Abstract
BackgroundIt is commonly assumed that a heterotrophic ancestor of the supergroup Archaeplastida/Plantae engulfed a cyanobacterium that was transformed into a primary plastid; however, it is still unclear how nuclear-encoded proteins initially were imported into the new organelle. Most proteins targeted to primary plastids carry a transit peptide and are transported post-translationally using Toc and Tic translocons. There are, however, several proteins with N-terminal signal peptides that are directed to higher plant plastids in vesicles derived from the endomembrane system (ES). The existence of these proteins inspired a hypothesis that all nuclear-encoded, plastid-targeted proteins initially carried signal peptides and were targeted to the ancestral primary plastid via the host ES.ResultsWe present the first phylogenetic analyses of Arabidopsis thaliana α-carbonic anhydrase (CAH1), Oryza sativa nucleotide pyrophosphatase/phosphodiesterase (NPP1), and two O. sativa α-amylases (αAmy3, αAmy7), proteins that are directed to higher plant primary plastids via the ES. We also investigated protein disulfide isomerase (RB60) from the green alga Chlamydomonas reinhardtii because of its peculiar dual post- and co-translational targeting to both the plastid and ES. Our analyses show that these proteins all are of eukaryotic rather than cyanobacterial origin, and that their non-plastid homologs are equipped with signal peptides responsible for co-translational import into the host ES. Our results indicate that vesicular trafficking of proteins to primary plastids evolved long after the cyanobacterial endosymbiosis (possibly only in higher plants) to permit their glycosylation and/or transport to more than one cellular compartment.ConclusionsThe proteins we analyzed are not relics of ES-mediated protein targeting to the ancestral primary plastid. Available data indicate that Toc- and Tic-based translocation dominated protein import into primary plastids from the beginning. Only a handful of host proteins, which already were targeted through the ES, later were adapted to reach the plastid via the vesicular trafficking. They represent a derived class of higher plant plastid-targeted proteins with an unusual evolutionary history.ReviewersThis article was reviewed by Prof. William Martin, Dr. Philippe Deschamps (nominated by Dr. Purificacion Lopez-Garcia) and Dr Simonetta Gribaldo.
Highlights
It is commonly assumed that a heterotrophic ancestor of the supergroup Archaeplastida/Plantae engulfed a cyanobacterium that was transformed into a primary plastid; it is still unclear how nuclearencoded proteins initially were imported into the new organelle
Thanks to additional and comprehensive investigations of α-amylase 3 from Oryza sativa (αAmy3) [28] and α-amylase 7 from Oryza sativa (αAmy7) [29,30], it is certain that they are targeted to both primary plastids and the external cell wall matrix via the endomembrane system (ES); αAmy7 differs from αAmy3 by the presence of an N-linked oligosaccharide side chain, which results in its trafficking through the Golgi apparatus [29,30,47]
It is possible that other amylases are targeted to plastids via the Golgi apparatus as well, because inhibition of Golgi secretion using brefeldin A results in dramatically increased starch accumulation in Arabidopsis, tobacco, and Chlamydomonas plastids [48]
Summary
It is commonly assumed that a heterotrophic ancestor of the supergroup Archaeplastida/Plantae engulfed a cyanobacterium that was transformed into a primary plastid; it is still unclear how nuclearencoded proteins initially were imported into the new organelle. There are, several proteins with N-terminal signal peptides that are directed to higher plant plastids in vesicles derived from the endomembrane system (ES) The existence of these proteins inspired a hypothesis that all nuclear-encoded, plastidtargeted proteins initially carried signal peptides and were targeted to the ancestral primary plastid via the host ES. Sometime prior to 1.5 billion years ago a phagotrophic eukaryote engulfed a cyanobacterium that was initially established as a permanent endosymbiont [1,2] This process, called a primary endosymbiosis, eventually resulted in a primary plastid surrounded by two membranes. Descendants of this original plastid are present in three eukaryotic lineages comprising the supergroup Archaeplastida (formerly Plantae); these are the Glaucophyta, Rhodophyta and Viridiplantae, including green algae and land plants [3,4,5,6]. The enormous difference in the number endosymbiont genes that reside in the nucleus, versus those retained in the plastid, reflects massive transfer (called endosymbiotic gene transfer, EGT) to the host nuclear genome, as well as loss of numerous bacterial genes that were no longer needed in a fully integrated organelle [14,15,16,17]
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