A model worker: Multifaceted modulation of AUXIN RESPONSE FACTOR3 orchestrates plant reproductive phases

The key phytohormone auxin is involved in practically every aspect of plant growth and development. Auxin regulates these processes by controlling gene expression through functionally distinct AUXIN RESPONSE FACTORs (ARFs). As a noncanonical ARF, ARF3/ETTIN (ETT) mediates auxin responses to orchestrate multiple developmental processes during the reproductive phase. The arf3 mutation has pleiotropic effects on reproductive development, causing abnormalities in meristem homeostasis, floral determinacy, phyllotaxy, floral organ patterning, gynoecium morphogenesis, ovule development, and self-incompatibility. The importance of ARF3 is also reflected in its precise regulation at the transcriptional, posttranscriptional, translational, and epigenetic levels. Recent studies have shown that ARF3 controls dynamic shoot apical meristem (SAM) maintenance in a non-cell autonomous manner. Here, we summarize the hierarchical regulatory mechanisms by which ARF3 is regulated and the diverse roles of ARF3 regulating developmental processes during the reproductive phase.

[1]  A. Lanctot At home and away: A mobile transcription factor regulates meristem development in discrete spatial domains , 2022, Plant physiology.

[2]  Kecheng Zhang,et al.  Cell- and non-cell-autonomous AUXIN RESPONSE FACTOR3 controls meristem proliferation and phyllotactic patterns. , 2022, Plant physiology.

[3]  Y. Machida,et al.  Roles of ASYMMETRIC LEAVES2 (AS2) and Nucleolar Proteins in the Adaxial–Abaxial Polarity Specification at the Perinucleolar Region in Arabidopsis , 2020, International journal of molecular sciences.

[4]  Xigang Liu,et al.  Same Actor in Different Stages: Genes in Shoot Apical Meristem Maintenance and Floral Meristem Determinacy in Arabidopsis , 2020, Frontiers in Ecology and Evolution.

[5]  Yuehui He,et al.  Roles of Brassinosteroids in Plant Reproduction , 2020, International journal of molecular sciences.

[6]  Teva Vernoux,et al.  WUSCHEL acts as an auxin response rheostat to maintain apical stem cells in Arabidopsis , 2019, Nature Communications.

[7]  S. Kepinski,et al.  Direct ETTIN-auxin interaction controls chromatin states in gynoecium development , 2019, bioRxiv.

[8]  Erlei Shang,et al.  Control of floral stem cell activity in Arabidopsis , 2019, Plant signaling & behavior.

[9]  Nobutoshi Yamaguchi,et al.  The Roles of Plant Hormones and Their Interactions with Regulatory Genes in Determining Meristem Activity , 2019, International journal of molecular sciences.

[10]  Xiujuan Yang,et al.  Establishing a framework for female germline initiation in the plant ovule. , 2019, Journal of experimental botany.

[11]  Matthew R. Tucker,et al.  Revisiting the Female Germline and Its Expanding Toolbox. , 2019, Trends in plant science.

[12]  Nobutoshi Yamaguchi,et al.  When to stop: an update on molecular mechanisms of floral meristem termination. , 2019, Journal of experimental botany.

[13]  Neetu Verma Transcriptional regulation of anther development in Arabidopsis. , 2019, Gene.

[14]  Matthew R. Tucker,et al.  Translating auxin responses into ovules, seeds and yield: Insight from Arabidopsis and the cereals. , 2019, Journal of integrative plant biology.

[15]  J. Lohmann,et al.  From signals to stem cells and back again , 2018, Current opinion in plant biology.

[16]  B. Usadel,et al.  The Multifaceted Role of Pectin Methylesterase Inhibitors (PMEIs) , 2018, International journal of molecular sciences.

[17]  A. Boudaoud,et al.  Evidence for the Regulation of Gynoecium Morphogenesis by ETTIN via Cell Wall Dynamics1 , 2018, Plant Physiology.

[18]  P. Mas,et al.  Auxin sensing is a property of an unstructured domain in the Auxin Response Factor ETTIN of Arabidopsis thaliana , 2018, Scientific Reports.

