SEPALLATA3: the 'glue' for MADS box transcription factor complex formation

BackgroundPlant MADS box proteins play important roles in a plethora of developmental processes. In order to regulate specific sets of target genes, MADS box proteins dimerize and are thought to assemble into multimeric complexes. In this study a large-scale yeast three-hybrid screen is utilized to provide insight into the higher-order complex formation capacity of the Arabidopsis MADS box family. SEPALLATA3 (SEP3) has been shown to mediate complex formation and, therefore, special attention is paid to this factor in this study.ResultsIn total, 106 multimeric complexes were identified; in more than half of these at least one SEP protein was present. Besides the known complexes involved in determining floral organ identity, various complexes consisting of combinations of proteins known to play a role in floral organ identity specification, and flowering time determination were discovered. The capacity to form this latter type of complex suggests that homeotic factors play essential roles in down-regulation of the MADS box genes involved in floral timing in the flower via negative auto-regulatory loops. Furthermore, various novel complexes were identified that may be important for the direct regulation of the floral transition process. A subsequent detailed analysis of the APETALA3, PISTILLATA, and SEP3 proteins in living plant cells suggests the formation of a multimeric complex in vivo.ConclusionsOverall, these results provide strong indications that higher-order complex formation is a general and essential molecular mechanism for plant MADS box protein functioning and attribute a pivotal role to the SEP3 'glue' protein in mediating multimerization.

• Publication year

  2009

• Venue

  Genome Biology

• Publication date

  2009-02-25

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.1186/gb-2009-10-2-r24PMID 19243611PMCID 2688274
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• MADS-box gene expression in lateral primordia, meristems and differentiated tissues of Arabidopsis thaliana roots

  2014cited by this paper
• In planta localisation patterns of MADS domain proteins during floral development in Arabidopsis thaliana

  2009influential reference
• AGL61 Interacts with AGL80 and Is Required for Central Cell Development in Arabidopsis1[W][OA]

  2008cited by this paper
• The class E floral homeotic protein SEPALLATA3 is sufficient to loop DNA in ‘floral quartet’-like complexes in vitro

  2008cited by this paper
• The MADS Domain Protein DIANA Acts Together with AGAMOUS-LIKE80 to Specify the Central Cell in Arabidopsis Ovules[W]

  2008cited by this paper
• At-TAX: a whole genome tiling array resource for developmental expression analysis and transcript identification in Arabidopsis thaliana

  2008cited by this paper
• Interaction study of MADS-domain proteins in tomato.

  2008cited by this paper
• AGAMOUS-LIKE24 and SHORT VEGETATIVE PHASE determine floral meristem identity in Arabidopsis.

  2008cited by this paper
• The AGL62 MADS Domain Protein Regulates Cellularization during Endosperm Development in Arabidopsis[W]

  2008cited by this paper
• AGL23, a type I MADS-box gene that controls female gametophyte and embryo development in Arabidopsis.

  2008cited by this paper
• AGAMOUS-LIKE 17, a novel flowering promoter, acts in a FT-independent photoperiod pathway.

  2008cited by this paper
• Nucleolar release of Hand1 acts as a molecular switch to determine cell fate

  2007cited by this paper
• Tagging of MADS domain proteins for chromatin immunoprecipitation

  2007cited by this paper
• MADS-complexes regulate transcriptome dynamics during pollen maturation

  2007cited by this paper
• The Homeotic Protein AGAMOUS Controls Late Stamen Development by Regulating a Jasmonate Biosynthetic Gene in Arabidopsis[W]

  2007cited by this paper
• Genetic and Molecular Interactions between BELL1 and MADS Box Factors Support Ovule Development in Arabidopsis[W]

  2007cited by this paper
• The MADS domain factors AGL15 and AGL18 act redundantly as repressors of the floral transition in Arabidopsis.

