title: Arabidopsis BIRD Zinc Finger Proteins Jointly Stabilize Tissue Boundaries by Confining the Cell Fate Regulator SHORT-ROOT and Contributing to Fate Specification.
abstract: Plant cells cannot rearrange their positions; therefore, sharp tissue boundaries must be accurately programmed. Movement of the cell fate regulator SHORT-ROOT from the stele to the ground tissue has been associated with transferring positional information across tissue boundaries. The zinc finger BIRD protein JACKDAW has been shown to constrain SHORT-ROOT movement to a single layer, and other BIRD family proteins were postulated to counteract JACKDAW's role in restricting SHORT-ROOT action range. Here, we report that regulation of SHORT-ROOT movement requires additional BIRD proteins whose action is critical for the establishment and maintenance of the boundary between stele and ground tissue. We show that BIRD proteins act in concert and not in opposition. The exploitation of asymmetric redundancies allows the separation of two BIRD functions: constraining SHORT-ROOT spread through nuclear retention and transcriptional regulation of key downstream SHORT-ROOT targets, including SCARECROW and CYCLIND6. Our data indicate that BIRD proteins promote formative divisions and tissue specification in the Arabidopsis thaliana root meristem ground tissue by tethering and regulating transcriptional competence of SHORT-ROOT complexes. As a result, a tissue boundary is not "locked in" after initial patterning like in many animal systems, but possesses considerable developmental plasticity due to continuous reliance on mobile transcription factors.
authors.affiliation: Plant Developmental Biology, Wageningen University, Wageningen 6708PB, The Netherlands Molecular Genetics, Department of Biology, Utrecht University, Utrecht 3581CH, The Netherlands.
authors.forename: Yuchen
authors.initials: Y
authors.lastname: Long
authors.affiliation: Plant Developmental Biology, Wageningen University, Wageningen 6708PB, The Netherlands Molecular Genetics, Department of Biology, Utrecht University, Utrecht 3581CH, The Netherlands.
authors.forename: Wouter
authors.initials: W
authors.lastname: Smet
authors.affiliation: Molecular Genetics, Department of Biology, Utrecht University, Utrecht 3581CH, The Netherlands.
authors.forename: Alfredo
authors.initials: A
authors.lastname: Cruz-Ramírez
authors.affiliation: Molecular Genetics, Department of Biology, Utrecht University, Utrecht 3581CH, The Netherlands.
authors.forename: Bas
authors.initials: B
authors.lastname: Castelijns
authors.affiliation: Molecular Genetics, Department of Biology, Utrecht University, Utrecht 3581CH, The Netherlands.
authors.forename: Wim
authors.initials: W
authors.lastname: de Jonge
authors.affiliation: Institute of Biotechnology and Department of Biosciences, University of Helsinki, Helsinki 00014, Finland.
authors.forename: Ari Pekka
authors.initials: AP
authors.lastname: Mähönen
authors.affiliation: Cell Biology, Faculty of Science, Utrecht University, Utrecht 3581CH, The Netherlands.
authors.forename: Benjamin P
authors.initials: BP
authors.lastname: Bouchet
authors.affiliation: Bioinformatics, Plant Sciences, Wageningen University, Wageningen 6708PB, The Netherlands.
authors.forename: Gabino Sanchez
authors.initials: GS
authors.lastname: Perez
authors.affiliation: Cell Biology, Faculty of Science, Utrecht University, Utrecht 3581CH, The Netherlands.
authors.forename: Anna
authors.initials: A
authors.lastname: Akhmanova
authors.affiliation: Plant Developmental Biology, Wageningen University, Wageningen 6708PB, The Netherlands Molecular Genetics, Department of Biology, Utrecht University, Utrecht 3581CH, The Netherlands.
authors.forename: Ben
authors.initials: B
authors.lastname: Scheres
authors.affiliation: Plant Developmental Biology, Wageningen University, Wageningen 6708PB, The Netherlands Molecular Genetics, Department of Biology, Utrecht University, Utrecht 3581CH, The Netherlands ikram.blilou@wur.nl.
