Recruitment of Archaeal DTD is a Key Event in the Emergence of Land Plants

Land plant evolution is a major leap in the history of life that took place during the Neoproterozoic Era (∼800 Mya). Charophyceae, a class of rhyzophytic green algae emerged as a land plant with innovations in biochemical, cytological and developmental adaptations and played a crucial role in establishing life on the land. One such striking architectural innovation is “root” that experience harsh environmental assaults such as floods, waterlogging and therefore is the epicentre for anaerobic fermentation, which produces toxic acetaldehyde. Here, we show that such produced acetaldehyde makes N-ethyl-adducts on a central component of translation machinery aa-tRNA. The Plant kingdom is unique among life forms in possessing two chirality-based proofreading systems represented by D-aminoacyl-tRNA deacylases (DTD1 and DTD2), derived from Bacteria and Archaea. We identified a unique role of archaeal derived chiral proofreading module DTD2 that selectively deacylates N-ethyl-D-aminoacyl-tRNAs (NEDATs) in plants. NEDAT deacylase function is exclusive to DTD2, as no other proofreading modules with similar substrates like canonical DTD1 and peptidyl-tRNA hydrolase (PTH) can clear NEDATs. Thus, the study elucidates the cause of hypersensitivity of DTD2 knockout plants for both ethanol and acetaldehyde. We further show NEDAT elimination is rooted in Archaea which possess the biosynthesis machinery for ethanol fermentation similar to plants. While absent in other algal branches, DTD2 can be identified in plants from land plant ancestors-Charophytes onwards. DTD2 is the only gene that has only archaeal origin among the genes ascribed for architectural and genomic innovations that happened in the land plant ancestors. The work has uncovered an important gene transfer event from methanogenic archaea to the charophytes in the oldest terrestrial ecosystem bog that contains excess of D-amino acids and deprived of oxygen.