  2007influential reference
• Specification of Arabidopsis floral meristem identity by repression of flowering time genes

  2007influential reference
• Control of Floral Meristem Determinacy in Petunia by MADS-Box Transcription Factors1[W]

  2006cited by this paper
• AGL80 Is Required for Central Cell and Endosperm Development in Arabidopsis[W]

  2006influential reference
• The Arabidopsis thaliana AAA protein CDC48A interacts in vivo with the somatic embryogenesis receptor-like kinase 1 receptor at the plasma membrane.

  2006influential reference
• The Arabidopsis FLC protein interacts directly in vivo with SOC1 and FT chromatin and is part of a high-molecular-weight protein complex.

  2006cited by this paper
• In vivo imaging of MADS-box transcription factor interactions.

  2006influential reference
• A Bsister MADS-box gene involved in ovule and seed development in petunia and Arabidopsis.

  2006cited by this paper
• Protein interactions of MADS box transcription factors involved in flowering in Lolium perenne.

  2006cited by this paper
• DILIMOT: discovery of linear motifs in proteins

  2006influential reference
• Polycomb-group proteins repress the floral activator AGL19 in the FLC-independent vernalization pathway.

  2006influential reference
• AGL24, SHORT VEGETATIVE PHASE, and APETALA1 Redundantly Control AGAMOUS during Early Stages of Flower Development in Arabidopsis[W]

  2006cited by this paper
• trans meets cis in MADS science.

  2006cited by this paper
• A gene expression map of Arabidopsis thaliana development

  2005influential reference
• Comprehensive Interaction Map of the Arabidopsis MADS Box Transcription Factorsw⃞

  2005cited by this paper
• Faculty Opinions recommendation of Comprehensive interaction map of the Arabidopsis MADS Box transcription factors.

  2005cited by this paper
• Transcriptional Profile of the Arabidopsis Root Quiescent Centerw⃞

  2005cited by this paper
• The evolution of the SEPALLATA subfamily of MADS-box genes: a preangiosperm origin with multiple duplications throughout angiosperm history.

  2005cited by this paper
• Mutant analysis, protein–protein interactions and subcellular localization of the Arabidopsis Bsister (ABS) protein

  2005cited by this paper
• The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity.

  2004influential reference
• The homeotic protein AGAMOUS controls microsporogenesis by regulation of SPOROCYTELESS

  2004cited by this paper
• Heterodimerization and Endocytosis of Arabidopsis Brassinosteroid Receptors BRI1 and AtSERK3 (BAK1)

  2004cited by this paper
• Identification and Characterization of Four Chrysanthemum MADS-Box Genes, Belonging to the APETALA1/FRUITFULL and SEPALLATA3 Subfamilies1

  2004cited by this paper
• Defining subdomains of the K domain important for protein–protein interactions of plant MADS proteins

  2004influential reference
• Transcript profiling of transcription factor genes during silique development in Arabidopsis

  2004cited by this paper
• The K domain mediates heterodimerization of the Arabidopsis floral organ identity proteins, APETALA3 and PISTILLATA.

  2003cited by this paper
• Molecular and Phylogenetic Analyses of the Complete MADS-Box Transcription Factor Family in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.011544.

  2003influential reference
• Dissection of floral induction pathways using global expression analysis

  2003influential reference
• Analysis of the petunia MADS-box transcription factor family

  2003cited by this paper
• AGL24 acts as a promoter of flowering in Arabidopsis and is positively regulated by vernalization.

  2003influential reference
• Modes of intercellular transcription factor movement in the Arabidopsis apex

  2003cited by this paper
• The MADS Box Gene FBP2 Is Required for SEPALLATA Function in Petunia Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010280.

  2003cited by this paper
• The Polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1.

  2003cited by this paper
• MADS-Box Protein Complexes Control Carpel and Ovule Development in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.015123.

  2003influential reference
• Transcription factors do it together: the hows and whys of studying protein-protein interactions.

  2002cited by this paper
• Evolution of class B floral homeotic proteins: obligate heterodimerization originated from homodimerization.

  2002cited by this paper
• Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method.

  2002cited by this paper
• AGAMOUS-LIKE 24, a dosage-dependent mediator of the flowering signals

  2002cited by this paper
• GATEWAY vectors for Agrobacterium-mediated plant transformation.

