A Review of Auxin Response Factors (ARFs) in Plants
Identifieur interne : 000419 ( Pmc/Corpus ); précédent : 000418; suivant : 000420A Review of Auxin Response Factors (ARFs) in Plants
Auteurs : Si-Bei Li ; Zong-Zhou Xie ; Chun-Gen Hu ; Jin-Zhi ZhangSource :
- Frontiers in Plant Science [ 1664-462X ] ; 2016.
Abstract
Auxin is a key regulator of virtually every aspect of plant growth and development from embryogenesis to senescence. Previous studies have indicated that auxin regulates these processes by controlling gene expression via a family of functionally distinct DNA-binding
Url:
DOI: 10.3389/fpls.2016.00047
PubMed: 26870066
PubMed Central: 4737911
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">A Review of Auxin Response Factors (ARFs) in Plants</title><author><name sortKey="Li, Si Bei" sort="Li, Si Bei" uniqKey="Li S" first="Si-Bei" last="Li">Si-Bei Li</name></author><author><name sortKey="Xie, Zong Zhou" sort="Xie, Zong Zhou" uniqKey="Xie Z" first="Zong-Zhou" last="Xie">Zong-Zhou Xie</name></author><author><name sortKey="Hu, Chun Gen" sort="Hu, Chun Gen" uniqKey="Hu C" first="Chun-Gen" last="Hu">Chun-Gen Hu</name></author><author><name sortKey="Zhang, Jin Zhi" sort="Zhang, Jin Zhi" uniqKey="Zhang J" first="Jin-Zhi" last="Zhang">Jin-Zhi Zhang</name></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26870066</idno><idno type="pmc">4737911</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4737911</idno><idno type="RBID">PMC:4737911</idno><idno type="doi">10.3389/fpls.2016.00047</idno><date when="2016">2016</date><idno type="wicri:Area/Pmc/Corpus">000419</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">A Review of Auxin Response Factors (ARFs) in Plants</title><author><name sortKey="Li, Si Bei" sort="Li, Si Bei" uniqKey="Li S" first="Si-Bei" last="Li">Si-Bei Li</name></author><author><name sortKey="Xie, Zong Zhou" sort="Xie, Zong Zhou" uniqKey="Xie Z" first="Zong-Zhou" last="Xie">Zong-Zhou Xie</name></author><author><name sortKey="Hu, Chun Gen" sort="Hu, Chun Gen" uniqKey="Hu C" first="Chun-Gen" last="Hu">Chun-Gen Hu</name></author><author><name sortKey="Zhang, Jin Zhi" sort="Zhang, Jin Zhi" uniqKey="Zhang J" first="Jin-Zhi" last="Zhang">Jin-Zhi Zhang</name></author></analytic><series><title level="j">Frontiers in Plant Science</title><idno type="eISSN">1664-462X</idno><imprint><date when="2016">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Auxin is a key regulator of virtually every aspect of plant growth and development from embryogenesis to senescence. Previous studies have indicated that auxin regulates these processes by controlling gene expression via a family of functionally distinct DNA-binding <italic>auxin response factors</italic> (<italic>ARFs</italic>). <italic>ARFs</italic> are likely components that confer specificity to auxin response through selection of target genes as transcription factors. They bind to auxin response DNA elements (AuxRE) in the promoters of auxin-regulated genes and either activate or repress transcription of these genes depending on a specific domain in the middle of the protein. Genetic studies have implicated various <italic>ARFs</italic> in distinct developmental processes through loss-of-function mutant analysis. Recent advances have provided information on the regulation of <italic>ARF</italic> gene expression, the role of <italic>ARFs</italic> in growth and developmental processes, protein–protein interactions of ARFs and target genes regulated by <italic>ARFs</italic> in plants. In particular, protein interaction and structural studies of ARF proteins have yielded novel insights into the molecular basis of auxin-regulated transcription. These results provide the foundation for predicting the contributions of <italic>ARF</italic> genes to the biology of other plants.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Blanc, G" uniqKey="Blanc G">G. Blanc</name></author><author><name sortKey="Hokamp, K" uniqKey="Hokamp K">K. Hokamp</name></author><author><name sortKey="Wolfe, K H" uniqKey="Wolfe K">K. H. Wolfe</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Boer, D R" uniqKey="Boer D">D. R. Boer</name></author><author><name sortKey="Freire Rios, A" uniqKey="Freire Rios A">A. Freire-Rios</name></author><author><name sortKey="Van Den Berg, W A" uniqKey="Van Den Berg W">W. A. van den Berg</name></author><author><name sortKey="Saaki, T" uniqKey="Saaki T">T. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Front Plant Sci</journal-id><journal-id journal-id-type="iso-abbrev">Front Plant Sci</journal-id><journal-id journal-id-type="publisher-id">Front. Plant Sci.</journal-id><journal-title-group><journal-title>Frontiers in Plant Science</journal-title></journal-title-group><issn pub-type="epub">1664-462X</issn><publisher><publisher-name>Frontiers Media S.A.</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26870066</article-id><article-id pub-id-type="pmc">4737911</article-id><article-id pub-id-type="doi">10.3389/fpls.2016.00047</article-id><article-categories><subj-group subj-group-type="heading"><subject>Plant Science</subject><subj-group><subject>Focused Review</subject></subj-group></subj-group></article-categories><title-group><article-title>A Review of Auxin Response Factors (ARFs) in Plants</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Li</surname><given-names>Si-Bei</given-names></name><xref ref-type="author-notes" rid="fn002"><sup>†</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/224425/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Xie</surname><given-names>Zong-Zhou</given-names></name><xref ref-type="author-notes" rid="fn002"><sup>†</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/312066/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Hu</surname><given-names>Chun-Gen</given-names></name><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/224416/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Zhang</surname><given-names>Jin-Zhi</given-names></name><xref