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Studies on DNA-Binding Selectivity of WRKY Transcription Factors Lend Structural Clues Into WRKY-Domain Function

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Studies on DNA-Binding Selectivity of WRKY Transcription Factors Lend Structural Clues Into WRKY-Domain Function Plant Mol Biol (2008) 68:81–92 DOI 10.1007/s11103-008-9353-1 Studies on DNA-binding selectivity of WRKY transcription factors lend structural clues into WRKY-domain function Ingo Ciolkowski Æ Dierk Wanke Æ Rainer P. Birkenbihl Æ Imre E. Somssich Received: 3 December 2007 / Accepted: 21 May 2008 / Published online: 4 June 2008 Ó The Author(s) 2008 Abstract WRKY transcription factors have been shown amino acid substitutions within the DNA binding region of to play a major role in regulating, both positively and AtWRKY11 strongly impinge on its binding activity. negatively, the plant defense transcriptome. Nearly all Additionally, all five factors were found localized exclu- studied WRKY factors appear to have a stereotypic binding sively to the plant cell nucleus and to be capable of trans- preference to one DNA element termed the W-box. How activating expression of a reporter gene construct in vivo. specificity for certain promoters is accomplished therefore remains completely unknown. In this study, we tested five Keywords Arabidopsis promoters Á Nuclear localization Á distinct Arabidopsis WRKY transcription factor subfamily Transactivation Á W-box element members for their DNA binding selectivity towards vari- ants of the W-box embedded in neighboring DNA sequences. These studies revealed for the first time dif- Introduction ferences in their binding site preferences, which are partly dependent on additional adjacent DNA sequences outside Transcription factors act in concert with other components of the TTGACY-core motif. A consensus WRKY binding of the transcriptional machinery to modulate the expression site derived from these studies was used for in silico of target genes in a temporal and spatial manner. In gen- analysis to identify potential target genes within the Ara- eral, they do so by binding to short defined nucleotide bidopsis genome. Furthermore, we show that even subtle motifs (cis-elements) within the regulatory regions of genes that are under their control. Different classes of transcription factors have characteristic DNA-binding Electronic supplementary material The online version of this domains that discriminate between distinct cis-regulatory article (doi:10.1007/s11103-008-9353-1) contains supplementary elements at target sites within the genome. Our studies material, which is available to authorized users. have been focused on a family of zinc-finger type tran- I. Ciolkowski Á D. Wanke Á R. P. Birkenbihl Á scription factors, designated WRKY. WRKY factors I. E. Somssich (&) comprise a large family of DNA-binding proteins found in Department of Plant Microbe Interactions, Max Planck Institute all plants (Eulgem and Somssich 2007). Although not for Plant Breeding Research, Carl-von-Linne´-Weg 10, 50829 Koln, Germany completely restricted to the plant kingdom, this family has e-mail: [email protected] expanded enormously in higher plants whereas they appear to have been lost in yeast and animal lineages (U¨ lker and Present Address: Somssich 2004). WRKY proteins have been implicated in I. Ciolkowski Justus-Liebig-Universita¨t Giessen, IPAZ, Heinrich-Buff-Ring the regulation of developmental processes such as trichome 26-32, 35392 Giessen, Germany and seed development and leaf senescence (Hinderhofer and Zentgraf 2001; Johnson et al. 2002; Luo et al. 2005), Present Address: but their major functions appear to be in helping the plant D. Wanke ¨ ZMBP – Pflanzenphysiologie, Auf der Morgenstelle 1, 72076 to cope with various abiotic and biotic stresses (Ulker and Tubingen, Germany Somssich 2004; Journot-Catalino et al. 2006; Li et al. 123 82 Plant Mol Biol (2008) 68:81–92 2006; Wang et al. 2006; Xu et al. 2006; Zheng et al. 2006; exclusively to the nucleus and that all have in vivo trans- Shen et al. 2007). activation capabilities. All WRKY proteins contain a 60 amino acid long pep- tide region, termed the WRKY domain, which constitutes their DNA binding regions. Apart from the invariant name- Materials and methods giving amino acid residues W R K and Y, this domain also contains conserved cysteine and histidine residues that bind Recombinant fusion proteins one zinc atom and form a finger-like structure. Both the WRKY residues as well as the zinc finger motif are The AtWRKY cDNA fragments were obtained with spe- required for proper DNA binding of the protein (Maeo cific Gateway-primers in RT-PCR reactions and cloned in- et al. 2001). Based on the number of WRKY domains and frame into the modified bacterial expression vector the pattern of the zinc-finger motif, WRKY factors have pGEX2T (Pharmacia) or into the vector pQE30a (Qiagen) been classified into three major groups (Eulgem et al. and verified by sequencing. The C-terminal protein con- 2000). The number of family members in higher plants can struct of WRKY11 (WRKY CTD) consisted of 98 amino range from 74 in Arabidopsis, 98 to 102 in rice or even acids encompassing