Maternal inheritance and stage-specific variation of the apicoplast in Toxoplasma gondii during development in the intermediate and definitive host

David J. P. Ferguson, Fiona L. Henriquez, Michael J. Kirisits, Stephen P. Muench, Sean T. Prigge, David W. Rice, Craig W. Roberts, Rima L. McLeod

Research output: Contribution to journalArticle

57 Citations (Scopus)

Abstract

The structure and location of Toxoplasma gondii apicoplasts were examined in intermediate and definitive hosts and shown to vary in a stage-specific manner. Immunocytochemistry and electron microscopy studies were used to identify changes in the morphology of apicoplasts and in their enoyl reductase (ENR) content during asexual and sexual development. Apicoplasts in tachyzoites were small, multimembraned organelles anterior to nuclei that divided and segregated with the nuclei during endodyogeny. In nonproliferating bradyzoites within mature tissue cysts (1 to 24 months), apicoplasts had high levels of ENR. During coccidian development, asexual multiplication (endopolygeny), resulting in simultaneous formation of up to 30 daughters (merozoites), involved an initial growth phase associated with repeated nuclear divisions during which apicoplasts appeared as single, elongated, branched structures with increased levels of ENR. At initiation of merozoite formation, enlarged apicoplasts divided simultaneously, with constrictions, into portions that segregated to developing daughters. In sexual stages, apicoplast division did not occur during microgametogony, and apicoplasts were absent from the microgametes that were formed. In contrast, during macrogametogony, the apicoplast appeared as a large, branched, perinuclear structure that had very high levels of ENR in the absence of nuclear division. Marked increases in the size of apicoplasts and levels of ENR may be related to requirements of the macrogametocytes to synthesize and store all components necessary for oocyst formation and subsequent extracellular sporulation. Thus, it is shown that apicoplasts are present and contain ENR in all T. gondii life cycle stages except microgametes, which will result in maternal inheritance of the organelle.

Original languageEnglish
Pages (from-to)814-26
Number of pages13
JournalEukaryotic Cell
Volume4
Issue number4
DOIs
Publication statusPublished - Apr 2005
Externally publishedYes

Fingerprint

Apicoplasts
Toxoplasma
Oxidoreductases
Cell Nucleus Division
Merozoites
Organelles
Maternal Inheritance
Sexual Development
Oocysts
Life Cycle Stages
Constriction

Keywords

  • Animals
  • Brain
  • Cats
  • Enoyl-(Acyl-Carrier-Protein) Reductase (NADH)
  • Life Cycle Stages
  • Lung
  • Maternal Behavior
  • Mice
  • Microscopy, Immunoelectron
  • Organelles
  • Oxidoreductases
  • Plastids
  • Toxoplasma
  • Toxoplasmosis, Animal

Cite this

Ferguson, David J. P. ; Henriquez, Fiona L. ; Kirisits, Michael J. ; Muench, Stephen P. ; Prigge, Sean T. ; Rice, David W. ; Roberts, Craig W. ; McLeod, Rima L. / Maternal inheritance and stage-specific variation of the apicoplast in Toxoplasma gondii during development in the intermediate and definitive host. In: Eukaryotic Cell. 2005 ; Vol. 4, No. 4. pp. 814-26.
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Maternal inheritance and stage-specific variation of the apicoplast in Toxoplasma gondii during development in the intermediate and definitive host. / Ferguson, David J. P.; Henriquez, Fiona L.; Kirisits, Michael J.; Muench, Stephen P.; Prigge, Sean T.; Rice, David W.; Roberts, Craig W.; McLeod, Rima L.

In: Eukaryotic Cell, Vol. 4, No. 4, 04.2005, p. 814-26.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Maternal inheritance and stage-specific variation of the apicoplast in Toxoplasma gondii during development in the intermediate and definitive host

AU - Ferguson, David J. P.

AU - Henriquez, Fiona L.

AU - Kirisits, Michael J.

AU - Muench, Stephen P.

