The role of ARGONAUTE1 (AGO1) in meristem formation and identity

Developmental Biology

Volumn 280, Issue 2, 2005, Pages 504-517

  Kidner, Catherine A ^a   Martienssen, Robert A ^a,b,c  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^b ROYAL BOTANIC GARDEN EDINBURGH   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

AGO1; Meristem; miRNA; RNA interference

Indexed keywords

ARABIDOPSIS AGAMOUS PROTEIN; MICRORNA;

ARTICLE; CONTROLLED STUDY; FLOWERING; GENE CONTROL; GENE EXPRESSION; GENE FUNCTION; GENE OVEREXPRESSION; MERISTEM; NONHUMAN; PLANT CELL; PLANT DEVELOPMENT; PLANT GENETICS; PLANT LEAF; PRIORITY JOURNAL; RNA INTERFERENCE; STEM CELL;

ERAGROSTIS RIGIDIOR;

EID: 18844424626     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2005.01.031     Document Type: Article

References (111)

1. P. Achard, A. Herr, D.C. Baulcombe, and N.P. Harberd Modulation of floral development by a gibberellin-regulated microRNA Development 131 2004 3357 3365
2. M. Aida, T. Ishida, H. Fukaki, H. Fujisawa, and M. Tasaka Genes involved in organ separation in Arabidopsis: an analysis of the cup shaped cotyledon mutant Plant Cell 9 1997 841 857
3. M. Aida, T. Ishida, and M. Tasaka Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes Development 126 1999 1563 1570
4. M.J. Aukerman, and H. Sakai Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes Plant Cell 15 2003 2730 2741
5. N. Bao, K.W. Lye, and M.K. Barton MicroRNA binding sites in Arabidopsis class III HD-ZIP mRNAs are required for methylation of the template chromosome Dev. Cell 7 2004 653 662
6. D.P. Bartel MicroRNAs: genomics, biogenesis, mechanism and function Cell 116 2004 281 297
7. M.K. Barton, and R.S. Poethig Formation of the shoot apical meristem Arabidopsis thaliana-An analysis of development in the wild type and in the shoot meristemless mutant Development vol. 119 1993 823 831
8. E. Bernstein, A.A. Caudy, S.M. Hammond, and G.J. Hannon Role for a bidentate ribonuclease in the initiation step of RNA interference Nature 409 2001 363 366
9. A.M. Bhatt, T. Page, E.J. Lawson, C. Lister, and C. Dean Use of Ac as an insertional mutagen in Arabidopsis Plant J. 9 1996 935 945
10. M.A. Blazquez, L.N. Soowal, I. Lee, and D. Weigel LEAFY expression and flower initiation in Arabidopsis Development 124 1997 3835 3844
11. K. Bohmert, I. Camus, C. Bellini, D. Bouchez, M. Caboche, and C. Benning AGO1 defines a novel locus of Arabidopsis controlling leaf development EMBO J. 17 1998 170 180
12. E. Bonnet, J. Wuyts, P. Rouze, and Y. Van De Peer Detection of 91 potential conserved plant microRNAs in Arabidopsis thaliana and Oryza sativa identifies important target genes Proc. Natl. Acad. Sci. U. S. A. 101 2004 11511 11516
13. S. Boutet, F. Vazquez, J. Liu, C. Beclin, M. Fagard, A. Gratias, J.B. Morel, P. Crete, X. Chen, and H. Vaucheret Arabidopsis HEN1: a genetic link between endogenous miRNA controlling development and siRNA controlling transgene silencing and virus resistance Curr. Biol. 13 2003 843 848
14. M.E. Byrne, R. Barley, M. Curtis, J.M. Arroyo, M. Dunham, A. Hudson, and R.A. Martienssen Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis Nature 408 2000 967 971
15. M.E. Byrne, J. Simorowski, and R.A. Martienssen Asymmetric leaves1 reveals knox gene redundancy in Arabidopsis Development 129 2002 1957 1965
