Evolution of Protein Targeting into “Complex” Plastids: The “Secretory Transport Hypothesis”

Kilian, Oliver; Kroth, Peter G.

doi:10.1055/s-2003-42710

Cited by 16 publications

(24 citation statements)

References 74 publications

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“…The mode of protein translocation into secondary plastids of diatoms is still under debate (Kilian and Kroth 2003). A ''vesicular shuttle model'' (Gibbs 1979) and a ''translocator model '' (Cavalier-Smith 1999, 2003McFadden 1999) are discussed.…”

Section: Discussionmentioning

confidence: 99%

“…Secretory transport might have been the first protein import system into early primary plastids, which first may have developed the Tic and then the Toc complex (Kilian and Kroth 2003). The ''ASAFAP''-motif may therefore even be a relic of a former import system being present in the ancestor of all plastids before the transit peptide system was developed.…”

Section: Discussionmentioning

confidence: 99%

“…The plastid genomes of the diatom Phaeodactylum tricornutum and the cryptophyte Guillardia theta contain only 162 and 177 genes (Douglas and Penny 1999;Oudot-Le Secq et al 2007), however, a plastid proteome size similar to that of higher plants must be assumed because photosynthesis is a rather complex process. Plastid protein import is therefore an important process for diatoms and cryptophytes, but the mode of protein translocation into these complex plastids derived from red algae is still mysterious (Kilian and Kroth 2003). Presequences of nucleus encoded plastid proteins consist of a signal peptide followed by a transit peptide-like domain (Pancic and Strotmann 1993).…”

Section: Introductionmentioning

confidence: 99%

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Protein targeting into complex diatom plastids: functional characterisation of a specific targeting motif

et al. 2007

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Plastids of diatoms and related algae evolved by secondary endocytobiosis, the uptake of a eukaryotic alga into a eukaryotic host cell and its subsequent reduction into an organelle. As a result diatom plastids are surrounded by four membranes. Protein targeting of nucleus encoded plastid proteins across these membranes depends on N-terminal bipartite presequences consisting of a signal and a transit peptide-like domain. Diatoms and cryptophytes share a conserved amino acid motif of unknown function at the cleavage site of the signal peptides (ASA-FAP), which is particularly important for successful plastid targeting. Screening genomic databases we found that in rare cases the very conserved phenylalanine within the motif may be replaced by tryptophan, tyrosine or leucine. To test such unusual presequences for functionality and to better understand the role of the motif and putative receptor proteins involved in targeting, we constructed presequence:GFP fusion proteins with or without modifications of the ''ASAFAP''-motif and expressed them in the diatom Phaeodactylum tricornutum. In this comprehensive mutational analysis we found that only the aromatic amino acids phenylalanine, tryptophan, tyrosine and the bulky amino acid leucine at the +1 position of the predicted signal peptidase cleavage site allow plastid import, as expected from the sequence comparison of native plastid targeting presequences of P. tricornutum and the cryptophyte Guillardia theta. Deletions within the signal peptide domains also impaired plastid import, showing that the presence of F at the N-terminus of the transit peptide together with a cleavable signal peptide is crucial for plastid import.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Protein targeting into complex diatom plastids: functional characterisation of a specific targeting motif

et al. 2007

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“…A significant hurdle in this pathway is the necessity to acquire appropriate targeting information that allows nucleus-encoded proteins to be directed to the plastid and to traverse additional membranes in the process. Understanding the mechanism of targeting and translocation in organisms with complex plastids has been key to understanding how the transition from algal symbiont to plastid occurred (12,35,47,50,63,74).In protists with four membranes around the plastid, the outermost membrane often has ribosomes attached and is typically continuous with the endoplasmic reticulum (ER) (23). Proteins directed to these plastids possess bipartite targeting sequences, with an N-terminal signal sequence…”

mentioning

confidence: 99%

Analysis of Euglena gracilis Plastid-Targeted Proteins Reveals Different Classes of Transit Sequences