[19]  Jian‐Kang Zhu,et al.  Dynamics and function of DNA methylation in plants , 2018, Nature Reviews Molecular Cell Biology.

[20]  C. Reutenauer,et al.  Golden ratio and phyllotaxis, a clear mathematical link , 2018, Journal of mathematical biology.

[21]  Y. An,et al.  Dynamic DNA Methylation in Plant Growth and Development , 2018, International journal of molecular sciences.

[22]  Y. Machida,et al.  Arabidopsis Zinc-Finger-Like Protein ASYMMETRIC LEAVES2 (AS2) and Two Nucleolar Proteins Maintain Gene Body DNA Methylation in the Leaf Polarity Gene ETTIN (ARF3) , 2018, Plant & cell physiology.

[23]  Z. D. Zhang,et al.  AUXIN RESPONSE FACTOR3 plays distinct role during early flower development , 2018, Plant signaling & behavior.

[24]  Yuling Jiao,et al.  AUXIN RESPONSE FACTOR3 Regulates Floral Meristem Determinacy by Repressing Cytokinin Biosynthesis and Signaling , 2018, Plant Cell.

[25]  Ken-ichiro Hayashi,et al.  Feedback from Lateral Organs Controls Shoot Apical Meristem Growth by Modulating Auxin Transport. , 2018, Developmental cell.

[26]  D. Weijers,et al.  Auxin Response Factors — output control in auxin biology , 2017, bioRxiv.

[27]  M. Trick,et al.  Auxin-Induced Modulation of ETTIN Activity Orchestrates Gene Expression in Arabidopsis[OPEN] , 2017, Plant Cell.

[28]  Xuemei Chen,et al.  The THO Complex Non-Cell-Autonomously Represses Female Germline Specification through the TAS3-ARF3 Module , 2017, Current Biology.

[29]  M. Heisler,et al.  Auxin Acts through MONOPTEROS to Regulate Plant Cell Polarity and Pattern Phyllotaxis , 2016, Current Biology.

[30]  Antonio Serrano-Mislata,et al.  Control of Oriented Tissue Growth through Repression of Organ Boundary Genes Promotes Stem Morphogenesis , 2016, Developmental cell.

[31]  J. Friml,et al.  A noncanonical auxin-sensing mechanism is required for organ morphogenesis in Arabidopsis , 2016, Genes & development.

[32]  Xuemei Chen,et al.  FAR-RED ELONGATED HYPOCOTYL3 activates SEPALLATA2 but inhibits CLAVATA3 to regulate meristem determinacy and maintenance in Arabidopsis , 2016, Proceedings of the National Academy of Sciences.

[33]  J. Chandler Auxin response factors. , 2016, Plant, cell & environment.

[34]  D. Wagner,et al.  Transcriptional Responses to the Auxin Hormone. , 2016, Annual review of plant biology.

[35]  Chun-Gen Hu,et al.  A Review of Auxin Response Factors (ARFs) in Plants , 2016, Front. Plant Sci..

[36]  S. de Folter,et al.  Hormonal control of the development of the gynoecium. , 2016, Current opinion in plant biology.

[37]  F. Nogueira,et al.  The ASYMMETRIC LEAVES Complex Employs Multiple Modes of Regulation to Affect Adaxial-Abaxial Patterning and Leaf Complexity[OPEN] , 2015, Plant Cell.

[38]  R. Franks,et al.  Auxin and cytokinin act during gynoecial patterning and the development of ovules from the meristematic medial domain , 2015, Wiley interdisciplinary reviews. Developmental biology.

[39]  M. Herrero,et al.  Transition from two to one integument in Prunus species: expression pattern of INNER NO OUTER (INO), ABERRANT TESTA SHAPE (ATS) and ETTIN (ETT). , 2015, The New phytologist.

[40]  D. Gonzalez,et al.  TCP15 modulates cytokinin and auxin responses during gynoecium development in Arabidopsis. , 2015, The Plant journal : for cell and molecular biology.

[41]  J. Lohmann,et al.  Arabidopsis HECATE genes function in phytohormone control during gynoecium development , 2015, Development.

