CoChat
Sign Up
Cited by 26Plant Molecular Biology ResearchPlant Gene Expression AnalysisDevelopmental Biology and Gene Regulation

The DOI matches its Crossref record; 4 of the 4 references it cites were found in a registry or an index.

SEPALLATA-driven MADS transcription factor tetramerization is required for inner whorl floral organ development

Open access
Hugouvieux, Veronique, Blanc-Mathieu, Romain, Janeau, Aline, Paul, Michel, Lucas, Jeremy, Xu, Xiaocai, Ye, Hailong, Lai, Xuelei, Le Hir, Sarah, Guillotin, Audrey, Galien, Antonin, Yan, Wenhao, Nanao, Max, Kaufmann, Kerstin, Parcy, François, Zubieta, Chloe·2024·The Plant Cell
DOI 10.1093/plcell/koae151PMC PMC11371193

Published version of a preprint

Open this paper in CoChat — free accountOpen PDF

Abstract

MADS transcription factors are master regulators of plant reproduction and flower development. The SEPALLATA (SEP) subfamily of MADS transcription factors is required for the development of floral organs and plays roles in inflorescence architecture and development of the floral meristem. SEPALLATAs act as organizers of MADS complexes, forming both heterodimers and heterotetramers in vitro. To date, the MADS complexes characterized in angiosperm floral organ development contain at least 1 SEPALLATA protein. Whether DNA binding by SEPALLATA-containing dimeric MADS complexes is sufficient for launching floral organ identity programs, however, is not clear as only defects in floral meristem determinacy were observed in tetramerization-impaired SEPALLATA mutant proteins. Here, we used a combination of genome-wide-binding studies, high-resolution structural studies of the SEP3/AGAMOUS (AG) tetramerization domain, structure-based mutagenesis and complementation experiments in Arabidopsis (Arabidopsis thaliana) sep1 sep2 sep3 and sep1 sep2 sep3 ag-4 plants transformed with versions of SEP3 encoding tetramerization mutants. We demonstrate that while SEP3 heterodimers can bind DNA both in vitro and in vivo and recognize the majority of SEP3 wild-type-binding sites genome-wide, tetramerization is required not only for floral meristem determinacy but also for floral organ identity in the second, third, and fourth whorls.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1093/plcell/koae151

