Phytoalexin gene regulation in Arabidopsis thaliana – On the verge of a paradigm shift?

Phytoalexins are plant-specialized metabolites that are biosynthesized de novo in response to pathogens. Their biosynthesis is highly diverse, with different plant lineages biosynthesizing unique molecules. A common notion is that individual plant species produce one type of phytoalexin molecule. Arabidopsis is well known to produce an indole alkaloid phytoalexin, named camalexin, as an important component in its defense against microbial pathogens. However, studies collectively demonstrate that Arabidopsis produces a diverse array of phytoalexin molecules from different branches of primary and specialized metabolism. The signaling proteins that stimulate phytoalexin synthesis are highly conserved in plants, yet each transcription factor that they converge upon has been reported to regulate the biosynthesis of a specific class of phytoalexin metabolite. We have conducted this review because recent studies have demonstrated that homologs of Arabidopsis transcription factors regulate dissimilar phytoalexin biosynthetic pathways in other plant species. These findings challenge the paradigm that each transcription factor has a role in regulating a specific class of specialized metabolite. Here, we review the diverse phytoalexin biosynthetic pathways of Arabidopsis, the transcription factors that regulate them, and recent discoveries on their regulatory mechanisms. We discuss important discoveries in crop plant species that suggest that the Arabidopsis transcription factors WRKY33, ERF1, ANAC042, MYB15, MYB72, and the protein JAZ1, are part of a 'core' phytoalexin regulatory network that is conserved, yet regulates distinct phytoalexin pathways in different plant lineages. Finally, we highlight important questions raised by the recent discoveries that, once solved, will provide major advances in our understanding of the evolution of biochemical defenses in plants. Recent evidence demonstrates that these conserved transcription factors can be manipulated to enhance phytoalexin production and pathogen resistance in crop plants.