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The potato PR-10a gene, which is induced upon wounding, elicitor treatment or infection with the oomycete Phytophthora infestans contains at least two regulatory regions. One comprises a positive regulatory element, which was shown to be bound by the factor PBF­2, and a negative regulatory element (silencer), which the protein SEBF binds (Després et al., 1995). The Whirly and SEBF proteins were isolated using a similar technique. The two PR-10a promoter regulatory elements were immobilized on magnetic beads and incubated with potato tuber extracts (Desveaux et al., 2000; Boyle and Brisson, 2001). PBF­2 (now called StWhy1; Solanum tuberosum Whirly1) was isolated using the positive regulatory element (Desveaux et al., 2000), while SEBF was isolated using the negative regulatory element (Boyle and Brisson, 2001). Both proteins were later found to belong to small families of plant proteins as compared to the large ERF, MYB and WRKY families. Interestingly, both StWhy1 and SEBF genes were found to encode a plastid transit peptide at the N terminus (Boyle and Brisson, 2001; Desveaux et al., 2004). Every plant species, where sufficient DNA sequence information is available, contains at least two Whirly members, one directed to plastids and one directed to mitochondria (Desveaux et al., 2005), which suggests a specific role for these proteins inside organelles.

Both proteins show an uncharacteristic preference for single­stranded DNA (ssDNA) (Desveaux et al., 2000; Boyle and Brisson, 2001). Furthermore,

Transcription Factor Families and Plant Defence 155 both StWhy1 and SEBF have shown sequence specificity when tested by electrophoretic mobility shift assays. The DNA­binding activity of StWhy1 is induced in potato tubers in response to wounding or an elicitor (Després et al., 1995). This binding activity correlates with the induced expression of the PR-10a gene. Furthermore, ChIP experiments indicated that the protein is present on the promoter of the gene only when tubers are wounded or treated with an elicitor (Desveaux et al., 2004; González­Lamothe et al., 2008).

Overexpression of StWhy1 in potato protoplasts or in yeast confirmed that the protein can activate transcription (Desveaux et al., 2000). In Arabidopsis, two TILLING (targeted induced local lesion in genome) lines containing different point mutations in the AtWhy1 gene were shown to be more susceptible to infection by H. parasitica. Another TILLING line was recently isolated that contains a point mutation in the same gene but leads to increased resistance to the same pathogen (Desveaux, D., Wilton, M., Parent, J.­S. and Brisson, N., unpublished work). Altogether these data support a role for Whirlies in defence responses.

The crystal structure of StWhy1 was solved by X­ray crystallography (Desveaux et al., 2002). Like all the members of its family, StWhy1 contains a Whirly domain, which contains approximately 200 amino acids and consists of two four­stranded antiparallel β­sheets packed perpendicularly against each other and three α­helices. The Whirlies adopt a tetrameric fold in solution. The tetramerization is mediated by the α­helices whereas the β­sheets constitute the putative ssDNA­binding platform. The conserved Whirly domain is necessary and sufficient for ssDNA binding. The structure of StWhy1 is similar to the structure of the mitochondrial guide RNA­binding proteins 1 and 2 (MRP1/2). The structure of MRP1/2 has been solved in complex with guide RNA by X­ray crystallography (Schumacher et al., 2006). However, since both Whirly and MRP1/2 proteins do not possess significant sequence similarity and the residues involved in the RNA binding by MRP1/2 are not conserved in the Whirlies, it seems unlikely that these proteins share a common binding mechanism. Preliminary crystallographic analysis of a StWhy2–ssDNA complex suggests that although the residues contacting ssDNA are located on the β­sheets, the nucleic acid binding mechanism is different for the Whirlies and the MRPs (Cappadocia, L., Sygusch, J., Brisson, N., unpublished results).

SEBF binds ssDNA in a sequence­specific manner (Boyle and Brisson, 2001). The consensus­binding site of SEBF (called the SE element) was found to be C/TTGTCNC. Members of the SEBF family possess two consensus­

sequence RNA binding domains (cs­RBDI and II; also called RNA­recognition motifs (RRM)) arranged in tandem and separated by a glycine­rich linker. SEBF binds to the SE through its cs­RBDII (González­Lamothe et al., 2008). ChIP studies indicate that SEBF binds its element in the promoter of PR­10a in unstimulated cells only. SEBF is released from the promoter upon wounding or treatment with an elicitor, while the same treatment leads to the binding of the activator StWhy1 to a nearby element. Remarkably, the binding of SEBF to the promoter requires the presence of the ERF factor Pti4, which interacts with SEBF through its ERF DNA­binding domain to form the core of a repressosome (Gonzalez­Lamothe et al., 2008).