Cites

4 of 4 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 74

  1. Becker, 2003, Distinct MADS-box gene expression patterns in the reproductive cones of the gymnosperm Gnetum gnemon, Dev Genes Evol, 213, 567, 10.1007/s00427-003-0358-0 · DOI
  2. Bensmihen, 2004, Analysis of an activated ABI5 allele using a new selection method for transgenic Arabidopsis seeds, FEBS Lett., 561, 127, 10.1016/S0014-5793(04)00148-6 · DOI
  3. Boekel, 2015, Multi-omic data analysis using Galaxy, Nat Biotechnol, 33, 137, 10.1038/nbt.3134 · DOI
  4. Chojnowski, 2019, Sequence assignment for low-resolution modelling of protein crystal structures, Acta Crystallogr Sect Struct Biol, 75, 753, 10.1107/S2059798319009392 · DOI
  5. Clough, 1998, Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana, Plant J Cell Mol Biol, 16, 735, 10.1046/j.1365-313x.1998.00343.x · DOI
  6. Coen, 1991, The war of the whorls: genetic interactions controlling flower development, Nature, 353, 31, 10.1038/353031a0 · DOI
  7. Dinneny, 2006, NUBBIN and JAGGED define stamen and carpel shape in Arabidopsis, Development, 133, 1645, 10.1242/dev.02335 · DOI
  8. Dinneny, 2004, The role of JAGGED in shaping lateral organs, Development, 131, 1101, 10.1242/dev.00949 · DOI
  9. Ditta, 2004, The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity, Curr Biol, 14, 1935, 10.1016/j.cub.2004.10.028 · DOI
  10. Doublie, 2007, Production of selenomethionyl proteins in prokaryotic and eukaryotic expression systems, Methods Mol Biol, 363, 91, 10.1007/978-1-59745-209-0_5 · DOI
  11. Dreni, 2022, Tracing the evolution of the SEPALLATA subfamily across angiosperms associated with neo- and sub-functionalization for reproductive and agronomically relevant traits, Plants, 11, 2934, 10.3390/plants11212934 · DOI
  12. Egea-Cortines, 1999, Ternary complex formation between the MADS-box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus, EMBO J, 18, 5370, 10.1093/emboj/18.19.5370 · DOI
  13. Emsley, 2010, Features and development of Coot, Acta Crystallogr Biol Crystallogr, 66, 486, 10.1107/S0907444910007493 · DOI · Paper page
  14. Eshed, 2001, Establishment of polarity in lateral organs of plants, Curr Biol CB, 11, 1251, 10.1016/S0960-9822(01)00392-X · DOI
  15. Gabadinho, 2010, MxCuBE: a synchrotron beamline control environment customized for macromolecular crystallography experiments, J Synchrotron Radiat, 17, 700, 10.1107/S0909049510020005 · DOI
  16. Gaspar, 2018, Improved peak-calling with MACS2, bioRxiv
  17. Gaspar, 2018, NGmerge: merging paired-end reads via novel empirically-derived models of sequencing errors, BMC Bioinformatics, 19, 536, 10.1186/s12859-018-2579-2 · DOI
  18. Goto, 2001, Turning floral organs into leaves, leaves into floral organs, Curr Opin Genet Dev, 11, 449, 10.1016/S0959-437X(00)00216-1 · DOI
  19. Gramzow, 2010, On the origin of MADS-domain transcription factors, Trends Genet, 26, 149, 10.1016/j.tig.2010.01.004 · DOI
  20. Gramzow, 2010, A hitchhiker's guide to the MADS world of plants, Genome Biol, 11, 214, 10.1186/gb-2010-11-6-214 · DOI
  21. Honma, 2001, Complexes of MADS-box proteins are sufficient to convert leaves into floral organs, Nature, 409, 525, 10.1038/35054083 · DOI
  22. Hugouvieux, 2018, Tetramerization of MADS family transcription factors SEPALLATA3 and AGAMOUS is required for floral meristem determinacy in Arabidopsis, Nucleic Acids Res, 46, 4966, 10.1093/nar/gky205 · DOI
  23. Hugouvieux, 2018, MADS transcription factors cooperate: complexities of complex formation, J Exp Bot, 69, 1821, 10.1093/jxb/ery099 · DOI
  24. Immink, 2009, SEPALLATA3: the “glue” for MADS box transcription factor complex formation, Genome Biol, 10, R24, 10.1186/gb-2009-10-2-r24 · DOI
  25. Jalili, 2018, Using combined evidence from replicates to evaluate ChIP-seq peaks, Bioinformatics, 34, 2338, 10.1093/bioinformatics/bty119 · DOI
  26. Jetha, 2014, Arabidopsis SEPALLATA proteins differ in cooperative DNA-binding during the formation of floral quartet-like complexes, Nucleic Acids Res, 42, 10927, 10.1093/nar/gku755 · DOI
  27. Kabsch, 2010, Xds, Acta Crystallogr Biol Crystallogr, 66, 125, 10.1107/S0907444909047337 · DOI · Paper page
  28. Karplus, 2015, Assessing and maximizing data quality in macromolecular crystallography, Curr Opin Struct Biol, 34, 60, 10.1016/j.sbi.2015.07.003 · DOI
  29. Kaufmann, 2005, MIKC-type MADS-domain proteins: structural modularity, protein interactions and network evolution in land plants, Gene, 347, 183, 10.1016/j.gene.2004.12.014 · DOI
  30. Kaufmann, 2009, Target genes of the MADS transcription factor SEPALLATA3: integration of developmental and hormonal pathways in the Arabidopsis flower, PLoS Biol, 7, e1000090, 10.1371/journal.pbio.1000090 · DOI
  31. Kaufmann, 2010, Chromatin immunoprecipitation (ChIP) of plant transcription factors followed by sequencing (ChIP-SEQ) or hybridization to whole genome arrays (ChIP-CHIP), Nat Protoc, 5, 457, 10.1038/nprot.2009.244 · DOI
  32. Kwantes, 2012, How MIKC* MADS-box genes originated and evidence for their conserved function throughout the evolution of vascular plant gametophytes, Mol Biol Evol, 29, 293, 10.1093/molbev/msr200 · DOI
  33. Labun, 2019, CHOPCHOP v3: expanding the CRISPR web toolbox beyond genome editing, Nucleic Acids Res., 47, W171, 10.1093/nar/gkz365 · DOI
  34. Lai, 2020, Genome-wide binding of SEPALLATA3 and AGAMOUS complexes determined by sequential DNA-affinity purification sequencing, Nucleic Acids Res, 48, 9637, 10.1093/nar/gkaa729 · DOI
  35. Lai, 2021, The intervening domain is required for DNA-binding and functional identity of plant MADS transcription factors, Nat Commun, 12, 4760, 10.1038/s41467-021-24978-w · DOI
  36. Langmead, 2012, Fast gapped-read alignment with Bowtie 2, Nat Methods, 9, 357, 10.1038/nmeth.1923 · DOI · Paper page
  37. Li, 2009, The sequence alignment/map format and SAMtools, Bioinformatics, 25, 2078, 10.1093/bioinformatics/btp352 · DOI · Paper page
  38. McAbee, 2006, ABERRANT TESTA SHAPE encodes a KANADI family member, linking polarity determination to separation and growth of Arabidopsis ovule integuments, Plant J, 46, 522, 10.1111/j.1365-313X.2006.02717.x · DOI