ref-type="author-notes" rid="fn001"><sup>*</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/201406/overview"></uri></contrib></contrib-group><aff><institution>Key Laboratory of Horticultural Plant Biology, Ministry of Education, College of Horticulture and Forestry Science, Huazhong Agricultural University</institution><country>Wuhan, China</country></aff><author-notes><fn fn-type="edited-by"><p>Edited by: Elena Prats, Consejo Superior de Investigaciones Científicas, Spain</p></fn><fn fn-type="edited-by"><p>Reviewed by: Lei Zhang, Washington State University, USA; Caiguo Zhang, University of Colorado, Denver, USA</p></fn><corresp id="fn001">*Correspondence: <email xlink:type="simple">jinzhizhang@mail.hzau.edu.cn</email>; <email xlink:type="simple">jinzhi327320094@126.com</email></corresp><fn fn-type="other" id="fn002"><p>†These authors have contributed equally to this work.</p></fn></author-notes><pub-date pub-type="epub"><day>03</day><month>2</month><year>2016</year></pub-date><pub-date pub-type="collection"><year>2016</year></pub-date><volume>7</volume><elocation-id>47</elocation-id><history><date date-type="received"><day>04</day><month>11</month><year>2015</year></date><date date-type="accepted"><day>12</day><month>1</month><year>2016</year></date></history><permissions><copyright-statement>Copyright © 2016 Li, Xie, Hu and Zhang.</copyright-statement><copyright-year>2016</copyright-year><copyright-holder>Li, Xie, Hu and Zhang</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</license-p></license></permissions><abstract><p>Auxin is a key regulator of virtually every aspect of plant growth and development from embryogenesis to senescence. Previous studies have indicated that auxin regulates these processes by controlling gene expression via a family of functionally distinct DNA-binding <italic>auxin response factors</italic> (<italic>ARFs</italic>). <italic>ARFs</italic> are likely components that confer specificity to auxin response through selection of target genes as transcription factors. They bind to auxin response DNA elements (AuxRE) in the promoters of auxin-regulated genes and either activate or repress transcription of these genes depending on a specific domain in the middle of the protein. Genetic studies have implicated various <italic>ARFs</italic> in distinct developmental processes through loss-of-function mutant analysis. Recent advances have provided information on the regulation of <italic>ARF</italic> gene expression, the role of <italic>ARFs</italic> in growth and developmental processes, protein–protein interactions of ARFs and target genes regulated by <italic>ARFs</italic> in plants. In particular, protein interaction and structural studies of ARF proteins have yielded novel insights into the molecular basis of auxin-regulated transcription. These results provide the foundation for predicting the contributions of <italic>ARF</italic> genes to the biology of other plants.</p></abstract><kwd-group><kwd>auxin</kwd><kwd>ARF</kwd><kwd>auxin response DNA elements</kwd><kwd><italic>Arabidopsis</italic></kwd><kwd>DBD domain</kwd><kwd>a type I/II Phox and Bem1p (PB1)</kwd></kwd-group><counts><fig-count count="1"></fig-count><table-count count="1"></table-count><equation-count count="0"></equation-count><ref-count count="73"></ref-count><page-count count="7"></page-count><word-count count="6304"></word-count></counts></article-meta></front><body><sec sec-type="intro" id="s1"><title>Introduction</title><p>Auxins play a critical role in most major growth responses both throughout the different developmental stages of plants such as <bold>organogenesis</bold>, vascular tissue differentiation, apical dominance and root initiation, and tropism and on a cellular level cell in processes including extension, division, and differentiation (Guilfoyle and Hagen, <xref rid="B16" ref-type="bibr">2007</xref>; Mockaitis and Estelle, <xref rid="B37" ref-type="bibr">2008</xref>; Su et al., <xref rid="B54" ref-type="bibr">2014</xref>). Three decades of studies have explored the rapid effects of auxin on gene expression and regulation (Di et al., <xref rid="B10" ref-type="bibr">2015b</xref>). A large number of candidate genes that are potentially regulated by auxins and that may function in growth and developmental processes have been identified in <italic>Arabidopsis</italic> and other plant species (Rosado et al., <xref rid="B46" ref-type="bibr">2012</xref>; Liu et al., <xref rid="B34" ref-type="bibr">2014b</xref>; Di et al., <xref rid="B10" ref-type="bibr">2015b</xref>; Guilfoyle, <xref rid="B15" ref-type="bibr">2015</xref>). Among these genes, members of the <italic>auxin response factors</italic> (<italic>ARF</italic>) family have been suggested to play a key role in regulating the expression of auxin response genes (Liscum and Reed, <xref rid="B30" ref-type="bibr">2002</xref>). To date, 22 <italic>ARF</italic> genes and one pseudogene have been isolated from <italic>Arabidopsis</italic> (Liscum and Reed, <xref rid="B30" ref-type="bibr">2002</xref>; Guilfoyle and Hagen, <xref rid="B16" ref-type="bibr">2007</xref>). <italic>ARF</italic> genes are expressed in dynamic and differential patterning during development, and genetic studies have shown that individual <italic>ARFs</italic> control distinct developmental processes (Rademacher et al., <xref rid="B43" ref-type="bibr">2012</xref>). Members of the ARF family of proteins contain domains associated with DNA binding, transcriptional activation or repression, and protein-protein interactions during auxin perception and signaling processes (Guilfoyle and Hagen, <xref rid="B16" ref-type="bibr">2007</xref>; Di et al., <xref rid="B9" ref-type="bibr">2015a</xref>). Recently, the <italic>ARF</italic> gene family has been also investigated in several plants based on the recent release of the genome such as citrus, <italic>Medicago truncatula</italic> and <italic>Gossypium raimondii</italic> using both bioinformatics and molecular analyses (Li et al., <xref rid="B28" ref-type="bibr">2015</xref>; Shen et al., <xref rid="B51" ref-type="bibr">2015a</xref>; Sun et al., <xref rid="B55" ref-type="bibr">2015</xref>). More importantly, a considerable amount of new information has been obtained regarding the mechanisms that control ARF protein activities, and gene expression profiles. This review will focus on recent advances that have provided insight into the roles played by <italic>ARFs</italic> in regulating a variety of plant growth and development processes and the mechanisms involved in this regulation in <italic>Arabidopsis</italic> and other plant species.