Small RNA-regulated networks and the evolution of novel structures in plants

Cold Spring Harbor Symposia on Quantitative Biology

Volumn 77, Issue , 2012, Pages 221-233

  Plavskin, Y ^a   Timmermans, M C P ^a  

^a Simons Center for Quantitative Biology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE PROTEIN; AUXIN; MICRORNA; POLYCOMB GROUP PROTEIN; RNA; SMALL RNA; UNCLASSIFIED DRUG; MICRORNA 390; PLANT RNA;

3' UNTRANSLATED REGION; ARTICLE; BINDING SITE; GENE EXPRESSION; GENE REGULATORY NETWORK; GENE SILENCING; NONHUMAN; PIGMENTATION; PLANT APICAL DOMINANCE; PLANT EVOLUTION; PLEIOTROPY; PRIORITY JOURNAL; PROMOTER REGION; ROOT HAIR; BIOGENESIS; DEVELOPMENTAL GENE; EVOLUTIONARY DEVELOPMENTAL BIOLOGY; GENETIC CONSERVATION; MOLECULAR EVOLUTION; PLANT DEVELOPMENT; PLANT STRUCTURES;

BASE SEQUENCE; BIOLOGICAL EVOLUTION; GENE REGULATORY NETWORKS; MICRORNAS; MOLECULAR SEQUENCE DATA; PLANT DEVELOPMENT; RNA, PLANT; RNA, SMALL INTERFERING;

EID: 84881510393     PISSN: 00917451     EISSN: None     Source Type: Book Series    
DOI: 10.1101/sqb.2013.77.014878     Document Type: Article

References (127)

1. Abdel-Ghany SE, Pilon M. 2008. microRNA-mediated systemic down-regulation of copper protein expression in response to low copper availability in Arabidopsis. J Biol Chem 283: 15932-15945.
2. Addo-Quaye C, Eshoo TW, Bartel DP, Axtell MJ. 2008. Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Curr Biol 18: 758-762.
3. Addo-Quaye C, Miller W, Axtell MJ. 2009. CleaveLand: A pipeline for using degradome data to find cleaved small RNA targets. Bioinformatics 25: 130-131.
4. Allen E, Xie Z, Gustafson AM, Sung G-H, Spatafora JW, Carrington JC. 2004. Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana. Nat Genet 36: 1282-1290.
5. Allen E, Xie Z, Gustafson AM, Carrington JC. 2005. micro-RNA-directed phasing during transacting siRNA biogenesis in plants. Cell 121: 207-221.
6. Alon U. 2006. An introduction to systems biology: Design principles of biological circuits, 1st ed., pp. 34-37. Chapman and Hall/CRC Press, Boca Raton, FL.
7. Aoyama T, Hiwatashi Y, Shigyo M, Kofuji R, Kubo M, Ito M, Hasebe M. 2012. AP2-type transcription factors determine stem cell identity in the moss Physcomitrella patens. Development 139: 3120-3129.
8. Arazi T, Talmor-Neiman M, Stav R, Riese M, Huijser P, Baul-combe DC. 2005. Cloning and characterization of micro-RNAs from moss. Plant J 43: 837-848.
9. Arif MA, Fattash I, Ma Z, Cho SH, Beike AK, Reski R, Axtell MJ, Frank W. 2012. DICER-LIKE3 activity in Physcomitrella patens DICER-LIKE4 mutants causes severe developmental dysfunction and sterility. Mol Plant 5: 1281-1294.
10. Ashton NW, Grimsley NH, Cove DJ. 1979. Analysis of gametophytic development in the moss, Physcomitrella patens, using auxin and cytokinin resistant mutants. Planta 144: 427-435.
11. Axtell MJ, Bowman JL. 2008. Evolution of plant microRNAs and their targets. Trends Plant Sci 13: 343-349.
12. Axtell MJ, Jan C, Rajagopalan R, Bartel DP. 2006. A two-hit trigger for siRNA biogenesis in plants. Cell 127: 565-577.
13. Axtell MJ, Snyder JA, Bartel DP. 2007. Common functions for diverse small RNAs of land plants. Plant Cell 19: 1750-1769.
14. Axtell MJ, Westholm JO, Lai EC. 2011. Vive la différence: Biogenesis and evolution of microRNAs in plants and animals. Genome Biol 12: 221.