authors.forename: Ikram
authors.initials: I
authors.lastname: Blilou
mesh_terms: D017360:Arabidopsis / Q000166:cytology* / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D018506:Gene Expression Regulation, Plant / Q000235:genetics / Q000502:physiology; D018519:Meristem / Q000166:cytology* / Q000378:metabolism; D018517:Plant Roots / Q000166:cytology / Q000378:metabolism
chemical_list: D029681:Arabidopsis Proteins; C100978:SCR protein, Arabidopsis
references.citation: Science. 2007 Apr 20;316(5823):421-5
references.pmid: 17446396
references.citation: BMC Genomics. 2006;7:158
references.pmid: 16784536
references.citation: Cell. 1999 Nov 24;99(5):473-83
references.pmid: 10589676
references.citation: Cell. 2000 May 26;101(5):555-67
references.pmid: 10850497
references.citation: Genes Dev. 2000 Dec 1;14(23):2938-43
references.pmid: 11114883
references.citation: Nature. 2001 Sep 20;413(6853):307-11
references.pmid: 11565032
references.citation: Development. 2003 Sep;130(18):4351-62
references.pmid: 12900451
references.citation: Nature. 2003 Nov 13;426(6963):181-6
references.pmid: 14614507
references.citation: Nucleic Acids Res. 2004;32(5):1710-20
references.pmid: 15020707
references.citation: Development. 2004 Jun;131(12):2817-26
references.pmid: 15142972
references.citation: BMC Genomics. 2004 Jul 5;5(1):39
references.pmid: 15236668
references.citation: Genes Dev. 2004 Aug 15;18(16):1964-9
references.pmid: 15314023
references.citation: Curr Biol. 2004 Oct 26;14(20):1847-51
references.pmid: 15498493
references.citation: Development. 1993 Sep;119(1):71-84
references.pmid: 8275865
references.citation: Science. 1995 Dec 22;270(5244):1980-3
references.pmid: 8533088
references.citation: Cell. 1996 Aug 9;86(3):423-33
references.pmid: 8756724
references.citation: Plant Physiol. 1996 Mar;110(3):945-55
references.pmid: 8819871
references.citation: Cell. 1998 May 15;93(4):593-603
references.pmid: 9604934
references.citation: Plant J. 1998 May;14(4):425-30
references.pmid: 9670559
references.citation: Plant J. 1998 Dec;16(6):735-43
references.pmid: 10069079
references.citation: Development. 2005 Dec;132(24):5387-98
references.pmid: 16291794
references.citation: Cell. 2005 Dec 29;123(7):1337-49
references.pmid: 16377572
references.citation: Semin Cell Dev Biol. 2007 Apr;18(2):171-7
references.pmid: 17398125
references.citation: Nat Protoc. 2006;1(4):1939-46
references.pmid: 17487180
references.citation: PLoS Biol. 2006 May;4(5):e143
references.pmid: 16640459
references.citation: Nat Protoc. 2007;2(7):1565-72
references.pmid: 17585298
references.citation: J Biosci Bioeng. 2007 Jul;104(1):34-41
references.pmid: 17697981
references.citation: Genes Dev. 2007 Sep 1;21(17):2196-204
references.pmid: 17785527
references.citation: PLoS One. 2007;2(10):e1011
references.pmid: 17925859
references.citation: Nature. 2007 Oct 25;449(7165):1008-13
references.pmid: 17960234
references.citation: Plant Cell. 2008 Jun;20(6):1494-503
references.pmid: 18523061
references.citation: Plant J. 2009 Mar;57(5):785-97
references.pmid: 19000160
references.citation: Nat Methods. 2010 Feb;7(2):137-9
references.pmid: 20081836
references.citation: Curr Biol. 2010 Mar 9;20(5):452-7
references.pmid: 20171102
references.citation: Nature. 2010 Apr 8;464(7290):913-6
references.pmid: 20220754
references.citation: Development. 2010 May;137(9):1523-9
references.pmid: 20356954
references.citation: Plant J. 2010 Mar;61(5):893-903
references.pmid: 20015064
references.citation: Nature. 2010 Jul 1;466(7302):128-32
references.pmid: 20596025
references.citation: Science. 2010 Aug 27;329(5995):1065-7
references.pmid: 20798316
references.citation: Curr Biol. 2011 Sep 27;21(18):1559-64
references.pmid: 21924907
references.citation: Plant Mol Biol. 2011 Nov;77(4-5):489-99
references.pmid: 21935722
references.citation: Curr Biol. 2011 Nov 22;21(22):1918-23
references.pmid: 22079112
references.citation: Dev Cell. 2011 Dec 13;21(6):1144-55
references.pmid: 22172675
references.citation: Plant Physiol. 2012 Apr;158(4):1769-78
references.pmid: 22312006
references.citation: Cell. 2012 Aug 31;150(5):1002-15
references.pmid: 22921914
references.citation: Plant J. 2013 Apr;74(1):148-59
references.pmid: 23294290
references.citation: Plant Signal Behav. 2012 Dec;7(12):1573-7
references.pmid: 23072993
references.citation: Dev Cell. 2014 Feb 10;28(3):295-309
references.pmid: 24486153
references.citation: Plant Cell. 2014 Mar;26(3):862-75
references.pmid: 24632533
references.citation: Proc Natl Acad Sci U S A. 2014 May 27;111(21):7861-6
references.pmid: 24821766
references.citation: Biochemistry. 2006 May 30;45(21):6570-80
references.pmid: 16716067
references.citation: Cell. 1999 Nov 24;99(5):463-72
references.pmid: 10589675