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Development 131 (14): 3357-3365

Modulation of floral development by a gibberellin-regulated microRNA

Patrick Achard1, Alan Herr2, David C. Baulcombe2, and Nicholas P. Harberd1,*

1 Department of Cell and Developmental Biology, John Innes Centre, Norwich NR4 7UH, UK
2 Sainsbury Laboratory, John Innes Centre, Norwich NR4 7UH, UK

* Author for correspondence (e-mail: nicholas.harberd{at}

Accepted for publication 1 April 2004.

Abstract: Floral initiation and floral organ development are both regulated by the phytohormone gibberellin (GA). For example, in short-day photoperiods, the Arabidopsis floral transition is strongly promoted by GA-mediated activation of the floral meristem-identity gene LEAFY. In addition, anther development and pollen microsporogenesis depend on GA-mediated opposition of the function of specific members of the DELLA family of GA-response repressors. We describe the role of a microRNA (miR159) in the regulation of short-day photoperiod flowering time and of anther development. MiR159 directs the cleavage of mRNA encoding GAMYB-related proteins. These proteins are transcription factors that are thought to be involved in the GA-promoted activation of LEAFY, and in the regulation of anther development. We show that miR159 levels are regulated by GA via opposition of DELLA function, and that both the sequence of miR159 and the regulation of miR159 levels by DELLA are evolutionarily conserved. Finally, we describe the phenotypic consequences of transgenic over-expression of miR159. Increased levels of miR159 cause a reduction in LEAFY transcript levels, delay flowering in short-day photoperiods, and perturb anther development. We propose that miR159 is a phytohormonally regulated homeostatic modulator of GAMYB activity, and hence of GAMYB-dependent developmental processes.