  2002cited by this paper
• Analysis of MADS box protein–protein interactions in living plant cells

  2002cited by this paper
• Plant biology: Floral quartets

  2001cited by this paper
• Turning floral organs into leaves, leaves into floral organs.

  2001influential reference
• Function and evolution of the plant MADS-box gene family

  2001cited by this paper
• Complexes of MADS-box proteins are sufficient to convert leaves into floral organs

  2001influential reference
• APETALA1 and SEPALLATA3 interact to promote flower development.

  2001cited by this paper
• Coiled coils: a highly versatile protein folding motif.

  2001cited by this paper
• Conversion of leaves into petals in Arabidopsis.

  2001cited by this paper
• Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis.

  2000influential reference
• Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis.

  2000influential reference
• A MADS domain gene involved in the transition to flowering in Arabidopsis.

  2000influential reference
• B and C floral organ identity functions require SEPALLATA MADS-box genes

  2000influential reference
• An ancestral MADS-box gene duplication occurred before the divergence of plants and animals.

  2000cited by this paper
• Ternary complex formation between the MADS‐box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus

  1999cited by this paper
• Analysis of the C-terminal region of Arabidopsis thaliana APETALA1 as a transcription activation domain

  1999cited by this paper
• MultiCoil: A program for predicting two‐and three‐stranded coiled coils

  1997cited by this paper
• Nuclear localization of the Arabidopsis APETALA3 and PISTILLATA homeotic gene products depends on their simultaneous expression.

  1996cited by this paper
• A highly sensitive and non-lethal beta-galactosidase plate assay for yeast.

  1996cited by this paper
• The Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class organ identity function.

  1996cited by this paper
• Dimerization specificity of Arabidopsis MADS domain homeotic proteins APETALA1, APETALA3, PISTILLATA, and AGAMOUS.

  1996cited by this paper
• Non-cell-autonomous function of the Antirrhinum floral homeotic proteins DEFICIENS and GLOBOSA is exerted by their polar cell-to-cell trafficking.

  1996cited by this paper
• Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast.

  1996cited by this paper
• A highly sensitive and non-lethal β-galactosidase plate assay for yeast

  1996cited by this paper
• Diverse roles for MADS box genes in Arabidopsis development.

  1995influential reference
• Functional analysis of the Antirrhinum floral homeotic DEFICIENS gene in vivo and in vitro by using a temperature-sensitive mutant.

  1995cited by this paper
• Predicting coiled coils by use of pairwise residue correlations.

  1995cited by this paper
• Ectopic expression of the floral homeotic gene AGAMOUS in transgenic Arabidopsis plants alters floral organ identity.

  1992cited by this paper
• The war of the whorls: genetic interactions controlling flower development

  1991cited by this paper
• Genes directing flower development in Arabidopsis.

  1989cited by this paper
• Versuch die Metamorphose der Pflanzen zu erklären

  1973cited by this paper

• Fruit firmness in Rosaceae: Mechanisms and genetic insights

  2026cites this paper
• The origin, evolution, and diversification of MADS-box transcription factors in green plants

  2025cites this paper
• Deciphering the Molecular Mechanisms That Control Ovule Development in Pomegranate

  2025cites this paper
• Research Progress on the Regulation of Plant Floral Organ Development by the MADS-box Gene Family

  2025cites this paper
• Mechanisms driving functional divergence of transcription factor paralogs

  2025cites this paper
• Saffron CsSEP3 regulates flowering time and flower organ morphogenesis.

  2025cites this paper
• Promoter Motif Profiling and Binding Site Distribution Analysis of Transcription Factors Predict Auto- and Cross-Regulatory Mechanisms in Arabidopsis Flowering Genes

  2025cites this paper
• Temporal Shifts in Hormone Signaling Networks Orchestrate Soybean Floral Development Under Field Conditions: An RNA-Seq Study

  2025cites this paper
• The floral ABCs of Hydnora, one of the most bizarre parasitic plants in the world, and its autotrophic relatives of the order Piperales

  2025cites this paper
• A brief look into protein-protein interactions orchestrating flower and fruit development.