16. M.E. Byrne, A.T. Groover, J.R. Fontana, and R.A. Martienssen Phyllotactic pattern and stem cell fate are determined by the Arabidopsis homeobox gene BELLRINGER Development 130 2003 3941 3950
17. G.H. Cardon, S. Hohmann, K. Nettesheim, H. Saedler, and P. Huijser Functional analysis of the Arabidopsis thaliana SBP-box gene SPL3: a novel gene involved in the floral transition Plant J. 12 1997 367 377
18. G. Cardon, S. Hohmann, J. Klein, K. Nettesheim, H. Saedler, and P. Huijser Molecular characterisation of the Arabidopsis SBP-box genes Gene 237 1999 91 104
19. M.A. Carmell, Z. Xuan, M.Q. Zhang, and G.J. Hannon The Argonaute family: tentacles that reach into RNAi, developmental control, stem cell maintenance, and tumorigenesis Genes Dev. 16 2002 2733 2742
20. A.A. Caudy, M. Myers, G.J. Hannon, and S.M. Hammond Fragile X-related protein and VIG associate with the RNA interference machinery Genes Dev. 16 2002 2491 2496
21. L. Cerutti, N. Mian, and A. Bateman Domains in gene silencing and cell differentiation proteins: the novel PAZ domain and redefinition of the Piwi domain Trends Biochem. Sci. 25 2000 481 482
22. S.W. Chan, D. Zilberman, Z. Xie, L.K. Johansen, J.C. Carrington, and S.E. Jacobsen RNA silencing genes control de novo DNA methylation Science 303 2004 1336
23. X. Chen A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development Science 303 2004 2022 2025
24. S.E. Clark, S.E. Jacobsen, J.Z. Levin, and E.M. Meyerowitz The CLAVATA and SHOOT MERISTEMLESS loci competitively regulate meristem activity in Arabidopsis Development 122 1996 1567 1575
25. D.N. Cox, A. Chao, J. Baker, L. Chang, D. Qiao, and H. Lin A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal Genes Dev. 12 1998 3715 3727
26. D.N. Cox, A. Chao, and H. Lin piwi encodes a nucleoplasmic factor whose activity modulates the number and division rate of germline stem cells Development 127 2000 503 514
27. N.R. Dudley, J.C. Labbe, and B. Goldstein Using RNA interference to identify genes required for RNA interference Proc. Natl. Acad. Sci. U. S. A. 99 2002 4191 4196
28. J.F. Emery, S.K. Floyd, J. Alvarez, Y. Eshed, N.P. Hawker, A. Izhaki, S.F. Baum, and J.L. Bowman Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes Curr. Biol. 13 2003 1768 1774
29. K. Endrizzi, B. Moussian, A. Haecker, J.Z. Levin, and T. Laux The SHOOT MERISTEMLESS gene is required for maintenance of undifferentiated cells in Arabidopsis shoot and floral meristems and acts at a different regulatory level than the meristem genes WUSCHEL and ZWILLE Plant J. 10 1996 967 979
30. E.J. Finnegan, R. Margis, and P.M. Waterhouse Posttranscriptional gene silencing is not compromised in the Arabidopsis CARPEL FACTORY (DICER-like1) mutant, a homolog of Dicer-1 from Drosophila Curr. Biol. 13 2003 236 240
31. S.K. Floyd, and J.L. Bowman Gene regulation: ancient microRNA target sequences in plants Nature 428 2004 485 486
32. J.L. Gallois, C. Woodward, G.V. Reddy, and R. Sablowski Combined SHOOT MERISTEMLESS and WUSCHEL trigger ectopic organogenesis in Arabidopsis Development 129 2002 3207 3217
33. G.F. Gocal, C.C. Sheldon, F. Gubler, T. Moritz, D.J. Bagnall, C.P. MacMillan, S.F. Li, R.W. Parish, E.S. Dennis, D. Weigel, and R.W. King GAMYB-like genes, flowering, and gibberellin signaling in Arabidopsis Plant Physiol. 127 2001 1682 1693