[42]  Y. Machida,et al.  The complex of ASYMMETRIC LEAVES (AS) proteins plays a central role in antagonistic interactions of genes for leaf polarity specification in Arabidopsis , 2015, Wiley interdisciplinary reviews. Developmental biology.

[43]  Xigang Liu,et al.  Epigenetic Mechanisms Are Critical for the Regulation of WUSCHEL Expression in Floral Meristems1 , 2015, Plant Physiology.

[44]  Toshiro Ito,et al.  Regulation of floral stem cell termination in Arabidopsis , 2015, Front. Plant Sci..

[45]  J. Kieber,et al.  The Yin-Yang of Hormones: Cytokinin and Auxin Interactions in Plant Development , 2015, Plant Cell.

[46]  T. Guilfoyle The PB1 Domain in Auxin Response Factor and Aux/IAA Proteins: A Versatile Protein Interaction Module in the Auxin Response[OPEN] , 2015, Plant Cell.

[47]  Laila Moubayidin,et al.  Dynamic Control of Auxin Distribution Imposes a Bilateral-to-Radial Symmetry Switch during Gynoecium Development , 2014, Current Biology.

[48]  Xuemei Chen,et al.  AUXIN RESPONSE FACTOR 3 integrates the functions of AGAMOUS and APETALA2 in floral meristem determinacy. , 2014, The Plant journal : for cell and molecular biology.

[49]  Madelaine E Bartlett,et al.  Meristem identity and phyllotaxis in inflorescence development , 2014, Front. Plant Sci..

[50]  Zhongchi Liu,et al.  A model for an early role of auxin in Arabidopsis gynoecium morphogenesis , 2014, Front. Plant Sci..

[51]  R. Yu,et al.  Molecule mechanism of stem cells in Arabidopsis thaliana , 2014, Pharmacognosy reviews.

[52]  Dhinesh Kumar,et al.  Transcription factor-mediated cell-to-cell signalling in plants. , 2014, Journal of experimental botany.

[53]  Wolfgang Busch,et al.  A regulatory framework for shoot stem cell control integrating metabolic, transcriptional, and phytohormone signals. , 2014, Developmental cell.

[54]  Iain W. Manfield,et al.  Structural Basis for DNA Binding Specificity by the Auxin-Dependent ARF Transcription Factors , 2014, Cell.

[55]  S. Masiero,et al.  An integrative model of the control of ovule primordia formation. , 2013, The Plant journal : for cell and molecular biology.

[56]  Y. Eshed,et al.  Dual regulation of ETTIN (ARF3) gene expression by AS1-AS2, which maintains the DNA methylation level, is involved in stabilization of leaf adaxial-abaxial partitioning in Arabidopsis , 2013, Development.

[57]  Y. Machida,et al.  Meta-Analyses of Microarrays of Arabidopsis asymmetric leaves1 (as1), as2 and Their Modifying Mutants Reveal a Critical Role for the ETT Pathway in Stabilization of Adaxial–Abaxial Patterning and Cell Division During Leaf Development , 2013, Plant & cell physiology.

[58]  Xuemei Chen,et al.  POWERDRESS and Diversified Expression of the MIR172 Gene Family Bolster the Floral Stem Cell Network , 2013, PLoS genetics.

[59]  T. Okabe Systematic variations in divergence angle. , 2012, Journal of theoretical biology.

[60]  N. Raikhel,et al.  Arabidopsis ribosomal proteins control developmental programs through translational regulation of auxin response factors , 2012, Proceedings of the National Academy of Sciences.

[61]  J. Nasrallah,et al.  Non-cell-autonomous regulation of crucifer self-incompatibility by Auxin Response Factor ARF3 , 2012, Proceedings of the National Academy of Sciences.

[62]  Qi Xie,et al.  Pattern of Auxin and Cytokinin Responses for Shoot Meristem Induction Results from the Regulation of Cytokinin Biosynthesis by AUXIN RESPONSE FACTOR31[W][OA] , 2012, Plant Physiology.

[63]  E. Benková,et al.  The Transcription Factors BEL1 and SPL Are Required for Cytokinin and Auxin Signaling During Ovule Development in Arabidopsis[W] , 2012, Plant Cell.