</p><boxed-text position="float"><label>KEY CONCEPT 1</label><caption><title>Organogenesis</title></caption><p>An adult plant consists of many specialized cell organizations: tissues and organs. Tissues consist of cells of uniform shape and specialized function, such as meristem, cortex, and phloem. Several tissues are organized together to form an organ, such as leaves, roots, flowers, and fruit. The process of initiation and development of an organ is called organogenesis.</p></boxed-text></sec><sec id="s2"><title>Molecular structure of ARF family proteins</title><p>The plants response to auxin involves changes in gene regulation (Liscum and Reed, <xref rid="B30" ref-type="bibr">2002</xref>). Genes that are up-regulated or down-regulated by auxin contain AuxRE in their promoters, which bind transcription factors of the ARF family (Guilfoyle and Hagen, <xref rid="B16" ref-type="bibr">2007</xref>; Mockaitis and Estelle, <xref rid="B37" ref-type="bibr">2008</xref>). The identification of the AuxRE sequence led to the isolation of <italic>Arabidopsis ARF1</italic> (Ulmasov et al., <xref rid="B58" ref-type="bibr">1997</xref>), and subsequent genetic, genomic, and molecular studies have identified 22 <italic>ARF</italic> genes in <italic>Arabidopsis</italic> (Liscum and Reed, <xref rid="B30" ref-type="bibr">2002</xref>). The <italic>ARF</italic> gene family is a modular transcription factor family consisting of several domains that have remained conserved despite hundreds of millions of years of evolution (Finet et al., <xref rid="B12" ref-type="bibr">2012</xref>). Most ARF proteins consist of an N-terminal <bold>B3-type DNA binding domain (DBD)</bold>, a variable middle region that functions as an activation domain (AD) or repression domain (RD), and a carboxy-terminal dimerization domain (CTD: domain III/IV), which is involved in protein–protein interactions by dimerizing with auxin/indole-3-acetic acid (Aux/IAA) family genes as well as between ARFs (Kim et al., <xref rid="B25" ref-type="bibr">1997</xref>; Guilfoyle and Hagen, <xref rid="B16" ref-type="bibr">2007</xref>; Piya et al., <xref rid="B42" ref-type="bibr">2014</xref>). The DBD is classified as a plant-specific B3-type protein domain, but requires additional amino-terminal and carboxyterminal amino acids for efficient <italic>in vitro</italic> binding to TGTCTC/GAGACA site (Tiwari et al., <xref rid="B57" ref-type="bibr">2003</xref>). The first four bases of the recognition site are absolutely required for ARF binding, while more variation is tolerated in the last two bases (Boer et al., <xref rid="B2" ref-type="bibr">2014</xref>). The AD and RD are located just carboxyterminal to the DBD and contain biased amino acid sequences (Ulmasov et al., <xref rid="B59" ref-type="bibr">1999</xref>). The AD is enriched in glutamine along with leucine (L) and serine (S) residues, while the RD is enriched in glycine (Q), leucine (L), serine (S), and proline (P) residues (Ulmasov et al., <xref rid="B59" ref-type="bibr">1999</xref>). The amino acid composition of the middle region is critical in determining ARF function, with S-rich ARFs acting as transcriptional repressors and Q-rich ARFs acting transcriptional activators by protoplast transfection assays (Tiwari et al., <xref rid="B57" ref-type="bibr">2003</xref>; Guilfoyle and Hagen, <xref rid="B16" ref-type="bibr">2007</xref>). Five ARF proteins (ARF5/ARF6/ARF7/ARF8/ARF19) were characterized as transcriptional activators based on transient assays in transfected protoplasts, the other ARFs were classified as repressors (Ulmasov et al., <xref rid="B59" ref-type="bibr">1999</xref>; Tiwari et al., <xref rid="B57" ref-type="bibr">2003</xref>). A recent crystallographic study revealed that two additional domains associate with the DBDs of some ARFs, and these are a dimerization domain (DD) and a Tudor-like ancillary domain within the C-terminal region of the flanking domain (FD). The DD facilitates cooperative binding of the B3 DBD to selected AuxREs. However, the function of Tudor-like ancillary domain has not been determined (Guilfoyle and Hagen, <xref rid="B17" ref-type="bibr">2012</xref>; Boer et al., <xref rid="B2" ref-type="bibr">2014</xref>; Guilfoyle, <xref rid="B15" ref-type="bibr">2015</xref>; Korasick et al., <xref rid="B26" ref-type="bibr">2015</xref>). Not all ARFs contain the five domains described above. In addition, the III–IV region of some ARF protein may form a type I/II Phox and Bem1p (PB1) protein–protein interaction domain, which provides both positive and negative electrostatic interfaces for directional protein interaction (Guilfoyle and Hagen, <xref rid="B17" ref-type="bibr">2012</xref>; Guilfoyle, <xref rid="B15" ref-type="bibr">2015</xref>; Korasick et al., <xref rid="B26" ref-type="bibr">2015</xref>).