34. T.A. Golden, S.E. Schauer, J.D. Lang, S. Pien, A.R. Mushegian, U. Grossniklaus, D.W. Meinke, and A. Ray SHORT INTEGUMENTS1/SUSPENSOR1/CARPEL FACTORY, a Dicer homolog, is a maternal effect gene required for embryo development in Arabidopsis Plant Physiol. 130 2002 808 822
35. J. Goodrich, P. Puangsomlee, M. Martin, D. Long, E.M. Meyerowitz, and G. Coupland A Polycomb-group gene regulates homeotic gene expression in Arabidopsis Nature 386 1997 44 51
36. A. Grishok, A.E. Pasquinelli, D. Conte, N. Li, S. Parrish, I. Ha, D.L. Baillie, A. Fire, G. Ruvkun, and C.C. Mello Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing Cell 106 2001 23 34
37. Q. Gu, C. Ferrándiz, M.F. Yanofsky, and R. Martienssen The FRUITFULL MADS-box gene mediates cell differentiation during Arabidopsis fruit development Development 125 1998 1509 1517
38. A.J. Hamilton, and D.C. Baulcombe A species of small antisense RNA in posttranscriptional gene silencing in plants Science 286 1999 950 952
39. S.M. Hammond, S. Boettcher, A.A. Caudy, R. Kobayashi, and G.J. Hannon Argonaute2, a link between genetic and biochemical analyses of RNAi Science 293 2001 1146 1150
40. M.H. Han, S. Goud, L. Song, and N. Fedoroff The Arabidopsis double-stranded RNA-binding protein HYL1 plays a role in microRNA-mediated gene regulation Proc. Natl. Acad. Sci. U. S. A. 101 2004 1093 1098
41. A.N. Harris, and P.M. Macdonald Aubergine encodes a Drosophila polar granule component required for pole cell formation and related to eIF2C Development 128 2001 2823 2832
42. K. Hibara, S. Takada, and M. Tasaka CUC1 gene activates the expression of SAM-related genes to induce adventitious shoot formation Plant J. 36 2003 687 696
43. C. Hunter, H. Sun, and R.S. Poethig The Arabidopsis heterochronic gene ZIPPY is an ARGONAUTE family member Curr. Biol. 13 2003 1734 1739
44. S.E. Jacobsen, M.P. Running, and E.M. Meyerowitz Disruption of an RNA helicase/RNAse III gene in Arabidopsis causes unregulated cell division in floral meristems Development 126 1999 5231 5243
45. L. Jones, A.J. Hamilton, O. Voinnet, C.L. Thomas, A.J. Maule, and D.C. Baulcombe RNA-DNA interactions and DNA methylation in post-transcriptional gene silencing Plant Cell 11 1999 2291 2301
46. M.W. Jones-Rhoades, and D.P. Bartel Computational identification of plant MicroRNAs and their targets. Including a Stress-Induced miRNA Mol. Cell 14 2004 787 799
47. M.T. Juarez, J.S. Kui, J. Thomas, B.A. Heller, and M.C. Timmermans microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity Nature 428 2004 84 88
48. Y. Kataoka, M. Takeichi, and T. Uemura Developmental roles and molecular characterization of a Drosophila homologue of Arabidopsis Argonaute1, the founder of a novel gene superfamily Genes Cells 6 2001 313 325
49. A. Katz, M. Oliva, A. Mosquna, O. Hakim, and N. Ohad FIE and CURLY LEAF polycomb proteins interact in the regulation of homeobox gene expression during sporophyte development Plant J. 37 2004 707 719
50. C.A. Kidner, and R.A. Martienssen Spatially restricted microRNA directs leaf polarity through ARGONAUTE1 Nature 428 2004 81 84
51. M. Lagos-Quintana, R. Rauhut, W. Lendeckel, and T. Tuschl Identification of novel genes coding for small expressed RNAs Science 294 2001 853 858