  2025cites this paper
• Targets and mechanisms of epigenetic regulation in the temperate cereal vernalisation process

  2025cites this paper
• A critical review of the importance of FAR-RELATED SEQUENCE (FRS)- FRS-RELATED FACTOR (FRF) transcription factors in plants.

  2025cites this paper
• Characterization analyses of MADS-box genes highlighting their functions with seed development in Ricinus communis

  2025cites this paper
• Evolutionary Dynamics and Expression Divergence of the MADS-Box Gene Family During Recent Speciation of AA-Genome Oryza Species

  2025cites this paper
• An insertion of transposon in Tepi gene confers male sterility of marigold

  2025cites this paper
• Comparative transcriptomics of seed nourishing tissues: uncovering conserved and divergent pathways in seed plants

  2024cites this paper
• Genome-wide characterization and expression analysis of MADS-box transcription factor gene family in Perilla frutescens

  2024cites this paper
• Transcriptome wide analysis of MADS box genes in Crocus sativus and interplay of CstMADS19-CstMADS26 in orchestrating apocarotenoid biosynthesis.

  2024cites this paper
• Alternative splicing variants of IiSEP3 in Isatis indigotica are involved in floral transition and flower development.

  2024cites this paper
• The SEPALLATA-like CaSEP5 gene regulates flower sepal, pedicel, and fruit development in pepper (Capsicum annuum L.)

  2024cites this paper
• The SEP homologous gene TEMARY regulates inflorescence phenotypes in Hydrangea Macrophylla

  2024cites this paper
• Uncoupling FRUITFULL’s functions through modification of a protein motif identified by co-ortholog analysis

  2024cites this paper
• LsFUL-LsSMU2 module positively controls bolting time in leaf lettuce (Lactuca sativa L.) under high temperature.

  2024cites this paper
• Characterization of FchAGL9 and FchSHP, two MADS-boxes related to softening of Fragaria chiloensis fruit.

  2024cites this paper
• Global gene expression profile and functional analysis reveal the conservation of reproduction-associated gene networks in Gossypium hirsutum

  2024cites this paper
• The MADS-box genes SOC1 and AGL24 antagonize XAL2 functions in Arabidopsis thaliana root development

  2024cites this paper
• SEPALLATA-driven MADS transcription factor tetramerization is required for inner whorl floral organ development.

  2024cites this paper
• The overall regulatory network and contributions of ABC(D)E model genes in yellowhorn flower development

  2024cites this paper
• The transcription factors and pathways underpinning male reproductive development in Arabidopsis

  2024cites this paper
• MADS1-regulated lemma and awn development benefits barley yield

  2024cites this paper
• Interaction among homeodomain transcription factors mediates ethylene biosynthesis during pear fruit ripening

  2024cites this paper
• The effector SJP3 interferes with pistil development by sustaining SHORT VEGETATIVE PHASE 3 expression in jujube.

  2024cites this paper
• MADS8 is indispensable for female reproductive development at high ambient temperatures in cereal crops

  2023cites this paper
• Functional conservation and divergence of SEPALLATA-like genes in floral development in Cymbidium sinense

  2023cites this paper
• Antagonistic MADS-box transcription factors SEEDSTICK and SEPALLATA3 form a transcriptional regulatory network that regulates seed oil accumulation.

  2023cites this paper
• Cracking the Floral Quartet Code: How Do Multimers of MIKCC-Type MADS-Domain Transcription Factors Recognize Their Target Genes?

