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During development of flowering plants, some MIKC-type MADS-domain transcription factors (MTFs) exert their regulatory function as heterotetrameric complexes bound to two sites on the DNA of target genes. This way they constitute "floral quartets" or related "floral quartet-like complexes" (FQCs), involving a unique multimeric system of paralogous protein interactions. Tetramerization of MTFs is brought about mainly by interactions of keratin-like (K) domains. The K-domain associated with the more ancient DNA-binding MADS-domain during evolution in the stem group of extant streptophytes (charophyte green algae + land plants). However, whether this was sufficient for MTF tetramerization and FQC formation to occur, remains unknown. Here, we provide biophysical and bioinformatic data indicating that FQC formation likely originated in the stem group of land plants in a sublineage of MIKC-type genes termed MIKCC-type genes. In the stem group of this gene lineage, the duplication of the most downstream exon encoding the K-domain led to a C-terminal elongation of the second K-domain helix, thus, generating the tetramerization interface found in extant MIKCC-type proteins. In the stem group of the sister lineage of the MIKCC-type genes, termed MIKC*-type genes, the duplication of two other K-domain exons occurred, extending the K-domain at its N-terminal end. Our data indicate that this structural change prevents heterodimerization between MIKCC-type and MIKC*-type proteins. This way, two largely independent gene regulatory networks could be established, featuring MIKCC-type or MIKC*-type proteins, respectively, that control different aspects of plant development.

Competing Interests: Conflict of Interest statement. The authors declare no conflict of interest.