52. N.C. Lau, E.P. Lim le, E.G. Weinstein, and V.P. Bartel da An abundant class of tiny RNAs with probable regulatory roles in Caenorhabditis elegans Science 294 2001 858 862
53. P. Laufs, A. Peaucelle, H. Morin, and J. Traas MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristems Development 131 2004 4311 4322
54. R.C. Lee, and V. Ambros An extensive class of small RNAs in Caenorhabditis elegans Science 294 2001 862 864
55. I. Lee, D.S. Wolfe, O. Nilsson, and D. Weigel A LEAFY co-regulator encoded by UNUSUAL FLORAL ORGANS Curr. Biol. 7 1997 95 104
56. B. Lehnertz, Y. Ueda, A.A. Derijck, U. Braunschweig, L. Perez-Burgos, S. Kubicek, T. Chen, E. Li, T. Jenuwein, and A.H. Peters Suv39h-mediated histone H3 lysine 9 methylation directs DNA methylation to major satellite repeats at pericentric heterochromatin Curr. Biol. 13 2003 1192 1200
57. M. Lenhard, G. Jurgens, and T. Laux The WUSCHEL and SHOOTMERISTEMLESS genes fulfil complementary roles in Arabidopsis shoot meristem regulation Development 129 2002 3195 3206
58. J.Z. Levin, and E.M. Meyerowitz UFO: an Arabidopsis gene involved in both floral meristem and floral organ development Plant Cell 7 1995 529 548
59. W.C. Lin, B. Shuai, and P.S. Springer The Arabidopsis LATERAL ORGAN BOUNDARIES-domain gene ASYMMETRIC LEAVES2 functions in the repression of KNOX gene expression and in adaxial-abaxial patterning Plant Cell 15 2003 2241 2252
60. A. Lingel, B. Simon, E. Izaurralde, and M. Sattler Structure and nucleic-acid binding of the Drosophila Argonaute 2 PAZ domain Nature 426 2003 465 469
61. Z. Lippman, B. May, C. Yordan, T. Singer, and R. Martienssen Distinct mechanisms determine transposon inheritance and methylation via small interfering RNA and histone modification PLoS Biol. 1 2003 E67
62. J. Liu, E. Bernstein, and G.J. Hannon AGO is the catalytic enzyme of RNAi Science 305 2004 1437 1441
63. C. Llave, K.D. Kasschau, M.A. Rector, and J.C. Carrington Endogenous and silencing-associated small RNAs in plants Plant Cell 14 2002 1605 1619
64. C. Llave, Z. Xie, K.D. Kasschau, and J.C. Carrington Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA Science 297 2002 2053 2056
65. J.A. Long, and M.K. Barton The development of apical embryonic pattern in Arabidopsis Development 125 1998 3027 3035
66. C. Lu, and N. Fedoroff A mutation in the Arabidopsis HYL1 gene encoding a dsRNA binding protein affects responses to abscisic acid, auxin, and cytokinin Plant Cell 12 2000 2351 2366
67. K. Lynn, A. Fernandez, M. Aida, J. Sedbrook, M. Tasaka, P. Masson, and M.K. Barton The PINHEAD/ZWILLE gene acts pleiotropically in Arabidopsis development and has overlapping functions with the ARGONAUTE1 gene Development 126 1999 469 481
68. A.C. Mallory, D.V. Dugas, D.P. Bartel, and B. Bartel MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs Curr. Biol. 14 2004 1035 1046
69. A.C. Mallory, B.J. Reinhart, M.W. Jones-Rhoades, G. Tang, P.D. Zamore, M.K. Barton, and D.P. Bartel MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5′ region EMBO J. 23 2004 3356 3364
70. M.A. Mandel, and M.F. Yanofsky The Arabidopsis Agl8 mads box gene is expressed in inflorescence meristems and is negatively regulated by apetala1 Plant Cell 7 1995 1763 1771
71. M. Matzke, A.J. Matzke, and J.M. Kooter RNA: guiding gene silencing Science 293 2001 1080 1083
