Auxin and Ethylene Induce Flavonol Accumulation through Distinct Transcriptional Networks
Auxin and ethylene are key regulators of plant growth and development, and thus the transcriptional networks that mediate responses to these hormones have been the subject of intense research. This study dissected the hormonal cross talk regulating the synthesis of flavonols and examined their impac...
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| Published in | Plant physiology (Bethesda) Vol. 156; no. 1; pp. 144 - 164 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Rockville, MD
American Society of Plant Biologists
01.05.2011
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Auxin and ethylene are key regulators of plant growth and development, and thus the transcriptional networks that mediate responses to these hormones have been the subject of intense research. This study dissected the hormonal cross talk regulating the synthesis of flavonols and examined their impact on root growth and development. We analyzed the effects of auxin and an ethylene precursor on roots of wild-type and hormone-insensitive Arabidopsis (Arabidopsis thaliana) mutants at the transcript, protein, and metabolite levels at high spatial and temporal resolution. Indole-3-acetic acid (IAA) and 1-aminocyclopropane-lcarboxylic acid (ACC) differentially increased flavonol pathway transcripts and flavonol accumulation, altering the relative abundance of quercetin and kaempferol. The IAA, but not ACC, response is lost in the transport inhibitor responsei (tirl) auxin receptor mutant, while ACC responses, but not IAA responses, are lost in ethylene insensitive! (ein!) and ethylene resistantl (etrl) ethylene signaling mutants. A kinetic analysis identified increases in transcripts encoding the transcriptional regulators MYB12, Transparent Testa Glabra!, and Production of Anthocyanin Pigment after hormone treatments, which preceded increases in transcripts encoding flavonoid biosynthetic enzymes. In addition, mybll mutants were insensitive to the effects of auxin and ethylene on flavonol metabolism. The equivalent phenotypes for transparent testai (tt4), which makes no flavonols, and tt7, which makes kaempferol but not quercetin, showed that quercetin derivatives are the inhibitors of basipetal root auxin transport, gravitropism, and elongation growth. Collectively, these experiments demonstrate that auxin and ethylene regulate flavonol biosynthesis through distinct signaling networks involving TIR1 and EIN2/ETR1, respectively, both of which converge on MYB12. This study also provides new evidence that quercetin is the flavonol that modulates basipetal auxin transport. |
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| AbstractList | Auxin and ethylene are key regulators of plant growth and development, and thus the transcriptional networks that mediate responses to these hormones have been the subject of intense research. This study dissected the hormonal cross talk regulating the synthesis of flavonols and examined their impact on root growth and development. We analyzed the effects of auxin and an ethylene precursor on roots of wild-type and hormone-insensitive Arabidopsis (Arabidopsis thaliana) mutants at the transcript, protein, and metabolite levels at high spatial and temporal resolution. Indole-3-acetic acid (IAA) and 1-aminocyclopropane-1-carboxylic acid (ACC) differentially increased flavonol pathway transcripts and flavonol accumulation, altering the relative abundance of quercetin and kaempferol. The IAA, but not ACC, response is lost in the transport inhibitor response1 (tir1) auxin receptor mutant, while ACC responses, but not IAA responses, are lost in ethylene insensitive2 (ein2) and ethylene resistant1 (etr1) ethylene signaling mutants. A kinetic analysis identified increases in transcripts encoding the transcriptional regulators MYB12, Transparent Testa Glabra1, and Production of Anthocyanin Pigment after hormone treatments, which preceded increases in transcripts encoding flavonoid biosynthetic enzymes. In addition, myb12 mutants were insensitive to the effects of auxin and ethylene on flavonol metabolism. The equivalent phenotypes for transparent testa4 (tt4), which makes no flavonols, and tt7, which makes kaempferol but not quercetin, showed that quercetin derivatives are the inhibitors of