156 J.-S. Parent et al.

The RRM is a highly plastic domain (reviewed in Maris et al., 2005) capable of interacting with DNA, RNA and even proteins with a broad range of affinities and specificities. Much of our understanding of the DNA/RNA binding by the RRM domain comes from the numerous structures of RRM­

containing proteins in complex with DNA or RNA that have been determined by X­ray crystallography and NMR spectroscopy. A prototypical RRM domain contains approximately 90 amino acids and consists of a four­stranded antiparallel β­sheet packed along two α­helices. The β­sheet constitutes the main DNA/RNA­binding surface while loops and/or N­ and C­terminal regions contribute additional DNA/RNA­binding residues. Two RNP (ribonucleoprotein) motifs, termed RNP1 ([ILF]­[FY]­[ILV]­X­N­L) and RNP2 ([RK]­G­[FY]­[GA]­

[FY]­[ILV]­x­[FY]) constitute the hallmark of the RRM domain and contain basic and aromatic residues involved in DNA/RNA binding. These motifs are located on the central strands of the β­sheet where they mediate the non­sequence­

specific recognition of a pair of nucleotides. Additional non­conserved residues are responsible for the sequence­specific binding of those nucleotides. Each RRM domain can accommodate between two and eight nucleotides. Some proteins, as is the case for SEBF, possess two or multiple copies of the RRM domain arranged in tandem. In most cases, such an arrangement will permit the binding of two adjacent stretches of the same DNA/RNA molecule (Auweter et al., 2006) providing an extended DNA/RNA­binding interface. In other cases, the relative orientation of the RRM domains will favour the looping of the RNA/DNA and the binding to distant sites (Maris et al., 2005). The linker, in addition to its RRM domain positioning role, can also contribute amino acids that are involved in DNA/RNA binding. The plasticity of the RRM domain prevents us from building an accurate model for the binding of SEBF to ssDNA.

The structural basis for sequence­specific recognition consequently awaits the structure of a SEBF–ssDNA complex.

Other TFs have been found to be involved in plant defence. However, they do not seem to be part of well­characterized groups as do the other proteins we have described above. For example, the Arabidopsis gene LSD1 was found to be involved in HR­related cell death (Aviv et al., 2002). Mutant plants of this gene are more susceptible to P. syringae. In a subsequent study, a paralogue gene, LSD-One-Like1 (LOL1) was shown to function as the opposite of LSD1 and to have the opposite effect on resistance (Epple et al., 2003). These genes however could not be grouped into a coherent family and there are no structural data available for analysis.

6.7 Concluding Remarks

Considerable progress has been made during the last few years in our understanding of how transcription is regulated through the action of transcription factors in eukaryotes. In plants, thanks to the rapid advances in genome sequencing and the powerful genetic tools now available, we have witnessed the identification of many families of TFs that play a role in defence

Transcription Factor Families and Plant Defence 157 responses and have started unravelling the function of a few of these factors.

However, when compared to other fields, progress in the study of plant TFs has been slow. A major reason for this is certainly the amazing complexity of plant TF gene families, which often requires that double or even triple KO be produced to obtain a testable phenotype. Progress has been even slower in the biochemical characterization of TFs, with only a few laboratories in the world actively involved in this area. Here again plants add an additional layer of complexity since transient expression studies, an essential tool in the study of transcription, can only be done using protoplasts or other complex approaches such as gene bombardment or Agrobacterium infection. There is no doubt also that the lack of a robust in vitro transcription system in plants has impaired progress in this field. However, one must be hopeful that the rapid development of new technologies that is taking place in biochemistry and genomic research will help not only to identify new TFs but also to understand how these factors contribute to the important remodelling of the transcriptome that takes place during defence responses.

Acknowledgements

The authors wish to thank the Natural Sciences and Engineering Research Council of Canada and the Fonds de la Recherche sur la Nature et les Technologies du Québec for financial support.

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