72. J.R. McConnell, J. Emery, Y. Eshed, N. Bao, J. Bowman, and M.K. Barton Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots Nature 411 2001 709 713
73. N.A. McHale, and R.E. Koning MicroRNA-directed cleavage of Nicotiana sylvestris PHAVOLUTA mRNA regulates the vascular cambium and structure of apical meristems Plant Cell 16 2004 1730 1740
74. G. Meister, M. Landthaler, A. Patkaniowska, Y. Dorsett, G. Teng, and T. Tuschl Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs Mol. Cell. 15 2004 185 197
75. J.B. Morel, C. Godon, P. Mourrain, C. Beclin, S. Boutet, F. Feuerbach, F. Proux, and H. Vaucheret Fertile hypomorphic ARGONAUTE (ago1) mutants impaired in post-transcriptional gene silencing and virus resistance Plant Cell 14 2002 629 639
76. M.A. Moreno, L.C. Harper, R.W. Krueger, S.L. Dellaporta, and M. Freeling liguleless1 encodes a nuclear-localized protein required for induction of ligules and auricles during maize leaf organogenesis Genes Dev. 11 1997 616 628
77. B. Moussian, H. Schoof, A. Haecker, G. Jurgens, and T. Laux Role of the ZWILLE gene in the regulation of central shoot meristem cell fate during Arabidopsis embryogenesis EMBO J. 17 1998 1799 1809
78. B. Moussian, A. Haecker, and T. Laux ZWILLE buffers meristem stability in Arabidopsis thaliana Dev. Genes Evol. 213 2003 534 540
79. K.L. Newman, A.G. Fernandez, and M.K. Barton Regulation of axis determinacy by the Arabidopsis PINHEAD gene Plant Cell 14 2002 3029 3042
80. N. Ori, Y. Eshed, G. Chuck, J.L. Bowman, and S. Hake Mechanisms that control knox gene expression in the Arabidopsis shoot Development 127 2000 5523 5532
81. J.F. Palatnik, E. Allen, X. Wu, C. Schommer, R. Schwab, J.C. Carrington, and D. Weigel Control of leaf morphogenesis by microRNAs Nature 425 2003 257 263
82. M. Pal-Bhadra, U. Bhadra, and J.A. Birchler Cosuppression in Drosophila: gene silencing of Alcohol dehydrogenase by white-Adh transgenes is Polycomb dependent Cell 90 1997 479 490
83. M. Pal-Bhadra, U. Bhadra, and J.A. Birchler RNAi related mechanisms affect both transcriptional and posttranscriptional transgene silencing in Drosophila Mol. Cell 9 2002 315 327
84. F. Parcy, O. Nilsson, M.A. Busch, I. Lee, and D. Weigel A genetic framework for floral patterning Nature 395 1998 561 566
85. W. Park, J. Li, R. Song, J. Messing, and X. Chen CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana Curr. Biol. 12 2002 1484 1495
86. A. Peragine, M. Yoshikawa, G. Wu, H.L. Albrecht, and R.S. Poethig SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis Genes Dev. 18 2004 2368 2379
87. T.A. Rand, K. Ginalski, N.V. Grishin, and X. Wang Biochemical identification of Argonaute 2 as the sole protein required for RNA-induced silencing complex activity Proc. Natl. Acad. Sci. U. S. A. 101 2004 14385 14389
88. B.J. Reinhart, and D.P. Bartel Small RNAs correspond to centromere heterochromatic repeats Science 297 2002 1831
89. B.J. Reinhart, E.G. Weinstein, M.W. Rhoades, B. Bartel, and D.P. Bartel MicroRNAs in plants Genes Dev. 16 2002 1616 1626
90. M.W. Rhoades, B.J. Reinhart, L.P. Lim, C.B. Burge, B. Bartel, and D.P. Bartel Prediction of plant microRNA targets Cell 110 2002 513 520
91. J. Sambrook, E.F. Fritsch, and T. Maniatis Molecular cloning: a laboratory manual 1989 Cold Spring Harbor Press Cold Spring Harbor, New York