  39. McCoy, 2007, Solving structures of protein complexes by molecular replacement with Phaser, Acta Crystallogr Biol Crystallogr, 63, 32, 10.1107/S0907444906045975 · DOI
  40. Melzer, 2014, DEF- and GLO-like proteins may have lost most of their interaction partners during angiosperm evolution, Ann Bot, 114, 1431, 10.1093/aob/mcu094 · DOI
  41. Melzer, 2009, Reconstitution of “floral quartets” in vitro involving class B and class E floral homeotic proteins, Nucleic Acids Res, 37, 2723, 10.1093/nar/gkp129 · DOI
  42. Melzer, 2009, The class E floral homeotic protein SEPALLATA3 is sufficient to loop DNA in “floral quartet”-like complexes in vitro, Nucleic Acids Res, 37, 144, 10.1093/nar/gkn900 · DOI
  43. Melzer, 2010, The naked and the dead: the ABCs of gymnosperm reproduction and the origin of the angiosperm flower, Semin Cell Dev Biol, 21, 118, 10.1016/j.semcdb.2009.11.015 · DOI
  44. Mendes, 2013, MADS domain transcription factors mediate short-range DNA looping that is essential for target gene expression in Arabidopsis, Plant Cell, 25, 2560, 10.1105/tpc.112.108688 · DOI
  45. Monaco, 2013, Automatic processing of macromolecular crystallography X-ray diffraction data at the ESRF, J Appl Crystallogr, 46, 804, 10.1107/S0021889813006195 · DOI
  46. Morel, 2019, Divergent functional diversification patterns in the SEP/AGL6/AP1 MADS-box transcription factor superclade, Plant Cell, 31, 3033, 10.1105/tpc.19.00162 · DOI
  47. Murshudov, 1997, Refinement of macromolecular structures by the maximum-likelihood method, Acta Crystallogr D Biol Crystallogr, 53, 240, 10.1107/S0907444996012255 · DOI
  48. Pelaz, 2000, B and C floral organ identity functions require SEPALLATA MADS-box genes, Nature, 405, 200, 10.1038/35012103 · DOI
  49. Pelaz, 2001, Conversion of leaves into petals in Arabidopsis, Curr Biol, 11, 182, 10.1016/S0960-9822(01)00024-0 · DOI
  50. Pellegrini, 1995, Structure of serum response factor core bound to DNA, Nature, 376, 490, 10.1038/376490a0 · DOI
  51. Puranik, 2014, Structural basis for the oligomerization of the MADS domain transcription factor SEPALLATA3 in Arabidopsis, Plant Cell, 26, 3603, 10.1105/tpc.114.127910 · DOI
  52. Qiu, 2023, Updated phylogeny and protein structure predictions revise the hypothesis on the origin of MADS-box transcription factors in land plants, Mol Biol Evol, 40, msad194, 10.1093/molbev/msad194 · DOI
  53. Ruelens, 2017, The origin of floral organ identity quartets, Plant Cell, 29, 229, 10.1105/tpc.16.00366 · DOI
  54. Rümpler, 2023, The origin of floral quartet formation—ancient exon duplications shaped the evolution of MIKC-type MADS-domain transcription factor interactions, Mol Biol Evol, 40, msad088, 10.1093/molbev/msad088 · DOI
  55. Rumpler, 2018, A conserved leucine zipper-like motif accounts for strong tetramerization capabilities of SEPALLATA-like MADS-domain transcription factors, J Exp Bot, 69, 1943, 10.1093/jxb/ery063 · DOI
  56. Shindo, 1999, Characterization of MADS genes in the gymnosperm Gnetum parvifolium and its implication on the evolution of reproductive organs in seed plants, Evol Dev, 1, 180, 10.1046/j.1525-142x.1999.99024.x · DOI
  57. Sieburth, 1995, Genetic separation of third and fourth whorl functions of AGAMOUS, Plant Cell, 7, 1249
  58. Skinner, 2023, The Arabidopsis INNER NO OUTER (INO) gene acts exclusively and quantitatively in regulation of ovule outer integument development, Plant Direct, 7, e485, 10.1002/pld3.485 · DOI
  59. Skubák, 2018, A new MR-SAD algorithm for the automatic building of protein models from low-resolution X-ray data and a poor starting model, IUCrJ, 5, 166, 10.1107/S2052252517017961 · DOI
  60. Smaczniak, 2012, Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development, Proc Natl Acad Sci U S A, 109, 1560, 10.1073/pnas.1112871109 · DOI
  61. Tan, 1998, Crystal structure of the yeast MATalpha2/MCM1/DNA ternary complex, Nature, 391, 660, 10.1038/35563 · DOI
  62. Tanabe, 2005, Characterization of MADS-box genes in charophycean green algae and its implication for the evolution of MADS-box genes, Proc Natl Acad Sci U S A, 102, 2436, 10.1073/pnas.0409860102 · DOI
  63. The Galaxy Community, 2022, The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2022 update, Nucleic Acids Res, 50, W345, 10.1093/nar/gkac247 · DOI
  64. Theissen, 2001, Development of floral organ identity: stories from the MADS house, Curr Opin Plant Biol, 4, 75, 10.1016/S1369-5266(00)00139-4 · DOI
  65. Theissen, 2001, Plant biology. Floral quartets, Nature, 409, 469, 10.1038/35054172 · DOI
  66. Uimari, 2004, Integration of reproductive meristem fates by a SEPALLATA-like MADS-box gene, Proc Natl Acad Sci., 101, 15817, 10.1073/pnas.0406844101 · DOI
  67. van Mourik, 2015, Plant functional genomics: methods and protocols, 93, 10.1007/978-1-4939-2444-8_5 · DOI
  68. Wang, 2010, Molecular interactions of orthologues of floral homeotic proteins from the gymnosperm Gnetum gnemon provide a clue to the evolutionary origin of “floral quartets”, Plant J, 64, 177, 10.1111/j.1365-313X.2010.04325.x · DOI
  69. Wasserman, 2004, Applied bioinformatics for the identification of regulatory elements, Nat Rev Genet., 5, 276, 10.1038/nrg1315 · DOI
  70. Williams, 2018, MolProbity: more and better reference data for improved all-atom structure validation, Protein Sci Publ Protein Soc, 27, 293, 10.1002/pro.3330 · DOI · Paper page
  71. Yan, 2016, Efficient multiplex mutagenesis by RNA-guided Cas9 and its use in the characterization of regulatory elements in the AGAMOUS gene, Plant Methods, 12, 23, 10.1186/s13007-016-0125-7 · DOI
  72. Yanofsky, 1990, The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors, Nature, 346, 35, 10.1038/346035a0 · DOI
  73. Zahn, 2005, The evolution of the SEPALLATA subfamily of MADS-box genes: a preangiosperm origin with multiple duplications throughout angiosperm history, Genetics, 169, 2209, 10.1534/genetics.104.037770 · DOI
  74. Zander, 2016, Merging of synchrotron serial crystallographic data by a genetic algorithm, Acta Crystallogr Struct Biol, 72, 1026, 10.1107/S2059798316012079 · DOI

