Synchronization of developmental processes and defense signaling by growth regulating transcription factors
Growth regulating factors (GRFs) are a conserved class of transcription factor in seed plants. GRFs are involved in various aspects of tissue differentiation and organ development. The implication of GRFs in biotic stress response has also been recently reported, suggesting a role of these transcrip...
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| description | Growth regulating factors (GRFs) are a conserved class of transcription factor in seed plants. GRFs are involved in various aspects of tissue differentiation and organ development. The implication of GRFs in biotic stress response has also been recently reported, suggesting a role of these transcription factors in coordinating the interaction between developmental processes and defense dynamics. However, the molecular mechanisms by which GRFs mediate the overlaps between defense signaling and developmental pathways are elusive. Here, we report large scale identification of putative target candidates of Arabidopsis GRF1 and GRF3 by comparing mRNA profiles of the grf1/grf2/grf3 triple mutant and those of the transgenic plants overexpressing miR396-resistant version of GRF1 or GRF3. We identified 1,098 and 600 genes as putative targets of GRF1 and GRF3, respectively. Functional classification of the potential target candidates revealed that GRF1 and GRF3 contribute to the regulation of various biological processes associated with defense response and disease resistance. GRF1 and GRF3 participate specifically in the regulation of defense-related transcription factors, cell-wall modifications, cytokinin biosynthesis and signaling, and secondary metabolites accumulation. GRF1 and GRF3 seem to fine-tune the crosstalk between miRNA signaling networks by regulating the expression of several miRNA target genes. In addition, our data suggest that GRF1 and GRF3 may function as negative regulators of gene expression through their association with other transcription factors. Collectively, our data provide new insights into how GRF1 and GRF3 might coordinate the interactions between defense signaling and plant growth and developmental pathways. |
| doi_str_mv | 10.1371/journal.pone.0098477 |
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GRFs are involved in various aspects of tissue differentiation and organ development. The implication of GRFs in biotic stress response has also been recently reported, suggesting a role of these transcription factors in coordinating the interaction between developmental processes and defense dynamics. However, the molecular mechanisms by which GRFs mediate the overlaps between defense signaling and developmental pathways are elusive. Here, we report large scale identification of putative target candidates of Arabidopsis GRF1 and GRF3 by comparing mRNA profiles of the grf1/grf2/grf3 triple mutant and those of the transgenic plants overexpressing miR396-resistant version of GRF1 or GRF3. We identified 1,098 and 600 genes as putative targets of GRF1 and GRF3, respectively. Functional classification of the potential target candidates revealed that GRF1 and GRF3 contribute to the regulation of various biological processes associated with defense response and disease resistance. GRF1 and GRF3 participate specifically in the regulation of defense-related transcription factors, cell-wall modifications, cytokinin biosynthesis and signaling, and secondary metabolites accumulation. GRF1 and GRF3 seem to fine-tune the crosstalk between miRNA signaling networks by regulating the expression of several miRNA target genes. In addition, our data suggest that GRF1 and GRF3 may function as negative regulators of gene expression through their association with other transcription factors. Collectively, our data provide new insights into how GRF1 and GRF3 might coordinate the interactions between defense signaling and plant growth and developmental pathways.