[64]  C. Gasser,et al.  ETTIN (ARF3) physically interacts with KANADI proteins to form a functional complex essential for integument development and polarity determination in Arabidopsis , 2012, Development.

[65]  C. D. de Oliveira,et al.  A combinatorial TIR1/AFB-Aux/IAA co-receptor system for differential sensing of auxin , 2012, Nature chemical biology.

[66]  Yuval Eshed,et al.  The Arabidopsis O-Linked N-Acetylglucosamine Transferase SPINDLY Interacts with Class I TCPs to Facilitate Cytokinin Responses in Leaves and Flowers[C][W] , 2012, Plant Cell.

[67]  A. Koltunow,et al.  The Female Gametophyte , 2011, The arabidopsis book.

[68]  T. Girin,et al.  INDEHISCENT and SPATULA Interact to Specify Carpel and Valve Margin Tissue and Thus Promote Seed Dispersal in Arabidopsis[W] , 2011, Plant Cell.

[69]  Xuemei Chen,et al.  AGAMOUS Terminates Floral Stem Cell Maintenance in Arabidopsis by Directly Repressing WUSCHEL through Recruitment of Polycomb Group Proteins[W] , 2011, Plant Cell.

[70]  B. Snel,et al.  Arabidopsis PLETHORA Transcription Factors Control Phyllotaxis , 2011, Current Biology.

[71]  Xuemei Chen,et al.  ARGONAUTE10 and ARGONAUTE1 Regulate the Termination of Floral Stem Cells through Two MicroRNAs in Arabidopsis , 2011, PLoS genetics.

[72]  Edwards Allen,et al.  miRNAs in the biogenesis of trans-acting siRNAs in higher plants. , 2010, Seminars in cell & developmental biology.

[73]  Krystyna A. Kelly,et al.  Putative Arabidopsis THO/TREX mRNA export complex is involved in transgene and endogenous siRNA biosynthesis , 2010, Proceedings of the National Academy of Sciences.

[74]  Toshiro Ito,et al.  Floral stem cells: from dynamic balance towards termination. , 2010, Biochemical Society transactions.

[75]  M. Crespi,et al.  miR390, Arabidopsis TAS3 tasiRNAs, and Their AUXIN RESPONSE FACTOR Targets Define an Autoregulatory Network Quantitatively Regulating Lateral Root Growth[W] , 2010, Plant Cell.

[76]  F. Bao,et al.  SEUSS and SEUSS-LIKE Transcriptional Adaptors Regulate Floral and Embryonic Development in Arabidopsis1[C][W][OA] , 2009, Plant Physiology.

[77]  John F. Atkins,et al.  A profusion of upstream open reading frame mechanisms in polyamine-responsive translational regulation , 2009, Nucleic acids research.

[78]  K. Ng,et al.  AGAMOUS Controls GIANT KILLER, a Multifunctional Chromatin Modifier in Reproductive Organ Patterning and Differentiation , 2009, PLoS biology.

[79]  K. Ng,et al.  A timing mechanism for stem cell maintenance and differentiation in the Arabidopsis floral meristem. , 2009, Genes & development.

[80]  Anika Wiese-Klinkenberg,et al.  Sucrose Control of Translation Mediated by an Upstream Open Reading Frame-Encoded Peptide1[W][OA] , 2009, Plant Physiology.

[81]  F. Nogueira,et al.  Pattern formation via small RNA mobility. , 2009, Genes & development.

[82]  J. Bowman,et al.  REBELOTE, SQUINT, and ULTRAPETALA1 Function Redundantly in the Temporal Regulation of Floral Meristem Termination in Arabidopsis thaliana[W] , 2008, The Plant Cell Online.

[83]  Queenie K.-G. Tan,et al.  An Arabidopsis F-box protein acts as a transcriptional co-factor to regulate floral development , 2008, Development.

[84]  S. Nelson,et al.  Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning , 2008, Nature.

[85]  Xuemei Chen,et al.  miR172 regulates stem cell fate and defines the inner boundary of APETALA3 and PISTILLATA expression domain in Arabidopsis floral meristems. , 2007, The Plant journal : for cell and molecular biology.

