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

FLORENT SN; MENTINK RA.; UEDA T; MORENO JE; ROMANI F; KANAZAWA T; DIERSCHKE T; BOWMAN JL; BANIC E; GOODGER JQD; ZACHGO, SABINE; TSIANTIS M

Washington

Congreso; Plant Biology 2020; 2020

American Society of Plant Biologists

New model organisms, as the liverwort Marchantiapolymorpha, provide the opportunity to assess the role of genes in amacroevolutionary scale. The origin of a terrestrial flora (~450 Mya) requiredadaptation to novel biotic and abiotic stressors where transcription factorsplay critical functions. Oil bodies, a synapomorphy of liverworts, accumulatesecondary metabolites, but their function and development are poorlyunderstood. Oil bodies of M. polymorpha develop within specializedscattered cells as one single large organelle. Here, we study the role of thesingle class I homeodomain leucine-zipper (C1HDZ) transcription in M.polymorpha. In flowering plants, these transcription factors primarilymodulate responses to abiotic stress. However, little is known about their rolein other plant lineages. To unveil the physiological role of the singleortholog gene, MpC1HDZ, of M. polymorpha we generated loss-of-functionalleles. The most prominent phenotype of the mutants was the strong reductionof oil body cell number. We found a wild-type response of the mutants to abioticstress. However, Mpc1hdz mutant plants were more susceptible to pill bugherbivory, and total plant extracts from the mutant exhibited reducedantibacterial activity. Transcriptomic analysis of the mutant revealed areduction in expression of genes related to secondary metabolism. In agreement,metabolomic analysis also showed a strong depletion in oil body specific terpenoidcompounds, such as mono- and sesquiterpenes. Moreover, MpC1HDZ is expressed inearly stages of oil body cell development and its expression maxima precededoil body cell differentiation. Our results provide genetic evidence in a long-standingquestion in liverworts. Oil bodies are required for defense against herbivory,but not for abiotic stress tolerance. Also, C1HDZ transcription factor inMarchantia present a divergent function respect to vascular plants, positivelyregulating oil body cell differentiation. Thus, C1HDZ function in abioticstress might have evolved later during vascular plant evolution.