Expansion of a core regulon by transposable elements promotes Arabidopsis chemical diversity and pathogen defense

Abstract

Plants synthesize hundreds of thousands of ecologically specialized, lineage-specific metabolites through biosynthetic gene duplication and functional specialization. However, the rewiring of duplicated genes into existing regulatory networks remains unclear. We show that the duplicated gene CYP82C2 was recruited into the WRKY33 regulon and indole-3-carbonylnitrile (ICN) biosynthetic pathway through exaptation of a retroduplicated LINE retrotransposon (EPCOT3) into a novel enhancer. The stepwise development of a chromatin-accessible WRKY33-binding site on EPCOT3 potentiated the regulatory neofunctionalization of CYP82C2 and the evolution of inducible defense metabolite 4-hydroxy-ICN in Arabidopsis thaliana. Transposable elements (TEs) have long been recognized to have the potential to rewire regulatory networks; these results establish a more complete understanding of how duplicated genes and TEs contribute in concert to chemical diversity and pathogen defense.