Titel:	The Origin of Floral Quartet Formation-Ancient Exon Duplications Shaped the Evolution of MIKC-type MADS-domain Transcription Factor Interactions.
Autor/in / Beteiligte Person:	Rümpler, F ; Tessari, C ; Gramzow, L ; Gafert, C ; Blohs, M ; Theißen, G
Link:	Full Text Finder (Volltext)
Zeitschrift:	Molecular biology and evolution, Jg. 40 (2023-05-02), Heft 5
Veröffentlichung:	2003- : New York, NY : Oxford University Press ; <i>Original Publication</i>: [Chicago, Ill.] : University of Chicago Press, [c1983-, 2023
Medientyp:	academicJournal
ISSN:	1537-1719 (electronic)
DOI:	10.1093/molbev/msad088
Schlagwort:	Phylogeny Genes, Plant Exons Plant Proteins genetics Gene Expression Regulation, Plant Transcription Factors metabolism MADS Domain Proteins genetics
Sonstiges:	Nachgewiesen in: MEDLINE Sprachen: English Publication Type: Journal Article; Research Support, Non-U.S. Gov't Language: English [Mol Biol Evol] 2023 May 02; Vol. 40 (5). MeSH Terms: Transcription Factors* / metabolism ; MADS Domain Proteins* / genetics ; Phylogeny ; Genes, Plant ; Exons ; Plant Proteins / genetics ; Gene Expression Regulation, Plant References: Plant Cell. 2017 Feb;29(2):229-242. (PMID: 28100708) ; Ann Bot. 2007 Sep;100(3):603-19. (PMID: 17670752) ; Gene. 2005 Mar 14;347(2):183-98. (PMID: 15777618) ; Nucleic Acids Res. 2009 Jan;37(1):144-57. (PMID: 19033361) ; J Struct Biol. 2006 Aug;155(2):140-5. (PMID: 16870472) ; Mol Biol Evol. 2011 Jan;28(1):501-11. (PMID: 20724380) ; FEBS J. 2021 May;288(10):3120-3134. (PMID: 32885587) ; Mol Biol Evol. 2012 Jan;29(1):293-302. (PMID: 21813465) ; Proc Natl Acad Sci U S A. 2006 Aug 1;103(31):11647-52. (PMID: 16868079) ; Proc Natl Acad Sci U S A. 2014 Nov 11;111(45):E4859-68. (PMID: 25355905) ; Development. 2012 Sep;139(17):3081-98. (PMID: 22872082) ; J Exp Bot. 2018 Apr 9;69(8):1943-1954. (PMID: 29474620) ; Plant Mol Biol. 2004 May;55(1):45-59. (PMID: 15604664) ; Mol Biol Evol. 2013 Apr;30(4):772-80. (PMID: 23329690) ; Electrophoresis. 1997 Dec;18(15):2714-23. (PMID: 9504803) ; BMC Syst Biol. 2014 Jan 27;8:9. (PMID: 24468197) ; Nature. 2001 Jan 25;409(6819):469-71. (PMID: 11206529) ; Front Plant Sci. 2018 Apr 18;9:510. (PMID: 29720991) ; Biol Direct. 2008 May 21;3:20. (PMID: 18495041) ; Nature. 2006 Sep 28;443(7110):415-20. (PMID: 17006507) ; EMBO J. 1999 Oct 1;18(19):5370-9. (PMID: 10508169) ; J Biol Chem. 1991 Jul 25;266(21):13661-71. (PMID: 1856200) ; Nucleic Acids Res. 2003 Jul 1;31(13):3537-9. (PMID: 12824361) ; Plant Mol Biol. 2000 Apr;42(6):819-32. (PMID: 10890530) ; Gene. 2003 Oct 16;316:1-21. (PMID: 14563547) ; Mol Biol Evol. 2002 Jun;19(6):801-14. (PMID: 12032236) ; Nat Rev Genet. 2010 Dec;11(12):830-42. (PMID: 21063441) ; Plant Cell. 2014 Sep;26(9):3603-15. (PMID: 25228343) ; Nucleic Acids Res. 2009 May;37(8):2723-36. (PMID: 19276203) ; Genome Biol. 2009 Feb 25;10(2):R24. (PMID: 19243611) ; Plant J. 2010 Oct;64(2):177-90. (PMID: 21070403) ; Plant Cell. 2013 Jul;25(7):2560-72. (PMID: 23847151) ; Mol Biol Evol. 2018 Nov 1;35(11):2618-2638. (PMID: 30053121) ; EMBO J. 1990 Apr;9(4):973-9. (PMID: 2182324) ; C R Biol. 2005 Jun;328(6):521-48. (PMID: 15950160) ; Mol Biol Evol. 2010 May;27(5):1201-11. (PMID: 20080864) ; Adv Protein Chem. 2005;70:37-78. (PMID: 15837513) ; Genome Biol. 2010;11(6):214. (PMID: 20587009) ; Proc Natl Acad Sci U S A. 2005 Feb 15;102(7):2436-41. (PMID: 15699346) ; Cell. 1986 Mar 14;44(5):681-7. (PMID: 3948245) ; Nucleic Acids Res. 2018 Jun 1;46(10):4966-4977. (PMID: 29562355) ; Development. 2016 Sep 15;143(18):3259-71. (PMID: 27624831) ; Cell. 2018 Jul 12;174(2):448-464.e24. (PMID: 30007417) ; Eur J Biochem. 1995 Apr 1;229(1):1-13. (PMID: 7744019) ; Plant Physiol. 2007 Jan;143(1):447-60. (PMID: 17071640) ; Trends Biochem Sci. 2008 May;33(5):220-9. (PMID: 18406148) ; Plant Cell. 2005 May;17(5):1424-33. (PMID: 15805477) ; Proc Natl Acad Sci U S A. 2012 Jan 31;109(5):1560-5. (PMID: 22238427) ; Curr Opin Plant Biol. 2001 Feb;4(1):75-85. (PMID: 11163172) ; Nucleic Acids Res. 2014;42(17):10927-42. (PMID: 25183521) Contributed Indexing: Keywords: MADS-box gene; MIKC-type MADS-domain transcription factor; cooperative DNA binding; floral quartet; keratin-like domain; protein–protein interaction Substance Nomenclature: 0 (Transcription Factors) ; 0 (MADS Domain Proteins) ; 0 (Plant Proteins) Entry Date(s): Date Created: 20230412 Date Completed: 20230503 Latest Revision: 20230510 Update Code: 20240514 PubMed Central ID: PMC10152394

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The Origin of Floral Quartet Formation-Ancient Exon Duplications Shaped the Evolution of MIKC-type MADS-domain Transcription Factor Interactions.