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Specification of Leaf Polarity in Arabidopsis via the trans-Acting siRNA Pathway

2006; Elsevier BV; Volume: 16; Issue: 9 Linguagem: Inglês

10.1016/j.cub.2006.03.064

1879-0445

Damien Garcia, Sarah A. Collier, Mary E. Byrne, Robert A. Martienssen,

Plant Genetic and Mutation Studies

Plants leaves develop proximodistal, dorsoventral (adaxial-abaxial), and mediolateral patterns following initiation. The Myb domain gene PHANTASTICA (PHAN) is required for adaxial fate in many plants [1Waites R. Selvadurai H.R. Oliver I.R. Hudson A. The PHANTASTICA gene encodes a MYB transcription factor involved in growth and dorsoventrality of lateral organs in Antirrhinum.Cell. 1998; 93: 779-789Abstract Full Text Full Text PDF PubMed Scopus (408) Google Scholar, 2Tattersall A.D. Turner L. Knox M.R. Ambrose M.J. Ellis T.H. Hofer J.M. The mutant crispa reveals multiple roles for PHANTASTICA in pea compound leaf development.Plant Cell. 2005; 17: 1046-1060Crossref PubMed Scopus (77) Google Scholar], but the Arabidopsis ortholog ASYMMETRIC LEAVES1 (AS1) has milder effects, suggesting that alternate or redundant pathways exist [3Byrne M.E. Barley R. Curtis M. Arroyo J.M. Dunham M. Hudson A. Martienssen R.A. Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis.Nature. 2000; 408: 967-971Crossref PubMed Scopus (597) Google Scholar, 4Xu L. Xu Y. Dong A. Sun Y. Pi L. Huang H. Novel as1 and as2 defects in leaf adaxial-abaxial polarity reveal the requirement for ASYMMETRIC LEAVES1 and 2 and ERECTA functions in specifying leaf adaxial identity.Development. 2003; 130: 4097-4107Crossref PubMed Scopus (270) Google Scholar]. We describe enhancers of as1 with more elongate and dissected leaves. As well as RDR6, an RNA-dependent RNA polymerase previously proposed to influence as1 through microRNA [5Li H. Xu L. Wang H. Yuan Z. Cao X. Yang Z. Zhang D. Xu Y. Huang H. The putative RNA-dependent RNA polymerase RDR6 acts synergistically with ASYMMETRIC LEAVES1 and 2 to repress BREVIPEDICELLUS and microRNA165/166 in Arabidopsis leaf development.Plant Cell. 2005; 17: 2157-2171Crossref PubMed Scopus (150) Google Scholar], these enhancers disrupt ARGONAUTE7 (AGO7)/ZIPPY, SUPPRESSOR OF GENE SILENCING3 (SGS3), and DICER-LIKE4 (DCL4), which instead regulate trans-acting small interfering RNA (ta-siRNA) [6Allen E. Xie Z. Gustafson A.M. Carrington J.C. microRNA-directed phasing during trans-acting siRNA biogenesis in plants.Cell. 2005; 121: 207-221Abstract Full Text Full Text PDF PubMed Scopus (1627) Google Scholar, 7Gasciolli V. Mallory A.C. Bartel D.P. Vaucheret H. Partially redundant functions of Arabidopsis DICER-like enzymes and a role for DCL4 in producing trans-acting siRNAs.Curr. Biol. 2005; 15: 1494-1500Abstract Full Text Full Text PDF PubMed Scopus (430) Google Scholar, 8Peragine A. Yoshikawa M. Wu G. Albrecht H.L. Poethig R.S. SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis.Genes Dev. 2004; 18: 2368-2379Crossref PubMed Scopus (668) Google Scholar, 9Vazquez F. Vaucheret H. Rajagopalan R. Lepers C. Gasciolli V. Mallory A.C. Hilbert J.L. Bartel D.P. Crete P. Endogenous trans-acting siRNAs regulate the accumulation of Arabidopsis mRNAs.Mol. Cell. 2004; 16: 69-79Abstract Full Text Full Text PDF PubMed Scopus (599) Google Scholar, 10Xie Z. Allen E. Wilken A. Carrington J.C. DICER-LIKE 4 functions in trans-acting small interfering RNA biogenesis and vegetative phase change in Arabidopsis thaliana.Proc. Natl. Acad. Sci. USA. 2005; 102: 12984-12989Crossref PubMed Scopus (402) Google Scholar, 11Yoshikawa M. Peragine A. Park M.Y. Poethig R.S. A pathway for the biogenesis of trans-acting siRNAs in Arabidopsis.Genes Dev. 2005; 19: 2164-2175Crossref PubMed Scopus (526) Google Scholar, 12Williams L. Carles C.C. Osmont K.S. Fletcher J.C. 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. 2005; 102: 9703-9708Crossref PubMed Scopus (225) Google Scholar]. Microarray analysis revealed that the AUXIN RESPONSE FACTOR genes ETTIN (ETT)/ARF3 and ARF4 were upregulated in ago7, whereas FILAMENTOUS FLOWER (FIL) was upregulated only in as1 ago7 double mutants. RDR6 and SGS3 likewise repress these genes, which specify abaxial fate [13Chen Q. Atkinson A. Otsuga D. Christensen T. Reynolds L. Drews G.N. The Arabidopsis FILAMENTOUS FLOWER gene is required for flower formation.Development. 1999; 126: 2715-2726PubMed Google Scholar, 14Sawa S. Ito T. Shimura Y. Okada K. FILAMENTOUS FLOWER controls the formation and development of arabidopsis inflorescences and floral meristems.Plant Cell. 1999; 11: 69-86Crossref PubMed Scopus (122) Google Scholar, 15Siegfried K.R. Eshed Y. Baum S.F. Otsuga D. Drews G.N. Bowman J.L. Members of the YABBY gene family specify abaxial cell fate in Arabidopsis.Development. 1999; 126: 4117-4128PubMed Google Scholar, 16Kumaran M.K. Bowman J.L. Sundaresan V. YABBY polarity genes mediate the repression of KNOX homeobox genes in Arabidopsis.Plant Cell. 2002; 14: 2761-2770Crossref PubMed Scopus (171) Google Scholar, 17Pekker I. Alvarez J.P. Eshed Y. Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity.Plant Cell. 2005; 17: 2899-2910Crossref PubMed Scopus (358) Google Scholar]. We show that the trans-acting siRNA gene TAS3, which targets ETT and ARF4, is expressed in the adaxial domain, and ett as1 ago7 triple mutants resemble as1. Thus FIL is downregulated redundantly by AS1 and by TAS3, acting through ETT, revealing a role for ta-siRNA in leaf polarity. RDR6 and DCL4 are required for systemic silencing, perhaps implicating ta-siRNA as a mobile signal.