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How protein targeting to primary plastids via the endomembrane system could have evolved? A new hypothesis based on phylogenetic studies.

Gagat P, Bodył A, Mackiewicz P - Biol. Direct (2013)

Bottom Line: 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.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Genomics, Faculty of Biotechnology, University of Wrocław, ul. Przybyszewskiego 63/77, Wrocław 51-148, Poland.

ABSTRACT

Background: It 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.

Results: We 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.

Conclusions: The 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.

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Related in: MedlinePlus

The Bayesian tree for α-amylases obtained in PhyloBayes under the LG + Γ(5) model. Sequence in which more than 50% algorithms recognized SP are indicated in bold. Numbers at nodes, in the presented order, correspond respectively to posterior probabilities estimated in PhyloBayes for LG + Γ(5) model (PP-LG) and CAT + Γ(5) model (PP-CAT), as well as support values resulting from bootstrap analysis in PhyMl (B-Ph) and TreeFinder (B-TF). Values of the posterior probabilities and bootstrap percentages lower than 0.5 and 50% were omitted or indicated by a dash “-“. All bacterial sequences, apart from cyanobacterial ones, are in white background.
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Figure 2: The Bayesian tree for α-amylases obtained in PhyloBayes under the LG + Γ(5) model. Sequence in which more than 50% algorithms recognized SP are indicated in bold. Numbers at nodes, in the presented order, correspond respectively to posterior probabilities estimated in PhyloBayes for LG + Γ(5) model (PP-LG) and CAT + Γ(5) model (PP-CAT), as well as support values resulting from bootstrap analysis in PhyMl (B-Ph) and TreeFinder (B-TF). Values of the posterior probabilities and bootstrap percentages lower than 0.5 and 50% were omitted or indicated by a dash “-“. All bacterial sequences, apart from cyanobacterial ones, are in white background.

Mentions: Α-amylases, like αAmy3 and αAmy7 from Oryza sativa, are widely distributed in animals, plants, fungi, bacteria, and archaeans (Figure 2) [34-36]. They catalyze the hydrolysis of α-1,4 glycosidic bonds, but differ in substrate specificity; αAmy3 shows higher reactivity with oligosaccharides, whereas αAmy7 targets soluble starch and starch granules [37,38]. Both enzymes are active in the starchy endosperm in germinating seeds where they play crucial roles in starch degradation and seed germination [39]. Expression and secretion of both proteins are similar in the aleurone layer, but there are unique time- and tissue-specific expression patterns in the embryo [39].


How protein targeting to primary plastids via the endomembrane system could have evolved? A new hypothesis based on phylogenetic studies.

Gagat P, Bodył A, Mackiewicz P - Biol. Direct (2013)

The Bayesian tree for α-amylases obtained in PhyloBayes under the LG + Γ(5) model. Sequence in which more than 50% algorithms recognized SP are indicated in bold. Numbers at nodes, in the presented order, correspond respectively to posterior probabilities estimated in PhyloBayes for LG + Γ(5) model (PP-LG) and CAT + Γ(5) model (PP-CAT), as well as support values resulting from bootstrap analysis in PhyMl (B-Ph) and TreeFinder (B-TF). Values of the posterior probabilities and bootstrap percentages lower than 0.5 and 50% were omitted or indicated by a dash “-“. All bacterial sequences, apart from cyanobacterial ones, are in white background.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3716720&req=5

Figure 2: The Bayesian tree for α-amylases obtained in PhyloBayes under the LG + Γ(5) model. Sequence in which more than 50% algorithms recognized SP are indicated in bold. Numbers at nodes, in the presented order, correspond respectively to posterior probabilities estimated in PhyloBayes for LG + Γ(5) model (PP-LG) and CAT + Γ(5) model (PP-CAT), as well as support values resulting from bootstrap analysis in PhyMl (B-Ph) and TreeFinder (B-TF). Values of the posterior probabilities and bootstrap percentages lower than 0.5 and 50% were omitted or indicated by a dash “-“. All bacterial sequences, apart from cyanobacterial ones, are in white background.
Mentions: Α-amylases, like αAmy3 and αAmy7 from Oryza sativa, are widely distributed in animals, plants, fungi, bacteria, and archaeans (Figure 2) [34-36]. They catalyze the hydrolysis of α-1,4 glycosidic bonds, but differ in substrate specificity; αAmy3 shows higher reactivity with oligosaccharides, whereas αAmy7 targets soluble starch and starch granules [37,38]. Both enzymes are active in the starchy endosperm in germinating seeds where they play crucial roles in starch degradation and seed germination [39]. Expression and secretion of both proteins are similar in the aleurone layer, but there are unique time- and tissue-specific expression patterns in the embryo [39].

Bottom Line: 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.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Genomics, Faculty of Biotechnology, University of Wrocław, ul. Przybyszewskiego 63/77, Wrocław 51-148, Poland.

ABSTRACT

Background: It 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.

Results: We 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.

Conclusions: The 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.

Show MeSH
Related in: MedlinePlus