Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks

Plant Cell

Volumn 25, Issue 7, 2013, Pages 2400-2415

  Fei, Qili ^a   Xia, Rui ^a   Meyers, Blake C ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA; DICOTYLEDONEAE;

LEUCINE RICH REPEAT PROTEINS; LEUCINE-RICH REPEAT PROTEINS; PLANT RNA; PROTEIN; SMALL INTERFERING RNA;

AMINO ACID SEQUENCE; BIOLOGICAL MODEL; CLASSIFICATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PLANT; REVIEW; RNA PROCESSING;

AMINO ACID SEQUENCE; BASE SEQUENCE; GENE EXPRESSION REGULATION, PLANT; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; PLANTS; PROTEINS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, PLANT; RNA, SMALL INTERFERING;

EID: 84883166485     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.114652     Document Type: Review

References (115)

1. Adenot, X., Elmayan, T., Lauressergues, D., Boutet, S., Bouché, N., Gasciolli, V., and Vaucheret, H. (2006). DRB4-dependent TAS3 trans-acting siRNAs control leaf morphology through AGO7. Curr. Biol. 16: 927-932.
2. 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.
3. Arif, M.A., Fattash, I., Ma, Z., Cho, S.H., Beike, A.K., Reski, R., Axtell, M.J., and Frank, W. (2012). DICER-LIKE3 activity in Physcomitrella patens DICER-LIKE4 mutants causes severe developmental dysfunction and sterility. Mol. Plant 5: 1281-1294.
4. Aukerman, M.J., and Sakai, H. (2003). Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. Plant Cell 15: 2730-2741.
5. Axtell, M.J. (2013). Classification and comparison of small RNAs from plants. Annu. Rev. Plant Biol. 64: 137-159.
6. Axtell, M.J., Jan, C., Rajagopalan, R., and Bartel, D.P. (2006). A two-hit trigger for siRNA biogenesis in plants. Cell 127: 565-577.
7. Axtell, M.J., and Staskawicz, B.J. (2003). Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112: 369-377.
8. Bomblies, K., Lempe, J., Epple, P., Warthmann, N., Lanz, C., Dangl, J.L., andWeigel, D. (2007). Autoimmune response as a mechanism for a Dobzhansky-Muller-type incompatibility syndrome in plants. PLoS Biol. 5: e236.
9. Bomblies, K., and Weigel, D. (2007). Hybrid necrosis: Autoimmunity as a potential gene-flow barrier in plant species. Nat. Rev. Genet. 8: 382-393.
10. Borsani, O., Zhu, J., Verslues, P.E., Sunkar, R., and Zhu, J.K. (2005). Endogenous siRNAs derived from a pair of natural cis-antisense transcripts regulate salt tolerance in Arabidopsis. Cell 123: 1279-1291.
11. 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. USA 107: 15269-15274.
12. Chen, H.M., Li, Y.H., and Wu, S.H. (2007). Bioinformatic prediction and experimental validation of a microRNA-directed tandem transacting siRNA cascade in Arabidopsis. Proc. Natl. Acad. Sci. USA 104: 3318-3323.
13. Chitwood, D.H., Nogueira, F.T., Howell, M.D., Montgomery, T.A., Carrington, J.C., and Timmermans, M.C. (2009). Pattern formation via small RNA mobility. Genes Dev. 23: 549-554.
14. Chitwood, D.H., and Timmermans, M.C. (2010). Small RNAs are on the move. Nature 467: 415-419.
15. Cho, S.H., Coruh, C., and Axtell, M.J. (2012). miR156 and miR390 regulate tasiRNA accumulation and developmental timing in Physcomitrella patens. Plant Cell 24: 4837-4849.
16. Cuperus, J.T., Carbonell, A., Fahlgren, N., Garcia-Ruiz, H., Burke, R.T., Takeda, A., Sullivan, C.M., Gilbert, S.D., Montgomery, T.A., and Carrington, J.C. (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.
17. Dangl, J.L., and Jones, J.D.G. (2001). Plant pathogens and integrated defence responses to infection. Nature 411: 826-833.
18. Deakin, W.J., and Broughton, W.J. (2009). Symbiotic use of pathogenic strategies: Rhizobial protein secretion systems. Nat. Rev. Microbiol. 7: 312-320.