</p><boxed-text position="float"><label>KEY CONCEPT 2</label><caption><title>B3-type DNA binding domain (DBD)</title></caption><p>It is a highly conserved domain found exclusively in transcription factors (TFs) of higher plants. It consists of 100–120 residues, includes seven beta strands and two alpha helices. There are three main families of TFs that contain B3 domain in Arabidopsis: ARF Auxin response factors (ARF), Abscisic acid insensitive 3 (ABI3), and Related to ABI3/VP1 (RAV).</p></boxed-text><p>Since, cloning of the first <italic>ARF</italic> gene from <italic>Arabidopsis</italic> (Ulmasov et al., <xref rid="B58" ref-type="bibr">1997</xref>), <italic>ARF</italic> genes from 15 plant species have been identified based on genome-wide analysis studies (Table <xref ref-type="table" rid="T1">1</xref>). For example, 22 genes from tomato (Zouine et al., <xref rid="B76" ref-type="bibr">2014</xref>), 25 genes from rice (Wang et al., <xref rid="B64" ref-type="bibr">2007</xref>), 19 genes from sweet orange (Li et al., <xref rid="B28" ref-type="bibr">2015</xref>), 24 genes from <italic>Medicago truncatula</italic> (Shen et al., <xref rid="B51" ref-type="bibr">2015a</xref>), 47 genes from banana (Hu et al., <xref rid="B21" ref-type="bibr">2015</xref>), and 39 genes from <italic>Populus trichocarpa</italic> (Kalluri et al., <xref rid="B23" ref-type="bibr">2007</xref>) were identified. Most ARF proteins from these plant species are nuclear proteins with described protein domains consistent with previous reports on the homologous genes from <italic>Arabidopsis</italic> (Table <xref ref-type="table" rid="T1">1</xref>). However, some differences in the ARF protein family were also found between <italic>Arabidopsis</italic> and other plant species. For example, ARF3, ARF13, and ARF17 lack Domains III/IV, and ARF23 consists of a truncated DBD only in <italic>Arabidopsis</italic> (Guilfoyle and Hagen, <xref rid="B16" ref-type="bibr">2007</xref>). Only one pseudogene (a truncated DBD) was found in citrus plants among these plant species (Li et al., <xref rid="B28" ref-type="bibr">2015</xref>), whereas a large number of truncated proteins (lacking Domains III/IV) have been found in rice (Wang et al., <xref rid="B64" ref-type="bibr">2007</xref>), maize (Liu et al., <xref rid="B35" ref-type="bibr">2011</xref>), banana (Hu et al., <xref rid="B21" ref-type="bibr">2015</xref>), and <italic>M. truncatula</italic> (Shen et al., <xref rid="B51" ref-type="bibr">2015a</xref>) compared with <italic>Arabidopsis</italic>. Interestingly, some plant species contain more <italic>ARF</italic> genes than <italic>Arabidopsis</italic> (Table <xref ref-type="table" rid="T1">1</xref>). One explanation for the higher number of <italic>ARF</italic> genes encoded in these genome could be that large-scale duplication event occurred early in the evolution of these plants (Blanc et al., <xref rid="B1" ref-type="bibr">2003</xref>). It is noteworthy that most information about <italic>ARFs</italic> function, expression, and regulation comes from studies in annual herbaceous plants such as <italic>Arabidopsis</italic>, rice, and tomato (Guilfoyle and Hagen, <xref rid="B16" ref-type="bibr">2007</xref>; Wang et al., <xref rid="B64" ref-type="bibr">2007</xref>; Kumar et al., <xref rid="B27" ref-type="bibr">2011</xref>), while relatively few reports focus on other plant species.</p><table-wrap id="T1" position="float"><label>Table 1</label><caption><p><bold>Summary of <italic><bold>ARF</bold></italic> genes in 16 plant species based on genome-wide analysis</bold>.</p></caption><table frame="hsides" rules="groups"><thead><tr><th valign="top" align="left" rowspan="1" colspan="1"><bold>Species</bold></th><th valign="top" align="center" rowspan="1" colspan="1"><bold>Gene No</bold></th><th valign="top" align="center" rowspan="1" colspan="1"><bold>Pseudogene No</bold></th><th valign="top" align="left" rowspan="1" colspan="1"><bold>Truncated protein No</bold>.</th><th valign="top" align="left" rowspan="1" colspan="1"><bold>Complete protein No</bold>.</th><th valign="top" align="left" rowspan="1" colspan="1"><bold>References</bold></th></tr></thead><tbody><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>Arabidopsis thaliana</italic></td><td valign="top" align="center" rowspan="1" colspan="1">23</td><td valign="top" align="center" rowspan="1" colspan="1">1</td><td valign="top" align="left" rowspan="1" colspan="1">3 (DBD, MR)</td><td valign="top" align="left" rowspan="1" colspan="1">19 (DBD, MR, CTD)</td><td valign="top" align="left" rowspan="1" colspan="1">Hagen and Guilfoyle, <xref rid="B18" ref-type="bibr">2002</xref></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>Oryza sativa</italic></td><td valign="top" align="center" rowspan="1" colspan="1">25</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="left" rowspan="1" colspan="1">6 (DBD, MR)</td><td valign="top" align="left" rowspan="1" colspan="1">19 (DBD, MR, CTD)</td><td valign="top" align="left" rowspan="1" colspan="1">Wang et al., <xref rid="B64" ref-type="bibr">2007</xref></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>Citrus sinensis</italic></td><td valign="top" align="center" rowspan="1" colspan="1">19</td><td valign="top" align="center" rowspan="1" colspan="1">1</td><td valign="top" align="left" rowspan="1" colspan="1">3 (DBD, MR)</td><td valign="top" align="left" rowspan="1" colspan="1">15(DBD, MR, CTD)</td><td valign="top" align="left" rowspan="1" colspan="1">Li et al., <xref rid="B28" ref-type="bibr">2015</xref></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>Solanum lycopersicum</italic></td><td valign="top" align="center" rowspan="1" colspan="1">21</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="left" rowspan="1" colspan="1">7 (DBD, MR)</td><td valign="top" align="left" rowspan="1" colspan="1">14 (DBD, MR, CTD)</td><td valign="top" align="left" rowspan="1" colspan="1">Wu et al., <xref rid="B71" ref-type="bibr">2011</xref></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>Glycine max</italic></td><td