MpNPR modulates lineage-specific oil body development and defence against gastropod herbivory in Marchantia polymorpha

The transition to land exposed early plants to novel biotic constraints, creating strong selection pressures that drove the evolution of the plant immune system. Extant land plants comprise two major groups, tracheophytes and bryophytes, which include liverworts, hornworts and mosses. These two groups diverged early after land colonization, and thus, immune mechanisms have also been subjected to independent evolution. Here, we investigated the function of the unique NPR in the liverwort Marchantia polymorpha and report that it exhibits a specialised immune function relative to its orthologs in tracheophytes. We show that MpNPR modulates the formation of oil bodies, a synapomorphy of liverworts, which function as storage organelles for secondary metabolites and defence against arthropods. We found that MpNPR interacts with MpERF13, a transcription factor controlling oil body differentiation, and that plants with altered levels of MpNPR are misregulated in the expression of MpERF13-dependent genes. Furthermore, we uncover that MpNPR and MpERF13 are required for the defence against snail herbivory. Finally, we show that the ability of MpNPR to induce oil body formation and resistance to gastropods is fully dependent on MpERF13. Taken together, our results demonstrate that NPR mediates a novel regulatory pathway in lineage-specific oil body formation and immunity against gastropod herbivory through the MpERF13 TF in Marchantia, while also pinpoint a novel specialised evolutionary trajectory of NPR in liverworts.