SGS3 and SGS2/SDE1/RDR6 Are Required for Juvenile Development and the Production of Trans-acting SiRNAs in Arabidopsis

Overview

Journal Genes Dev

Specialty Molecular Biology

Date 2004 Oct 7

PMID 15466488

Citations 432

Authors

Angela Peragine

Manabu Yoshikawa

Gang Wu

Heidi L Albrecht

R Scott Poethig

Affiliations

Soon will be listed here.

Abstract

Higher plants undergo a transition from a juvenile to an adult phase of vegetative development prior to flowering. Screens for mutants that undergo this transition precociously produced alleles of two genes required for posttranscriptional gene silencing (PTGS)--SUPPRESSOR OF GENE SILENCING3 (SGS3) and SUPPRESSOR OF GENE SILENCING2(SGS2)/SILENCING DEFECTIVE1 (SDE1)/RNA-DEPENDENT POLYMERASE6 (RDR6). Loss-of-function mutations in these genes have a phenotype similar to that of mutations in the Argonaute gene ZIPPY (ZIP). Epistasis analysis suggests that ZIP, SGS3, SGS2/SDE1/RDR6, and the putative miRNA export receptor, HASTY (HST), operate in the same pathway(s). Microarray analysis revealed a small number of genes whose mRNA is increased in ZIP, SGS3, and SGS2/SDE1/RDR6 mutants, as well as genes that are up-regulated in SGS3 and SGS2/SDE1/RDR6 mutants, but not in ZIP mutants. One of these latter genes (At5g18040) is silenced posttranscriptionally in trans by the sRNA255 family of endogenous, noncoding, small interfering RNAs (siRNAs). The increase in At5g18040 mRNA in SGS3 and SGS2/SDE1/RDR6 mutants is attributable to the absence of sRNA255-like siRNAs in these mutants. These results demonstrate a role for endogenous siRNAs in the regulation of gene expression, and suggest that PTGS plays a central role in the temporal control of shoot development in plants.

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References

Lee R, Ambros V . An extensive class of small RNAs in Caenorhabditis elegans. Science. 2001; 294(5543):862-4. DOI: 10.1126/science.1065329. View

Shiu P, Metzenberg R . Meiotic silencing by unpaired DNA: properties, regulation and suppression. Genetics. 2002; 161(4):1483-95. PMC: 1462203. DOI: 10.1093/genetics/161.4.1483. View

Klahre U, Crete P, Leuenberger S, Iglesias V, Meins Jr F . High molecular weight RNAs and small interfering RNAs induce systemic posttranscriptional gene silencing in plants. Proc Natl Acad Sci U S A. 2002; 99(18):11981-6. PMC: 129380. DOI: 10.1073/pnas.182204199. View

Tsukaya H, Shoda K, Kim G, Uchimiya H . Heteroblasty in Arabidopsis thaliana (L.) Heynh. Planta. 2000; 210(4):536-42. DOI: 10.1007/s004250050042. View

Boutet S, Vazquez F, Liu J, Beclin C, Fagard M, Gratias A . Arabidopsis HEN1: a genetic link between endogenous miRNA controlling development and siRNA controlling transgene silencing and virus resistance. Curr Biol. 2003; 13(10):843-8. PMC: 5137371. DOI: 10.1016/s0960-9822(03)00293-8. View

Hamilton A, Voinnet O, Chappell L, Baulcombe D . Two classes of short interfering RNA in RNA silencing. EMBO J. 2002; 21(17):4671-9. PMC: 125409. DOI: 10.1093/emboj/cdf464. View

Ambros V, Bartel B, Bartel D, Burge C, Carrington J, Chen X . A uniform system for microRNA annotation. RNA. 2003; 9(3):277-9. PMC: 1370393. DOI: 10.1261/rna.2183803. View

Park W, Li J, Song R, Messing J, Chen X . CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana. Curr Biol. 2002; 12(17):1484-95. PMC: 5137372. DOI: 10.1016/s0960-9822(02)01017-5. View

Greenwood M . Juvenility and maturation in conifers: current concepts. Tree Physiol. 1995; 15(7_8):433-438. DOI: 10.1093/treephys/15.7-8.433. View

10.

Simmer F, Tijsterman M, Parrish S, Koushika S, Nonet M, Fire A . Loss of the putative RNA-directed RNA polymerase RRF-3 makes C. elegans hypersensitive to RNAi. Curr Biol. 2002; 12(15):1317-9. DOI: 10.1016/s0960-9822(02)01041-2. View

11.

Hoekenga O, Muszynski M, Cone K . Developmental patterns of chromatin structure and DNA methylation responsible for epigenetic expression of a maize regulatory gene. Genetics. 2000; 155(4):1889-902. PMC: 1461212. DOI: 10.1093/genetics/155.4.1889. View

12.

Chien J, Sussex I . Differential regulation of trichome formation on the adaxial and abaxial leaf surfaces by gibberellins and photoperiod in Arabidopsis thaliana (L.) Heynh. Plant Physiol. 1996; 111(4):1321-8. PMC: 161017. DOI: 10.1104/pp.111.4.1321. View

13.

Elbashir S, Lendeckel W, Tuschl T . RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev. 2001; 15(2):188-200. PMC: 312613. DOI: 10.1101/gad.862301. View

14.

Mourelatos Z, Dostie J, Paushkin S, Sharma A, Charroux B, Abel L . miRNPs: a novel class of ribonucleoproteins containing numerous microRNAs. Genes Dev. 2002; 16(6):720-8. PMC: 155365. DOI: 10.1101/gad.974702. View

15.

Hunter C, Sun H, Poethig R . The Arabidopsis heterochronic gene ZIPPY is an ARGONAUTE family member. Curr Biol. 2003; 13(19):1734-9. DOI: 10.1016/j.cub.2003.09.004. View

16.

Bollman K, Aukerman M, Park M, Hunter C, Berardini T, Poethig R . HASTY, the Arabidopsis ortholog of exportin 5/MSN5, regulates phase change and morphogenesis. Development. 2003; 130(8):1493-504. DOI: 10.1242/dev.00362. View

17.

Cogoni C, Macino G . Gene silencing in Neurospora crassa requires a protein homologous to RNA-dependent RNA polymerase. Nature. 1999; 399(6732):166-9. DOI: 10.1038/20215. View

18.

Cardon G, Hohmann S, Nettesheim K, Saedler H, Huijser P . Functional analysis of the Arabidopsis thaliana SBP-box gene SPL3: a novel gene involved in the floral transition. Plant J. 1997; 12(2):367-77. DOI: 10.1046/j.1365-313x.1997.12020367.x. View

19.

Lagos-Quintana M, Rauhut R, Yalcin A, Meyer J, Lendeckel W, Tuschl T . Identification of tissue-specific microRNAs from mouse. Curr Biol. 2002; 12(9):735-9. DOI: 10.1016/s0960-9822(02)00809-6. View

20.

Clarke J, Tack D, Findlay K, Van Montagu M, Van Lijsebettens M . The SERRATE locus controls the formation of the early juvenile leaves and phase length in Arabidopsis. Plant J. 1999; 20(4):493-501. DOI: 10.1046/j.1365-313x.1999.00623.x. View