15. Banks JA, Nishiyama T, Hasebe M, Bowman JL, Gribskov M, Depamphilis C, Albert VA, Aono N, Aoyama T, Ambrose BA, et al. 2011. The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332: 960-963.
16. Bartel DP. 2004. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116: 281-297.
17. Basu S, Sun H, Brian L, Quatrano RL, Muday GK. 2002. Early embryo development in Fucus distichus is auxin sensitive. Plant Physiol 130: 292-302.
18. Bergmann DC, Lukowitz W, Somerville CR. 2004. Stomatal development and pattern controlled by a MAPKK kinase. Science 304: 1494-1497.
19. BharathanG,GoliberTE,MooreC,KesslerS,PhamT,SinhaNR. 2002. Homologies in leaf form inferred from KNOXI gene expression during development. Science 296: 1858-1860.
20. Carlsbecker A, Lee J-Y, Roberts CJ, Dettmer J, Lehesranta S, Zhou J, Lindgren O, Moreno-Risueno MA, Vatén A, Thitamadee S, et al. 2010. Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 465: 316-321.
21. Carroll SB, Grenier J, Weatherbee S. 2004. From DNA to diversity: Molecular genetics and the evolution of animal design, 2nd ed., pp. 161-171, 208-209. Wiley-Blackwell, Oxford.
22. Chapman EJ, Carrington JC. 2007. Specialization and evolution of endogenous small RNA pathways. Nat Rev Genet 8:884-896.
23. Chen X. 2009. Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol 25: 21-44.
24. Chen JG, Ullah H, Young JC, Sussman MR, Jones AM. 2001. ABP1 is required for organized cell elongation and division in Arabidopsis embryogenesis. Genes Dev 15: 902-911.
25. Chitwood DH, Nogueira FTS, Howell MD, Montgomery TA, Carrington JC, Timmermans MCP. 2009. Pattern formation via small RNA mobility. Genes Dev 23: 549-554.
26. Chuck G, Cigan AM, Saeteurn K, Hake S. 2007. The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nat Genet 39: 544-549.
27. Clop A, Marcq F, Takeda H, Pirottin D, Tordoir X, Bibé B, Bouix J, Caiment F, Elsen J-M, Eychenne F, et al. 2006. A mutation creating a potential illegitimate microRNA target site in the myostatin gene affects muscularity in sheep. Nat Genet 38: 813-818.
28. Crane PR, Friis EM, Pedersen KR. 1995. The origin and early diversification of angiosperms. Nature 374: 27-33.
29. Cuperus JT, Fahlgren N, Carrington JC. 2011. Evolution and functional diversification of MIRNA genes. Plant Cell 23: 431-442.
30. DeSmetI,VossU,LauS,WilsonM,ShaoN,TimmeRE,Swarup R, Kerr I, Hodgman C, Bock R, et al. 2011. Unraveling the evolution of auxin signaling. Plant Physiol 155: 209-221.
31. Doebley J, Stec A, Gustus C. 1995. teosinte branched1 and the origin of maize: Evidence for epistasis and the evolution of dominance. Genetics 141: 333-346.
32. Ebert MS, Sharp PA. 2012. Roles for microRNAs in conferring robustness to biological processes. Cell 149: 515-524.
33. Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, Izhaki A, Baum SF, Bowman JL. 2003. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol 13: 1768-1774.
34. Erwin DH, Davidson EH. 2009. The evolution of hierarchical gene regulatory networks. Nat Rev Genet 10: 141-148.
35. Fahlgren N, Montgomery TA, Howell MD, Allen E, Dvorak SK, Alexander AL, Carrington JC. 2006. Regulation of AUXIN RESPONSE FACTOR3 by TAS3 tasiRNA affects developmental timing and patterning in Arabidopsis. Curr Biol 16: 939-944.
36. Fahlgren N, Jogdeo S, Kasschau KD, Sullivan CM, Chapman EJ, Laubinger S, Smith LM, Dasenko M, Givan SA, Weigel D, et al. 2010. microRNA gene evolution in Arabidopsis lyrata and Arabidopsis thaliana. Plant Cell 22: 1074-1089.
37. Finet C, Jaillais Y. 2012. AUXOLOGY: When auxin meets plant evo-devo. Dev Biol 369: 19-31.
38. Finet C, Berne-Dedieu A, Scutt CP, Marlétaz F. 2012. Evolution of the ARF gene family in land plants: Old domains, new tricks. Mol Biol Evol doi: 10.1093/molbev/mss220.