Key Words: miR159 • GAMYB • Flowering • Photoperiod • Anther

miRNAs in the crosstalk between phytohormone signalling pathways.
J. Curaba, M. B. Singh, and P. L. Bhalla (2014)
J. Exp. Bot. 65, 1425-1438
   Abstract »    Full Text »    PDF »
The role of microRNAs in the control of flowering time.
E. Spanudakis and S. Jackson (2014)
J. Exp. Bot. 65, 365-380
   Abstract »    Full Text »    PDF »
Gibberellin-Induced Expression of Fe Uptake-Related Genes in Arabidopsis.
K. Matsuoka, J. Furukawa, H. Bidadi, M. Asahina, S. Yamaguchi, and S. Satoh (2014)
Plant Cell Physiol. 55, 87-98
   Abstract »    Full Text »    PDF »
Molecular Mechanism of microRNA396 Mediating Pistil Development in Arabidopsis.
G. Liang, H. He, Y. Li, F. Wang, and D. Yu (2014)
Plant Physiology 164, 249-258
   Abstract »    Full Text »    PDF »
Exogenous Gibberellins Induce Wheat Spike Development under Short Days Only in the Presence of VERNALIZATION1.
S. Pearce, L. S. Vanzetti, and J. Dubcovsky (2013)
Plant Physiology 163, 1433-1445
   Abstract »    Full Text »    PDF »
An NAC Transcription Factor Controls Ethylene-Regulated Cell Expansion in Flower Petals.
H. Pei, N. Ma, J. Tian, J. Luo, J. Chen, J. Li, Y. Zheng, X. Chen, Z. Fei, and J. Gao (2013)
Plant Physiology 163, 775-791
   Abstract »    Full Text »    PDF »
Regulation of Stamen Development by Coordinated Actions of Jasmonate, Auxin, and Gibberellin in Arabidopsis.
S. Song, T. Qi, H. Huang, and D. Xie (2013)
Mol Plant 6, 1065-1073
   Abstract »    Full Text »    PDF »
Flowering time control in ornamental gloxinia (Sinningia speciosa) by manipulation of miR159 expression.
X. Li, H. Bian, D. Song, S. Ma, N. Han, J. Wang, and M. Zhu (2013)
Ann. Bot. 111, 791-799
   Abstract »    Full Text »    PDF »
Addressing the Role of microRNAs in Reprogramming Leaf Growth during Drought Stress in Brachypodium distachyon.
E. Bertolini, W. Verelst, D. S. Horner, L. Gianfranceschi, V. Piccolo, D. Inze, M. E. Pe, and E. Mica (2013)
Mol Plant
   Abstract »    Full Text »    PDF »
Identification and profiling of arsenic stress-induced microRNAs in Brassica juncea.
S. Srivastava, A. K. Srivastava, P. Suprasanna, and S. F. D'Souza (2013)
J. Exp. Bot. 64, 303-315
   Abstract »    Full Text »    PDF »
Spatial control of flowering by DELLA proteins in Arabidopsis thaliana.
V. C. Galvao, D. Horrer, F. Kuttner, and M. Schmid (2012)
Development 139, 4072-4082
   Abstract »    Full Text »    PDF »
Identification of new microRNA-regulated genes by conserved targeting in plant species.
U. Chorostecki, V. A. Crosa, A. F. Lodeyro, N. G. Bologna, A. P. Martin, N. Carrillo, C. Schommer, and J. F. Palatnik (2012)
Nucleic Acids Res. 40, 8893-8904
   Abstract »    Full Text »    PDF »
Transcriptome-Wide Characterization of miRNA-Directed and Non-miRNA-Directed Endonucleolytic Cleavage Using Degradome Analysis Under Low Ambient Temperature in Phalaenopsis aphrodite subsp. formosana.
F.-M. An and M.-T. Chan (2012)
Plant Cell Physiol. 53, 1737-1750
   Abstract »    Full Text »    PDF »
Interspecific RNA Interference of SHOOT MERISTEMLESS-Like Disrupts Cuscuta pentagona Plant Parasitism.
A. Alakonya, R. Kumar, D. Koenig, S. Kimura, B. Townsley, S. Runo, H. M. Garces, J. Kang, A. Yanez, R. David-Schwartz, et al. (2012)
PLANT CELL 24, 3153-3166
   Abstract »    Full Text »    PDF »
Spatially distinct regulatory roles for gibberellins in the promotion of flowering of Arabidopsis under long photoperiods.
A. Porri, S. Torti, M. Romera-Branchat, and G. Coupland (2012)
Development 139, 2198-2209
   Abstract »    Full Text »    PDF »
The interaction of plant biotic and abiotic stresses: from genes to the field.
N. J. Atkinson and P. E. Urwin (2012)
J. Exp. Bot. 63, 3523-3543
   Abstract »    Full Text »    PDF »
Small RNA Profiling in Two Brassica napus Cultivars Identifies MicroRNAs with Oil Production- and Development-Correlated Expression and New Small RNA Classes.
Y.-T. Zhao, M. Wang, S.-X. Fu, W.-C. Yang, C.-K. Qi, and X.-J. Wang (2012)
Plant Physiology 158, 813-823
   Abstract »    Full Text »    PDF »
Developmental Plasticity in Plants.
M. de Jong and O. Leyser (2012)