valign="top" align="center" rowspan="1" colspan="1">51</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="left" rowspan="1" colspan="1">8 (DBD, MR)</td><td valign="top" align="left" rowspan="1" colspan="1">43 (DBD, MR, CTD)</td><td valign="top" align="left" rowspan="1" colspan="1">Van Ha et al., <xref rid="B60" ref-type="bibr">2013</xref></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>Zea mays</italic></td><td valign="top" align="center" rowspan="1" colspan="1">36</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="left" rowspan="1" colspan="1">11 (DBD, MR)</td><td valign="top" align="left" rowspan="1" colspan="1">25 (DBD, MR, CTD)</td><td valign="top" align="left" rowspan="1" colspan="1">Liu et al., <xref rid="B35" ref-type="bibr">2011</xref></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>Populus trichocarpa</italic></td><td valign="top" align="center" rowspan="1" colspan="1">39</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="left" rowspan="1" colspan="1">0</td><td valign="top" align="left" rowspan="1" colspan="1">35 (DBD, MR, CTD)</td><td valign="top" align="left" rowspan="1" colspan="1">Kalluri et al., <xref rid="B23" ref-type="bibr">2007</xref></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Banana</td><td valign="top" align="center" rowspan="1" colspan="1">47</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="left" rowspan="1" colspan="1">12 (DBD, MR)</td><td valign="top" align="left" rowspan="1" colspan="1">35 (DBD, MR, CTD)</td><td valign="top" align="left" rowspan="1" colspan="1">Hu et al., <xref rid="B21" ref-type="bibr">2015</xref></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>Brassica rapa</italic></td><td valign="top" align="center" rowspan="1" colspan="1">31</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="left" rowspan="1" colspan="1">4 (DBD, MR)</td><td valign="top" align="left" rowspan="1" colspan="1">27 (DBD, MR, CTD)</td><td valign="top" align="left" rowspan="1" colspan="1">Mun et al., <xref rid="B38" ref-type="bibr">2012</xref></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>Vitis vinifera</italic></td><td valign="top" align="center" rowspan="1" colspan="1">19</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="left" rowspan="1" colspan="1">2 (DBD, MR)</td><td valign="top" align="left" rowspan="1" colspan="1">17 (DBD, MR, CTD)</td><td valign="top" align="left" rowspan="1" colspan="1">Wan et al., <xref rid="B63" ref-type="bibr">2014</xref></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>Medicago truncatula</italic></td><td valign="top" align="center" rowspan="1" colspan="1">24</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="left" rowspan="1" colspan="1">14 (DBD, MR)</td><td valign="top" align="left" rowspan="1" colspan="1">10 (DBD, MR, CTD)</td><td valign="top" align="left" rowspan="1" colspan="1">Shen et al., <xref rid="B51" ref-type="bibr">2015a</xref></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>Gossypium raimondii</italic></td><td valign="top" align="center" rowspan="1" colspan="1">35</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="left" rowspan="1" colspan="1">7 (DBD, MR)</td><td valign="top" align="left" rowspan="1" colspan="1">28 (DBD, MR, CTD)</td><td valign="top" align="left" rowspan="1" colspan="1">Sun et al., <xref rid="B55" ref-type="bibr">2015</xref></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>Cucumis sativus</italic></td><td valign="top" align="center" rowspan="1" colspan="1">15</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="left" rowspan="1" colspan="1">1 (DBD, MR)</td><td valign="top" align="left" rowspan="1" colspan="1">14 (DBD, MR, CTD)</td><td valign="top" align="left" rowspan="1" colspan="1">Liu and Hu, <xref rid="B33" ref-type="bibr">2013</xref></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>Eucalyptus grandis</italic></td><td valign="top" align="center" rowspan="1" colspan="1">17</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="left" rowspan="1" colspan="1">3 (DBD, MR)</td><td valign="top" align="left" rowspan="1" colspan="1">14 (DBD, MR, CTD)</td><td valign="top" align="left" rowspan="1" colspan="1">Yu et al., <xref rid="B73" ref-type="bibr">2014</xref></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>Malus domestica</italic></td><td valign="top" align="center" rowspan="1" colspan="1">31</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="left" rowspan="1" colspan="1">8 (DBD, MR)</td><td valign="top" align="left" rowspan="1" colspan="1">23 (DBD, MR, CTD)</td><td valign="top" align="left" rowspan="1" colspan="1">Luo et al., <xref rid="B36" ref-type="bibr">2014</xref></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"><italic>Carica papaya L</italic>.</td><td valign="top" align="center" rowspan="1" colspan="1">11</td><td valign="top" align="center" rowspan="1" colspan="1">0</td><td valign="top" align="left" rowspan="1" colspan="1">3(DBD, MR)</td><td valign="top" align="left" rowspan="1" colspan="1">7 (DBD, MR, CTD)</td><td valign="top" align="left" rowspan="1" colspan="1">Liu et al., <xref rid="B31" ref-type="bibr">2015</xref></td></tr></tbody></table></table-wrap></sec><sec id="s3"><title>Activation, interaction, and regulatory mechanisms of <italic>ARFs</italic> in plants</title><p>The <italic>ARF</italic> genes encode proteins with full-length DBDs that may recognize and compete for target sites in promoters of auxin response genes (Tiwari et al., <xref rid="B57" ref-type="bibr">2003</xref>). Therefore, there has been increased interest to determining when and where these genes are expressed and what regulates their expression (Hagen and Guilfoyle, <xref rid="B18" ref-type="bibr">2002</xref>; Guilfoyle and Hagen, <xref rid="B16" ref-type="bibr">2007</xref>). It has long been recognized that ARFs directly bind to AuxREs in the promoters of auxin responsive genes through their DNA-binding domain (Wang and Estelle, <xref