Limits...
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.

Show MeSH

Related in: MedlinePlus

Part of the Bayesian tree from Figure 2for α-amylases of green algae and land plants obtained in PhyloBayes under the LG + Γ(5) model. Sequences experimentally proved to be imported to plastids are in red font. Sequence in which more than 50% algorithms recognized signal peptide are indicated in bold and those which possess plastid transit peptide or mitochondrial transit peptide are signed respectively (pTP) and (mTP). Proteins that were shown to be located in the cell wall by mass spectrometry are indicated by (W). Other explanations as in Figure 2.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3716720&req=5

Figure 3: Part of the Bayesian tree from Figure 2for α-amylases of green algae and land plants obtained in PhyloBayes under the LG + Γ(5) model. Sequences experimentally proved to be imported to plastids are in red font. Sequence in which more than 50% algorithms recognized signal peptide are indicated in bold and those which possess plastid transit peptide or mitochondrial transit peptide are signed respectively (pTP) and (mTP). Proteins that were shown to be located in the cell wall by mass spectrometry are indicated by (W). Other explanations as in Figure 2.

Mentions: Phylogenetic trees of α-amylases produced by different methods show congruent topologies (Figures 2 and 3), and indicate that α-amylases were acquired independently by various groups of eukaryotes from bacteria via horizontal gene transfer (HGT) (Figure 2). There are at least four such eukaryotic clades scattered among bacteria that clearly are separated from each other. Respectively, these clades contain sequences from (i) ciliates, fungi, and placozoans, (ii) insects, (iii) fungi, and (iv) green plants. It is important to note, however, that green plant α-amylases are not of cyanobacterial origin; that is, they do not group together in our phylogenetic analyses (Figures 2 and 3). Moreover, alternative tree topologies that assume monophyly of plant and cyanobacterial sequences all are rejected with high confidence by all tests applied (see Methods).


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)

Part of the Bayesian tree from Figure 2for α-amylases of green algae and land plants obtained in PhyloBayes under the LG + Γ(5) model. Sequences experimentally proved to be imported to plastids are in red font. Sequence in which more than 50% algorithms recognized signal peptide are indicated in bold and those which possess plastid transit peptide or mitochondrial transit peptide are signed respectively (pTP) and (mTP). Proteins that were shown to be located in the cell wall by mass spectrometry are indicated by (W). Other explanations as in Figure 2.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Part of the Bayesian tree from Figure 2for α-amylases of green algae and land plants obtained in PhyloBayes under the LG + Γ(5) model. Sequences experimentally proved to be imported to plastids are in red font. Sequence in which more than 50% algorithms recognized signal peptide are indicated in bold and those which possess plastid transit peptide or mitochondrial transit peptide are signed respectively (pTP) and (mTP). Proteins that were shown to be located in the cell wall by mass spectrometry are indicated by (W). Other explanations as in Figure 2.
Mentions: Phylogenetic trees of α-amylases produced by different methods show congruent topologies (Figures 2 and 3), and indicate that α-amylases were acquired independently by various groups of eukaryotes from bacteria via horizontal gene transfer (HGT) (Figure 2). There are at least four such eukaryotic clades scattered among bacteria that clearly are separated from each other. Respectively, these clades contain sequences from (i) ciliates, fungi, and placozoans, (ii) insects, (iii) fungi, and (iv) green plants. It is important to note, however, that green plant α-amylases are not of cyanobacterial origin; that is, they do not group together in our phylogenetic analyses (Figures 2 and 3). Moreover, alternative tree topologies that assume monophyly of plant and cyanobacterial sequences all are rejected with high confidence by all tests applied (see Methods).

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