39. Flagel LE, Wendel JF. 2009. Gene duplication and evolutionary novelty in plants. New Phytol 183: 557-564.
40. Floyd SK, Bowman JL. 2006. Distinct developmental mechanisms reflect the independent origins of leaves in vascular plants. Curr Biol 16: 1911-1917.
41. Fraser GJ, Hulsey CD, Bloomquist RF, Uyesugi K, Manley NR, Streelman JT. 2009. An ancient gene network is co-opted for teeth on old and new jaws. PLoS Biol 7: e31.
42. Fujita T, Sakaguchi H, Hiwatashi Y, Wagstaff SJ, Ito M, Degu-chi H, Sato T, Hasebe M. 2008. Convergent evolution of shoots in land plants: Lack of auxin polar transport in moss shoots. Evol Dev 10: 176-186.
43. Garcia D, Collier SA, Byrne ME, Martienssen RA. 2006. Specification of leaf polarity in Arabidopsis via the transacting siRNA pathway. Curr Biol 16: 933-938.
44. Gifford EM, Foster AS. 1989. Morphology and evolution of vascular plants, pp. 327-333, 485-486, 505. W.H. Freeman, San Francisco
45. Goethe von JW. 1790. Versuch die Metamorphose der Pflanzen zu erklären.
46. Guo M, Thomas J, Collins G, Timmermans MC. 2008. Direct repression of KNOX loci by the ASYMMETRIC LEAVES1 complex of Arabidopsis. Plant Cell 20: 48-58.
47. Hay A, Tsiantis M. 2006. The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta. Nat Genet 38: 942-94
48. Hornstein E, Shomron N. 2006. Canalization of development by microRNAs. Nat Genet 38: S20-S24.
49. Howell MD, Fahlgren N, Chapman EJ, Cumbie JS, Sullivan CM, Givan SA, Kasschau KD, Carrington JC. 2007. Genome-wide analysis of the RNA-DEPENDENT RNA POLY-MERASE6/DICER-LIKE4 pathway in Arabidopsis reveals dependency on miRNA-and tasiRNA-directed targeting. Plant Cell 19: 926-942.
50. Hunter C, Sun H, Poethig RS. 2003. The Arabidopsis hetero-chronic gene ZIPPY is an ARGONAUTE family member. Curr Biol 13: 1734-1739.
51. Hunter C, Willmann MR, Wu G, Yoshikawa M, la Luz Gutiér-rez-Nava de M, Poethig SR. 2006. Transacting siRNA-me-diated repression of ETTIN and ARF4 regulates heteroblasty in Arabidopsis. Development 133: 2973-2981.
52. Husbands AY, Chitwood DH, Plavskin Y, Timmermans MCP. 2009. Signals and prepatterns: New insights into organ polarity in plants. Genes Dev 23: 1986-1997.
53. Jang G, Dolan L. 2011. Auxin promotes the transition from chloronema to caulonema in moss protonema by positively regulating PpRSL1 and PpRSL2 in Physcomitrella patens. New Phytol 192: 319-327.
54. Jang G, Yi K, Pires ND, Menand B, Dolan L. 2011. RSL genes are sufficient for rhizoid system development in early diverging land plants. Development 138: 2273-2281.
55. Javelle M, Timmermans MCP. 2012. In situ localization of small RNAsinplants byusing LNA probes. Nat Protoc7: 533-541.
56. Johri MM, Desai S. 1973. Auxin regulation of caulonema formation in moss protonema. Nature New Biol 245: 223-224.
57. Jones-RhoadesMW, Bartel DP, BartelB.2006.MicroRNAS and their regulatory rolesinplants. Annu Rev Plant Biol 57:19-53.
58. Juarez MT, Kui JS, Thomas J, Heller BA, Timmermans MCP. 2004a. microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428: 84-88.
59. Juarez MT, Twigg RW, Timmermans MCP. 2004b. Specification of adaxial cell fate during maize leaf development. Development 131: 4533-4544.
60. Kasschau KD, Fahlgren N, Chapman EJ, Sullivan CM, Cumbie JS, Givan SA, Carrington JC. 2007. Genome-wide profiling and analysis of Arabidopsis siRNAs. PLoS Biol 5: e57.