rid="B66" ref-type="bibr">2014</xref>). ARF binding to AuxREs in particular requires C-terminal amino acids (Guilfoyle and Hagen, <xref rid="B17" ref-type="bibr">2012</xref>). It has been proposed that the C-terminal domain enhances DNA binding by enabling ARF dimerization. Both ARF and Aux/IAA proteins contain conserved sequences near the C-terminus termed domains III and IV (Guilfoyle and Hagen, <xref rid="B17" ref-type="bibr">2012</xref>). These domains mediate ARF-ARF, ARF-Aux/IAA, and Aux/IAA-Aux/IAA interactions as determined by yeast two-hybrid and <bold>bimolecular fluorescence complementation assays</bold> (Korasick et al., <xref rid="B26" ref-type="bibr">2015</xref>). ARF regulation is well-studied, and a working model for ARF activation is now well-established (Figure <xref ref-type="fig" rid="F1">1</xref>) (Salehin et al., <xref rid="B48" ref-type="bibr">2015</xref>). At low auxin levels, Aux/IAA proteins form dimers with ARFs to inhibit ARF activity by recruiting the co-repressor TOPLESS (TPL), which results in the repression of auxin-responsive genes (Figure <xref ref-type="fig" rid="F1">1A</xref>) (Szemenyei et al., <xref rid="B56" ref-type="bibr">2008</xref>). At higher auxin levels, Aux/IAAs bind to the SCF<sup>TIR1∕AFB</sup> complex and subsequently become ubiquitinated and degraded by the 26S proteasome. The ARF is then released and can regulate the transcription of its target auxin response genes (Figure <xref ref-type="fig" rid="F1">1B</xref>) (Wang and Estelle, <xref rid="B66" ref-type="bibr">2014</xref>). Recent structural studies of ARFs have led to exciting new insight into the molecular function of the ARF-Aux/IAA pathway. Crystal structures showed that the C-terminal domains of ARF5 and ARF7 conform to a well-known PB1 domain that confers protein-protein interactions with other PB1 domain proteins through electrostatic contacts (Boer et al., <xref rid="B2" ref-type="bibr">2014</xref>; Guilfoyle, <xref rid="B15" ref-type="bibr">2015</xref>). Further experiments confirmed the importance of these charged amino acids in conferring ARF and Aux/IAA interactions as proposed by the crystal structure of the PB1 domain (Korasick et al., <xref rid="B26" ref-type="bibr">2015</xref>). In addition to the PB1 domain, a second protein-protein interaction module that functions in ARF-ARF dimerization and facilitates DNA binding has recently been revealed from structure-function analysis and saturating binding site selection on the ARF1 and ARF5 DNA binding domains (Boer et al., <xref rid="B2" ref-type="bibr">2014</xref>). These studies provide an atomic-level explanation for DNA-binding specificity in the auxin pathway.</p><boxed-text position="float"><label>KEY CONCEPT 3</label><caption><title>Bimolecular fluorescence complementation assays</title></caption><p>It is a technology typically used to validate protein interactions. It is based on the association of fluorescent protein fragments that are attached to components of the same macromolecular complex. Through the Visualization and analysis of the intensity and distribution of fluorescence in live cells, one can identify both the location and interaction partners of proteins of interest.</p></boxed-text><fig id="F1" position="float"><label>Figure 1</label><caption><p><bold>The key components in auxin perception and signaling in <italic><bold>Arabidopsis</bold></italic></bold>. ARF proteins contain a non-conserved AD or RD flanked by an N-terminal DBD (composed of a B3 domain, a dimerization domain: DD, and a Tudor-like ancillary domain within the C-terminal region of the flanking domain: FD) and a C-terminal PB1 domain (previously referred to as domain III/IV). Parts of the DD and FD are found both N-terminal and C-terminal to the B3 domain. In this pathway, the TRANSPORT INHIBITOR RESPONSE 1/AUXIN SIGNALING F-BOX proteins (TIR1/AFBs) are F-box proteins that, together with other proteins (ASK1, CUL1, RBX), form the ubiquitin protein ligase complex, SCF<sup>TIR1</sup>. At low auxin levels <bold>(A)</bold>, the Aux/IAA proteins form multimers with ARFs and recruit TPL to the chromatin. High levels of auxin <bold>(B)</bold> promote ubiquitination and degradation of Aux/IAAs through SCF<sup>TIR1∕AFB</sup> and the 26S proteasome (Kim et al., <xref rid="B25" ref-type="bibr">1997</xref>; Guilfoyle and Hagen, <xref rid="B16" ref-type="bibr">2007</xref>, <xref rid="B17" ref-type="bibr">2012</xref>; Szemenyei et al., <xref rid="B56" ref-type="bibr">2008</xref>; Boer et al., <xref rid="B2" ref-type="bibr">2014</xref>; Guilfoyle, <xref rid="B15" ref-type="bibr">2015</xref>; Korasick et al., <xref rid="B26" ref-type="bibr">2015</xref>; Salehin et al., <xref rid="B48" ref-type="bibr">2015</xref>).</p></caption><graphic xlink:href="fpls-07-00047-g0001"></graphic></fig><p>In addition to the interaction between themselves, the ARFs have also been reported to regulate and be regulated by other transcription factors (Wang and Estelle, <xref rid="B66" ref-type="bibr">2014</xref>). A recent study showed that a <italic>MYB</italic> transcription factor (<italic>MYB77</italic>) interacts with the ARF7 protein and that this interaction results in a strong reduction in lateral root numbers in <italic>Arabidopsis</italic> (Shin et al., <xref rid="B53" ref-type="bibr">2007</xref>). Moreover, it has been shown that the bHLH transcription factor BIGPETALp (BPEp) interacts with ARF8 to effect petal growth. This interaction is mediated through the BPEp C-terminal domain and the C-terminal domain of ARF8 (Varaud et al., <xref rid="B61" ref-type="bibr">2011</xref>). The <italic>Arabidopsis</italic> BREVIS RADIX (BRX) transcriptional co-regulator interacts with domain III/IV of ARF5 in yeast two-hybrid assays as well as <italic>in vitro</italic> pull-down assays, and this interaction enhances the transcriptional activation potential of this ARF (Guilfoyle