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PMID: 15282547 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5' region.

The EMBO journal ·Vol. 23 ·No. 16 ·2004-08-18 ·Pages 3356-64

Mallory AC, Reinhart BJ, Jones-Rhoades MW, Tang G, Zamore PD, Barton MK, Bartel DP

Abstract

MicroRNAs (miRNAs) are approximately 22-nucleotide noncoding RNAs that can regulate gene expression by directing mRNA degradation or inhibiting productive translation. Dominant mutations in PHABULOSA (PHB) and PHAVOLUTA (PHV) map to a miR165/166 complementary site and impair miRNA-guided cleavage of these mRNAs in vitro. Here, we confirm that disrupted miRNA pairing, not changes in PHB protein sequence, causes the developmental defects in phb-d mutants. In planta, disrupting miRNA pairing near the center of the miRNA complementary site had far milder developmental consequences than more distal mismatches. These differences correlated with differences in miRNA-directed cleavage efficiency in vitro, where mismatch scanning revealed more tolerance for mismatches at the center and 3' end of the miRNA compared to mismatches to the miRNA 5' region. In this respect, miR165/166 resembles animal miRNAs in its pairing requirements. Pairing to the 5' portion of the small silencing RNA appears crucial regardless of the mode of post-transcriptional repression or whether it occurs in plants or animals, supporting a model in which this region of the silencing RNA nucleates pairing to its target.