basipetal root auxin transport, gravitropism, and elongation growth. Collectively, these experiments demonstrate that auxin and ethylene regulate flavonol biosynthesis through distinct signaling networks involving TIR1 and EIN2/ETR1, respectively, both of which converge on MYB12. This study also provides new evidence that quercetin is the flavonol that modulates basipetal auxin transport. Auxin and ethylene are key regulators of plant growth and development, and thus the transcriptional networks that mediate responses to these hormones have been the subject of intense research. This study dissected the hormonal cross talk regulating the synthesis of flavonols and examined their impact on root growth and development. We analyzed the effects of auxin and an ethylene precursor on roots of wild-type and hormone-insensitive Arabidopsis ( Arabidopsis thaliana ) mutants at the transcript, protein, and metabolite levels at high spatial and temporal resolution. Indole-3-acetic acid (IAA) and 1-aminocyclopropane-1-carboxylic acid (ACC) differentially increased flavonol pathway transcripts and flavonol accumulation, altering the relative abundance of quercetin and kaempferol. The IAA, but not ACC, response is lost in the transport inhibitor response1 ( tir1 ) auxin receptor mutant, while ACC responses, but not IAA responses, are lost in ethylene insensitive2 ( ein2 ) and ethylene resistant1 ( etr1 ) ethylene signaling mutants. A kinetic analysis identified increases in transcripts encoding the transcriptional regulators MYB12 , Transparent Testa Glabra1 , and Production of Anthocyanin Pigment after hormone treatments, which preceded increases in transcripts encoding flavonoid biosynthetic enzymes. In addition, myb12 mutants were insensitive to the effects of auxin and ethylene on flavonol metabolism. The equivalent phenotypes for transparent testa4 ( tt4 ), which makes no flavonols, and tt7 , which makes kaempferol but not quercetin, showed that quercetin derivatives are the inhibitors of basipetal root auxin transport, gravitropism, and elongation growth. Collectively, these experiments demonstrate that auxin and ethylene regulate flavonol biosynthesis through distinct signaling networks involving TIR1 and EIN2/ETR1, respectively, both of which converge on MYB12. This study also provides new evidence that quercetin is the flavonol that modulates basipetal auxin transport. Auxin and ethylene are key regulators of plant growth and development, and thus the transcriptional networks that mediate responses to these hormones have been the subject of intense research. This study dissected the hormonal cross talk regulating the synthesis of flavonols and examined their impact on root growth and development. We analyzed the effects of auxin and an ethylene precursor on roots of wild-type and hormone-insensitive Arabidopsis (Arabidopsis thaliana) mutants at the transcript, protein, and metabolite levels at high spatial and temporal resolution. Indole-3-acetic acid (IAA) and 1-aminocyclopropane-lcarboxylic acid (ACC) differentially increased flavonol pathway transcripts and flavonol accumulation, altering the relative abundance of quercetin and kaempferol. The IAA, but not ACC, response is lost in the transport inhibitor responsei (tirl) auxin receptor mutant, while ACC responses, but not IAA responses, are lost in ethylene insensitive! (ein!) and ethylene resistantl (etrl) ethylene signaling mutants. A kinetic analysis identified increases in transcripts encoding the transcriptional regulators MYB12, Transparent Testa Glabra!, and Production of Anthocyanin Pigment after hormone treatments, which preceded increases in transcripts encoding flavonoid biosynthetic enzymes. In addition, mybll mutants were insensitive to the effects of auxin and ethylene on flavonol metabolism. The equivalent phenotypes for transparent testai (tt4), which makes no flavonols, and tt7, which makes kaempferol but not quercetin, showed that quercetin derivatives are the inhibitors of basipetal root auxin transport, gravitropism, and elongation growth. Collectively, these experiments demonstrate that auxin and ethylene regulate flavonol biosynthesis through distinct signaling networks involving TIR1 and EIN2/ETR1, respectively, both of which converge on MYB12. This study also provides new evidence that quercetin is the flavonol that modulates