Location: Chemistry ResearchTitle: The evolution of strictly monofunctional naphthoquinol C3 methyltransferases is vital in cyanobacteria and plastids
|STUTTS, LAUREN - University Of Florida|
|LATIMER, SCOTT - University Of Florida|
|BATYRSHINA, ZHANIYA - University Of Florida|
|DICKINSON, GABRIELLA - University Of Florida|
|BASSET, GILLES - University Of Florida|
Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/1/2023
Publication Date: 7/21/2023
Citation: Stutts, L., Latimer, S., Batyrshina, Z., Dickinson, G., Alborn, H.T., Block, A.K., Basset, G.J. 2023. Cyanobacteria and plastids harbor strictly monofunctional naphthoquinol C-methyltransferases. The Plant Cell. https://doi.org/10.1093/plcell/koad202.
Interpretive Summary: Scientists have long been searching for the driving forces behind natural selection. ARS researchers from the Center for Medical, Agricultural, and Veterinary Entomology in Gainesville, FL and scientists from the University of Florida recently uncovered one such force of selection in plants. While studying enzymes involved in making vitamin K and Coenzyme Q, the scientists noticed that plants had versions of an enzyme that had lost one of its two functions. Biochemical engineering to restore the second function in plants led to the production of a novel herbicidal compound. This research showed that plants evolved to remove a function of this enzyme to avoid producing a toxic compound, as well as uncovered a potentially new herbicide.
Technical Abstract: UbiE (EC 2.1.201)/MenG (EC 220.127.116.11) C-methyltransferases catalyze pivotal ring methylations in the biosynthetic pathways of respiratory and phtosynthetic quinones. Phylogenetic reconstructions uncovered a puzzling evolutionary pattern, where prokaryotic and eukaryotic UbiE/MenG homologs segregate into two clades. Clade 1 members are universally distributed throughout eukaryotic and prokaryotic lineages, excluding cyanobacteria, and include mitochondrial COQ5 enzymes required for ubiquinone biosynthesis. Clade 2 members, in contrast, are specific to cyanobacteria and plastids. Functional complementation assays of an E. coli ubiE/menG mutant indicated that clade 1 members display activity with both demethyl-benzoquinonols and demethyl-naphthoquinols, independently of the quinone profile of their original taxa, while clade 2 members have evolved strict substrate specificity for demethyl-naphthoquinols. Expression of bifunctional Arabidopsis COQ5 in the cyanobacterium Synechocystis or its retargeting to Arabidopsis plastids resulted in the synthesis of a new-to-nature methylated variant of plastoquinone-9. Accumulation of methyl-plastoquinone-9 was acutely cytotoxic, leading to the emergence of suppressor mutations in Synechosystis and seedling lethality in Arabidopsis. These data demonstrate that in cyanobacteria and plastids, co-ocuurence of phylloquinone and plastoquinone have driven the unprecedented evolution of mono-functional demethylnaphthoquinol methyltransferases, and explain why plants cannot capture the intrinsic bi-functionality of UbiE/MenG to simultaneously synthesize their respiratory and photosynthetic quinones.