Cold Spring Harb Symp Quant Biol 77, 63-73
   Abstract »    Full Text »    PDF »
Dominant and Pleiotropic Effects of a GAI Gene in Wheat Results from a Lack of Interaction between DELLA and GID1.
J. Wu, X. Kong, J. Wan, X. Liu, X. Zhang, X. Guo, R. Zhou, G. Zhao, R. Jing, X. Fu, et al. (2011)
Plant Physiology 157, 2120-2130
   Abstract »    Full Text »    PDF »
A Mechanistic Link between STM and CUC1 during Arabidopsis Development.
S. V. Spinelli, A. P. Martin, I. L. Viola, D. H. Gonzalez, and J. F. Palatnik (2011)
Plant Physiology 156, 1894-1904
   Abstract »    Full Text »    PDF »
MicroRNAs in the shoot apical meristem of soybean.
C. E. Wong, Y.-T. Zhao, X.-J. Wang, L. Croft, Z.-H. Wang, F. Haerizadeh, J. S. Mattick, M. B. Singh, B. J. Carroll, and P. L. Bhalla (2011)
J. Exp. Bot. 62, 2495-2506
   Abstract »    Full Text »    PDF »
A DELLA in Disguise: SPATULA Restrains the Growth of the Developing Arabidopsis Seedling.
E.-M. Josse, Y. Gan, J. Bou-Torrent, K. L. Stewart, A. D. Gilday, C. E. Jeffree, F. E. Vaistij, J. F. Martinez-Garcia, F. Nagy, I. A. Graham, et al. (2011)
PLANT CELL 23, 1337-1351
   Abstract »    Full Text »    PDF »
The final split: the regulation of anther dehiscence.
Z. A. Wilson, J. Song, B. Taylor, and C. Yang (2011)
J. Exp. Bot. 62, 1633-1649
   Abstract »    Full Text »    PDF »
Efficient Silencing of Endogenous MicroRNAs Using Artificial MicroRNAs in Arabidopsis thaliana.
A. L. Eamens, C. Agius, N. A. Smith, P. M. Waterhouse, and M.-B. Wang (2011)
Mol Plant 4, 157-170
   Abstract »    Full Text »    PDF »
Contributions of Flowering Time Genes to Sunflower Domestication and Improvement.
B. K. Blackman, D. A. Rasmussen, J. L. Strasburg, A. R. Raduski, J. M. Burke, S. J. Knapp, S. D. Michaels, and L. H. Rieseberg (2011)
Genetics 187, 271-287
   Abstract »    Full Text »    PDF »
Complex Regulation of Two Target Genes Encoding SPX-MFS Proteins by Rice miR827 in Response to Phosphate Starvation.
S.-I. Lin, C. Santi, E. Jobet, E. Lacut, N. El Kholti, W. M. Karlowski, J.-L. Verdeil, J. C. Breitler, C. Perin, S.-S. Ko, et al. (2010)
Plant Cell Physiol. 51, 2119-2131
   Abstract »    Full Text »    PDF »
The MicroRNA159-Regulated GAMYB-like Genes Inhibit Growth and Promote Programmed Cell Death in Arabidopsis.
M. M. Alonso-Peral, J. Li, Y. Li, R. S. Allen, W. Schnippenkoetter, S. Ohms, R. G. White, and A. A. Millar (2010)
Plant Physiology 154, 757-771
   Abstract »    Full Text »    PDF »
The Plant Homeo Domain finger protein, VIN3-LIKE 2, is necessary for photoperiod-mediated epigenetic regulation of the floral repressor, MAF5.
D.-H. Kim and S. Sung (2010)
PNAS 107, 17029-17034
   Abstract »    Full Text »    PDF »
Auxin regulation of the microRNA390-dependent transacting small interfering RNA pathway in Arabidopsis lateral root development.
E. K. Yoon, J. H. Yang, J. Lim, S. H. Kim, S.-K. Kim, and W. S. Lee (2010)
Nucleic Acids Res. 38, 1382-1391
   Abstract »    Full Text »    PDF »
Co-ordination of developmental processes by small RNAs during leaf development.
A. Pulido and P. Laufs (2010)
J. Exp. Bot. 61, 1277-1291
   Abstract »    Full Text »    PDF »
A Systems Model of Vesicle Trafficking in Arabidopsis Pollen Tubes.
N. Kato, H. He, and A. P. Steger (2010)
Plant Physiology 152, 590-601
   Abstract »    Full Text »    PDF »
Conservation and divergence of microRNAs and their functions in Euphorbiaceous plants.
C. Zeng, W. Wang, Y. Zheng, X. Chen, W. Bo, S. Song, W. Zhang, and M. Peng (2010)
Nucleic Acids Res. 38, 981-995
   Abstract »    Full Text »    PDF »
miR319a targeting of TCP4 is critical for petal growth and development in Arabidopsis.
A. Nag, S. King, and T. Jack (2009)
PNAS 106, 22534-22539
   Abstract »    Full Text »    PDF »
A loop-to-base processing mechanism underlies the biogenesis of plant microRNAs miR319 and miR159.
N. G. Bologna, J. L. Mateos, E. G. Bresso, and J. F. Palatnik (2009)
EMBO J. 28, 3646-3656
   Abstract »    Full Text »    PDF »
Uncovering Small RNA-Mediated Responses to Phosphate Deficiency in Arabidopsis by Deep Sequencing.