19. de la Luz Gutiérrez-Nava, M., Aukerman, M.J., Sakai, H., Tingey, S.V., and Williams, R.W. (2008). Artificial trans-acting siRNAs confer consistent and effective gene silencing. Plant Physiol. 147: 543-551.
20. Devers, E.A., Branscheid, A., May, P., and Krajinski, F. (2011). Stars and symbiosis: MicroRNA-and microRNA*-mediated transcript cleavage involved in arbuscular mycorrhizal symbiosis. Plant Physiol. 156: 1990-2010.
21. DeYoung, B.J., and Innes, R.W. (2006). Plant NBS-LRR proteins in pathogen sensing and host defense. Nat. Immunol. 7: 1243-1249.
22. Ding, J., Lu, Q., Ouyang, Y., Mao, H., Zhang, P., Yao, J., Xu, C., Li, X., Xiao, J., and Zhang, Q. (2012b). A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. Proc. Natl. Acad. Sci. USA 109: 2654-2659.
23. Ding, J., Shen, J., Mao, H., Xie, W., Li, X., and Zhang, Q. (2012a). RNA-directed DNA methylation is involved in regulating photoperiodsensitive male sterility in rice. Mol. Plant 5: 1210-1216.
24. Dunoyer, P., Schott, G., Himber, C., Meyer, D., Takeda, A., Carrington, J.C., and Voinnet, O. (2010). Small RNA duplexes function as mobile silencing signals between plant cells. Science 328: 912-916.
25. Fahlgren, N., Montgomery, T.A., Howell, M.D., Allen, E., Dvorak, S.K., Alexander, A.L., and Carrington, J.C. (2006). Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr. Biol. 16: 939-944.
26. 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.
27. Feller, A., Machemer, K., Braun, E.L., and Grotewold, E. (2011). Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J. 66: 94-116.
28. Finlay, R.D. (2008). Ecological aspects of mycorrhizal symbiosis: With special emphasis on the functional diversity of interactions involving the extraradical mycelium. J. Exp. Bot. 59: 1115-1126.
29. Fukudome, A., Kanaya, A., Egami, M., Nakazawa, Y., Hiraguri, A., Moriyama, H., and Fukuhara, T. (2011). Specific requirement of DRB4, a dsRNA-binding protein, for the in vitro dsRNA-cleaving activity of Arabidopsis Dicer-like 4. RNA 17: 750-760.
30. Gasciolli, V., Mallory, A.C., Bartel, D.P., and Vaucheret, H. (2005). Partially redundant functions of Arabidopsis DICER-like enzymes and a role for DCL4 in producing trans-acting siRNAs. Curr. Biol. 15: 1494-1500.
31. Geurts, R., Fedorova, E., and Bisseling, T. (2005). Nod factor signaling genes and their function in the early stages of Rhizobium infection. Curr. Opin. Plant Biol. 8: 346-352.
32. Heisel, S.E., Zhang, Y., Allen, E., Guo, L., Reynolds, T.L., Yang, X., Kovalic, D., and Roberts, J.K. (2008). Characterization of unique small RNA populations from rice grain. PLoS ONE 3: e2871.
33. Henderson, I.R., Zhang, X., Lu, C., Johnson, L., Meyers, B.C., Green, P.J., and Jacobsen, S.E. (2006). Dissecting Arabidopsis thaliana DICER function in small RNA processing, gene silencing and DNA methylation patterning. Nat. Genet. 38: 721-725.
34. Howell, M.D., Fahlgren, N., Chapman, E.J., Cumbie, J.S., Sullivan, C.M., Givan, S.A., Kasschau, K.D., and Carrington, J.C. (2007). Genome-wide analysis of the RNA-DEPENDENT RNA POLYMERASE6/ DICER-LIKE4 pathway in Arabidopsis reveals dependency on miRNA-and tasiRNA-directed targeting. Plant Cell 19: 926-942.
35. Hsieh, L.C., Lin, S.I., Shih, A.C., Chen, J.W., Lin, W.Y., Tseng, C.Y., Li, W.H., and Chiou, T.J. (2009). Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol. 151: 2120-2132.