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0098477</identifier><identifier>PMID: 24875638</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Abiotic stress ; Adaptation, Biological ; Arabidopsis ; Arabidopsis - physiology ; Arabidopsis Proteins ; Arabidopsis thaliana ; Biological activity ; Biology and Life Sciences ; Biosynthesis ; Calcium-Binding Proteins ; Cell walls ; Cellular stress response ; Cluster Analysis ; Crosstalk ; Cytokines - metabolism ; Differentiation (biology) ; Disease Resistance ; DNA binding proteins ; Gene expression ; Gene Expression Profiling ; Gene Expression Regulation, Plant ; Gene regulation ; Genes ; Genetic engineering ; Growth ; Hormones - biosynthesis ; Infections ; Kinases ; Metabolites ; MicroRNA ; MicroRNAs - genetics ; miRNA ; Molecular modelling ; Organ Specificity - genetics ; Pathways ; Physiological aspects ; Plant diseases ; Plant growth ; Plant sciences ; Promoter Regions, Genetic ; Protein Binding ; Proteins ; ras-GRF1 ; Ribonucleic acid ; RNA ; Secondary metabolites ; Signal Transduction ; Signaling ; Synchronism ; Synchronization ; Target recognition ; Transcription factors ; Transcription Factors - genetics ; Transcription Factors - metabolism ; Transgenic plants</subject><ispartof>PloS one, 2014-05, Vol.9 (5), p.e98477-e98477</ispartof><rights>COPYRIGHT 2014 Public Library of Science</rights><rights>2014 Liu et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2014 Liu et al 2014 Liu et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c758t-16706fa5bb21d3f66e37b200283697afdba615260ed526f3c38da41b488d14373</citedby><cites>FETCH-LOGICAL-c758t-16706fa5bb21d3f66e37b200283697afdba615260ed526f3c38da41b488d14373</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4038601/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4038601/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,728,781,785,865,886,2103,2929,23868,27926,27927,53793,53795</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24875638$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Blazquez, Miguel A.</contributor><creatorcontrib>Liu, Jinyi</creatorcontrib><creatorcontrib>Rice, J Hollis</creatorcontrib><creatorcontrib>Chen, Nana</creatorcontrib><creatorcontrib>Baum, Thomas J</creatorcontrib><creatorcontrib>Hewezi, Tarek</creatorcontrib><title>Synchronization of developmental processes and defense signaling by growth regulating transcription factors</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Growth regulating factors (GRFs) are a conserved class of transcription factor in seed plants. GRFs are involved in various aspects of tissue differentiation and organ development. The implication of GRFs in biotic stress response has also been recently reported, suggesting a role of these transcription factors in coordinating the interaction between developmental processes and defense dynamics. However, the molecular mechanisms by which GRFs mediate the overlaps between defense signaling and developmental pathways are elusive. Here, we report large scale identification of putative target candidates of Arabidopsis GRF1 and GRF3 by comparing mRNA profiles of the grf1/grf2/grf3 triple mutant and those of the transgenic plants overexpressing miR396-resistant version of GRF1 or GRF3. We identified 1,098 and 600 genes as putative targets of GRF1 and GRF3, respectively. Functional classification of the potential target candidates revealed that GRF1 and GRF3 contribute to the regulation of various biological processes associated with defense response and disease resistance. GRF1 and GRF3 participate specifically in the regulation of defense-related transcription factors, cell-wall modifications, cytokinin biosynthesis and signaling, and secondary metabolites accumulation. GRF1 and GRF3 seem to fine-tune the crosstalk between miRNA signaling networks by regulating the expression of several miRNA target genes. In addition, our data suggest that GRF1 and GRF3 may function as negative regulators of gene expression through their association with other transcription factors. Collectively, our data provide new insights into how GRF1 and GRF3 might coordinate the interactions between defense signaling and plant growth and developmental pathways.