Arabidopsis LEAFY COTYLEDON1 Mediates Postembryonic Development via Interacting with PHYTOCHROME-INTERACTING FACTOR4[OPEN]

LEC1 interacts with PIF4 to mediate postembryonic development through coregulating expression of hypocotyl elongation-related genes via direct binding to the G-box element in the dark. Plants undergo postembryonic growth during the developmental transition from germinating seeds to seedlings. Recent studies suggest LEAFY COTYLEDON1 (LEC1), initially identified as a central regulator in embryogenesis and seed maturation in Arabidopsis thaliana, plays a distinct role in postembryonic development. However, the mechanism by which LEC1 regulates nonembryonic development still remains elusive. In this study, we observed etiolation-related phenotypes in early seedlings of lec1 mutants and inducible LEC1 overexpression transgenic lines. Consistent with this, LEC1 promotes the expression of hypocotyl elongation-related genes in a darkness-dependent manner in spite of the comparable LEC1 transcript levels in the light- and dark-grown seedlings. Furthermore, we show that LEC1 interacts with PHYTOCHROME-INTERACTING FACTOR4 (PIF4), a major transcription modulator in postgermination development, to interdependently regulate hypocotyl elongation-related genes via direct binding to G-box element in the dark. Moreover, loss of LEC1 function suppresses the elongated hypocotyl phenotype of PIF-overaccumulating plants; conversely, inducible overexpression of LEC1 does not rescue the short hypocotyl in pif4 mutants. Our findings reveal that LEC1 acts as a coactivator of PIFs in transcriptional regulation during postembryonic growth, providing a possible mechanism by which plants fine-tune morphological development for their survival during the transition from the embryonic phase to seedling establishment.

[1]  Xingliang Hou,et al.  Nuclear factor Y-mediated H3K27me3 demethylation of the SOC1 locus orchestrates flowering responses of Arabidopsis , 2014, Nature Communications.

[2]  S. Prat,et al.  BR-dependent phosphorylation modulates PIF4 transcriptional activity and shapes diurnal hypocotyl growth , 2016 .

[3]  A. Burlingame,et al.  A mutually assured destruction mechanism attenuates light signaling in Arabidopsis , 2014, Science.

[4]  Rongcheng Lin,et al.  The Chromatin-Remodeling Factor PICKLE Integrates Brassinosteroid and Gibberellin Signaling during Skotomorphogenic Growth in Arabidopsis[C][W] , 2014, Plant Cell.

[5]  P. Leivar,et al.  PIFs: Systems Integrators in Plant Development[W] , 2014, Plant Cell.

[6]  S. Powers,et al.  bZIP67 Regulates the Omega-3 Fatty Acid Content of Arabidopsis Seed Oil by Activating FATTY ACID DESATURASE3[W][OPEN] , 2013, Plant Cell.

[7]  Xuncheng Liu,et al.  PHYTOCHROME INTERACTING FACTOR3 Associates with the Histone Deacetylase HDA15 in Repression of Chlorophyll Biosynthesis and Photosynthesis in Etiolated Arabidopsis Seedlings[W][OA] , 2013, Plant Cell.

[8]  Rongcheng Lin,et al.  Arabidopsis Chromatin Remodeling Factor PICKLE Interacts with Transcription Factor HY5 to Regulate Hypocotyl Cell Elongation[C][W] , 2013, Plant Cell.

[9]  T. Speed,et al.  A Quartet of PIF bHLH Factors Provides a Transcriptionally Centered Signaling Hub That Regulates Seedling Morphogenesis through Differential Expression-Patterning of Shared Target Genes in Arabidopsis , 2013, PLoS genetics.

[10]  A. Junker,et al.  Multifunctionality of the LEC1 transcription factor during plant development , 2012, Plant signaling & behavior.

[11]  I. Xenarios,et al.  Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. , 2012, The Plant journal : for cell and molecular biology.

[12]  V. Calvenzani,et al.  Interactions and CCAAT-Binding of Arabidopsis thaliana NF-Y Subunits , 2012, PloS one.

