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

Abstract

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 stresss 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..

The liverwort oil body is formed by redirection of the secretory pathway

“…In this study, we demonstrated that the oil body reduces Marchantia herbivory using mutant plants with excess or without oil bodies. Consistently, a mutant of the MpC1HDZ transcription factor with a reduced number of the oil body was also recently shown to exhibit increased herbivory 37 . The secondary metabolites stored in the liverwort oil body were also reported to exhibit a diverse range of bioactivities, e.g., anti-cancer and anti-virus activities 11 .…”

“…Lastly, we asked why liverworts possess oil bodies. Using fresh and alcohol-washed liverworts, the oil body was proposed to be an effective chemical protection from herbivores 36 , which was also recently supported by a feeding assay using Armadillidium vulgare (pill bug) 37 . We fed starved pill bugs with wild-type liverwort and genetically established mutants that contain extra or no oil bodies.…”

Molecular mechanisms involved in functional macroevolution of plant transcription factors

“…Studies have addressed the co-evolutionary history of the TALE homeodomain KNOX/ BELL TF complex. Their ability to heterodimerize and migrate to the nucleus is conserved in land plants and algae Horst et al, 2016;Dierschke et al, 2020). The KNOX-BELL heterodimerization is required to initiate the diploid program in Chlamydomonas zygotes (Lee et al, 2008).…”

Ties between Stress and Lipid Droplets Pre-date Seeds

“…However, LDs can be found in all tissues in varying numbers [4]; they are also very abundant in pollen [118] and the mesocarp of some fruits [119,120]. In non-seed plants, LDs are prominent in the spores of mosses [41,56] and in thalli of liverworts [121], where they play a role in defense against pathogens [122].…”

“…Finally, LDs are more than a mere bag of oil. Enzymes associated with LDs can play a role in specialized metabolism such as oxylipin generation [123], brassinosteroid metabolism [124,125], and, especially in liverworts, terpenoid metabolism [122,126]. LDs also harbor proteins important for protein turnover [127] and signaling [128,129].…”