61. Kenrick P, Crane PR. 1997. The origin and early evolution of plants on land. Nature 389: 33-39.
62. Keys DN, Lewis DL, Selegue JE, Pearson BJ, Goodrich LV, Johnson RL, Gates J, Scott MP, Carroll SB. 1999. Recruitment of a hedgehog regulatory circuit in butterfly eyespot evolution. Science 283: 532-534.
63. Kidner CA, Timmermans MCP, Byrne ME, Martienssen RA. 2002. Developmental genetics of the angiosperm leaf. Adv Bot Res 38: 191-234.
64. Kimura S, Koenig D, Kang J, Yoong FY, Sinha N. 2008. Natural variation in leaf morphology results from mutation of a novel KNOX gene. Curr Biol 18: 672-677.
65. Kramer EM, Irish VF. 1999. Evolution of genetic mechanisms controlling petal development. Nature 399: 144-148.
66. Lauter N, Kampani A, Carlson S, Goebel M, Moose SP. 2005. microRNA172 down-regulates glossy15 to promote vegetative phase change in maize. Proc Natl Acad Sci 102: 9412-9417.
67. Lee RC, Feinbaum RL, Ambros V. 1993. The C. elegans heter-ochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75: 843-854.
68. Levine E, McHale P, Levine H. 2007. Small regulatory RNAs may sharpen spatial expression patterns. PLoS Comput Biol 3: e233.
69. Leyser O. 2011. Auxin, self-organisation, and the colonial nature of plants. Curr Biol 21: R331-R337.
70. Liang G, Yang F, Yu D. 2010. MicroRNA395 mediates regulation of sulfate accumulation and allocation in Arabidopsis thaliana. Plant J 62: 1046-1057.
71. Lodha M, Marco CF, Timmermans MCP. 2008. Genetic and epigenetic regulation of stem cell homeostasis in plants. Cold Spring Harb Symp Quant Biol 73: 243-251.
72. Lukowitz W, Roeder A, Parmenter D, Somerville C. 2004. A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell 116: 109-119.
73. Ma Z, Coruh C, Axtell MJ. 2010. Arabidopsis lyrata small RNAs: Transient miRNA and small interfering RNA loci within the Arabidopsis genus. Plant Cell 22: 1090-1103.
74. Maizel A, Busch MA, Tanahashi T, Perkovic J, Kato M, Hasebe M, Weigel D. 2005. The floral regulator LEAFY evolves by substitutions in the DNA binding domain. Science 308: 260-263.
75. Mallory AC, Bartel DP, Bartel B. 2005. MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 17: 1360-1375.
76. Marin E, Jouannet V, Herz A, Lokerse AS, Weijers D, Vaucheret H, Nussaume L, Crespi MD, Maizel A. 2010. miR390, Arabi-dopsis TAS3 tasiRNAs, and their AUXIN RESPONSE FACTOR targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 22: 1104-1117.
77. Menand B, Calder G, Dolan L. 2007a. Both chloronemal and caulonemal cells expand by tip growth in the moss Physcomi-trella patens. J Exp Bot 58: 1843-1849.
78. Menand B, Yi K, Jouannic S, Hoffmann L, Ryan E, Linstead P, Schaefer DG, Dolan L. 2007b. An ancient mechanism controls the development of cells with a rooting function in land plants. Science 316: 1477-1480.
79. Meyers BC, Axtell MJ, Bartel B, Bartel DP, Baulcombe D, Bowman JL, Cao X, Carrington JC, Chen X, Green PJ, et al. 2008. Criteria for annotation of plant microRNAs. Plant Cell 20: 3186-3190.
80. Mi S, Cai T, Hu Y,Chen Y, Hodges E, Ni F, Wu L, Li S, Zhou H, Long C, et al. 2008. Sorting of small RNAs into Arabidopsis argonaute complexes is directed by the 50 terminal nucleotide. Cell 133: 116-127.
81. Middleton AM, Farcot E, Owen MR, Vernoux T. 2012. Modeling regulatory networks to understand plant development: Small is beautiful. Plant Cell 24: 3857-3858.
82. Mishler BD, Churchill SP. 1984. A cladistic approach to the phylogeny of the"bryophytes". Brittonia 36: 406.
83. MiyashimaS, Koi S,Hashimoto T, Nakajima K.2011. Non-cell-autonomous microRNA165 acts in a dose-dependent manner to regulate multiple differentiation status in the Arabidopsis root. Development 138: 2303-2313.
