Alanine zipper-like coiled-coil domains are necessary for homotypic dimerization of plant GAGA-factors in the nucleus and nucleolus

Dierk Wanke, Mareike L Hohenstatt, Marek Dynowski, Ulrich Bloss, Andreas Hecker, Kirstin Elgass, Sabine Hummel, Achim Hahn, Katharina Caesar, Frank E Schleifenbaum, Klaus Harter, Kenneth Wayne Berendzen

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Abstract

GAGA-motif binding proteins control transcriptional activation or repression of homeotic genes. Interestingly, there are no sequence similarities between animal and plant proteins. Plant BBR/BPC-proteins can be classified into two distinct groups: Previous studies have elaborated on group I members only and so little is known about group II proteins. Here, we focused on the initial characterization of AtBPC6, a group II protein from Arabidopsis thaliana. Comparison of orthologous BBR/BPC sequences disclosed two conserved signatures besides the DNA binding domain. A first peptide signature is essential and sufficient to target AtBPC6-GFP to the nucleus and nucleolus. A second domain is predicted to form a zipper-like coiled-coil structure. This novel type of domain is similar to Leucine zippers, but contains invariant alanine residues with a heptad spacing of 7 amino acids. By yeast-2-hybrid and BiFC-assays we could show that this Alanine zipper domain is essential for homotypic dimerization of group II proteins in vivo. Interhelical salt bridges and charge-stabilized hydrogen bonds between acidic and basic residues of the two monomers are predicted to form an interaction domain, which does not follow the classical knobs-into-holes zipper model. FRET-FLIM analysis of GFP/RFP-hybrid fusion proteins validates the formation of parallel dimers in planta. Sequence comparison uncovered that this type of domain is not restricted to BBR/BPC proteins, but is found in all kingdoms.
Original languageEnglish
Article numbere16070
Number of pages15
JournalPLoS ONE
Volume6
Issue number2
DOIs
Publication statusPublished - 2011
Externally publishedYes

Cite this

Wanke, Dierk ; Hohenstatt, Mareike L ; Dynowski, Marek ; Bloss, Ulrich ; Hecker, Andreas ; Elgass, Kirstin ; Hummel, Sabine ; Hahn, Achim ; Caesar, Katharina ; Schleifenbaum, Frank E ; Harter, Klaus ; Berendzen, Kenneth Wayne. / Alanine zipper-like coiled-coil domains are necessary for homotypic dimerization of plant GAGA-factors in the nucleus and nucleolus. In: PLoS ONE. 2011 ; Vol. 6, No. 2.
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title = "Alanine zipper-like coiled-coil domains are necessary for homotypic dimerization of plant GAGA-factors in the nucleus and nucleolus",
abstract = "GAGA-motif binding proteins control transcriptional activation or repression of homeotic genes. Interestingly, there are no sequence similarities between animal and plant proteins. Plant BBR/BPC-proteins can be classified into two distinct groups: Previous studies have elaborated on group I members only and so little is known about group II proteins. Here, we focused on the initial characterization of AtBPC6, a group II protein from Arabidopsis thaliana. Comparison of orthologous BBR/BPC sequences disclosed two conserved signatures besides the DNA binding domain. A first peptide signature is essential and sufficient to target AtBPC6-GFP to the nucleus and nucleolus. A second domain is predicted to form a zipper-like coiled-coil structure. This novel type of domain is similar to Leucine zippers, but contains invariant alanine residues with a heptad spacing of 7 amino acids. By yeast-2-hybrid and BiFC-assays we could show that this Alanine zipper domain is essential for homotypic dimerization of group II proteins in vivo. Interhelical salt bridges and charge-stabilized hydrogen bonds between acidic and basic residues of the two monomers are predicted to form an interaction domain, which does not follow the classical knobs-into-holes zipper model. FRET-FLIM analysis of GFP/RFP-hybrid fusion proteins validates the formation of parallel dimers in planta. Sequence comparison uncovered that this type of domain is not restricted to BBR/BPC proteins, but is found in all kingdoms.",
author = "Dierk Wanke and Hohenstatt, {Mareike L} and Marek Dynowski and Ulrich Bloss and Andreas Hecker and Kirstin Elgass and Sabine Hummel and Achim Hahn and Katharina Caesar and Schleifenbaum, {Frank E} and Klaus Harter and Berendzen, {Kenneth Wayne}",
year = "2011",
doi = "10.1371/journal.pone.0016070",
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Wanke, D, Hohenstatt, ML, Dynowski, M, Bloss, U, Hecker, A, Elgass, K, Hummel, S, Hahn, A, Caesar, K, Schleifenbaum, FE, Harter, K & Berendzen, KW 2011, 'Alanine zipper-like coiled-coil domains are necessary for homotypic dimerization of plant GAGA-factors in the nucleus and nucleolus', PLoS ONE, vol. 6, no. 2, e16070. https://doi.org/10.1371/journal.pone.0016070

