Oil Body Formation in Marchantia polymorpha Is Controlled by MpC1HDZ and Serves as a Defense against Arthropod Herbivores

• Published in: Current biology Vol. 30; no. 14; pp. 2815 - 2828.e8
• Main Authors: Romani, Facundo, Banić, Elizabeta, Florent, Stevie N., Kanazawa, Takehiko, Goodger, Jason Q.D., Mentink, Remco A., Dierschke, Tom, Zachgo, Sabine, Ueda, Takashi, Bowman, John L., Tsiantis, Miltos, Moreno, Javier E.
• Format: Journal Article
• Language: English
• Published: England Elsevier Inc 20.07.2020
• Subjects: biotic defense; cell differentiation; evolution; HD-ZIP; liverwort; Marchantia; MpC1HDZ; oil bodies; oil body cell; sesquiterpenes; terpene synthases; transcription factor; HD-ZIP; transcription factor; liverwort; cell differentiation; oil body cell; oil bodies; biotic defense; Marchantia; MpC1HDZ; evolution; terpene synthases; sesquiterpenes
• ISSN: 0960-9822; 1879-0445; 1879-0445
• DOI: 10.1016/j.cub.2020.05.081

The origin of a terrestrial flora in the Ordovician required adaptation to novel biotic and abiotic stressors. Oil bodies, a synapomorphy of liverworts, accumulate secondary metabolites, but their function and development are poorly understood. Oil bodies of Marchantia polymorpha develop within specialized cells as one single large organelle. Here, we show that a class I homeodomain leucine-zipper (C1HDZ) transcription factor controls the differentiation of oil body cells in two different ecotypes of the liverwort M. polymorpha, a model genetic system for early divergent land plants. In flowering plants, these transcription factors primarily modulate responses to abiotic stress, including drought. However, loss-of-function alleles of the single ortholog gene, MpC1HDZ, in M. polymorpha did not exhibit phenotypes associated with abiotic stress. Rather, Mpc1hdz mutant plants were more susceptible to herbivory, and total plant extracts of the mutant exhibited reduced antibacterial activity. Transcriptomic analysis of the mutant revealed a reduction in expression of genes related to secondary metabolism that was accompanied by a specific depletion of oil body terpenoid compounds. Through time-lapse imaging, we observed that MpC1HDZ expression maxima precede oil body formation, indicating that MpC1HDZ mediates differentiation of oil body cells. Our results indicate that M. polymorpha oil bodies, and MpC1HDZ, are critical for defense against herbivory, but not for abiotic stress tolerance. Thus, C1HDZ genes were co-opted to regulate separate responses to biotic and abiotic stressors in two distinct land plant lineages. [Display omitted] •Oil body cell differentiation in M. polymorpha is positively regulated by MpC1HDZ•High expression levels of MpC1HDZ precede oil body differentiation•Terpenoid-rich oil bodies protect the plant against arthropod herbivores Most of the chemical diversity of liverworts resides within oil body cells, a synapomorphy of the lineage. Romani, Banic et al. show that oil bodies defend the plant against arthropods. Moreover, oil body cell differentiation requires the MpC1HDZ transcription factor, which shows high gene expression levels prior to oil body differentiation.