84. Montgomery TA, Howell MD, Cuperus JT, Li D, Hansen JE, Alexander AL, Chapman EJ, Fahlgren N, Allen E, Carrington JC. 2008. Specificity of ARGONAUTE7-miR390 interaction and dual functionality in TAS3 transacting siRNA formation. Cell 133: 128-141.
85. Mukherji S, Ebert MS, Zheng GXY, Tsang JS, Sharp PA, van Oudenaarden A. 2011. MicroRNAs can generate thresholds in target gene expression. Nat Genet 43: 854-859.
86. Nagasaki H, Itoh J-I, Hayashi K, Hibara K-I, Satoh-Nagasawa N, Nosaka M, Mukouhata M, Ashikari M, Kitano H, Matsuoka M, et al. 2007. The small interfering RNA production pathway is required for shoot meristem initiation in rice. Proc Natl Acad Sci 104: 14867-14871.
87. Nogueira FT, Madi S, Chitwood DH, Juarez MT, Timmermans MC. 2007. Two small regulatory RNAs establish opposing fates of a developmental axis. Genes Dev 21: 750-755.
88. Nogueira FTS, Chitwood DH, Madi S, Ohtsu K, Schnable PS, Scanlon MJ, Timmermans MCP. 2009. Regulation of small RNA accumulation in the maize shoot apex. PLoS Genet 5: e1000320.
89. Parry G, Calderon-Villalobos LI, Prigge M, Peret B, Dharmasiri S, Itoh H, Lechner E, Gray WM, Bennett M, Estelle M. 2009. Complex regulation of the TIR1/AFB family of auxin receptors. Proc Natl Acad Sci 106: 22540-22545.
90. Peterson KJ, Dietrich MR, McPeek MA. 2009. microRNAs and metazoan macroevolution: Insights into canalization, complexity, and the Cambrian explosion. Bioessays 31: 736-747.
91. Pires ND, Dolan L. 2012. Morphological evolution in land plants: New designs with old genes. Philos Trans R Soc Lond, B, Biol Sci 367: 508-518.
92. Rajagopalan R, Vaucheret H, Trejo J, Bartel DP. 2006. A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 20: 3407-3425.
93. Raser JM, O'Shea EK. 2005. Noise in gene expression: Origins, consequences, and control. Science 309: 2010-2013.
94. Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP. 2002. Prediction of plant microRNA targets. Cell 110: 513-520.
95. Rosin FM, Kramer EM. 2009. Old dogs, new tricks: Regulatory evolution in conserved genetic modules leads to novel morphologies in plants. Dev Biol 332: 25-35.
96. Sakakibara K, Nishiyama T, Sumikawa N, Kofuji R, Murata T, Hasebe M. 2003. Involvement of auxin and a homeodomainleucine zipper I gene in rhizoid development of the moss Physcomitrella patens. Development 130: 4835-4846.
97. Shivaprasad PV, Chen H-M, Patel K, Bond DM, Santos BACM, Baulcombe DC. 2012. A microRNA superfamily regulates nucleotide binding siteleucinerich repeats and other mRNAs. Plant Cell 24: 859-874.
98. Shomron N, Golan D, Hornstein E. 2009. An evolutionary perspective of animal microRNAs and their targets. J Biomed Biotechnol 2009: 594738.
99. Shpak ED, McAbee JM, Pillitteri LJ, Torii KU. 2005. Stomatal patterning and differentiation by synergistic interactions of receptor kinases. Science 309: 290-293.
100. Sieber P, Wellmer F, Gheyselinck J, Riechmann JL, Meyerowitz EM. 2007. Redundancy and specialization among plant microRNAs: Role of the MIR164 family in developmental robustness. Development 134: 1051-1060.
101. Skopelitis DS, Husbands AY, Timmermans MCP. 2012. Plant small RNAs as morphogens. Curr Opin Cell Biol 24: 217-224.
102. Stern DL, Orgogozo V. 2008. The loci of evolution: How predictable is genetic evolution? Evolution 62: 2155-2177.
103. Stern DL, Orgogozo V. 2009. Is genetic evolution predictable? Science 323: 746-751.
104. Studer A, Zhao Q, Ross-Ibarra J, Doebley J. 2011. Identification of a functional transposon insertion in the maize domestication gene tb1. Nat Genet 43: 1160-1163.
105. Sunkar R, Girke T, Jain PK, Zhu J-K. 2005. Cloning and characterization of microRNAs from rice. Plant Cell 17: 1397-1411.