92. A. Schmidt, G. Palumbo, M.P. Bozzetti, P. Tritto, S. Pimpinelli, and U. Schafer Genetic and molecular characterization of sting, a gene involved in crystal formation and meiotic drive in the male germ line of Drosophila melanogaster Genetics 151 1999 749 760
93. H. Schoof, M. Lenhard, A. Haecker, K.F. Mayer, G. Jurgens, and T. Laux The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes [In Process Citation] Cell 100 2000 635 644
94. J.J. Song, J. Liu, N.H. Tolia, J. Schneiderman, S.K. Smith, R.A. Martienssen, G.J. Hannon, and L. Joshua-Tor The crystal structure of the Argonaute2 PAZ domain reveals an RNA binding motif in RNAi effector complexes Nat. Struct. Biol. 10 2003 1026 1032
95. J.J. Song, G.J. Hannon, and L. Joshua-Tor Crystal structure of AGO Science 305 2004 1434 1437
96. V. Sundaresan, P. Springer, T. Volpe, S. Haward, J.D.G. Jones, C. Dean, H. Ma, and R. Martienssen Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements Genes Dev. 9 1995 1797 1810
97. H. Tabara, M. Sarkissian, W.G. Kelly, J. Fleenor, A. Grishok, L. Timmons, A. Fire, and C.C. Mello The rde-1 gene, RNA interference, and transposon silencing in C. elegans Cell 99 1999 123 132
98. G. Tang, and P.D. Zamore Biochemical dissection of RNA silencing in plants Methods Mol. Biol. 257 2004 223 244
99. V. Vance, and H. Vaucheret RNA silencing in plants-Defense and counterdefense Science 292 2001 2277 2280
100. H. Vaucheret, F. Vazquez, P. Crete, and D.P. Bartel The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development Genes Dev. 18 2004 1187 1197
101. F. Vazquez, V. Gasciolli, P. Crete, and H. Vaucheret The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not posttranscriptional transgene silencing Curr. Biol. 14 2004 346 351
102. O. Voinnet, Y.M. Pinto, and D.C. Baulcombe Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants Proc. Natl. Acad. Sci. U. S. A. 96 1999 14147 14152
103. T.A. Volpe, C. Kidner, I.M. Hall, G. Teng, S.I. Grewal, and R.A. Martienssen Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi Science 297 2002 1833 1837
104. J.F. Wang, H. Zhou, Y.Q. Chen, Q.J. Luo, and L.H. Qu Identification of 20 microRNAs from Oryza sativa Nucleic Acids Res. 32 2004 1688 1695
105. D. Weigel, J. Alvarez, D.R. Smyth, M.F. Yanofsky, and E.M. Meyerowitz LEAFY controls floral meristem identity in Arabidopsis Cell 69 1992 843 859
106. R.W. Williams, and G.M. Rubin ARGONAUTE1 is required for efficient RNA interference in Drosophila embryos Proc. Natl. Acad. Sci. U. S. A. 99 2002 6889 6894
107. Z. Xie, K.D. Kasschau, and J.C. Carrington Negative feedback regulation of Dicer-like1 in Arabidopsis by microRNA-guided mRNA degradation Curr. Biol. 13 2003 784 789
108. Z. Xie, L.K. Johansen, A.M. Gustafson, K.D. Kasschau, A.D. Lellis, D. Zilberman, S.E. Jacobsen, and J.C. Carrington Genetic and functional diversification of small RNA pathways in plants PLoS Biol. 2 2004 E104
109. K.S. Yan, S. Yan, A. Farooq, A. Han, L. Zeng, and M.M. Zhou Structure and conserved RNA binding of the PAZ domain Nature 426 2003 468 474
110. D. Zilberman, X. Cao, and S.E. Jacobsen ARGONAUTE4 control of locus-specific siRNA accumulation and DNA and histone methylation Science 299 2003 716 719
111. S.C. Zondlo, and V.F. Irish CYP78A5 encodes a cytochrome P450 that marks the shoot apical meristem boundary in Arabidopsis Plant J. 19 1999 259 268