[86]  E. Mellerowicz,et al.  New insights into pectin methylesterase structure and function. , 2007, Trends in plant science.

[87]  Patrick Laufs,et al.  Plants expressing a miR164-resistant CUC2 gene reveal the importance of post-meristematic maintenance of phyllotaxy in Arabidopsis , 2007, Development.

[88]  M. Pellegrini,et al.  Genome-wide High-Resolution Mapping and Functional Analysis of DNA Methylation in Arabidopsis , 2006, Cell.

[89]  Gang Wu,et al.  Trans-acting siRNA-mediated repression of ETTIN and ARF4 regulates heteroblasty in Arabidopsis , 2006, Development.

[90]  G. Sandberg,et al.  STY1 regulates auxin homeostasis and affects apical-basal patterning of the Arabidopsis gynoecium. , 2006, The Plant journal : for cell and molecular biology.

[91]  J. Carrington,et al.  Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA Affects Developmental Timing and Patterning in Arabidopsis , 2006, Current Biology.

[92]  R. Martienssen,et al.  Specification of Leaf Polarity in Arabidopsis via the trans-Acting siRNA Pathway , 2006, Current Biology.

[93]  J. Bowman,et al.  ABERRANT TESTA SHAPE encodes a KANADI family member, linking polarity determination to separation and growth of Arabidopsis ovule integuments. , 2006, The Plant journal : for cell and molecular biology.

[94]  A. Roeder,et al.  Fruit Development in Arabidopsis , 2006, The arabidopsis book.

[95]  P. Prusinkiewicz,et al.  A plausible model of phyllotaxis , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[96]  T. Wada,et al.  The Arabidopsis STV1 Protein, Responsible for Translation Reinitiation, Is Required for Auxin-Mediated Gynoecium Patterningw⃞ , 2005, The Plant Cell Online.

[97]  Y. Eshed,et al.  Auxin Response Factors Mediate Arabidopsis Organ Asymmetry via Modulation of KANADI Activityw⃞ , 2005, The Plant Cell Online.

[98]  H. Vaucheret MicroRNA-Dependent Trans-Acting siRNA Production , 2005, Science's STKE.

[99]  J. Fletcher,et al.  Molecular mechanisms of flower development: an armchair guide , 2005, Nature Reviews Genetics.

[100]  Karen S. Osmont,et al.  A database analysis method identifies an endogenous trans-acting short-interfering RNA that targets the Arabidopsis ARF2, ARF3, and ARF4 genes. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[101]  J. Ecker,et al.  Functional Genomic Analysis of the AUXIN RESPONSE FACTOR Gene Family Members in Arabidopsis thaliana: Unique and Overlapping Functions of ARF7 and ARF19w⃞ , 2005, The Plant Cell Online.

[102]  T. Koshiba,et al.  Disruption and overexpression of auxin response factor 8 gene of Arabidopsis affect hypocotyl elongation and root growth habit, indicating its possible involvement in auxin homeostasis in light condition. , 2004, The Plant journal : for cell and molecular biology.

[103]  Gang Wu,et al.  SGS3 and SGS2/SDE1/RDR6 are required for juvenile development and the production of trans-acting siRNAs in Arabidopsis. , 2004, Genes & development.

[104]  P. Zambryski,et al.  The role of SEUSS in auxin response and floral organ patterning , 2004, Development.

[105]  T. Vision,et al.  Contrasting Modes of Diversification in the Aux/IAA and ARF Gene Families1[w] , 2004, Plant Physiology.

[106]  G. Jürgens,et al.  Local, Efflux-Dependent Auxin Gradients as a Common Module for Plant Organ Formation , 2003, Cell.

[107]  A. Groover,et al.  Phyllotactic pattern and stem cell fate are determined by the Arabidopsis homeobox gene BELLRINGER , 2003, Development.

[108]  J. Long,et al.  STY1 and STY2 promote the formation of apical tissues during Arabidopsis gynoecium development. , 2002, Development.

[109]  Kevin Struhl,et al.  TREX is a conserved complex coupling transcription with messenger RNA export , 2002, Nature.