36. Hunter, C., Willmann, M.R., Wu, G., Yoshikawa, M., de la Luz Gutiérrez-Nava, M., and Poethig, S.R. (2006). Trans-acting siRNAmediated repression of ETTIN and ARF4 regulates heteroblasty in Arabidopsis. Development 133: 2973-2981.
37. International Brachypodium Initiative (2010). Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature 463: 763-768.
38. Jin, H., and Martin, C. (1999). Multifunctionality and diversity within the plant MYB-gene family. Plant Mol. Biol. 41: 577-585.
39. Johnson, C., Kasprzewska, A., Tennessen, K., Fernandes, J., Nan, G.L., Walbot, V., Sundaresan, V., Vance, V., and Bowman, L.H. (2009). Clusters and superclusters of phased small RNAs in the developing inflorescence of rice. Genome Res. 19: 1429-1440.
40. Jones, J.D., and Dangl, J.L. (2006). The plant immune system. Nature 444: 323-329.
41. Källman, T., Chen, J., Gyllenstrand, N., and Lagercrantz, U. (2013). A significant fraction of 21-nucleotide small RNA originates from phased degradation of resistance genes in several perennial species. Plant Physiol. 162: 741-754.
42. Kim, J., Lim, C.J., Lee, B.W., Choi, J.P., Oh, S.K., Ahmad, R., Kwon, S.Y., Ahn, J., and Hur, C.G. (2012). A genome-wide comparison of NB-LRR type of resistance gene analogs (RGA) in the plant kingdom. Mol. Cells 33: 385-392.
43. Krasnikova, M.S., Milyutina, I.A., Bobrova, V.K., Ozerova, L.V., Troitsky, A.V., Solovyev, A.G., and Morozov, S.Y. (2009). Novel miR390-dependent transacting siRNA precursors in plants revealed by a PCR-based experimental approach and database analysis. J. Biomed. Biotechnol. 2009: 952304.
44. Lauressergues, D., Delaux, P.M., Formey, D., Lelandais-Brière, C., Fort, S., Cottaz, S., Bécard, G., Niebel, A., Roux, C., and Combier, J.P. (2012). The microRNA miR171h modulates arbuscular mycorrhizal colonization of Medicago truncatula by targeting NSP2. Plant J. 72: 512-522.
45. 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.
46. Lee, T.F., Gurazada, S.G., Zhai, J., Li, S., Simon, S.A., Matzke, M.A., Chen, X., and Meyers, B.C. (2012). RNA polymerase V-dependent small RNAs in Arabidopsis originate from small, intergenic loci including most SINE repeats. Epigenetics 7: 781-795.
47. Li, F., and Ding, S.W. (2006). Virus counterdefense: Diverse strategies for evading the RNA-silencing immunity. Annu. Rev. Microbiol. 60: 503-531.
48. Li, F., Orban, R., and Baker, B. (2012a). SoMART: A web server for plant miRNA, tasiRNA and target gene analysis. Plant J. 70: 891-901.
49. Li, F., Pignatta, D., Bendix, C., Brunkard, J.O., Cohn, M.M., Tung, J., Sun, H., Kumar, P., and Baker, B. (2012b). MicroRNA regulation of plant innate immune receptors. Proc. Natl. Acad. Sci. USA 109: 1790-1795.
50. 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.
51. Lin-Wang, K., Bolitho, K., Grafton, K., Kortstee, A., Karunairetnam, S., McGhie, T.K., Espley, R.V., Hellens, R.P., and Allan, A.C. (2010). An R2R3 MYB transcription factor associated with regulation of the anthocyanin biosynthetic pathway in Rosaceae. BMC Plant Biol. 10: 50.
52. Lozano, R., Ponce, O., Ramirez, M., Mostajo, N., and Orjeda, G. (2012). Genome-wide identification and mapping of NBS-encoding resistance genes in Solanum tuberosum group phureja. PLoS ONE 7: e34775.
53. Lurin, C., et al. (2004). Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16: 2089-2103.
54. Mackey, D., Belkhadir, Y., Alonso, J.M., Ecker, J.R., and Dangl, J.L. (2003). Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112: 379-389.
55. Madsen, L.H., Tirichine, L., Jurkiewicz, A., Sullivan, J.T., Heckmann., A.B., Bek, A.S., Ronson, C.W., James, E.K., and Stougaard, J. (2010). The molecular network governing nodule organogenesis and infection in the model legume Lotus japonicus. Nat. Commun. 1: 10.