basipetal auxin transport. Auxin and ethylene are key regulators of plant growth and development, and thus the transcriptional networks that mediate responses to these hormones have been the subject of intense research. This study dissected the hormonal cross talk regulating the synthesis of flavonols and examined their impact on root growth and development. We analyzed the effects of auxin and an ethylene precursor on roots of wild-type and hormone-insensitive Arabidopsis (Arabidopsis thaliana) mutants at the transcript, protein, and metabolite levels at high spatial and temporal resolution. Indole-3-acetic acid (IAA) and 1-aminocyclopropane-1-carboxylic acid (ACC) differentially increased flavonol pathway transcripts and flavonol accumulation, altering the relative abundance of quercetin and kaempferol. The IAA, but not ACC, response is lost in the transport inhibitor response1 (tir1) auxin receptor mutant, while ACC responses, but not IAA responses, are lost in ethylene insensitive2 (ein2) and ethylene resistant1 (etr1) ethylene signaling mutants. A kinetic analysis identified increases in transcripts encoding the transcriptional regulators MYB12, Transparent Testa Glabra1, and Production of Anthocyanin Pigment after hormone treatments, which preceded increases in transcripts encoding flavonoid biosynthetic enzymes. In addition, myb12 mutants were insensitive to the effects of auxin and ethylene on flavonol metabolism. The equivalent phenotypes for transparent testa4 (tt4), which makes no flavonols, and tt7, which makes kaempferol but not quercetin, showed that quercetin derivatives are the inhibitors of basipetal root auxin transport, gravitropism, and elongation growth. Collectively, these experiments demonstrate that auxin and ethylene regulate flavonol biosynthesis through distinct signaling networks involving TIR1 and EIN2/ETR1, respectively, both of which converge on MYB12. This study also provides new evidence that quercetin is the flavonol that modulates basipetal auxin transport.Auxin and ethylene are key regulators of plant growth and development, and thus the transcriptional networks that mediate responses to these hormones have been the subject of intense research. This study dissected the hormonal cross talk regulating the synthesis of flavonols and examined their impact on root growth and development. We analyzed the effects of auxin and an ethylene precursor on roots of wild-type and hormone-insensitive Arabidopsis (Arabidopsis thaliana) mutants at the transcript, protein, and metabolite levels at high spatial and temporal resolution. Indole-3-acetic acid (IAA) and 1-aminocyclopropane-1-carboxylic acid (ACC) differentially increased flavonol pathway transcripts and flavonol accumulation, altering the relative abundance of quercetin and kaempferol. The IAA, but not ACC, response is lost in the transport inhibitor response1 (tir1) auxin receptor mutant, while ACC responses, but not IAA responses, are lost in ethylene insensitive2 (ein2) and ethylene resistant1 (etr1) ethylene signaling mutants. A kinetic analysis identified increases in transcripts encoding the transcriptional regulators MYB12, Transparent Testa Glabra1, and Production of Anthocyanin Pigment after hormone treatments, which preceded increases in transcripts encoding flavonoid biosynthetic enzymes. In addition, myb12 mutants were insensitive to the effects of auxin and ethylene on flavonol metabolism. The equivalent phenotypes for transparent testa4 (tt4), which makes no flavonols, and tt7, which makes kaempferol but not quercetin, showed that quercetin derivatives are the inhibitors of basipetal root auxin transport, gravitropism, and elongation growth. Collectively, these experiments demonstrate that auxin and ethylene regulate flavonol biosynthesis through distinct signaling networks involving TIR1 and EIN2/ETR1, respectively, both of which converge on MYB12. This study also provides new evidence that quercetin is the flavonol that modulates basipetal auxin transport. |
| Author | Ramirez, Melissa V. Ray, W. Keith Muday, Gloria K. Winkel, Brenda S.J. Vallabhaneni, Prashanthi Lewis, Daniel R. Helm, Richard F. Miller, Nathan D. |
| AuthorAffiliation | Department of Biology, Wake Forest University, Winston-Salem, North Carolina 27109 (D.R.L., G.K.M.); Department of Biological Sciences (M.V.R., P.V., B.S.J.W.) and Department of Biochemistry (W.K.R., R.F.H.), Virginia Tech, Blacksburg, Virginia 24061; and Department of Botany, University of Wisconsin, Madison, Wisconsin 53706 (N.D.M.) |