L.-C. Hsieh, S.-I. Lin, A. C.-C. Shih, J.-W. Chen, W.-Y. Lin, C.-Y. Tseng, W.-H. Li, and T.-J. Chiou (2009)
Plant Physiology 151, 2120-2132
   Abstract »    Full Text »    PDF »
MicroRNAs in the Rhizobia Legume Symbiosis.
S. A. Simon, B. C. Meyers, and D. J. Sherrier (2009)
Plant Physiology 151, 1002-1008
   Full Text »    PDF »
Comprehensive prediction of novel microRNA targets in Arabidopsis thaliana.
L. Alves-Junior, S. Niemeier, A. Hauenschild, M. Rehmsmeier, and T. Merkle (2009)
Nucleic Acids Res. 37, 4010-4021
   Abstract »    Full Text »    PDF »
Small RNA analysis in Petunia hybrida identifies unusual tissue-specific expression patterns of conserved miRNAs and of a 24mer RNA.
P. Tedder, E. Zubko, D. R. Westhead, and P. Meyer (2009)
RNA 15, 1012-1020
   Abstract »    Full Text »    PDF »
Gibberellin as a factor in floral regulatory networks.
E. Mutasa-Gottgens and P. Hedden (2009)
J. Exp. Bot. 60, 1979-1989
   Abstract »    Full Text »    PDF »
Gibberellin Modulates Anther Development in Rice via the Transcriptional Regulation of GAMYB.
K. Aya, M. Ueguchi-Tanaka, M. Kondo, K. Hamada, K. Yano, M. Nishimura, and M. Matsuoka (2009)
PLANT CELL 21, 1453-1472
   Abstract »    Full Text »    PDF »
Salicylic acid deficiency in NahG transgenic lines and sid2 mutants increases seed yield in the annual plant Arabidopsis thaliana.
M. E. Abreu and S. Munne-Bosch (2009)
J. Exp. Bot. 60, 1261-1271
   Abstract »    Full Text »    PDF »
Submergence-responsive MicroRNAs are Potentially Involved in the Regulation of Morphological and Metabolic Adaptations in Maize Root Cells.
Z. Zhang, L. Wei, X. Zou, Y. Tao, Z. Liu, and Y. Zheng (2008)
Ann. Bot. 102, 509-519
   Abstract »    Full Text »    PDF »
Deep sequencing of tomato short RNAs identifies microRNAs targeting genes involved in fruit ripening.
S. Moxon, R. Jing, G. Szittya, F. Schwach, R. L. Rusholme Pilcher, V. Moulton, and T. Dalmay (2008)
Genome Res. 18, 1602-1609
   Abstract »    Full Text »    PDF »
Sequence Variation of MicroRNAs and Their Binding Sites in Arabidopsis.
I. M. Ehrenreich and M. D. Purugganan (2008)
Plant Physiology 146, 1974-1982
   Abstract »    Full Text »    PDF »
Genetic analysis reveals functional redundancy and the major target genes of the Arabidopsis miR159 family.
R. S. Allen, J. Li, M. I. Stahle, A. Dubroue, F. Gubler, and A. A. Millar (2007)
PNAS 104, 16371-16376
   Abstract »    Full Text »    PDF »
The GIGANTEA-Regulated MicroRNA172 Mediates Photoperiodic Flowering Independent of CONSTANS in Arabidopsis.
J.-H. Jung, Y.-H. Seo, P. J. Seo, J. L. Reyes, J. Yun, N.-H. Chua, and C.-M. Park (2007)
PLANT CELL 19, 2736-2748
   Abstract »    Full Text »    PDF »
Mechanisms of Cross Talk between Gibberellin and Other Hormones.
D. Weiss and N. Ori (2007)
Plant Physiology 144, 1240-1246
   Full Text »    PDF »
NUCLEAR PORE ANCHOR, the Arabidopsis Homolog of Tpr/Mlp1/Mlp2/Megator, Is Involved in mRNA Export and SUMO Homeostasis and Affects Diverse Aspects of Plant Development.
X. M. Xu, A. Rose, S. Muthuswamy, S. Y. Jeong, S. Venkatakrishnan, Q. Zhao, and I. Meier (2007)
PLANT CELL 19, 1537-1548
   Abstract »    Full Text »    PDF »
The plant stress hormone ethylene controls floral transition via DELLA-dependent regulation of floral meristem-identity genes.
P. Achard, M. Baghour, A. Chapple, P. Hedden, D. Van Der Straeten, P. Genschik, T. Moritz, and N. P. Harberd (2007)
PNAS 104, 6484-6489
   Abstract »    Full Text »    PDF »
The control of flowering in time and space.
K. E. Jaeger, A. Graf, and P. A. Wigge (2006)
J. Exp. Bot. 57, 3415-3418
   Abstract »    Full Text »    PDF »
Gibberellin Mobilizes Distinct DELLA-Dependent Transcriptomes to Regulate Seed Germination and Floral Development in Arabidopsis.
D. Cao, H. Cheng, W. Wu, H. M. Soo, and J. Peng (2006)
Plant Physiology 142, 509-525
   Abstract »    Full Text »    PDF »
Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3.
G. Wu and R. S. Poethig (2006)
Development 133, 3539-3547
   Abstract »    Full Text »    PDF »
NF-{kappa}B-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses.
K. D. Taganov, M. P. Boldin, K.-J. Chang, and D. Baltimore (2006)
