The Role of WRKY Transcription Factors in Plant Immunity

Abstract

Plants constantly face a plethora of abiotic and biotic stresses in their natural habitat. Adapting to such changes requires a great degree of phenotypic plasticity that is mainly determined by the plant's genome. We currently do not know how plants are able to integrate the multitude of partly synergistic/partly antagonistic environmental signals that enable them to respond properly under any given condition. What has become apparent, however, is that plants are capable of extensive reprogramming of their transcriptome in a highly dynamic and temporal manner. This regulation in response, leading to adaptive plasticity of plants in highly variable environments, is mainly achieved by enforcement of a network of various transcription factors (TFs). WRKY TFs are a large family of regulatory proteins forming such a network (Eulgem and Somssich, 2007). They are involved in various plant processes but most notably in coping with diverse biotic and abiotic stresses. In this update, we will restrict our attention to the role of WRKY TFs in plant immunity. The WRKY TF superfamily consists of 74 and 109 members in Arabidopsis (Arabidopsis thaliana) and rice (Oryza sativa), respectively (Eulgem and Somssich, 2007; Ross et al., 2007). Members of this family contain at least one conserved DNA-binding region, designated the WRKY domain, comprising the highly conserved WRKYGQK peptide sequence and a zinc finger motif (CX4–7CX22–23HXH/C). This domain generally binds to the DNA element termed the W box (C/TTGACT/C), although alternative binding sites have been identified (Sun et al., 2003; Cai et al., 2008; Ciolkowski et al., 2008; van Verk et al., 2008). WRKY family members are divided into three groups based on the number of WRKY domains and certain features of the zinc finger-like motifs (Eulgem et al., 2000). The NMR solution structure revealed that the C-terminal WRKY domain of Arabidopsis WRKY4 consists of a four-stranded β-sheet, with a zinc-binding pocket formed by the conserved Cys/His residues located at one end of the β-sheet, and the WRKYGQK residues, corresponding to the most N-terminal β-strand (strand β-1), kinked in the middle of the sequence by the Gly residue (Yamasaki et al., 2005). The concave curvature of strand β-1 induced by this kink is predicted to enable this strand to deeply enter the DNA groove and make contact with bases of the W box element. The crystal structure of the extended WRKY domain of Arabidopsis WRKY1 (AtWRKY1-C) revealed that this domain is composed of a globular structure with five β-strands forming an antiparallel β-sheet with an additional novel zinc-binding site at one end (Duan et al., 2007). One should note, however, that no crystal structure information exists of a WRKY domain associated with its DNA-binding site or for a full-length WRKY protein. WRKY factors were generally regarded as being plant specific, but their identification in the protist Giardia lamblia and the slime mold Dictyostelium discoideum imply an earlier origin (Ülker and Somssich, 2004; Pan et al., 2009). They may have evolutionary links with transposons such as Mutator-like elements and could have originated from a BED finger intermediate (an atypical zinc finger DNA-binding domain found both in cellular chromatin boundary element-binding proteins BEAF and DREF and in transposases from animals), although this is controversially debated (Babu et al., 2006; Yamasaki et al., 2008). Duplicated WRKY genes have been maintained in wild and cultivated plant species in the course of selection during domestication and polyploidization (Petitot et al., 2008). They have recently been associated with the viability of interploidy hybrids (Dilkes et al., 2008). Phylogenetic sequence analysis and comparative transcriptomics have revealed that they have retained their functions between monocots and dicots (Mangelsen et al., 2008). The majority of the analyzed WRKY genes respond to pathogen attack and to the endogenous signal molecule salicylic acid (SA; Eulgem and Somssich, 2007). Plant innate immunity is composed of two interconnected branches: (1) PTI, or pathogen-associated molecular pattern (PAMP)-triggered immunity, which is initiated by the recognition of molecular signatures of many pathogens and often activates downstream mitogen-activated protein (MAP) kinase cascades and defense genes; and (2) ETI, or effector-triggered immunity, driven by plant disease resistance proteins (major R gene products) that recognize directly or indirectly specific pathogen-derived effectors (Chisholm et al., 2006). PTI and ETI activate local as well as systemic defense responses (called systemic acquired resistance [SAR]), which are modulated by phytohormones, especially jasmonic acid (JA) and SA (Durrant and Dong, 2004; Bostock, 2005). JA-dependent plant defenses are generally activated by necrotrophic pathogens and chewing insects, whereas SA-dependent defenses are often triggered by biotrophic pathogens. JA and SA signaling usuall