Endomembrane structure and the chloroplast protein targeting pathway in Heterosigma akashiwo (raphidophyceae, chromista)

Koh Ichi Sugiyama, Izumi Mori, Koji Takahashi, Shoshi Muto, Ikuko Shihira-Ishikawa

Research output: Contribution to journalArticle

40 Citations (Scopus)

Abstract

Chloroplasts in heterokont algae are surrounded by four membranes and probably originated from a red algal endosymbiont that was engulfed and retained by eukaryotic host. Understanding how nuclear-encoded chloroplast proteins are translocated from file cytoplasm into the chloroplast across these membranes could give us some insights about how file endosymbiont was integrated into the host cell in the process of secondary symbiogenesis. In multiplastid heterokont algae such as raphidophytes, it has been unclear if the outermost of the four membranes surrounding the chloroplast (the chloroplast endoplasmic reticulum [CER] membrane) is continuous with the nuclear envelope and rough endoplasmic reticulum (ER). Here, we report detailed ultrastructural observations of the raphidophyte Heterosigma akashiwo (Hada) Hada ex Y. Ham et Chihara that show that the CER membranes were continuous with ER membranes that had attached ribosomes, implying that the chloroplast with three envelope membranes is located within the ER lumen, that is, topologically the same structure as that of monoplastid heterokont algae. However, the CER membrane of H. akashiwo had very few, if any, ribosomes attached, unlike the CER membranes in other heterokont algae. To verify that proteins are first targeted to the ER, we assayed protein import into canine microsomes using a precursor for a nuclear-encoded chloroplast protein, the fucoxanthin-chlorophyll a/ c protein of H. akashiwo. This demonstrated that the precursor has a functional signal sequence for ER targeting and is cotranslationally translocated into the ER, where a signal sequence of about 17 amino acids is removed. Based on these data, we hypothesize that in H. akashiwo, nuclear-encoded chloroplast protein precursors that have been cotranslationally transported into the ER lumen are sorted in the ER and transported to the chloroplasts through the ER lumen.

Original languageEnglish
Pages (from-to)1135-1144
Number of pages10
JournalJournal of Phycology
Volume36
Issue number6
DOIs
Publication statusPublished - 2000
Externally publishedYes

Fingerprint

chloroplast
endoplasmic reticulum
targeting
chloroplasts
algae
protein
membrane
proteins
alga
endosymbiont
endosymbionts
signal peptide
ribosomes
Raphidophyceae
Chromista
chlorophyll
rough endoplasmic reticulum
nuclear membrane
microsomes
ham

Keywords

  • Chloroplast
  • Endomembrane structure
  • Fucoxanthin-chlorophyll a/c binding protein (FCP)
  • Heterokont
  • Heterosigma akashiwo
  • Protein targeting
  • Secondary endosymbiosis
  • Signal sequence symbiogenesis

ASJC Scopus subject areas

  • Aquatic Science
  • Plant Science

Cite this

Endomembrane structure and the chloroplast protein targeting pathway in Heterosigma akashiwo (raphidophyceae, chromista). / Sugiyama, Koh Ichi; Mori, Izumi; Takahashi, Koji; Muto, Shoshi; Shihira-Ishikawa, Ikuko.

In: Journal of Phycology, Vol. 36, No. 6, 2000, p. 1135-1144.

Research output: Contribution to journalArticle

Sugiyama, Koh Ichi ; Mori, Izumi ; Takahashi, Koji ; Muto, Shoshi ; Shihira-Ishikawa, Ikuko. / Endomembrane structure and the chloroplast protein targeting pathway in Heterosigma akashiwo (raphidophyceae, chromista). In: Journal of Phycology. 2000 ; Vol. 36, No. 6. pp. 1135-1144.
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AB - Chloroplasts in heterokont algae are surrounded by four membranes and probably originated from a red algal endosymbiont that was engulfed and retained by eukaryotic host. Understanding how nuclear-encoded chloroplast proteins are translocated from file cytoplasm into the chloroplast across these membranes could give us some insights about how file endosymbiont was integrated into the host cell in the process of secondary symbiogenesis. In multiplastid heterokont algae such as raphidophytes, it has been unclear if the outermost of the four membranes surrounding the chloroplast (the chloroplast endoplasmic reticulum [CER] membrane) is continuous with the nuclear envelope and rough endoplasmic reticulum (ER). Here, we report detailed ultrastructural observations of the raphidophyte Heterosigma akashiwo (Hada) Hada ex Y. Ham et Chihara that show that the CER membranes were continuous with ER membranes that had attached ribosomes, implying that the chloroplast with three envelope membranes is located within the ER lumen, that is, topologically the same structure as that of monoplastid heterokont algae. However, the CER membrane of H. akashiwo had very few, if any, ribosomes attached, unlike the CER membranes in other heterokont algae. To verify that proteins are first targeted to the ER, we assayed protein import into canine microsomes using a precursor for a nuclear-encoded chloroplast protein, the fucoxanthin-chlorophyll a/ c protein of H. akashiwo. This demonstrated that the precursor has a functional signal sequence for ER targeting and is cotranslationally translocated into the ER, where a signal sequence of about 17 amino acids is removed. Based on these data, we hypothesize that in H. akashiwo, nuclear-encoded chloroplast protein precursors that have been cotranslationally transported into the ER lumen are sorted in the ER and transported to the chloroplasts through the ER lumen.

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KW - Secondary endosymbiosis

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