and Hagen, <xref rid="B17" ref-type="bibr">2012</xref>). In another recent report, HaIAA27 was shown to repress the transcriptional activation of the heat shock transcription factor HaHSFA9 in sunflower to repress its activity during seed development. As in the case of the ARFs, auxin also acts to relieve repression of the HaHSFA9 protein (Carranco et al., <xref rid="B3" ref-type="bibr">2010</xref>). Recent data also suggest that post-translational modifications of ARFs may constitute another layer of regulation of auxin signaling outputs (Wang and Estelle, <xref rid="B66" ref-type="bibr">2014</xref>; Hill, <xref rid="B20" ref-type="bibr">2015</xref>). Phosphorylation of ARF7 and ARF19 by BRASSINOSTEROID-INSENSITIVE2 (BIN2) can potentiate auxin signaling output during lateral root organogenesis (Cho et al., <xref rid="B5" ref-type="bibr">2014</xref>). Meanwhile, other previous report shows that BIN2 also phosphorylates ARF2 (Vert et al., <xref rid="B62" ref-type="bibr">2008</xref>). These data suggest that ARF phosphorylation suppresses their interaction with Aux/IAAs, thus enhancing DNA binding and transcriptional activity. In addition, there is a growing body of evidence on the posttranscriptional regulation of ARF transcript abundance by miRNA and <bold>transacting-small interfering RNAs (ta-siRNA)</bold>. While <italic>ARF6</italic> and <italic>ARF8</italic> are targets of miR167 and <italic>ARF10, ARF16</italic>, and <italic>ARF17</italic> are targeted by miR160, <italic>ARF2, ARF3</italic>, and <italic>ARF4</italic> are targets of TAS3 ta-siRNAs in <italic>Arabidopsis</italic> (Rhoades et al., <xref rid="B45" ref-type="bibr">2002</xref>; Williams et al., <xref rid="B69" ref-type="bibr">2005</xref>; Guilfoyle and Hagen, <xref rid="B16" ref-type="bibr">2007</xref>; Lin et al., <xref rid="B29" ref-type="bibr">2015</xref>).</p><boxed-text position="float"><label>KEY CONCEPT 4</label><caption><title>Transacting-small interfering RNAs (Ta-siRNAs)</title></caption><p>Ta-siRNAs are form of small interfering RNA (siRNA) that represses gene expression through post-transcriptional gene silencing in land plants. They are transcribed from the genome to form a polyadenylated, double-stranded segment of RNA that gets processed further, resulting in a segment of RNA that is 21-nucleotides long. These segments are incorporated into the RNA-induced Silencing Complex and direct the cleavage of target mRNA.</p></boxed-text></sec><sec id="s4"><title>Roles of <italic>ARFs</italic> in plant growth and developmental processes</title><p>The <italic>Arabidopsis</italic> genome encodes 23 ARF proteins (Rademacher et al., <xref rid="B44" ref-type="bibr">2011</xref>) and genetic analyses have shown that individual ARFs control distinct developmental processes based on their loss-of-function mutant phenotypes (Guilfoyle and Hagen, <xref rid="B16" ref-type="bibr">2007</xref>; Rademacher et al., <xref rid="B43" ref-type="bibr">2012</xref>). Although ARFs appear to have unique functions in some contexts, they display overlapping functions in others. For example, both <italic>ARF1</italic> and <italic>ARF2</italic> control leaf senescence and floral organ abscission in <italic>Arabidopsis</italic> (Ellis et al., <xref rid="B11" ref-type="bibr">2005</xref>), while <italic>ARF3</italic> interacts with KANADI proteins to form a functional complex essential for leaf polarity specification (Kelley et al., <xref rid="B24" ref-type="bibr">2012</xref>). A recent study indicated that <italic>ARF3</italic> integrates the functions of <italic>AGAMOUS</italic> (<italic>AG</italic>) and <italic>APETALA2</italic> (<italic>AP2</italic>) in floral meristem determinacy (Liu et al., <xref rid="B34" ref-type="bibr">2014b</xref>), while <italic>ARF4</italic> has been studied primarily for its role in organ polarity (Hunter et al., <xref rid="B22" ref-type="bibr">2006</xref>). However, the <italic>arf3arf4</italic> double mutant plant has reduced abaxial identity in all lateral organs, including leaves (Pekker et al., <xref rid="B41" ref-type="bibr">2005</xref>; Finet et al., <xref rid="B13" ref-type="bibr">2010</xref>). <italic>ARF5</italic> is critically required for embryonic root and flower formation (Hardtke and Berleth, <xref rid="B19" ref-type="bibr">1998</xref>) and embryo patterning and vasculature defects observed in <italic>arf5</italic> mutants are enhanced in <italic>arf5arf7</italic> double mutants (Hardtke and Berleth, <xref rid="B19" ref-type="bibr">1998</xref>). <italic>ARF8</italic> is reported to regulate fertilization and fruit development (Goetz et al., <xref rid="B14" ref-type="bibr">2006</xref>), and <italic>ARF6</italic> and <italic>ARF8</italic> act redundantly in flower maturation (Finet et al., <xref rid="B13" ref-type="bibr">2010</xref>). <italic>ARF19</italic> and <italic>ARF7</italic> act redundantly with in controlling leaf expansion and lateral root growth (Wilmoth et al., <xref rid="B70" ref-type="bibr">2005</xref>). While no phenotypic defects were reported for <italic>arf10</italic> or <italic>arf16</italic> single mutants (Okushima et al., <xref rid="B40" ref-type="bibr">2005</xref>), <italic>arf10arf16</italic> double mutants show a strong auxin phenotype that results in the absence of lateral root formation, which is not observed in neither the <italic>arf10</italic> or <italic>arf16</italic> single mutant (Wang et al., <xref rid="B65" ref-type="bibr">2005</xref>).