Alanine zipper-like coiled-coil domains are necessary for homotypic dimerization of plant GAGA-factors in the nucleus and nucleolus. / Wanke, Dierk; Hohenstatt, Mareike L; Dynowski, Marek; Bloss, Ulrich; Hecker, Andreas; Elgass, Kirstin; Hummel, Sabine; Hahn, Achim; Caesar, Katharina; Schleifenbaum, Frank E; Harter, Klaus; Berendzen, Kenneth Wayne.

In: PLoS ONE, Vol. 6, No. 2, e16070, 2011.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Alanine zipper-like coiled-coil domains are necessary for homotypic dimerization of plant GAGA-factors in the nucleus and nucleolus

AU - Wanke, Dierk

AU - Hohenstatt, Mareike L

AU - Dynowski, Marek

AU - Bloss, Ulrich

AU - Hecker, Andreas

AU - Elgass, Kirstin

AU - Hummel, Sabine

AU - Hahn, Achim

AU - Caesar, Katharina

AU - Schleifenbaum, Frank E

AU - Harter, Klaus

AU - Berendzen, Kenneth Wayne

PY - 2011

Y1 - 2011

N2 - GAGA-motif binding proteins control transcriptional activation or repression of homeotic genes. Interestingly, there are no sequence similarities between animal and plant proteins. Plant BBR/BPC-proteins can be classified into two distinct groups: Previous studies have elaborated on group I members only and so little is known about group II proteins. Here, we focused on the initial characterization of AtBPC6, a group II protein from Arabidopsis thaliana. Comparison of orthologous BBR/BPC sequences disclosed two conserved signatures besides the DNA binding domain. A first peptide signature is essential and sufficient to target AtBPC6-GFP to the nucleus and nucleolus. A second domain is predicted to form a zipper-like coiled-coil structure. This novel type of domain is similar to Leucine zippers, but contains invariant alanine residues with a heptad spacing of 7 amino acids. By yeast-2-hybrid and BiFC-assays we could show that this Alanine zipper domain is essential for homotypic dimerization of group II proteins in vivo. Interhelical salt bridges and charge-stabilized hydrogen bonds between acidic and basic residues of the two monomers are predicted to form an interaction domain, which does not follow the classical knobs-into-holes zipper model. FRET-FLIM analysis of GFP/RFP-hybrid fusion proteins validates the formation of parallel dimers in planta. Sequence comparison uncovered that this type of domain is not restricted to BBR/BPC proteins, but is found in all kingdoms.

AB - GAGA-motif binding proteins control transcriptional activation or repression of homeotic genes. Interestingly, there are no sequence similarities between animal and plant proteins. Plant BBR/BPC-proteins can be classified into two distinct groups: Previous studies have elaborated on group I members only and so little is known about group II proteins. Here, we focused on the initial characterization of AtBPC6, a group II protein from Arabidopsis thaliana. Comparison of orthologous BBR/BPC sequences disclosed two conserved signatures besides the DNA binding domain. A first peptide signature is essential and sufficient to target AtBPC6-GFP to the nucleus and nucleolus. A second domain is predicted to form a zipper-like coiled-coil structure. This novel type of domain is similar to Leucine zippers, but contains invariant alanine residues with a heptad spacing of 7 amino acids. By yeast-2-hybrid and BiFC-assays we could show that this Alanine zipper domain is essential for homotypic dimerization of group II proteins in vivo. Interhelical salt bridges and charge-stabilized hydrogen bonds between acidic and basic residues of the two monomers are predicted to form an interaction domain, which does not follow the classical knobs-into-holes zipper model. FRET-FLIM analysis of GFP/RFP-hybrid fusion proteins validates the formation of parallel dimers in planta. Sequence comparison uncovered that this type of domain is not restricted to BBR/BPC proteins, but is found in all kingdoms.

UR - http://www.ncbi.nlm.nih.gov/pubmed/21347358

U2 - 10.1371/journal.pone.0016070

DO - 10.1371/journal.pone.0016070

M3 - Article

VL - 6

JO - PLoS ONE

JF - PLoS ONE

SN - 1932-6203

IS - 2

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