Metadata

Authors
Hugouvieux, V., Blanc-Mathieu, R., Janeau, A., Paul, M., Lucas, J., Xu, X., Ye, H., Lai, X., Le Hir, S., Guillotin, A., Galien, A., Yan, W., Nanao, M., Kaufmann, K., Parcy, F., & Zubieta, C.
Affiliations
  • Laboratoire de Physiologie Cellulaire et Végétale, Université Grenoble-Alpes, CNRS, CEA, INRAE, IRIG-DBSCI , 17 rue des Martyrs, 38000 Grenoble , France
  • Centre National de la Recherche Scientifique (FR)
  • Humboldt-Universität zu Berlin (DE)
  • Huazhong Agricultural University (CN)
  • European Synchrotron Radiation Facility (FR)
Corresponding author
Yan, Wenhao
ORCID
Venue
The Plant Cell
Publisher
Oxford University Press (OUP)
Published
2024-05-21
Volume
36
Issue
9
Pages
3435-3450
ISSN
  • 1040-4651 (ISSN-L)
  • 1532-298X
DOI
10.1093/plcell/koae151
PMC
PMC11371193
OpenAlex
W4398167693
Cited by
26
References
4
Citations by year
2026: 8 · 2025: 16 · 2024: 1
FWCI
6.08
Type
journal article
Language
en
Open access
Licence
Locations
  • The Plant Cell (publishedVersion)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, other-oa)
Funders
  • Agence National de la Recherche (ANR-19-CE20-0021, ANR-21-CE11-0037)
  • Chemistry and Biology Health Graduate School of the University Grenoble Alpes (ANR-17-EURE-0003)
  • FRISBI (ANR-10-INBS-0005-02)
  • Seventh Framework Programme (871037)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Plant Gene Expression Analysis
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords
SEPALLATA, tetramerization, AGAMOUS, floral organ identity, floral meristem determinacy, DNA binding, Arabidopsis thaliana, structure-guided mutagenesis
MeSH terms
Mutation, Transcription Factors, Arabidopsis, Homeodomain Proteins, Gene Expression Regulation, Plant, Meristem, MADS Domain Proteins, Arabidopsis Proteins, Plants, Genetically Modified, Flowers, Protein Multimerization

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review