The microrNA156-SQUAMOSA promoter binding protein-like3 module regulates ambient temperature-responsive flowering via flowering locus in Arabidopsis

Jae Joon Kim, Jeong Hwan Lee, Wanhui Kim, Hye Seung Jung, Peter Huijser, Ji Hoon Ahn

Research output: Contribution to journalArticle

124 Citations (Scopus)

Abstract

The flowering time of plants is affected by modest changes in ambient temperature. However, little is known about the regulation of ambient temperature-responsive flowering by small RNAs. In this study, we show that the microRNA156 (miR156) SQUAMOSA PROMOTER BINDING PROTEIN-LIKE3 (SPL3) module directly regulates FLOWERING LOCUS T (FT) expression in the leaf to control ambient temperature-responsive flowering. Overexpression of miR156 led to more delayed flowering at a lower ambient temperature (16°C), which was associated with down-regulation of FT and FRUITFULL expression. Among miR156 target genes, SPL3 mRNA levels were mainly reduced, probably because miR156-mediated cleavage of SPL3 mRNA was higher at 16°C. Overexpression of miR156-resistant SPL3 [SPL3(2)] caused early flowering, regardless of the ambient temperature, which was associated with up-regulation of FT and FRUITFULL expression. Reduction of miR156 activity by target mimicry led to a phenotype similar to that of SUC2::rSPL3 plants. FT up-regulation was observed after dexamethasone treatment in GVG-rSPL3 plants. Misexpression and artificial microRNA-mediated suppression of FT in the leaf dramatically altered the ambient temperature-responsive flowering of plants overexpressing miR156 and SPL3(2). Chromatin immunoprecipitation assay showed that the SPL3 protein directly binds to GTAC motifs within the FT promoter. Lesions in TERMINAL FLOWER1, SHORT VEGETATIVE PHASE, and EARLY FLOWERING3 did not alter the expression of miR156 and SPL3. Taken together, our data suggest that the interaction between the miR156-SPL3 module and FT is part of the regulatory mechanism controlling flowering time in response to ambient temperature.

Original languageEnglish
Pages (from-to)461-478
Number of pages18
JournalPlant Physiology
Volume159
Issue number1
DOIs
Publication statusPublished - 2012 May 1

Fingerprint

Arabidopsis
binding proteins
ambient temperature
Carrier Proteins
promoter regions
flowering
loci
Temperature
Up-Regulation
Messenger RNA
Chromatin Immunoprecipitation
lesions (plant)
MicroRNAs
dexamethasone
Dexamethasone
microRNA
chromatin
Down-Regulation
leaves
Angiospermae

ASJC Scopus subject areas

  • Plant Science
  • Genetics
  • Physiology

Cite this

The microrNA156-SQUAMOSA promoter binding protein-like3 module regulates ambient temperature-responsive flowering via flowering locus in Arabidopsis. / Kim, Jae Joon; Lee, Jeong Hwan; Kim, Wanhui; Jung, Hye Seung; Huijser, Peter; Ahn, Ji Hoon.

In: Plant Physiology, Vol. 159, No. 1, 01.05.2012, p. 461-478.

Research output: Contribution to journalArticle

Kim, Jae Joon ; Lee, Jeong Hwan ; Kim, Wanhui ; Jung, Hye Seung ; Huijser, Peter ; Ahn, Ji Hoon. / The microrNA156-SQUAMOSA promoter binding protein-like3 module regulates ambient temperature-responsive flowering via flowering locus in Arabidopsis. In: Plant Physiology. 2012 ; Vol. 159, No. 1. pp. 461-478.
@article{04ef4866f76a4467ac059a19732758f4,
title = "The microrNA156-SQUAMOSA promoter binding protein-like3 module regulates ambient temperature-responsive flowering via flowering locus in Arabidopsis",
abstract = "The flowering time of plants is affected by modest changes in ambient temperature. However, little is known about the regulation of ambient temperature-responsive flowering by small RNAs. In this study, we show that the microRNA156 (miR156) SQUAMOSA PROMOTER BINDING PROTEIN-LIKE3 (SPL3) module directly regulates FLOWERING LOCUS T (FT) expression in the leaf to control ambient temperature-responsive flowering. Overexpression of miR156 led to more delayed flowering at a lower ambient temperature (16°C), which was associated with down-regulation of FT and FRUITFULL expression. Among miR156 target genes, SPL3 mRNA levels were mainly reduced, probably because miR156-mediated cleavage of SPL3 mRNA was higher at 16°C. Overexpression of miR156-resistant SPL3 [SPL3(2)] caused early flowering, regardless of the ambient temperature, which was associated with up-regulation of FT and FRUITFULL expression. Reduction of miR156 activity by target mimicry led to a phenotype similar to that of SUC2::rSPL3 plants. FT up-regulation was observed after dexamethasone treatment in GVG-rSPL3 plants. Misexpression and artificial microRNA-mediated suppression of FT in the leaf dramatically altered the ambient temperature-responsive flowering of plants overexpressing miR156 and SPL3(2). Chromatin immunoprecipitation assay showed that the SPL3 protein directly binds to GTAC motifs within the FT promoter. Lesions in TERMINAL FLOWER1, SHORT VEGETATIVE PHASE, and EARLY FLOWERING3 did not alter the expression of miR156 and SPL3. Taken together, our data suggest that the interaction between the miR156-SPL3 module and FT is part of the regulatory mechanism controlling flowering time in response to ambient temperature.",
author = "Kim, {Jae Joon} and Lee, {Jeong Hwan} and Wanhui Kim and Jung, {Hye Seung} and Peter Huijser and Ahn, {Ji Hoon}",
year = "2012",
month = "5",
day = "1",
doi = "10.1104/pp.111.192369",
language = "English",
volume = "159",
pages = "461--478",
journal = "Plant Physiology",
issn = "0032-0889",
publisher = "American Society of Plant Biologists",
number = "1",