the WRKY DNA binding domain and more in other species such as tobacco (U¨ lker and Somssich in addition carrying a 69His tag at its N-terminus 2004; Ross et al. 2007). MRGSHHHHHHMKRTVRVPAISAKIADIPPDEYSWR Gel-shift experiments, random binding site selection, KYGQKPIKGSPHPRGYYKCSTFRGCPARKHVERA DNA-ligand binding screens, yeast one-hybrid studies and LDDPAMLIVTYEGEHRHNQSAMQENISSSGINDLV cotransfection assays performed with different plant FASA. Mutations within the WRKY11 CTD were WRKY proteins have illustrated that the cis-element introduced using the megaprimer method (Ke and Mad- 50-TTGAC-C/T-30, termed the W-box, represents the ison 1997) and cloned into the Gateway compatible minimal consensus required for specific DNA binding (de vector pASK5 (IBA). A list of the primers used in this Pater et al. 1996; Rushton et al. 1996; Wang et al. 1998; study are given in the supplementary table (S-Table 1). Chen and Chen 2000; Cormack et al. 2002). Only in the Protein expression was carried out in E. coli strain case of the barley WRKY factor SUSIBA2 and the tobacco BL21(DE3) following addition of IPTG (1 mM) or 2 lg/ NtWRKY12 have additional DNA binding sites been ll anhydrous tetracyclin (IBA) for 3–4 h. Bacteria were identified, although SUSIBA2 also shows strong in vitro harvested by centrifugation. The pellet was resuspended binding to the W-box motif (Sun et al. 2003; van Verk and lysed under native conditions but including protease et al. 2008). Considering the size of the WRKY family inhibitors at 4°C (PIERCE, lysis protocol according to within a given species and the apparent stereotypic binding the instructions of the manufacturer). Due to technical preference of these proteins to the W-box, it is difficult to difficulties encountered in purifying the respective foresee how specificity for certain promoters is accom- recombinant WRKY proteins all subsequent experiments plished. A certain level of specificity may be conferred by were performed using total soluble E. coli protein additional nucleotide sequences flanking W-box elements extracts derived from bacteria expressing the WRKY with respective gene promoters. Furthermore, various cDNA construct or the control empty vector construct. WRKY subgroup family members within a single plant For western blot analyses proteins were separated by species may also differ somewhat in their DNA binding SDS-PAGE and blotted onto a PVDF membrane (Sar- requirements. Both of these aspects have not yet been torius). The membranes were probed with anti-GST directly addressed for WRKY transcription factors. Finally, antibody (Pharmacia) or anti-69HIS antibody and anti- the involvement of WRKY factors in diverse higher-order goat or anti-mouse IgG conjugated to alkaline phospha- nucleoprotein complexes can also be assumed and may in tase, respectively. Anti-strep antibody was directly fact be the major criteria in determining promoter selec- conjugated to alkaline phosphatase. Membranes were tivity and transcriptional output. developed with NBT-BCIP solution Sigma-fast (Sigma). In this study, we selected five Arabidopsis WRKY transcription factors representing the three major groups of Electrophoretic mobility shift assay (EMSA) WRKY proteins including three from the largest, namely group II. These factors were analyzed with respect to their Equivalent amounts of sense and antisense fragments of the in vitro binding capabilities to various W-box variants and respective oligonucleotides (Invitrogen) were annealed in promoter sequences containing W-box motifs. This anal- 40 mM Tris–HCl pH 7.5, 20 mM MgCl2, and 50 mM NaCl ysis already revealed clear as yet not observed binding site starting at 95°C and allowing to cool slowly to room tem- preferences between certain representatives. Furthermore, perature. About 1.5 ll of the solution corresponding to we show that all studied WRKY factors are localized 150 ng DNA was used for end-labeling with 5 U of terminal 123 Plant Mol Biol (2008) 68:81–92 83 transferase (Roche) and 20 lCi dCTP (Amersham) in a total Cis-element analysis volume of 25 ll according to the manufacturer’s instructions (Roche). The probes were purified on Sephadex G-25 col- The GenBank DNA sequence flat-files were downloaded umns and diluted to 5000 cpm/ll. Binding reactions were from the Entrez Plant Genomes Central at NCBI (http:// performed according to Maeo et al. (2001). Reaction mix www.ncbi.nlm.nih.gov/; NC_003070.5, NC_003071.3, which included 25 lg of total soluble bacterial protein NC_003074.4, NC_003075.3, NC_003076.4). Sequences of extract was incubated for 20-25 min to 25°C after addition either 1500 or 600 bp upstream of the annotated translation of the radioactively labeled probe then applied to the gel. Gel start sites (ATG) were extracted and compiled to FASTA electrophoresis was carried out at 4°C. Sequence of 19W2: formatted text with the aGenBankSQL script v3.3.4 (Ber- TTATTCAGCCATCAAAAGTTGACCAATAAT. For com- endzen et al. 2006), using the default code modifications. petition experiments unlabelled DNA was added as competitor Number of W-box motifs has been assessed counting their to the binding reaction and incubated for 10 min on ice.
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