</description><subject>Abiotic stress</subject><subject>Adaptation, Biological</subject><subject>Arabidopsis</subject><subject>Arabidopsis - physiology</subject><subject>Arabidopsis Proteins</subject><subject>Arabidopsis thaliana</subject><subject>Biological activity</subject><subject>Biology and Life Sciences</subject><subject>Biosynthesis</subject><subject>Calcium-Binding Proteins</subject><subject>Cell walls</subject><subject>Cellular stress response</subject><subject>Cluster Analysis</subject><subject>Crosstalk</subject><subject>Cytokines - metabolism</subject><subject>Differentiation (biology)</subject><subject>Disease Resistance</subject><subject>DNA binding proteins</subject><subject>Gene expression</subject><subject>Gene Expression Profiling</subject><subject>Gene Expression Regulation, Plant</subject><subject>Gene regulation</subject><subject>Genes</subject><subject>Genetic engineering</subject><subject>Growth</subject><subject>Hormones - biosynthesis</subject><subject>Infections</subject><subject>Kinases</subject><subject>Metabolites</subject><subject>MicroRNA</subject><subject>MicroRNAs - genetics</subject><subject>miRNA</subject><subject>Molecular modelling</subject><subject>Organ Specificity - genetics</subject><subject>Pathways</subject><subject>Physiological aspects</subject><subject>Plant diseases</subject><subject>Plant growth</subject><subject>Plant sciences</subject><subject>Promoter Regions, Genetic</subject><subject>Protein Binding</subject><subject>Proteins</subject><subject>ras-GRF1</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>Secondary metabolites</subject><subject>Signal Transduction</subject><subject>Signaling</subject><subject>Synchronism</subject><subject>Synchronization</subject><subject>Target recognition</subject><subject>Transcription factors</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><subject>Transgenic plants</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk1uL1DAUx4so7rr6DUQLgujDjLk1bV-EZfEysLDgqq8hzaWTMZPUpF0dP73pTHeZyj5IIAknv_M_Jyc5WfYcgiXEJXy38UNw3C4779QSgLoiZfkgO4U1RguKAH54tD_JnsS4AaDAFaWPsxNEqrKguDrNflzvnFgH78wf3hvvcq9zqW6U9d1WuZ7bvAteqBhVzLmT6UwrF1UeTZuCG9fmzS5vg__Vr_Og2sEmlWTsA3dRBNPtNTUXvQ_xafZIcxvVs2k9y759_PD14vPi8urT6uL8ciHKouoXkJaAal40DYISa0oVLhsEAKowrUuuZcMpLBAFSqZZY4EryQlsSFVJSHCJz7KXB93O-simOkUGCwxwDUgxEqsDIT3fsC6YLQ875rlhe4MPLeOhN8IqRgXHEsoiRa0IIaiiZaNFrTRFNa_hqPV-ijY0WyVFqlrgdiY6P3FmzVp_wwhIrwFgEngzCQT_c1CxZ1sThbKWO-WHQ951gdA-71f_oPffbqJani5gnPYprhhF2TlJGSNUV3WilvdQaUi1NSJ9Km2SfebwduaQmF797ls-xMhW11_-n736PmdfH7FrxW2_jt4O49eJc5AcQBF8jEHpuyJDwMaeuK0GG3uCTT2R3F4cP9Cd020T4L9Lnwit</recordid><startdate>20140529</startdate><enddate>20140529</enddate><creator>Liu, Jinyi</creator><creator>Rice, J Hollis</creator><creator>Chen, Nana</creator><creator>Baum, Thomas J</creator><creator>Hewezi, Tarek</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20140529</creationdate><title>Synchronization of developmental processes and defense signaling by growth regulating transcription factors</title><author>Liu, Jinyi ; Rice, J Hollis ; Chen, Nana ; Baum, Thomas J ; Hewezi, Tarek</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c758t-16706fa5bb21d3f66e37b200283697afdba615260ed526f3c38da41b488d14373</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Abiotic stress</topic><topic>Adaptation, Biological</topic><topic>Arabidopsis</topic><topic>Arabidopsis - physiology</topic><topic>Arabidopsis Proteins</topic><topic>Arabidopsis thaliana</topic><topic>Biological activity</topic><topic>Biology and Life Sciences</topic><topic>Biosynthesis</topic><topic>Calcium-Binding Proteins</topic><topic>Cell walls</topic><topic>Cellular stress response</topic><topic>Cluster Analysis</topic><topic>Crosstalk</topic><topic>Cytokines - metabolism</topic><topic>Differentiation (biology)</topic><topic>Disease Resistance</topic><topic>DNA binding proteins</topic><topic>Gene expression</topic><topic>Gene Expression Profiling</topic><topic>Gene Expression Regulation, Plant</topic><topic>Gene regulation</topic><topic>Genes</topic><topic>Genetic engineering</topic><topic>Growth</topic><topic>Hormones - biosynthesis</topic><topic>Infections</topic><topic>Kinases</topic><topic>Metabolites</topic><topic>MicroRNA</topic><topic>MicroRNAs - genetics</topic><topic>miRNA</topic><topic>Molecular modelling</topic><topic>Organ Specificity - genetics</topic><topic>Pathways</topic><topic>Physiological