Re-engineering a lost trait:IPD3, a master regulator of arbuscular mycorrhizal symbiosis, affects genes for immunity and metabolism of non-host Arabidopsis when restored long after its evolutionary loss

Abstract

AbstractArbuscular mycorrhizal symbiosis (AM) is a beneficial trait originating with the first land plants, which has subsequently been lost by species scattered throughout the radiation of plant diversity to the present day, including the modelArabidopsis thaliana. To explore why an apparently beneficial trait would be repeatedly lost, we generatedArabidopsisplants expressing a constitutively active form ofInteracting Protein of DMI3, a key transcription factor that enables AM within the Common Symbiosis Pathway, which was lost fromArabidopsisalong with the AM host trait. We characterize the transcriptomic effect of expressingIPD3inArabidopsiswith and without exposure to the AM fungus (AMF)Rhizophagus irregularis, and compare these results to the AM modelLotus japonicusand itsipd3knockout mutantcyclops-4. Despite its long history as a non-AM species, restoringIPD3in the form of its constitutively active DNA-binding domain toArabidopsisaltered expression of specific gene networks. Surprisingly, the effect of expressingIPD3inArabidopsisand knocking it out inLotuswas strongest in plants not exposed to AMF, which is revealed to be due to changes inIPD3genotype causing a transcriptional state which partially mimics AMF exposure in non-inoculated plants. Our results indicate that despite the long interval since loss of AM andIPD3inArabidopsis, molecular connections to symbiosis machinery remain in place in this nonAM species, with implications for both basic science and the prospect of engineering this trait for agriculture.