MeSH Terms
Alleles Amino Acid Sequence Animals Arabidopsis/genetics,growth & development Arabidopsis Proteins/genetics Base Pairing Base Sequence Gene Expression Regulation, Plant/genetics Homeodomain Proteins/genetics MicroRNAs/genetics,metabolism Mutation/genetics Phenotype Plant Leaves/genetics,growth & development Plants, Genetically Modified RNA, Messenger/genetics,metabolism RNA, Plant/genetics,metabolism
Chemicals
Arabidopsis Proteins Homeodomain Proteins MicroRNAs PHB protein, Arabidopsis RNA, Messenger RNA, Plant
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Mallory Allison C
Whitehead Institute for Biomedical Research, Cambridge, MA 02142-1479, USA.
Reinhart Brenda J
Jones-Rhoades Matthew W
Tang Guiliang
Zamore Phillip D
Barton M Kathryn
Bartel David P
References (67)
67 references, click to expand
  1. Thermodynamics of single mismatches in RNA duplexes.
    Biochemistry. 1999 Oct 26;38(43):14214-23 PMID: 10571995
  2. The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation.
    Dev Biol. 1999 Dec 15;216(2):671-80 PMID: 10642801
  3. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans.
    Nature. 2000 Feb 24;403(6772):901-6 PMID: 10706289
  4. RNA interference is mediated by 21- and 22-nucleotide RNAs.
    Genes Dev. 2001 Jan 15;15(2):188-200 PMID: 11157775
  5. Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots.
    Nature. 2001 Jun 7;411(6838):709-13 PMID: 11395776
  6. Short 5'-phosphorylated double-stranded RNAs induce RNA interference in Drosophila.
    Curr Biol. 2001 Nov 13;11(22):1776-80 PMID: 11719220
  7. Functional anatomy of siRNAs for mediating efficient RNAi in Drosophila melanogaster embryo lysate.
    EMBO J. 2001 Dec 3;20(23):6877-88 PMID: 11726523
  8. Two genetic circuits repress the Caenorhabditis elegans heterochronic gene lin-28 after translation initiation.
    Dev Biol. 2002 Mar 15;243(2):215-25 PMID: 11884032
  9. Positional effects of short interfering RNAs targeting the human coagulation trigger Tissue Factor.
    Nucleic Acids Res. 2002 Apr 15;30(8):1757-66 PMID: 11937629
  10. A system for stable expression of short interfering RNAs in mammalian cells.
    Science. 2002 Apr 19;296(5567):550-3 PMID: 11910072
  11. Both natural and designed micro RNAs can inhibit the expression of cognate mRNAs when expressed in human cells.
    Mol Cell. 2002 Jun;9(6):1327-33 PMID: 12086629
  12. MicroRNAs in plants.
    Genes Dev. 2002 Jul 1;16(13):1616-26 PMID: 12101121
  13. Endogenous and silencing-associated small RNAs in plants.
    Plant Cell. 2002 Jul;14(7):1605-19 PMID: 12119378
  14. Prediction of plant microRNA targets.
    Cell. 2002 Aug 23;110(4):513-20 PMID: 12202040
  15. CARPEL FACTORY, a Dicer homolog, and HEN1, a novel protein, act in microRNA metabolism in Arabidopsis thaliana.
    Curr Biol. 2002 Sep 3;12(17):1484-95 PMID: 12225663
  16. A microRNA in a multiple-turnover RNAi enzyme complex.
    Science. 2002 Sep 20;297(5589):2056-60 PMID: 12154197
  17. Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA.
    Science. 2002 Sep 20;297(5589):2053-6 PMID: 12242443
  18. RNAi in human cells: basic structural and functional features of small interfering RNA.
    Mol Cell. 2002 Sep;10(3):549-61 PMID: 12408823
  19. DICER-LIKE1: blind men and elephants in Arabidopsis development.
    Trends Plant Sci. 2002 Nov;7(11):487-91 PMID: 12417148
  20. A biochemical framework for RNA silencing in plants.
    Genes Dev. 2003 Jan 1;17(1):49-63 PMID: 12514099
  21. MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs.
    Curr Biol. 2004 Jun 22;14(12):1035-46 PMID: 15202996
  22. Micro RNAs are complementary to 3' UTR sequence motifs that mediate negative post-transcriptional regulation.
    Nat Genet. 2002 Apr;30(4):363-4 PMID: 11896390
  23. Kinetic analysis of the RNAi enzyme complex.
    Nat Struct Mol Biol. 2004 Jul;11(7):599-606 PMID: 15170178
  24. P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA unction.
    Dev Cell. 2003 Feb;4(2):205-17 PMID: 12586064
  25. siRNAs can function as miRNAs.
    Genes Dev. 2003 Feb 15;17(4):438-42 PMID: 12600936
  26. HASTY, the Arabidopsis ortholog of exportin 5/MSN5, regulates phase change and morphogenesis.
    Development. 2003 Apr;130(8):1493-504 PMID: 12620976
  27. bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila.
    Cell. 2003 Apr 4;113(1):25-36 PMID: 12679032
  28. The microRNAs of Caenorhabditis elegans.
    Genes Dev. 2003 Apr 15;17(8):991-1008 PMID: 12672692
  29. Negative feedback regulation of Dicer-Like1 in Arabidopsis by microRNA-guided mRNA degradation.
    Curr Biol. 2003 Apr 29;13(9):784-9 PMID: 12725739
  30. The Drosophila microRNA Mir-14 suppresses cell death and is required for normal fat metabolism.
    Curr Biol. 2003 Apr 29;13(9):790-5 PMID: 12725740
  31. MicroRNAs and other tiny endogenous RNAs in C. elegans.
    Curr Biol. 2003 May 13;13(10):807-18 PMID: 12747828
  32. Allele-specific silencing of dominant disease genes.
    Proc Natl Acad Sci U S A. 2003 Jun 10;100(12):7195-200 PMID: 12782788