56. Manavella, P.A., Koenig, D., and Weigel, D. (2012). Plant secondary siRNA production determined by microRNA-duplex structure. Proc. Natl. Acad. Sci. USA 109: 2461-2466.
57. Margis, R., Fusaro, A.F., Smith, N.A., Curtin, S.J., Watson, J.M., Finnegan, E.J., and Waterhouse, P.M. (2006). The evolution and diversification of Dicers in plants. FEBS Lett. 580: 2442-2450.
58. Marin, E., Jouannet, V., Herz, A., Lokerse, A.S., Weijers, D., Vaucheret, H., Nussaume, L., Crespi, M.D., and Maizel, A. (2010). miR390, Arabidopsis TAS3 tasiRNAs, and their AUXIN RESPONSE FACTOR targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 22: 1104-1117.
59. Matzke, M., Kanno, T., Daxinger, L., Huettel, B., and Matzke, A.J. (2009). RNA-mediated chromatin-based silencing in plants. Curr. Opin. Cell Biol. 21: 367-376.
60. McHale, L., Tan, X., Koehl, P., and Michelmore, R.W. (2006). Plant NBS-LRR proteins: Adaptable guards. Genome Biol. 7: 212.
61. Medzhitov, R., and Janeway, C.A., Jr.,. (1997). Innate immunity: The virtues of a nonclonal system of recognition. Cell 91: 295-298.
62. Meyers, B.C., et al. (2008). Criteria for annotation of plant microRNAs. Plant Cell 20: 3186-3190.
63. Meyers, B.C., Dickerman, A.W., Michelmore, R.W., Sivaramakrishnan, S., Sobral, B.W., and Young, N.D. (1999). Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J. 20: 317-332.
64. Meyers, B.C., Kozik, A., Griego, A., Kuang, H., and Michelmore, R.W. (2003). Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15: 809-834.
65. Ming, R., et al. (2008). The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452: 991-996.
66. Molnar, A., Melnyk, C.W., Bassett, A., Hardcastle, T.J., Dunn, R., and Baulcombe, D.C. (2010). Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328: 872-875.
67. Monaghan, J., and Zipfel, C. (2012). Plant pattern recognition receptor complexes at the plasma membrane. Curr. Opin. Plant Biol. 15: 349-357.
68. Montgomery, T.A., Howell, M.D., Cuperus, J.T., Li, D., Hansen, J.E., Alexander, A.L., Chapman, E.J., Fahlgren, N., Allen, E., and Carrington, J.C. (2008a). Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 trans-acting siRNA formation. Cell 133: 128-141.
69. Montgomery, T.A., Yoo, S.J., Fahlgren, N., Gilbert, S.D., Howell, M.D., Sullivan, C.M., Alexander, A., Nguyen, G., Allen, E., Ahn, J.H., and Carrington, J.C. (2008b). AGO1-miR173 complex initiates phased siRNA formation in plants. Proc. Natl. Acad. Sci. USA 105: 20055-20062.
70. Navarro, L., Jay, F., Nomura, K., He, S.Y., and Voinnet, O. (2008). Suppression of the microRNA pathway by bacterial effector proteins. Science 321: 964-967.
71. Oldroyd, G.E., and Downie, J.A. (2008). Coordinating nodule morphogenesis with rhizobial infection in legumes. Annu. Rev. Plant Biol. 59: 519-546.
72. O'Toole, N., Hattori, M., Andres, C., Iida, K., Lurin, C., Schmitz-Linneweber, C., Sugita, M., and Small, I. (2008). On the expansion of the pentatricopeptide repeat gene family in plants. Mol. Biol. Evol. 25: 1120-1128.
73. Pan, Q., Wendel, J., and Fluhr, R. (2000). Divergent evolution of plant NBS-LRR resistance gene homologues in dicot and cereal genomes. J. Mol. Evol. 50: 203-213.
74. 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.
75. Petroni, K., and Tonelli, C. (2011). Recent advances on the regulation of anthocyanin synthesis in reproductive organs. Plant Sci. 181: 219-229.