[110]  G. Hagen,et al.  Auxin Response Factors , 2001, Journal of Plant Growth Regulation.

[111]  J. Bowman,et al.  Establishment of polarity in lateral organs of plants , 2001, Current Biology.

[112]  D. Weigel,et al.  A Molecular Link between Stem Cell Regulation and Floral Patterning in Arabidopsis , 2001, Cell.

[113]  M. Lenhard,et al.  Termination of Stem Cell Maintenance in Arabidopsis Floral Meristems by Interactions between WUSCHEL and AGAMOUS , 2001, Cell.

[114]  R. Kerstetter,et al.  KANADI regulates organ polarity in Arabidopsis , 2001, Nature.

[115]  M. Heisler,et al.  SPATULA, a gene that controls development of carpel margin tissues in Arabidopsis, encodes a bHLH protein. , 2001, Development.

[116]  Trevor Lithgow,et al.  A protein complex containing Tho2, Hpr1, Mft1 and a novel protein, Thp2, connects transcription elongation with mitotic recombination in Saccharomyces cerevisiae , 2000, The EMBO journal.

[117]  J. Nemhauser,et al.  Auxin and ETTIN in Arabidopsis gynoecium morphogenesis. , 2000, Development.

[118]  J. Bowman,et al.  Distinct Mechanisms Promote Polarity Establishment in Carpels of Arabidopsis , 1999, Cell.

[119]  J L Bowman,et al.  Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. , 1999, Development.

[120]  D. Shibata,et al.  FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with a zinc finger and HMG-related domains. , 1999, Genes & development.

[121]  J. Nemhauser,et al.  ETTIN patterns the Arabidopsis floral meristem and reproductive organs. , 1997, Development.

[122]  J. Nemhauser,et al.  TOUSLED participates in apical tissue formation during gynoecium development in Arabidopsis. , 1997, The Plant cell.

[123]  Detlef Weigel,et al.  A LEAFY co-regulator encoded by UNUSUAL FLORAL ORGANS , 1997, Current Biology.

[124]  S. Dellaporta,et al.  Demethylation-Induced Developmental Pleiotropy in Arabidopsis , 1996, Science.

[125]  P. Zambryski,et al.  Arabidopsis gynoecium structure in the wild and in ettin mutants. , 1995, Development.

[126]  K. Feldmann,et al.  The Tousled gene in A. thaliana encodes a protein kinase homolog that is required for leaf and flower development , 1993, Cell.

[127]  E. Coen,et al.  The war of the whorls: genetic interactions controlling flower development , 1991, Nature.

[128]  J L Bowman,et al.  Genes directing flower development in Arabidopsis. , 1989, The Plant cell.

[129]  F. Wellmer,et al.  Molecular regulation of flower development. , 2019, Current topics in developmental biology.

[130]  J. Nasrallah Self-incompatibility in the Brassicaceae: Regulation and mechanism of self-recognition. , 2019, Current topics in developmental biology.

[131]  S. Simonini,et al.  Female reproductive organ formation: A multitasking endeavor. , 2019, Current topics in developmental biology.

[132]  Justin N. Vaughn,et al.  Regulation of plant translation by upstream open reading frames. , 2014, Plant science : an international journal of experimental plant biology.

[133]  M. Yoshikawa,et al.  Biogenesis of trans-acting siRNAs, endogenous secondary siRNAs in plants. , 2013, Genes & genetic systems.

[134]  C. Scutt,et al.  Evolution of the ARF gene family in land plants: old domains, new tricks. , 2013, Molecular biology and evolution.

[135]  Christophe Godin,et al.  The auxin signalling network translates dynamic input into robust patterning at the shoot apex , 2011, Molecular systems biology.

[136]  Mariana Benítez,et al.  Flower Development , 2010, The arabidopsis book.

[137]  Heino Hellwig,et al.  Phyllotaxis , 2010 .

[138]  Didier Reinhardt,et al.  Regulation of phyllotaxis. , 2005, The International journal of developmental biology.

[139]  J. Bowman,et al.  Molecular genetics of gynoecium development in Arabidopsis. , 1999, Current topics in developmental biology.

[140]  G. Jürgens,et al.  The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. , 1996, Development.