}

TY - JOUR

T1 - The microrNA156-SQUAMOSA promoter binding protein-like3 module regulates ambient temperature-responsive flowering via flowering locus in Arabidopsis

AU - Kim, Jae Joon

AU - Lee, Jeong Hwan

AU - Kim, Wanhui

AU - Jung, Hye Seung

AU - Huijser, Peter

AU - Ahn, Ji Hoon

PY - 2012/5/1

Y1 - 2012/5/1

N2 - The flowering time of plants is affected by modest changes in ambient temperature. However, little is known about the regulation of ambient temperature-responsive flowering by small RNAs. In this study, we show that the microRNA156 (miR156) SQUAMOSA PROMOTER BINDING PROTEIN-LIKE3 (SPL3) module directly regulates FLOWERING LOCUS T (FT) expression in the leaf to control ambient temperature-responsive flowering. Overexpression of miR156 led to more delayed flowering at a lower ambient temperature (16°C), which was associated with down-regulation of FT and FRUITFULL expression. Among miR156 target genes, SPL3 mRNA levels were mainly reduced, probably because miR156-mediated cleavage of SPL3 mRNA was higher at 16°C. Overexpression of miR156-resistant SPL3 [SPL3(2)] caused early flowering, regardless of the ambient temperature, which was associated with up-regulation of FT and FRUITFULL expression. Reduction of miR156 activity by target mimicry led to a phenotype similar to that of SUC2::rSPL3 plants. FT up-regulation was observed after dexamethasone treatment in GVG-rSPL3 plants. Misexpression and artificial microRNA-mediated suppression of FT in the leaf dramatically altered the ambient temperature-responsive flowering of plants overexpressing miR156 and SPL3(2). Chromatin immunoprecipitation assay showed that the SPL3 protein directly binds to GTAC motifs within the FT promoter. Lesions in TERMINAL FLOWER1, SHORT VEGETATIVE PHASE, and EARLY FLOWERING3 did not alter the expression of miR156 and SPL3. Taken together, our data suggest that the interaction between the miR156-SPL3 module and FT is part of the regulatory mechanism controlling flowering time in response to ambient temperature.

AB - The flowering time of plants is affected by modest changes in ambient temperature. However, little is known about the regulation of ambient temperature-responsive flowering by small RNAs. In this study, we show that the microRNA156 (miR156) SQUAMOSA PROMOTER BINDING PROTEIN-LIKE3 (SPL3) module directly regulates FLOWERING LOCUS T (FT) expression in the leaf to control ambient temperature-responsive flowering. Overexpression of miR156 led to more delayed flowering at a lower ambient temperature (16°C), which was associated with down-regulation of FT and FRUITFULL expression. Among miR156 target genes, SPL3 mRNA levels were mainly reduced, probably because miR156-mediated cleavage of SPL3 mRNA was higher at 16°C. Overexpression of miR156-resistant SPL3 [SPL3(2)] caused early flowering, regardless of the ambient temperature, which was associated with up-regulation of FT and FRUITFULL expression. Reduction of miR156 activity by target mimicry led to a phenotype similar to that of SUC2::rSPL3 plants. FT up-regulation was observed after dexamethasone treatment in GVG-rSPL3 plants. Misexpression and artificial microRNA-mediated suppression of FT in the leaf dramatically altered the ambient temperature-responsive flowering of plants overexpressing miR156 and SPL3(2). Chromatin immunoprecipitation assay showed that the SPL3 protein directly binds to GTAC motifs within the FT promoter. Lesions in TERMINAL FLOWER1, SHORT VEGETATIVE PHASE, and EARLY FLOWERING3 did not alter the expression of miR156 and SPL3. Taken together, our data suggest that the interaction between the miR156-SPL3 module and FT is part of the regulatory mechanism controlling flowering time in response to ambient temperature.

UR - http://www.scopus.com/inward/record.url?scp=84860582420&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84860582420&partnerID=8YFLogxK

U2 - 10.1104/pp.111.192369

DO - 10.1104/pp.111.192369

M3 - Article

C2 - 22427344

AN - SCOPUS:84860582420

VL - 159

SP - 461

EP - 478

JO - Plant Physiology

JF - Plant Physiology

SN - 0032-0889

IS - 1

ER -