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Abstract
The protein family 0016 (UPF0016) is conserved through evolution, and the few members characterized share a function in Mn2+ transport. So far, little is known about the history of these proteins in Eukaryotes. In Arabidopsis thaliana five such proteins, comprising four different subcellular localizations including chloroplasts, have been described, whereas non-photosynthetic Eukaryotes have only one. We used a phylogenetic approach to classify the eukaryotic proteins into two subgroups and performed gene-replacement studies to investigate UPF0016 genes of various origins. Replaceability can be scored readily in the Arabidopsis UPF0016 transporter mutant pam71, which exhibits a functional deficiency in photosystem II. The N-terminal region of the Arabidopsis PAM71 was used to direct selected proteins to chloroplast membranes. Transgenic pam71 lines overexpressing the closest plant homolog (CMT1), human TMEM165 or cyanobacterial MNX successfully restored photosystem II efficiency, manganese binding to photosystem II complexes and consequently plant growth rate and biomass production. Thus AtCMT1, HsTMEM165, and SynMNX can operate in the thylakoid membrane and substitute for PAM71 in a non-native environment, indicating that the manganese transport function of UPF0016 proteins is an ancient feature of the family. We propose that the two chloroplast-localized UPF0016 proteins, CMT1 and PAM71, in plants originated from the cyanobacterial endosymbiont that gave rise to the organelle.
Highlights
Cross-species replacement of genes in model organisms is a powerful tool with which to investigate whether the corresponding proteins retain their ancestral functions over a billion years of evolution
HsTMEM165 shows less resemblance to SynMNX, AtPAM71, and AtCMT1 than to the three AtPML proteins, or in other words SynMNX, AtPAM71, and AtCMT1 form a cluster. These observations allow us to conclude that the gene(s) encoding the chloroplast-localized proteins photosynthesis-affected mutant71 (PAM71) and chloroplast manganese transporter1 (CMT1) are derived from the cyanobacterial endosymbiosis that gave rise to chloroplasts
A gene-replacement analysis was conducted in the Arabidopsis mutant pam71 (Figure 3), which is characterized by diminished growth
Summary
Cross-species replacement of genes in model organisms is a powerful tool with which to investigate whether the corresponding proteins retain their ancestral functions over a billion years of evolution. Cross-Species Manganese Transporter Gene Replacement frequently be replaced by the cyanobacterial ortholog or vice versa (Savidge et al, 2002; Sattler et al, 2003; Lv et al, 2009; Armbruster et al, 2013; Proctor et al, 2018; Yoon et al, 2019). These examples of pairwise replacements can be expanded further with multiple replacement assays to gain insight into the history and evolution of gene families. Several studies have hypothesized that TMEM165 is a Golgi-localized Mn2+ and/or Ca2+ transporter (Demaegd et al, 2013; Potelle et al, 2016; Stribny et al, 2020)
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