  33. siRNA function in RNAi: a chemical modification analysis.
    RNA. 2003 Sep;9(9):1034-48 PMID: 12923253
  34. MicroRNAs and small interfering RNAs can inhibit mRNA expression by similar mechanisms.
    Proc Natl Acad Sci U S A. 2003 Aug 19;100(17):9779-84 PMID: 12902540
  35. Selective silencing by RNAi of a dominant allele that causes amyotrophic lateral sclerosis.
    Aging Cell. 2003 Aug;2(4):209-17 PMID: 12934714
  36. Control of leaf morphogenesis by microRNAs.
    Nature. 2003 Sep 18;425(6955):257-63 PMID: 12931144
  37. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes.
    Curr Biol. 2003 Oct 14;13(20):1768-74 PMID: 14561401
  38. Small RNAs with imperfect match to endogenous mRNA repress translation. Implications for off-target activity of small inhibitory RNA in mammalian cells.
    J Biol Chem. 2003 Nov 7;278(45):44312-9 PMID: 12952966
  39. Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes.
    Plant Cell. 2003 Nov;15(11):2730-41 PMID: 14555699
  40. Nucleotide sequence homology requirements of HIV-1-specific short hairpin RNA.
    Nucleic Acids Res. 2003 Nov 15;31(22):6444-9 PMID: 14602902
  41. microRNAs: runts of the genome assert themselves.
    Curr Biol. 2003 Dec 2;13(23):R925-36 PMID: 14654021
  42. The microRNA Registry.
    Nucleic Acids Res. 2004 Jan 1;32(Database issue):D109-11 PMID: 14681370
  43. A microRNA controlling left/right neuronal asymmetry in Caenorhabditis elegans.
    Nature. 2003 Dec 18;426(6968):845-9 PMID: 14685240
  44. Prediction of mammalian microRNA targets.
    Cell. 2003 Dec 26;115(7):787-98 PMID: 14697198
  45. MicroRNAs modulate hematopoietic lineage differentiation.
    Science. 2004 Jan 2;303(5654):83-6 PMID: 14657504
  46. MicroRNAs: genomics, biogenesis, mechanism, and function.
    Cell. 2004 Jan 23;116(2):281-97 PMID: 14744438
  47. The Arabidopsis double-stranded RNA-binding protein HYL1 plays a role in microRNA-mediated gene regulation.
    Proc Natl Acad Sci U S A. 2004 Jan 27;101(4):1093-8 PMID: 14722360
  48. The nuclear dsRNA binding protein HYL1 is required for microRNA accumulation and plant development, but not posttranscriptional transgene silencing.
    Curr Biol. 2004 Feb 17;14(4):346-51 PMID: 14972688
  49. Spatially restricted microRNA directs leaf polarity through ARGONAUTE1.
    Nature. 2004 Mar 4;428(6978):81-4 PMID: 14999284
  50. microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity.
    Nature. 2004 Mar 4;428(6978):84-8 PMID: 14999285
  51. Specificity of microRNA target selection in translational repression.
    Genes Dev. 2004 Mar 1;18(5):504-11 PMID: 15014042
  52. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14.
    Cell. 1993 Dec 3;75(5):843-54 PMID: 8252621
  53. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans.
    Cell. 1993 Dec 3;75(5):855-62 PMID: 8252622
  54. Spectrum of mutations induced by methyl and ethyl methanesulfonate at the hprt locus of normal and tag expressing Chinese hamster fibroblasts.
    Carcinogenesis. 1995 Jun;16(6):1281-5 PMID: 7788844
  55. The cold shock domain protein LIN-28 controls developmental timing in C. elegans and is regulated by the lin-4 RNA.
    Cell. 1997 Mar 7;88(5):637-46 PMID: 9054503
  56. Leaf polarity and meristem formation in Arabidopsis.
    Development. 1998 Aug;125(15):2935-42 PMID: 9655815
  57. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  58. A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development.
    Science. 2004 Mar 26;303(5666):2022-5 PMID: 12893888
  59. Identification of Drosophila MicroRNA targets.
    PLoS Biol. 2003 Dec;1(3):E60 PMID: 14691535
  60. Gene regulation: ancient microRNA target sequences in plants.
    Nature. 2004 Apr 1;428(6982):485-6 PMID: 15057819
  61. MicroRNA-directed cleavage of HOXB8 mRNA.
    Science. 2004 Apr 23;304(5670):594-6 PMID: 15105502
  62. Amphivasal vascular bundle 1, a gain-of-function mutation of the IFL1/REV gene, is associated with alterations in the polarity of leaves, stems and carpels.
    Plant Cell Physiol. 2004 Apr;45(4):369-85 PMID: 15111711
  63. Identification of virus-encoded microRNAs.
    Science. 2004 Apr 30;304(5671):734-6 PMID: 15118162
  64. Micromanagers of gene expression: the potentially widespread influence of metazoan microRNAs.
    Nat Rev Genet. 2004 May;5(5):396-400 PMID: 15143321
  65. Viral virulence protein suppresses RNA silencing-mediated defense but upregulates the role of microrna in host gene expression.
    Plant Cell. 2004 May;16(5):1302-13 PMID: 15100397
  66. The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development.
    Genes Dev. 2004 May 15;18(10):1187-97 PMID: 15131082
  67. Computational identification of plant microRNAs and their targets, including a stress-induced miRNA.
    Mol Cell. 2004 Jun 18;14(6):787-99 PMID: 15200956
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
2004-08-18
Epub
2004-00-29
Pages
3356-64
Language
English
Region
England
NLM ID
8208664
PMCID
PMC514513
Subset
IM
Analysis Services
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