  2023cites this paper
• TM3 and STM3 Promote Flowering Together with FUL2 and MBP20, but Act Antagonistically in Inflorescence Branching in Tomato

  2023cites this paper
• Dual specificity and target gene selection by the MADS-domain protein FRUITFULL

  2023cites this paper
• Ca2+‐Calmodulin regulates nuclear translocation of the rice seed‐specific MADS‐box transcription factor OsMADS29

  2023cites this paper
• One pattern analysis (OPA) for the quantitative determination of protein interactions in plant cells

  2023influential citation
• The emerging roles of circRNAs in traits associated with livestock breeding

  2023cites this paper
• Identification and characterization of class E genes involved in floral organ development in Dianthus chinensis

  2023cites this paper
• SEPALLATA-driven MADS transcription factor tetramerization is required for inner whorl floral organ development

  2023cites this paper
• AGAMOUS mediates timing of guard cell formation during gynoecium development

  2023cites this paper
• Flower Development in the Solanaceae.

  2023cites this paper
• Genome-wide and expression analyses of MADS-box genes in the tetraploid Coffea arabica L. and its diploid parental subgenomes

  2023cites this paper
• Arabidopsis AGAMOUS-LIKE16 and SUPPRESSOR OF CONSTANS 1 collaborate to regulate of genome-wide expression and flowering time.

  2023cites this paper
• Motif models proposing independent and interdependent impacts of nucleotides are related to high and low affinity transcription factor binding sites in Arabidopsis

  2022cites this paper
• The Origin of Floral Quartet Formation—Ancient Exon Duplications Shaped the Evolution of MIKC-type MADS-domain Transcription Factor Interactions

  2022cites this paper
• Integrated transcriptome and small RNA sequencing in revealing miRNA-mediated regulatory network of floral bud break in Prunus mume

  2022cites this paper
• An ortholog of the MADS-box gene SEPALLATA3 regulates stamen development in the woody plant Jatropha curcas

  2022cites this paper
• Characterization of Three SEPALLATA-Like MADS-Box Genes Associated With Floral Development in Paphiopedilum henryanum (Orchidaceae)

  2022cites this paper
• A phytoplasma effector acts as a ubiquitin-like mediator between floral MADS-box proteins and proteasome shuttle proteins.

  2022cites this paper
• Polycomb Proteins Control Floral Determinacy by H3K27me3-mediated Repression of Pluripotency Genes in Arabidopsis thaliana.

  2022cites this paper
• Heterologous Expression of LiSEP3 from Oriental Lilium Hybrid ‘Sorbonne’ Promotes the Flowering of Arabidopsis thaliana L

  2022cites this paper
• Dissecting SEPALLATA3 Splicing Variant Functions During Arabidopsis Vegetative Growth by amiRNA Technology

  2022cites this paper
• Whole-transcriptome profiles of Chrysanthemum seticuspe improve genome annotation and shed new light on mRNA–miRNA–lncRNA networks in ray florets and disc florets

  2022cites this paper
• Identification of MADS-Box Transcription Factors in Iris laevigata and Functional Assessment of IlSEP3 and IlSVP during Flowering

  2022cites this paper
• The protein-protein interaction landscape of transcription factors during gynoecium development in Arabidopsis.

  2022cites this paper
• SEP-like genes of Gossypium hirsutum promote flowering via targeting different loci in a concentration-dependent manner

  2022cites this paper
• BELL1 interacts with CRABS CLAW and INNER NO OUTER to regulate ovule and seed development in pomegranate

  2022cites this paper
• Context-specific functions of transcription factors controlling plant development: From leaves to flowers.

  2022cites this paper
• Cell identity specification in plants: lessons from flower development

  2021cites this paper
• The EAR Motif in the Arabidopsis MADS Transcription Factor AGAMOUS-Like 15 Is Not Necessary to Promote Somatic Embryogenesis

  2021cites this paper
• Transcription factor action orchestrates the complex expression pattern of CRABS CLAW, a gynoecium developmental regulator in Arabidopsis

  2021cites this paper
• The intervening domain is required for DNA-binding and functional identity of plant MADS transcription factors

  2021cites this paper
• MADS-Box Protein Complex VvAG2, VvSEP3 and VvAGL11 Regulates the Formation of Ovules in Vitis vinifera L. cv. ‘Xiangfei’

  2021cites this paper
• FRUITFULL-like genes regulate flowering time and inflorescence 3 architecture in tomato 4 5

  2021cites this paper
• The MADS-box gene FveSEP3 plays essential roles in flower organogenesis and fruit development in woodland strawberry