[13]  J. Keilwagen,et al.  Elongation-related functions of LEAFY COTYLEDON1 during the development of Arabidopsis thaliana. , 2012, The Plant journal : for cell and molecular biology.

[14]  Eunkyoo Oh,et al.  Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses , 2012, Nature Cell Biology.

[15]  B. Grimm,et al.  Studies on differential nuclear translocation mechanism and assembly of the three subunits of the Arabidopsis thaliana transcription factor NF-Y. , 2012, Molecular plant.

[16]  W. Muir,et al.  The CHD3 Remodeler PICKLE Associates with Genes Enriched for Trimethylation of Histone H3 Lysine 271[W][OA] , 2012, Plant Physiology.

[17]  Jinfang Chu,et al.  PIF4–Mediated Activation of YUCCA8 Expression Integrates Temperature into the Auxin Pathway in Regulating Arabidopsis Hypocotyl Growth , 2012, PLoS genetics.

[18]  W. Gray,et al.  PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) regulates auxin biosynthesis at high temperature , 2011, Proceedings of the National Academy of Sciences.

[19]  T. Mizuno,et al.  Phytochrome-interacting factor 4 and 5 (PIF4 and PIF5) activate the homeobox ATHB2 and auxin-inducible IAA29 genes in the coincidence mechanism underlying photoperiodic control of plant growth of Arabidopsis thaliana. , 2011, Plant & cell physiology.

[20]  Xingliang Hou,et al.  DELLAs modulate jasmonate signaling via competitive binding to JAZs. , 2010, Developmental cell.

[21]  M. Ni,et al.  Transcriptional and hormonal signaling control of Arabidopsis seed development. , 2010, Current opinion in plant biology.

[22]  S. Horvath,et al.  Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. , 2010, Proceedings of the National Academy of Sciences of the United States of America.

[23]  S. Howell,et al.  bZIP28 and NF-Y Transcription Factors Are Activated by ER Stress and Assemble into a Transcriptional Complex to Regulate Stress Response Genes in Arabidopsis[W][OA] , 2010, Plant Cell.

[24]  Maarten Koornneef,et al.  Natural modifiers of seed longevity in the Arabidopsis mutants abscisic acid insensitive3-5 (abi3-5) and leafy cotyledon1-3 (lec1-3). , 2009, The New phytologist.

[25]  S. Takeda,et al.  Arabidopsis NF-YB subunits LEC1 and LEC1-LIKE activate transcription by interacting with seed-specific ABRE-binding factors. , 2009, The Plant journal : for cell and molecular biology.

[26]  K. Halliday,et al.  Skotomorphogenesis: The Dark Side of Light Signalling , 2008, Current Biology.

[27]  E. Huq,et al.  Multiple Phytochrome-Interacting bHLH Transcription Factors Repress Premature Seedling Photomorphogenesis in Darkness , 2008, Current Biology.

[28]  Kristen K. Dang,et al.  Tissue-Specific Expression Patterns of Arabidopsis NF-Y Transcription Factors Suggest Potential for Extensive Combinatorial Complexity1[W][OA] , 2008, Plant Physiology.

[29]  Jian Zhang,et al.  LEAFY COTYLEDON1 Is a Key Regulator of Fatty Acid Biosynthesis in Arabidopsis1[C][W][OA] , 2008, Plant Physiology.

[30]  T. Yoshizumi,et al.  RETARDED GROWTH OF EMBRYO1, a New Basic Helix-Loop-Helix Protein, Expresses in Endosperm to Control Embryo Growth1[W] , 2008, Plant Physiology.

[31]  G. Choi,et al.  Decoding of light signals by plant phytochromes and their interacting proteins. , 2008, Annual review of plant biology.

[32]  C. Fankhauser,et al.  A molecular framework for light and gibberellin control of cell elongation , 2008, Nature.

[33]  X. Deng,et al.  Coordinated regulation of Arabidopsis thaliana development by light and gibberellins , 2008, Nature.