2006

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The plastid of Euglena gracilis was acquired secondarily through an endosymbiotic event with a eukaryotic green alga, and as a result, it is surrounded by a third membrane. This membrane complexity raises the question of how the plastid proteins are targeted to and imported into the organelle. To further explore plastid protein targeting in Euglena, we screened a total of 9,461 expressed sequence tag (EST) clusters (derived from 19,013 individual ESTs) for full-length proteins that are plastid localized to characterize their targeting sequences and to infer potential modes of translocation. Of the 117 proteins identified as being potentially plastid localized whose N-terminal targeting sequences could be inferred, 83 were unique and could be classified into two major groups. Class I proteins have tripartite targeting sequences, comprising (in order) an N-terminal signal sequence, a plastid transit peptide domain, and a predicted stop-transfer sequence. Within this class of proteins are the lumen-targeted proteins (class IB), which have an additional hydrophobic domain similar to a signal sequence and required for further targeting across the thylakoid membrane. Class II proteins lack the putative stop-transfer sequence and possess only a signal sequence at the N terminus, followed by what, in amino acid composition, resembles a plastid transit peptide. Unexpectedly, a few unrelated plastid-targeted proteins exhibit highly similar transit sequences, implying either a recent swapping of these domains or a conserved function. This work represents the most comprehensive description to date of transit peptides in Euglena and hints at the complex routes of plastid targeting that must exist in this organism.A fundamental problem in cell biology is the precise and efficient targeting of proteins synthesized by cytoplasmic ribosomes to their appropriate intracellular locations. Proteins destined for the endomembrane system, mitochondria, or the chloroplast usually have specific N-terminal targeting domains that are required for proper subcellular localization. These leader sequences are often removed by specific proteases at the protein's destination prior to it assuming its active conformation. For chloroplast-targeted proteins in plants and algae, an N-terminal transit peptide (TP) is both necessary and sufficient for correct plastid targeting (11). Transit peptides are not conserved in sequence but exhibit characteristic biochemical properties, such as an elevated content of the hydroxylated amino acids serine and threonine as well as a deficiency of acidic (aspartate and glutamate) amino acids (76). Within a typical chloroplast, there are six distinct locations to which the constituent proteins must be sorted, and some proteins have to cross up to three membranes (33). This complexity requires additional targeting information within the transit peptide, such as the signal sequence-like domain found in proteins targeted to the thylakoid membrane, or information contained within the mature portion of the protein itself...

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“…(25) The first step in their import is co-translational translocation through the PER membrane dependent on the Sec translocon. (84,91) In the ''vesicular'' model, transport through the periplastid membrane and the outer membrane of the plastid envelope are mediated by transport vesicles derived from the pinocytotic pathway of the red algal endosymbiont. (91,96) By contrast, the ''channel'' model postulates that two distinct pore proteins, Der and Toc75, are responsible for these targeting steps.…”

Section: Sugar/inorganic Phosphate Antiportersmentioning

confidence: 99%

Early steps in plastid evolution: current ideas and controversies

Bodył¹,

Mackiewicz²,

Stiller³

2009

BioEssays

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Some nuclear-encoded proteins are imported into higher plant plastids via the endomembrane (EM) system. Compared with multi-protein Toc and Tic translocons required for most plastid protein import, the relatively uncomplicated nature of EM trafficking led to suggestions that it was the original transport mechanism for nuclear-encoded endosymbiont proteins, and critical for the early stages of plastid evolution. Its apparent simplicity disappears, however, when EM transport is considered in light of selective constraints likely encountered during the conversion of stable endosymbionts into fully integrated organelles. From this perspective it is more parsimonious to presume the early evolution of post-translational protein import via simpler, ancestral forms of modern Toc and Tic plastid translocons, with EM trafficking arising later to accommodate glycosylation and/or protein targeting to multiple cellular locations. This hypothesis is supported by both empirical and comparative data, and is consistent with the relative paucity of EM-based transport to modern primary plastids.

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Evolution of Protein Targeting into “Complex” Plastids: The “Secretory Transport Hypothesis”

Cited by 16 publications

References 74 publications

Protein targeting into complex diatom plastids: functional characterisation of a specific targeting motif

Protein targeting into complex diatom plastids: functional characterisation of a specific targeting motif

Analysis of Euglena gracilis Plastid-Targeted Proteins Reveals Different Classes of Transit Sequences

Early steps in plastid evolution: current ideas and controversies

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