1105/tpc.110.082305
110. Wang, Y., Li, P., Cao, X., Wang, X., Zhang, A., and Li, X. (2009). Identification and expression analysis of miRNAs from nitrogen-fixing soybean nodules. Biochem. Biophys. Res. Commun. 378, 799-803. doi: 10.1016/j.bbrc.2008.11.140
111. Wong, C. E., Zhao, Y. T., Wang, X. J., Croft, L., Wang, Z. H., Haerizadeh, F., et al. (2011). MicroRNAs in the shoot apical meristem of soybean. J. Exp. Bot. 62, 2495-2506. doi: 10.1093/jxb/erq437
112. Yan, J., Cai, X., Luo, J., Sato, S., Jiang, Q., Yang, J., et al. (2010). The reduced leaflet genes encode key components of the trans-acting small interfering RNA pathway and regulate compound leaf and flower development in Lotus japonicus. Plant Physiol. 152, 797-807. doi: 10.1104/pp.109.140947
113. Young, N. D., Debellé, F., Oldroyd, G. E., Geurts, R., Cannon, S. B., Udvardi, M. K., et al. (2011). The Medicagogenome provides insight into the evolution of rhizobial symbioses. Nature 480, 520-524
114. 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
115. Zhang, X., Xia, J., Lii, Y. E., Barrera-Figueroa, B. E., Zhou, X., Gao, S., et al. (2012). Genome-wide analysis of plant nat-siRNAs reveals insights into their distribution, biogenesis and function. Genome Biol. 13, R20. doi: 10.1186/gb-2012-13-3-r20
116. Zhou, Z. S., Zeng, H. Q., Liu, Z. P., and Yang, Z. M. (2012). Genome-wide identification of Medicago truncatulamicroRNAs and their targets reveals their differentialregulation by heavy metal. Plant Cell Environ. 35, 86-99. doi: 10.1111/j.1365-3040.2011.02418.x
117. Zhu, H., Hu, F., Wang, R., Zhou, X., Sze, S. H., Liou, L. W., et al. (2011). Arabidopsis Argonaute10 specifically sequesters miR166/165 to regulate shoot apical meristem development. Cell 145, 242-256. doi: 10.1016/j.cell.2011.03.024