[34]  Hui Shen,et al.  Phytochrome Interacting Factors: central players in phytochrome-mediated light signaling networks. , 2007, Trends in plant science.

[35]  J. Sheen,et al.  Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis , 2007, Nature Protocols.

[36]  S. Upadhyay,et al.  The GCR1, GPA1, PRN1, NF-Y Signal Chain Mediates Both Blue Light and Abscisic Acid Responses in Arabidopsis1[W][OA] , 2007, Plant Physiology.

[37]  P. Quail,et al.  Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasome-mediated degradation. , 2006, Molecular cell.

[38]  Meng Chen,et al.  Light signal transduction in higher plants. , 2004, Annual review of genetics.

[39]  E. Huq,et al.  A Novel Molecular Recognition Motif Necessary for Targeting Photoactivated Phytochrome Signaling to Specific Basic Helix-Loop-Helix Transcription Factorsw⃞ , 2004, The Plant Cell Online.

[40]  G. Choi,et al.  Functional Characterization of Phytochrome Interacting Factor 3 in Phytochrome-Mediated Light Signal Transduction Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.014498. , 2003, The Plant Cell Online.

[41]  E. Huq,et al.  The Arabidopsis Basic/Helix-Loop-Helix Transcription Factor Family Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.013839. , 2003, The Plant Cell Online.

[42]  T. Lynch,et al.  Regulatory Networks in Seeds Integrating Developmental, Abscisic Acid, Sugar, and Light Signaling1 , 2003, Plant Physiology.

[43]  E. Huq,et al.  PIF4, a phytochrome‐interacting bHLH factor, functions as a negative regulator of phytochrome B signaling in Arabidopsis , 2002, The EMBO journal.

[44]  Robert B Goldberg,et al.  Arabidopsis LEAFY COTYLEDON1 Is Sufficient to Induce Embryo Development in Vegetative Cells , 1998, Cell.

[45]  F. Parcy,et al.  The ABSCISIC ACID-INSENSITIVE3, FUSCA3, and LEAFY COTYLEDON1 loci act in concert to control multiple aspects of Arabidopsis seed development. , 1997, The Plant cell.

[46]  X. Deng,et al.  LIGHT CONTROL OF SEEDLING DEVELOPMENT. , 1996, Annual review of plant physiology and plant molecular biology.

[47]  M. West,et al.  LEAFY COTYLEDON1 Is an Essential Regulator of Late Embryogenesis and Cotyledon Identity in Arabidopsis. , 1994, The Plant cell.

[48]  D. Meinke,et al.  Leafy Cotyledon Mutants of Arabidopsis. , 1994, The Plant cell.

[49]  J. Chory,et al.  Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. , 1993, The Plant cell.

[50]  S. Powers,et al.  bZIP 67 Regulates the Omega-3 Fatty Acid Content of Arabidopsis Seed Oil by Activating FATTY ACID DESATURASE 3 , 2013 .

[51]  P. Quail,et al.  PIFs: pivotal components in a cellular signaling hub. , 2011, Trends in plant science.

[52]  Kristen K. Dang,et al.  Tissue-Specific Expression Patterns of Arabidopsis NF-Y Transcription Factors Suggest Potential for Extensive Combinatorial Complexity , 2009 .

[53]  J. Chandler,et al.  BIM1, a bHLH protein involved in brassinosteroid signalling, controls Arabidopsis embryonic patterning via interaction with DORNRÖSCHEN and DORNRÖSCHEN-LIKE , 2008, Plant Molecular Biology.

[54]  Xiu-Jie Wang,et al.  LEAFY COTYLEDON 1 Is a Key Regulator of Fatty Acid Biosynthesis in Arabidopsis 1 [ C ] [ W ] [ OA ] , 2008 .

[55]  T. Yoshizumi,et al.  RETARDED GROWTH OF EMBRYO 1 , a New Basic Helix-Loop-Helix Protein , Expresses in Endosperm to Control Embryo Growth 1 [ W ] , 2008 .

[56]  J. Harada.  Role of Arabidopsis LEAFY COTYLEDON genes in seed development , 2001 .