106. Talmor-Neiman M, Stav R, Klipcan L, Buxdorf K, Baulcombe DC, Arazi T. 2006. Identification of transacting siRNAs in moss and an RNA-dependent RNA polymerase required for their biogenesis. Plant J 48: 511-521.
107. Tan X, Calderon-Villalobos LIA, Sharon M, Zheng C, Robinson CV, Estelle M, Zheng N. 2007. Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446: 640-645.
108. Timmermans MC, Schultes NP, Jankovsky JP, Nelson T. 1998. Leafbladeless1 is required for dorsoventrality of lateral organs in maize. Development 125: 2813-2823.
109. Torii KU, Mitsukawa N, Oosumi T, Matsuura Y, Yokoyama R, Whittier RF, Komeda Y. 1996. The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 8: 735-746.
110. Townsley BT, Sinha NR. 2012. A new development: Evolving concepts in leaf ontogeny. Annu Rev Plant Biol 63: 535-562.
111. Ulmasov T, Hagen G, Guilfoyle TJ. 1999. Activation and repression of transcription by auxin-response factors. Proc Natl Acad Sci 96: 5844-5849.
112. Vernoux T, Brunoud G, Farcot E, Morin V, Van den Daele H, Legrand J, Oliva M, Das P, Larrieu A, Wells D, et al. 2011. The auxin signalling network translates dynamic input into robust patterning at the shoot apex. Mol Syst Biol 7: 508.
113. Voinnet O. 2009. Origin, biogenesis, and activity of plant micro-RNAs. Cell 136: 669-687.
114. Wang H, Nussbaum-Wagler T, Li B, Zhao Q, Vigouroux Y, Faller M, Bomblies K, Lukens L, Doebley JF. 2005. The origin of the naked grains of maize. Nature 436: 714-719.
115. Wartlick O, Kicheva A, González-Gaitán M. 2009. Morphogen gradient formation. Cold Spring Harb Perspect Biol 1: a001255.
116. Werner T, Koshikawa S, Williams TM, Carroll SB. 2010. Generation of a novel wing colour pattern by the Wingless mor-phogen. Nature 464: 1143-1148.
117. Wienholds E, Kloosterman WP, Miska E, Alvarez-Saavedra E, Berezikov E, de Bruijn E, Horvitz HR, Kauppinen S, Plasterk RHA. 2005. microRNA expression in zebrafish embryonic development. Science 309: 310-311.
118. Wightman B, Ha I, Ruvkun G. 1993. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75: 855-862.
119. Williams L, Carles CC, Osmont KS, Fletcher JC. 2005. A database analysis method identifies an endogenous transacting short-interfering RNA that targets the Arabidopsis ARF2, ARF3, and ARF4 genes. Proc Natl Acad Sci 102: 9703-9708.
120. Wittkopp PJ, True JR, Carroll SB. 2002. Reciprocal functions of the Drosophila yellow and ebony proteins in the development and evolution of pigment patterns. Development 129: 1849-1858.
121. Wu G, Poethig RS. 2006. Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133: 3539-3547.
122. Wu MF, Tian Q, Reed JW. 2006. Arabidopsis microRNA167 controls patterns of ARF6 and ARF8 expression, and regulates both female and male reproduction. Development 133: 4211-4218.
123. WuG,Park MY, Conway SR, Wang J-W, Weigel D, Poethig RS. 2009. The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138: 750-759.
124. Yifhar T, Pekker I, Peled D, Friedlander G, Pistunov A, Sabban M, Wachsman G, Alvarez JP, Amsellem Z, Eshed Y. 2012. Failure of the tomato transacting short interfering RNA program to regulate AUXIN RESPONSE FACTOR3 and ARF4 underlies the wiry leaf syndrome. Plant Cell 24: 3575-3589.
125. Yoshikawa M. 2005. A pathway for the biogenesis of transacting siRNAs in Arabidopsis. Genes Dev 19: 2164-2175.
126. ZhaiJ, Jeong DH, De Paoli E, Park S, Rosen BD, Li Y, Gonzalez AJ, Yan Z, Kitto SL, Grusak MA, 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.
127. Zhao T, Li G, Mi S, Li S, Hannon GJ, Wang X-J, Qi Y. 2007. A complex system of small RNAs in the unicellular green alga Chlamydomonas reinhardtii. Genes Dev 21: 1190-1203.