  2021cites this paper
• The intervening domain is required for DNA-binding and functional identity of plant MADS transcription factors

  2021cites this paper
• The Sugar Content in the Tomato Ripe Fruit Correlates with the Expression Level of the RIN2i Isform of the Ripening Inhibitor Gene

  2021cites this paper
• Expression and Functional Analyses of Nymphaea caerulea MADS-Box Genes Contribute to Clarify the Complex Flower Patterning of Water Lilies

  2021cites this paper
• An overview of the endogenous and environmental factors related to the Coffea arabica flowering process

  2021cites this paper
• The MADS-box gene PpPI is a key regulator of the double-flower trait in peach.

  2021cites this paper
• ZjSEP3 modulates flowering time by regulating the LHY promoter

  2021cites this paper
• The MADS-domain factor AGAMOUS-Like18 promotes somatic embryogenesis.

  2021cites this paper
• Analysis of the structure and function of the tomato Solanum lycopersicum L. MADS-box gene SlMADS5

  2021cites this paper
• Genome-Wide Identification and Analysis of the MADS-Box Gene Family in American Beautyberry (Callicarpa americana)

  2021cites this paper
• Functional conservation and divergence of SEPALLATA-like genes in the development of two-type florets in marigold.

  2021cites this paper
• AGL16 regulates genome-wide gene expression and flowering time with partial dependency on SOC1 in Arabidopsis

  2021influential citation
• Molecular Cloning and Expression Profile of Class E Genes Related to Sepal Development in Nelumbo nucifera

  2021cites this paper
• One factor, many systems: the floral homeotic protein AGAMOUS and its epigenetic regulatory mechanisms.

  2021cites this paper
• Transcriptome analysis of gynoecium morphogenesis uncovers the chronology of gene regulatory network activity.

  2020cites this paper
• Revisiting the Role of Master Regulators in Tomato Ripening.

  2020cites this paper
• Regulatory mechanisms underlying florigenesis in Vanilla planifolia Andrews: A study of MADS-box gene family

  2020cites this paper
• Evo-devo of flowers and flowering genes: Salvia as a case study

  2020influential citation
• FRUITFULL-like genes regulate flowering time and inflorescence architecture in tomato

  2020cites this paper
• High-resolution temporal transcript profiling during Arabidopsis thaliana gynoecium morphogenesis uncovers the chronology of gene regulatory network activity and reveals novel developmental regulators

  2020cites this paper
• Genome-wide binding of SEPALLATA3 and AGAMOUS complexes determined by sequential DNA-affinity purification sequencing

  2020cites this paper
• Structural and Functional Diversification of SEPALLATA Genes TM5 and RIN in Tomato Species (Section Lycopersicon)

  2020cites this paper
• Ectopic expression of Chrysanthemum CDM19 in Arabidopsis reveals a novel function in carpel development

  2020cites this paper
• Characterization of Transcriptional Expression and Regulation of Carotenoid Cleavage Dioxygenase 4b in Grapes

  2020cites this paper
• Novel Imaging Modalities Shedding Light on Plant Biology: Start Small and Grow Big.

  2020cites this paper
• First approach to pod dehiscence in faba bean: genetic and histological analyses

  2020cites this paper
• Dissection of the Arabidopsis HUA-PEP gene activity reveals that ovule fate specification requires restriction of the floral A-function.

  2020cites this paper
• Allelic Mutations in the Ripening-Inhibitor Locus Generate Extensive Variation in Tomato Ripening1

  2020cites this paper
• Contrasted evolutionary trajectories of plant transcription factors.

  2020cites this paper
• Diversity and Expression Patterns of MADS-Box Genes in Gnetum luofuense—Implications for Functional Diversity and Evolution

  2019cites this paper
• MADS78 and MADS79 Are Essential Regulators of Early Seed Development in Rice1[OPEN]

  2019cites this paper
• REM34 and REM35 Control Female and Male Gametophyte Development in Arabidopsis thaliana

  2019cites this paper