| AuthorAffiliation_xml | – name: Department of Biology, Wake Forest University, Winston-Salem, North Carolina 27109 (D.R.L., G.K.M.); Department of Biological Sciences (M.V.R., P.V., B.S.J.W.) and Department of Biochemistry (W.K.R., R.F.H.), Virginia Tech, Blacksburg, Virginia 24061; and Department of Botany, University of Wisconsin, Madison, Wisconsin 53706 (N.D.M.) |
| Author_xml | – sequence: 1 givenname: Daniel R. surname: Lewis fullname: Lewis, Daniel R. – sequence: 2 givenname: Melissa V. surname: Ramirez fullname: Ramirez, Melissa V. – sequence: 3 givenname: Nathan D. surname: Miller fullname: Miller, Nathan D. – sequence: 4 givenname: Prashanthi surname: Vallabhaneni fullname: Vallabhaneni, Prashanthi – sequence: 5 givenname: W. Keith surname: Ray fullname: Ray, W. Keith – sequence: 6 givenname: Richard F. surname: Helm fullname: Helm, Richard F. – sequence: 7 givenname: Brenda S.J. surname: Winkel fullname: Winkel, Brenda S.J. – sequence: 8 givenname: Gloria K. surname: Muday fullname: Muday, Gloria K. |
| BackLink | http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=24132667$$DView record in Pascal Francis https://www.ncbi.nlm.nih.gov/pubmed/21427279$$D View this record in MEDLINE/PubMed |
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| CODEN | PPHYA5 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Some figures in this article are displayed in color online but in black and white in the print edition. Present address: Mycobacteria Research Laboratories, Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, CO 80523. The online version of this article contains Web-only data. www.plantphysiol.org/cgi/doi/10.1104/pp.111.172502 This work was supported by the National Science Foundation Arabidopsis 2010 Program (grant nos. IOB–0820717 to G.K.M. and 0820674 to B.S.J.W. and R.F.H.) and National Science Foundation Molecular Biochemistry (grant no. MCB–0445878 to B.S.J.W.), by the U.S. Department of Agriculture-National Research Initiative Competitive Grants Program (grant no. 2006–03406 to G.K.M.), by the National Science Foundation Major Research Instrumentation Program for purchase of the confocal microscope (grant no. MRI–0722926 to Anita McCauley and G.K.M.), and by the National Science Foundation Plant Genome Program (grant no. DBI–0621702 to Edgar Spalding). The authors responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) are: Brenda S.J. Winkel (winkel@vt.edu) and Gloria K. Muday (muday@wfu.edu). Open Access articles can be viewed online without a subscription. |
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| Snippet | Auxin and ethylene are key regulators of plant growth and development, and thus the transcriptional networks that mediate responses to these hormones have been... |
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| SubjectTerms | 1-aminocyclopropane-1-carboxylic acid Amino Acids, Cyclic - pharmacology Arabidopsis - cytology Arabidopsis - drug effects Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis Proteins - metabolism Arabidopsis thaliana Auxins Biological and medical sciences biosynthesis CELL BIOLOGY AND SIGNAL TRANSDUCTION Enzymes ethylene Ethylenes - pharmacology Flavonoids Flavonols Flavonols - metabolism Fluorescence Fundamental and applied biological sciences. Psychology Gene expression regulation Gene Expression Regulation, Plant - drug effects Gene Regulatory Networks Genes Glycosides - metabolism Gravitropism growth and development hormones indole acetic acid Indoleacetic Acids - pharmacology Insulin antibodies kaempferol mutants Mutation phenotype plant development Plant Growth Regulators - pharmacology Plant physiology and development Plant roots Plant Roots - cytology Plant Roots - drug effects Plant Roots - genetics Plant Roots - metabolism Plants Plants, Genetically Modified quercetin Quercetin - metabolism receptors Recombinant Fusion Proteins RNA, Plant - genetics root growth roots Seedlings - cytology Seedlings - drug effects Seedlings - genetics Seedlings - metabolism testa |
| Title | Auxin and Ethylene Induce Flavonol Accumulation through Distinct Transcriptional Networks |
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