76. Poethig, R.S., Peragine, A., Yoshikawa, M., Hunter, C., Willmann, M., and Wu, G. (2006). The function of RNAi in plant development. Cold Spring Harb. Symp. Quant. Biol. 71: 165-170.
77. Qiao, Y., et al. (2013). Oomycete pathogens encode RNA silencing suppressors. Nat. Genet. 45: 330-333.
78. 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.
79. 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.
80. Si-Ammour, A., Windels, D., Arn-Bouldoires, E., Kutter, C., Ailhas, J., Meins, F., and Vazquez, F. (2011). miR393 and secondary siRNAs regulate expression of the TIR1/AFB2 auxin receptor clade and auxinrelated development of Arabidopsis leaves. Plant Physiol. 157: 683-691.
81. Song, X., et al. (2012). Roles of DCL4 and DCL3b in rice phased small RNA biogenesis. Plant J. 69: 462-474.
82. Takos, A.M., Jaffé, F.W., Jacob, S.R., Bogs, J., Robinson, S.P., and Walker, A.R. (2006). Light-induced expression of a MYB gene regulates anthocyanin biosynthesis in red apples. Plant Physiol. 142: 1216-1232.
83. Talmor-Neiman, M., Stav, R., Klipcan, L., Buxdorf, K., Baulcombe, D.C., and Arazi, T. (2006). Identification of trans-acting siRNAs in moss and an RNA-dependent RNA polymerase required for their biogenesis. Plant J. 48: 511-521.
84. Tian, D., Traw, M.B., Chen, J.Q., Kreitman, M., and Bergelson, J. (2003). Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423: 74-77.
85. Valencia-Sanchez, M.A., Liu, J., Hannon, G.J., and Parker, R. (2006). Control of translation and mRNA degradation by miRNAs and siRNAs. Genes Dev. 20: 515-524.
86. Van der Biezen, E.A., and Jones, J.D. (1998). Plant diseaseresistance proteins and the gene-for-gene concept. Trends Biochem. Sci. 23: 454-456.
87. Vazquez, F., Vaucheret, H., Rajagopalan, R., Lepers, C., Gasciolli, V., Mallory, A.C., Hilbert, J.L., Bartel, D.P., and Crété, P. (2004). Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs. Mol. Cell 16: 69-79.
88. Voinnet, O. (2009). Origin, biogenesis, and activity of plant microRNAs. Cell 136: 669-687.
89. 2+-ATPase and triggers the formation of phased small interfering RNAs in tomato reproductive growth. Plant Cell 23: 3185-3203.
90. Whitham, S., Dinesh-Kumar, S.P., Choi, D., Hehl, R., Corr, C., and Baker, B. (1994). The product of the tobacco mosaic virus resistance gene N: Similarity to toll and the interleukin-1 receptor. Cell 78: 1101-1115.
91. Williams, L., Carles, C.C., Osmont, K.S., and Fletcher, J.C. (2005). A database analysis method identifies an endogenous trans-acting short-interfering RNA that targets the Arabidopsis ARF2, ARF3, and ARF4 genes. Proc. Natl. Acad. Sci. USA 102: 9703-9708.
92. Willmann, M.R., Endres, M.W., Cook, R.T., and Gregory, B.D. (2011). The functions of RNA-dependent RNA Polymerases in Arabidopsis. The Arabidopsis Book 9: e0146, doi/10.199/tab.0146.
93. Wu, L., Mao, L., andQi, Y. (2012). Roles of dicer-like and argonaute proteins in TAS-derived small interfering RNA-triggered DNA methylation. Plant Physiol. 160: 990-999.
94. Wu, L., Zhou, H., Zhang, Q., Zhang, J., Ni, F., Liu, C., andQi, Y. (2010). DNA methylation mediated by a microRNA pathway. Mol. Cell 38: 465-475.
95. Xia, R., Meyers, B.C., Liu, Z., Beers, E.P., and Ye, S. (2013). MicroRNA superfamilies descended from miR390 and their roles in secondary small interfering RNA biogenesis in eudicots. Plant Cell 25: 1555-1572.
96. Xia, R., Zhu, H., An, Y.Q., Beers, E.P., and Liu, Z. (2012). Apple miRNAs and tasiRNAs with novel regulatory networks. Genome Biol. 13: R47.