AU - Prigge, Sean T.

AU - Rice, David W.

AU - Roberts, Craig W.

AU - McLeod, Rima L.

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N2 - The structure and location of Toxoplasma gondii apicoplasts were examined in intermediate and definitive hosts and shown to vary in a stage-specific manner. Immunocytochemistry and electron microscopy studies were used to identify changes in the morphology of apicoplasts and in their enoyl reductase (ENR) content during asexual and sexual development. Apicoplasts in tachyzoites were small, multimembraned organelles anterior to nuclei that divided and segregated with the nuclei during endodyogeny. In nonproliferating bradyzoites within mature tissue cysts (1 to 24 months), apicoplasts had high levels of ENR. During coccidian development, asexual multiplication (endopolygeny), resulting in simultaneous formation of up to 30 daughters (merozoites), involved an initial growth phase associated with repeated nuclear divisions during which apicoplasts appeared as single, elongated, branched structures with increased levels of ENR. At initiation of merozoite formation, enlarged apicoplasts divided simultaneously, with constrictions, into portions that segregated to developing daughters. In sexual stages, apicoplast division did not occur during microgametogony, and apicoplasts were absent from the microgametes that were formed. In contrast, during macrogametogony, the apicoplast appeared as a large, branched, perinuclear structure that had very high levels of ENR in the absence of nuclear division. Marked increases in the size of apicoplasts and levels of ENR may be related to requirements of the macrogametocytes to synthesize and store all components necessary for oocyst formation and subsequent extracellular sporulation. Thus, it is shown that apicoplasts are present and contain ENR in all T. gondii life cycle stages except microgametes, which will result in maternal inheritance of the organelle.

AB - The structure and location of Toxoplasma gondii apicoplasts were examined in intermediate and definitive hosts and shown to vary in a stage-specific manner. Immunocytochemistry and electron microscopy studies were used to identify changes in the morphology of apicoplasts and in their enoyl reductase (ENR) content during asexual and sexual development. Apicoplasts in tachyzoites were small, multimembraned organelles anterior to nuclei that divided and segregated with the nuclei during endodyogeny. In nonproliferating bradyzoites within mature tissue cysts (1 to 24 months), apicoplasts had high levels of ENR. During coccidian development, asexual multiplication (endopolygeny), resulting in simultaneous formation of up to 30 daughters (merozoites), involved an initial growth phase associated with repeated nuclear divisions during which apicoplasts appeared as single, elongated, branched structures with increased levels of ENR. At initiation of merozoite formation, enlarged apicoplasts divided simultaneously, with constrictions, into portions that segregated to developing daughters. In sexual stages, apicoplast division did not occur during microgametogony, and apicoplasts were absent from the microgametes that were formed. In contrast, during macrogametogony, the apicoplast appeared as a large, branched, perinuclear structure that had very high levels of ENR in the absence of nuclear division. Marked increases in the size of apicoplasts and levels of ENR may be related to requirements of the macrogametocytes to synthesize and store all components necessary for oocyst formation and subsequent extracellular sporulation. Thus, it is shown that apicoplasts are present and contain ENR in all T. gondii life cycle stages except microgametes, which will result in maternal inheritance of the organelle.

KW - Animals

KW - Brain

KW - Cats

KW - Enoyl-(Acyl-Carrier-Protein) Reductase (NADH)

KW - Life Cycle Stages

KW - Lung

KW - Maternal Behavior

KW - Mice

KW - Microscopy, Immunoelectron

KW - Organelles

KW - Oxidoreductases

KW - Plastids

KW - Toxoplasma

KW - Toxoplasmosis, Animal

U2 - 10.1128/EC.4.4.814-826.2005

DO - 10.1128/EC.4.4.814-826.2005

M3 - Article

C2 - 15821140

VL - 4

SP - 814

EP - 826

JO - Eukaryotic Cell

JF - Eukaryotic Cell

SN - 1535-9778

IS - 4

ER -