aspects</topic><topic>Plant diseases</topic><topic>Plant growth</topic><topic>Plant sciences</topic><topic>Promoter Regions, Genetic</topic><topic>Protein Binding</topic><topic>Proteins</topic><topic>ras-GRF1</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>Secondary metabolites</topic><topic>Signal Transduction</topic><topic>Signaling</topic><topic>Synchronism</topic><topic>Synchronization</topic><topic>Target recognition</topic><topic>Transcription factors</topic><topic>Transcription Factors - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Liu, Jinyi</au><au>Rice, J Hollis</au><au>Chen, Nana</au><au>Baum, Thomas J</au><au>Hewezi, Tarek</au><au>Blazquez, Miguel A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Synchronization of developmental processes and defense signaling by growth regulating transcription factors</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2014-05-29</date><risdate>2014</risdate><volume>9</volume><issue>5</issue><spage>e98477</spage><epage>e98477</epage><pages>e98477-e98477</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Growth regulating factors (GRFs) are a conserved class of transcription factor in seed plants. GRFs are involved in various aspects of tissue differentiation and organ development. The implication of GRFs in biotic stress response has also been recently reported, suggesting a role of these transcription factors in coordinating the interaction between developmental processes and defense dynamics. However, the molecular mechanisms by which GRFs mediate the overlaps between defense signaling and developmental pathways are elusive. Here, we report large scale identification of putative target candidates of Arabidopsis GRF1 and GRF3 by comparing mRNA profiles of the grf1/grf2/grf3 triple mutant and those of the transgenic plants overexpressing miR396-resistant version of GRF1 or GRF3. We identified 1,098 and 600 genes as putative targets of GRF1 and GRF3, respectively. Functional classification of the potential target candidates revealed that GRF1 and GRF3 contribute to the regulation of various biological processes associated with defense response and disease resistance. GRF1 and GRF3 participate specifically in the regulation of defense-related transcription factors, cell-wall modifications, cytokinin biosynthesis and signaling, and secondary metabolites accumulation. GRF1 and GRF3 seem to fine-tune the crosstalk between miRNA signaling networks by regulating the expression of several miRNA target genes. In addition, our data suggest that GRF1 and GRF3 may function as negative regulators of gene expression through their association with other transcription factors. Collectively, our data provide new insights into how GRF1 and GRF3 might coordinate the interactions between defense signaling and plant growth and developmental pathways.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>24875638</pmid><doi>10.1371/journal.pone.0098477</doi><oa>free_for_read</oa></addata></record> |
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| subjects | Abiotic stress Adaptation, Biological Arabidopsis Arabidopsis - physiology Arabidopsis Proteins Arabidopsis thaliana Biological activity Biology and Life Sciences Biosynthesis Calcium-Binding Proteins Cell walls Cellular stress response Cluster Analysis Crosstalk Cytokines - metabolism Differentiation (biology) Disease Resistance DNA binding proteins Gene expression Gene Expression Profiling Gene Expression Regulation, Plant Gene regulation Genes Genetic engineering Growth Hormones - biosynthesis Infections Kinases Metabolites MicroRNA MicroRNAs - genetics miRNA Molecular modelling Organ Specificity - genetics Pathways Physiological aspects Plant diseases Plant growth Plant sciences Promoter Regions, Genetic Protein Binding Proteins ras-GRF1 Ribonucleic acid RNA Secondary metabolites Signal Transduction Signaling Synchronism Synchronization Target recognition Transcription factors Transcription Factors - genetics Transcription Factors - metabolism Transgenic plants |
| title | Synchronization of developmental processes and defense signaling by growth regulating transcription factors |
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