97. Xia, S., Cheng, Y.T., Huang, S., Win, J., Soards, A., Jinn, T.L., Jones, J., Kamoun, S., Chen, S., Zhang, Y., and Li, X. (2013). Regulation of transcription of NB-LRR-encoding genes SNC1 and RPP4 via H3K4 tri-methylation. Plant Physiol. 162: 1694-1705.
98. Xie, Z., Allen, E., Wilken, A., and Carrington, J.C. (2005). DICERLIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana. Proc. Natl. Acad. Sci. USA 102: 12984-12989.
99. Xu, X., et al; Potato Genome Sequencing Consortium (2011). Genome sequence and analysis of the tuber crop potato. Nature 475: 189-195.
100. Xue, J.Y., Wang, Y., Wu, P., Wang, Q., Yang, L.T., Pan, X.H., Wang, B., and Chen, J.Q. (2012). A primary survey on bryophyte species reveals two novel classes of nucleotide-binding site (NBS) genes. PLoS ONE 7: e36700.
101. Yang, L., Li, D., Li, Y., Gu, X., Huang, S., Garcia-Mas, J., andWeng, Y. (2013). A 1,681-locus consensus genetic map of cultivated cucumber including 67 NB-LRR resistance gene homolog and ten gene loci. BMC Plant Biol. 13: 53.
102. Yang, S., Tang, F., Gao, M., Krishnan, H.B., and Zhu, H. (2010). R gene-controlled host specificity in the legume-rhizobia symbiosis. Proc. Natl. Acad. Sci. USA 107: 18735-18740.
103. Yi, H., and Richards, E.J. (2007). A cluster of disease resistance genes in Arabidopsis is coordinately regulated by transcriptional activation and RNA silencing. Plant Cell 19: 2929-2939.
104. Yoshikawa, M., Iki, T., Tsutsui, Y., Miyashita, K., Poethig, R.S., Habu, Y., and Ishikawa, M. (2013). 39 Fragment of miR173-programmed RISC-cleaved RNA is protected from degradation in a complex with RISC and SGS3. Proc. Natl. Acad. Sci. USA 110: 4117-4122.
105. Yoshikawa, M., Peragine, A., Park, M.Y., and Poethig, R.S. (2005). A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis. Genes Dev. 19: 2164-2175.
106. Young, N.D., et al. (2011). The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480: 520-524.
107. Zhai, J., et al. (2011). MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, transacting siRNAs. Genes Dev. 25: 2540-2553.
108. Zhai, J., et al. (2013). Plant microRNAs display differential 39-trancation and tailing, modifications which are ARGONAUTE1-dependent and conserved across species. Plant Cell, doi/10.1105/tpc.113.114603.
109. Zhang, C., Li, G., Wang, J., and Fang, J. (2012b). Identification of trans-acting siRNAs and their regulatory cascades in grapevine. Bioinformatics 28: 2561-2568.
110. Zhang, C., Ng, D.W., Lu, J., and Chen, Z.J. (2012a). Roles of target site location and sequence complementarity in trans-acting siRNA formation in Arabidopsis. Plant J. 69: 217-226.
111. Zhang, Y., Goritschnig, S., Dong, X., and Li, X. (2003). A gain-offunction mutation in a plant disease resistance gene leads to constitutive activation of downstream signal transduction pathways in suppressor of npr1-1, constitutive 1. Plant Cell 15: 2636-2646.
112. Zhang, Y., and Li, X. (2005). A putative nucleoporin 96 Is required for both basal defense and constitutive resistance responses mediated by suppressor of npr1-1, constitutive 1. Plant Cell 17: 1306-1316.
113. Zhou, H., et al. (2012). Photoperiod-and thermo-sensitive genic male sterility in rice are caused by a point mutation in a novel noncoding RNA that produces a small RNA. Cell Res. 22: 649-660.
114. Zhou, T., Wang, Y., Chen, J.Q., Araki, H., Jing, Z., Jiang, K., Shen, J., and Tian, D. (2004). Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes. Mol. Genet. Genomics 271: 402-415.
115. Zhu, H., Xia, R., Zhao, B., An, Y.Q., Dardick, C.D., Callahan, A.M., and Liu, Z. (2012). Unique expression, processing regulation, and regulatory network of peach (Prunus persica) miRNAs. BMC Plant Biol. 12: 149.