The Sequential Action of miR156 and miR172 Regulates Developmental Timing in Arabidopsis

The transition from the juvenile to the adult phase of shoot development in plants is accompanied by changes in vegetative morphology and an increase in reproductive potential. Here, we describe the regulatory mechanism of this transition. We show that miR156 is necessary and sufficient for the expression of the juvenile phase, and regulates the timing of the juvenile-to-adult transition by coordinating the expression of several pathways that control different aspects of this process. miR156 acts by repressing the expression of functionally distinct SPL transcription factors. miR172 acts downstream of miR156 to promote adult epidermal identity. miR156 regulates the expression of miR172 via SPL9 which, redundantly with SPL10, directly promotes the transcription of miR172b. Thus, like the larval-to-adult transition in Caenorhabditis elegans, the juvenile-to-adult transition in Arabidopsis is mediated by sequentially operating miRNAs. miR156 and miR172 are positively regulated by the transcription factors they target, suggesting that negative feedback loops contribute to the stability of the juvenile and adult phases.

[1]  Xuemei Chen,et al.  miR172 regulates stem cell fate and defines the inner boundary of APETALA3 and PISTILLATA expression domain in Arabidopsis floral meristems. , 2007, The Plant journal : for cell and molecular biology.

[2]  Lynn Doucette-Stamm,et al.  A C . elegans genome-scale microRNA network contains composite feedback motifs with high flux capacity , 2008 .

[3]  N. Chua,et al.  The GIGANTEA-Regulated MicroRNA172 Mediates Photoperiodic Flowering Independent of CONSTANS in Arabidopsis[W][OA] , 2007, The Plant Cell Online.

[4]  Javier F. Palatnik,et al.  Specific effects of microRNAs on the plant transcriptome. , 2005, Developmental cell.

[5]  R. Poethig,et al.  Phase Change and the Regulation of Developmental Timing in Plants , 2003, Science.

[6]  H. Tsukaya,et al.  Heteroblasty in Arabidopsis thaliana (L.) Heynh , 2000, Planta.

[7]  S. Moose,et al.  microRNA172 down-regulates glossy15 to promote vegetative phase change in maize. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[8]  R. Poethig,et al.  Heterochronic effects of glossy15 mutations on epidermal cell identity in maize. , 1994, Development.

[9]  G. Horiguchi,et al.  The more and smaller cells mutants of Arabidopsis thaliana identify novel roles for SQUAMOSA PROMOTER BINDING PROTEIN-LIKE genes in the control of heteroblasty , 2009, Development.

[10]  E. Moss,et al.  Heterochronic Genes and the Nature of Developmental Time , 2007, Current Biology.

[11]  Gang Wu,et al.  Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3 , 2006, Development.

[12]  S. Hake,et al.  Regulation of developmental transitions. , 2005, Current opinion in plant biology.

[13]  C. Pikaard,et al.  Gateway-compatible vectors for plant functional genomics and proteomics. , 2006, The Plant journal : for cell and molecular biology.

[14]  A. Rougvie,et al.  Intrinsic and extrinsic regulators of developmental timing: from miRNAs to nutritional cues , 2005, Development.

[15]  B. Reinhart,et al.  Prediction of Plant MicroRNA Targets , 2002, Cell.

[16]  R. Geneve,et al.  Biotechnology of Ornamental Plants , 1996 .

[17]  M. Axtell,et al.  Evolution of plant microRNAs and their targets. , 2008, Trends in plant science.

[18]  R. Poethig,et al.  Phase change and the regulation of trichome distribution in Arabidopsis thaliana. , 1997, Development.

[19]  F. Slack,et al.  RAS Is Regulated by the let-7 MicroRNA Family , 2005, Cell.

[20]  W. Hackett.  Juvenility, Maturation, and Rejuvenation in Woody Plants , 2011 .

[21]  C. Dean,et al.  The Timing of Developmental Transitions in Plants , 2006, Cell.