</p><p>In the case of tomato, genetic studies have shown that the mechanism of <italic>ARF</italic> signaling is different to that of <italic>Arabidopsis</italic>. A total of 21 putative functional <italic>SlARFs</italic> have been identified in tomato (Zouine et al., <xref rid="B76" ref-type="bibr">2014</xref>). Although, <italic>SlARF3</italic> RNAi lines do not display phenotypes such as floral organogenes or developmental timing changes (Sessions et al., <xref rid="B50" ref-type="bibr">1997</xref>), <italic>SlARF3</italic> plays multiple roles in tomato development and is involved in the formation of epidermal cells and trichomes (Zhang et al., <xref rid="B75" ref-type="bibr">2015b</xref>). The functional analysis of <italic>SlARF9</italic> indicated that it regulates cell division during early tomato fruit development (DeJong et al., <xref rid="B8" ref-type="bibr">2015</xref>). A recent study confirmed that down-regulation of <italic>ARF6</italic> and <italic>ARF8</italic> by mi167 leads to floral development defects and female sterility in tomatoes. These results indicate that <italic>ARF6</italic> and <italic>ARF8</italic> have conserved roles in controlling growth and development of vegetative and flower organs in dicots (Liu et al., <xref rid="B32" ref-type="bibr">2014a</xref>). <italic>SlARF7</italic> acts as a negative regulator of fruit set until pollination and fertilization have taken place and moderates the auxin response during fruit growth in tomatoes (de Jong et al., <xref rid="B6" ref-type="bibr">2009</xref>). Meanwhile, <italic>SlARF7</italic> mediates cross-talk between auxin and gibberellin signaling during tomato fruit set and development (de Jong et al., <xref rid="B7" ref-type="bibr">2011</xref>). Interestingly, <italic>SlARF4</italic> is involved in the control of sugar metabolism during tomato fruit development (Sagar et al., <xref rid="B47" ref-type="bibr">2013</xref>). In soybeans, the miR167-directed regulation of <italic>GmARF8a</italic> and <italic>GmARF8b</italic> is required for nodulation and lateral root development (Wang et al., <xref rid="B68" ref-type="bibr">2015</xref>). In rice, <italic>OsARF16</italic> and <italic>OsARF12</italic> are required for iron deficiency response by regulating auxin redistribution (Wang et al., <xref rid="B67" ref-type="bibr">2014</xref>; Shen et al., <xref rid="B52" ref-type="bibr">2015b</xref>). <italic>OsARF3</italic> mediates the auxin response during de novo shoot regeneration (Cheng et al., <xref rid="B4" ref-type="bibr">2013</xref>). OsARF19 controls rice leaf angles through positively regulating <italic>OsGH3-5</italic> and <italic>brassinosteroid insensitive 1</italic> (<italic>OsBRI1</italic>) in rice (Zhang et al., <xref rid="B74" ref-type="bibr">2015a</xref>).</p></sec><sec id="s5"><title>Conclusion and perspectives</title><p>During the last 10 years, our understanding of <italic>ARF</italic> regulatory mechanism and their role during model plant growth and development has been greatly improved by forward and reverse genetic approaches. Nonetheless, there are still many gaps in our knowledge and we lack a deep understanding of these regulatory processes. For example, it is still not clear how repressors of <italic>ARFs</italic> regulate gene repression and how other transcription factors and signaling proteins interact with ARF proteins. However, a larger number of candidate genes that are regulated by <italic>ARFs</italic> have been identified both experimentally and through bioinformatics analysis in recent years. Therefore, it will be interesting to understand the function of these candidate genes and regulatory mechanism of some important ARF proteins. In addition, our knowledge of <italic>ARFs</italic> in plant species beyond model plants (typically <italic>Arabidopsis</italic>) is very limited. The great challenge will be to integrate knowledge about ARF regulation of different developmental processes across in plants, and to understand how these processes work in different plant species.</p></sec><sec id="s6"><title>Author contributions</title><p>JZ, SL, and ZX wrote the paper. CH provided some suggestions for the paper.</p><sec><title>Conflict of interest statement</title><p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p></sec></sec></body><back><ack><p>This research was supported financially by the National Natural Science Foundation of China (grant nos. 31130046, 31471863, 31360469, and 31372046), the Fundamental Research Funds for the Central Universities (2013PY083) and the International Foundation for Science No. C/5148-2.</p></ack><ref-list><title>References</title><ref id="B1"><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Blanc</surname><given-names>G.</given-names></name><name><surname>Hokamp</surname><given-names>K.</given-names></name><name><surname>Wolfe</surname><given-names>K. 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(<year>2014</year>). <article-title>Characterization of the tomato <italic>ARF</italic> gene family uncovers a multi-levels post-transcriptional regulation including alternative splicing</article-title>. <source>PLoS ONE</source><volume>9</volume>:<fpage>e84203</fpage>. <pub-id pub-id-type="doi">10.1371/journal.pone.0084203</pub-id><pub-id pub-id-type="pmid">24427281</pub-id></mixed-citation></ref></ref-list><bio id="d36e5183"><p><inline-graphic xlink:href="fpls-07-00047-i0001.gif"></inline-graphic><bold>Jin-Zhi Zhang</bold> Dr. Zhang engaged in research work at the Institute for Huazhong Agricultural University, China. He holds a Master and Ph.D. from Huazhong Agricultural University in the area of fruit molecular biology. After receiving his Ph.D., He worked as a visiting scholar investigates auxin biosynthesis and its regulation in the section of cell and developmental biology at University of California at San Diego. Zhang92s work utilizes an early-flowering mutant of citrus as a model system to investigate the developmental genetic mechanisms that control how flowers are formed and elaborated in past year. Now, he is also engaged in understanding the transcriptional mechanisms and signaling processes that control fruit development.</p></bio></back></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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