Switching secretory pathway direction for organelle acquisition in plants

Abstract

26Eukaryotic cells acquired novel organelles during evolution through mechanisms that 27 remain largely obscure. The existence of the unique oil body compartment is a 28 synapomorphy of liverworts that represents lineage-specific acquisition of this organelle 29 during evolution, although its origin, biogenesis, and physiological function are yet 30 unknown. We found that two Syntaxin 1 paralogs in the liverwort, Marchantia 31 polymorpha, are distinctly targeted to forming cell plates and the oil body, suggesting 32 these structures share some developmental similarity. Oil body formation is under the 33 regulation of an ERF/AP2-type transcription factor and loss of the oil body increased M. 34 polymorpha herbivory. These findings highlight a common strategy for the acquisition 35 of organelles with distinct functions in plants, via periodical switching in secretion 36 direction depending on cellular phase transition. 37 38 Main text: 39 Eukaryotic cells originated from prokaryotes by expanding their 40 endomembrane network during evolution, with the last eukaryotic common 41 ancestor (LECA) likely possessing a complex set of organelles 1 . New membrane 42 trafficking pathways were added to the LECA endomembrane network, some of 43 which were secondarily lost in a lineage-specific manner, resulting in divergent 44 and organism-specific membrane trafficking systems and organelle compositions 45 of extant eukaryotes 2-4 . It remains mostly unknown how organelles were acquired 46during evolution. We report that the liverwort-specific oil body was acquired by 47

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

“…However, the presence of a limited number of oil bodies in the mutants Article suggests that other transcriptional regulators could be relevant along with MpC1HDZ. For example, recently, MpERF13, a TF from the AP2-ERF family, was also shown to be involved in oil body cell differentiation [20].…”

“…Pfeffer, who gave oil bodies their name (O ¨lko¨rper), noted they were membrane bound [17], and later studies confirmed a single membrane [18,19], in which isoprenoid biosynthesis enzymes are localized [16]. A recent report showed that the oil body membrane results from the fusion of secretory vesicles that requires a cyclic switching of the secretory pathway regulated by MpERF13 transcription factor [20].…”