[22]  R. Kerstetter,et al.  The specification of leaf identity during shoot development. , 1998, Annual review of cell and developmental biology.

[23]  S. Gould,et al.  Ontogeny and Phylogeny , 1978 .

[24]  V. Ambros,et al.  The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14 , 1993, Cell.

[25]  Hajime Sakai,et al.  Regulation of Flowering Time and Floral Organ Identity by a MicroRNA and Its APETALA2-Like Target Genes Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.016238. , 2003, The Plant Cell Online.

[26]  A. Pasquinelli,et al.  Control of developmental timing by micrornas and their targets. , 2002, Annual review of cell and developmental biology.

[27]  Heinz Saedler,et al.  The miRNA156/157 recognition element in the 3' UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. , 2007, The Plant journal : for cell and molecular biology.

[28]  Detlef Weigel,et al.  Dual Effects of miR156-Targeted SPL Genes and CYP78A5/KLUH on Plastochron Length and Organ Size in Arabidopsis thaliana[W][OA] , 2008, The Plant Cell Online.

[29]  S. Hake,et al.  The maize tasselseed4 microRNA controls sex determination and meristem cell fate by targeting Tasselseed6/indeterminate spikelet1 , 2007, Nature Genetics.

[30]  Xuemei Chen,et al.  A MicroRNA as a Translational Repressor of APETALA2 in Arabidopsis Flower Development , 2004, Science.

[31]  R. W. Davis,et al.  Epidermal cell fate determination in Arabidopsis: patterns defined by a steroid-inducible regulator. , 1994, Science.

[32]  Sarah Hake,et al.  The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA , 2007, Nature Genetics.

[33]  Alessandro Fatica,et al.  A Minicircuitry Comprised of MicroRNA-223 and Transcription Factors NFI-A and C/EBPα Regulates Human Granulopoiesis , 2005, Cell.

[34]  S. Moose,et al.  Glossy15, an APETALA2-like gene from maize that regulates leaf epidermal cell identity. , 1996, Genes & development.

[35]  M. Todesco,et al.  Target mimicry provides a new mechanism for regulation of microRNA activity , 2007, Nature Genetics.

[36]  D. Wagner,et al.  Genomic identification of direct target genes of LEAFY. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Detlef Weigel,et al.  Dissection of floral induction pathways using global expression analysis , 2003, Development.

[38]  R. H. Zimmerman,et al.  Hormonal Aspects of Phase Change and Precocious Flowering , 1985 .

[39]  Marjori Matzke,et al.  Unexpected silencing effects from T-DNA tags in Arabidopsis. , 2008, Trends in plant science.

[40]  B. Reinhart,et al.  The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans , 2000, Nature.

[41]  F. Parcy.  Flowering: a time for integration. , 2005, The International journal of developmental biology.

[42]  T. Berardini,et al.  Cyclophilin 40 is required for microRNA activity in Arabidopsis , 2009, Proceedings of the National Academy of Sciences.

[43]  G. Hannon,et al.  A MicroRNA Feedback Circuit in Midbrain Dopamine Neurons , 2007, Science.

[44]  S. Moose,et al.  Glossy15 Controls the Epidermal Juvenile-to-Adult Phase Transition in Maize. , 1994, The Plant cell.

[45]  P. Huijser,et al.  Functional analysis of the Arabidopsis thaliana SBP-box gene SPL3: a novel gene involved in the floral transition. , 1997, The Plant journal : for cell and molecular biology.

[46]  S. Cohen,et al.  microRNA miR-14 acts to modulate a positive autoregulatory loop controlling steroid hormone signaling in Drosophila. , 2007, Genes & development.

[47]  Heinz Saedler,et al.  The microRNA regulated SBP-box genes SPL9 and SPL15 control shoot maturation in Arabidopsis , 2008, Plant Molecular Biology.

[48]  Qihui Zhu,et al.  Genome-wide identification and evolutionary analysis of the plant specific SBP-box transcription factor family. , 2008, Gene.