PNAS 103, 12481-12486
   Abstract »    Full Text »    PDF »
Overexpression of PRE1 and its Homologous Genes Activates Gibberellin-dependent Responses in Arabidopsis thaliana.
S. Lee, S. Lee, K.-Y. Yang, Y.-M. Kim, S.-Y. Park, S. Y. Kim, and M.-S. Soh (2006)
Plant Cell Physiol. 47, 591-600
   Abstract »    Full Text »    PDF »
Endogenous and Synthetic MicroRNAs Stimulate Simultaneous, Efficient, and Localized Regulation of Multiple Targets in Diverse Species.
J. P. Alvarez, I. Pekker, A. Goldshmidt, E. Blum, Z. Amsellem, and Y. Eshed (2006)
PLANT CELL 18, 1134-1151
   Abstract »    Full Text »    PDF »
Evolution of Arabidopsis microRNA families through duplication events.
C. Maher, L. Stein, and D. Ware (2006)
Genome Res. 16, 510-519
   Abstract »    Full Text »    PDF »
PLASTOCHRON2 Regulates Leaf Initiation and Maturation in Rice.
T. Kawakatsu, J.-I. Itoh, K. Miyoshi, N. Kurata, N. Alvarez, B. Veit, and Y. Nagato (2006)
PLANT CELL 18, 612-625
   Abstract »    Full Text »    PDF »
Integration of Plant Responses to Environmentally Activated Phytohormonal Signals.
P. Achard, H. Cheng, L. De Grauwe, J. Decat, H. Schoutteten, T. Moritz, D. Van Der Straeten, J. Peng, and N. P. Harberd (2006)
Science 311, 91-94
   Abstract »    Full Text »    PDF »
Short Silencing RNA: The Dark Matter of Genetics?.
Cold Spring Harb Symp Quant Biol 71, 13-20
   Abstract »    PDF »
MicroRNAs acting in a double-negative feedback loop to control a neuronal cell fate decision.
R. J. Johnston Jr., S. Chang, J. F. Etchberger, C. O. Ortiz, and O. Hobert (2005)
PNAS 102, 12449-12454
   Abstract »    Full Text »    PDF »
Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes.
L. Williams, S. P. Grigg, M. Xie, S. Christensen, and J. C. Fletcher (2005)
Development 132, 3657-3668
   Abstract »    Full Text »    PDF »
Novel and Mechanical Stress-Responsive MicroRNAs in Populus trichocarpa That Are Absent from Arabidopsis.
S. Lu, Y.-H. Sun, R. Shi, C. Clark, L. Li, and V. L. Chiang (2005)
PLANT CELL 17, 2186-2203
   Abstract »    Full Text »    PDF »
Expression of Arabidopsis MIRNA Genes.
Z. Xie, E. Allen, N. Fahlgren, A. Calamar, S. A. Givan, and J. C. Carrington (2005)
Plant Physiology 138, 2145-2154
   Abstract »    Full Text »    PDF »
MicroRNA-binding viral protein interferes with Arabidopsis development.
P. Chellappan, R. Vanitharani, and C. M. Fauquet (2005)
PNAS 102, 10381-10386
   Abstract »    Full Text »    PDF »
microRNA172 down-regulates glossy15 to promote vegetative phase change in maize.
N. Lauter, A. Kampani, S. Carlson, M. Goebel, and S. P. Moose (2005)
PNAS 102, 9412-9417
   Abstract »    Full Text »    PDF »
Antiquity of MicroRNAs and Their Targets in Land Plants.
M. J. Axtell and D. P. Bartel (2005)
PLANT CELL 17, 1658-1673
   Abstract »    Full Text »    PDF »
MicroRNA-Directed Regulation of Arabidopsis AUXIN RESPONSE FACTOR17 Is Essential for Proper Development and Modulates Expression of Early Auxin Response Genes.
A. C. Mallory, D. P. Bartel, and B. Bartel (2005)
PLANT CELL 17, 1360-1375
   Abstract »    Full Text »    PDF »
MicroRNA Directs mRNA Cleavage of the Transcription Factor NAC1 to Downregulate Auxin Signals for Arabidopsis Lateral Root Development.
H.-S. Guo, Q. Xie, J.-F. Fei, and N.-H. Chua (2005)
PLANT CELL 17, 1376-1386
   Abstract »    Full Text »    PDF »
The Arabidopsis GAMYB-Like Genes, MYB33 and MYB65, Are MicroRNA-Regulated Genes That Redundantly Facilitate Anther Development.
A. A. Millar and F. Gubler (2005)
PLANT CELL 17, 705-721
   Abstract »    Full Text »    PDF »
Analysis of Flowering Pathway Integrators in Arabidopsis.
J. Moon, H. Lee, M. Kim, and I. Lee (2005)
Plant Cell Physiol. 46, 292-299
   Abstract »    Full Text »    PDF »
ASRP: the Arabidopsis Small RNA Project Database.
A. M. Gustafson, E. Allen, S. Givan, D. Smith, J. C. Carrington, and K. D. Kasschau (2005)
Nucleic Acids Res. 33, D637-D640
   Abstract »    Full Text »    PDF »
A Conserved microRNA Signal Specifies Leaf Polarity.
Cold Spring Harb Symp Quant Biol 69, 409-418
   Abstract »    PDF »

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