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A multi-functional tubulovesicular network as the ancestral eukaryotic endomembrane system.

González-Sánchez JC, Costa R, Devos DP - Biology (Basel) (2015)

Bottom Line: One of the potential selective advantages provided by this organisation was the capacity to perform endocytosis.This possibility is illustrated by membrane organisations observed in current organisms in the three domains of life.Based on this, we propose a coherent model of autogenous eukaryotic endomembrane system evolution in which mitochondria are involved at a late stage.

View Article: PubMed Central - PubMed

Affiliation: Centro Andaluz de Biologia del Desarollo (CABD), Universidad Pablo de Olavide, Carretera de Utrera km 1, Seville 41013, Spain. jcgonsan@upo.es.

ABSTRACT
The origin of the eukaryotic endomembrane system is still the subject of much speculation. We argue that the combination of two recent hypotheses addressing the eukaryotic endomembrane's early evolution supports the possibility that the ancestral membranes were organised as a multi-functional tubulovesicular network. One of the potential selective advantages provided by this organisation was the capacity to perform endocytosis. This possibility is illustrated by membrane organisations observed in current organisms in the three domains of life. Based on this, we propose a coherent model of autogenous eukaryotic endomembrane system evolution in which mitochondria are involved at a late stage.

No MeSH data available.


Related in: MedlinePlus

Model for endomembrane system development with TVN as intermediary step. The figure represents schematics of putative intracellular membrane organisations, showcasing the different steps of the proposed hypothesis. Schemas not to scale. DNA is represented as a (wrapped) string. Prokaryotic periplasm is coloured in light grey and cytoplasm in white. Cytoplasmic and inner membranes (IM) are in black, outer membranes (OM) are in light grey. Mitochondrial and nuclear spaces are red and yellow, respectively. (a) diderm prokaryotes (Step one); (b) prokaryotes with IM vesicles (Step two); (c) prokaryotic intracellular membrane organisations, with IM invaginations (Step three); (d) intermediary organism with a multifunctional TVN (Step four); (e) ‘classical’ eukaryote with a fully developed and functionally differentiated endomembrane system (Step five).
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biology-04-00264-f003: Model for endomembrane system development with TVN as intermediary step. The figure represents schematics of putative intracellular membrane organisations, showcasing the different steps of the proposed hypothesis. Schemas not to scale. DNA is represented as a (wrapped) string. Prokaryotic periplasm is coloured in light grey and cytoplasm in white. Cytoplasmic and inner membranes (IM) are in black, outer membranes (OM) are in light grey. Mitochondrial and nuclear spaces are red and yellow, respectively. (a) diderm prokaryotes (Step one); (b) prokaryotes with IM vesicles (Step two); (c) prokaryotic intracellular membrane organisations, with IM invaginations (Step three); (d) intermediary organism with a multifunctional TVN (Step four); (e) ‘classical’ eukaryote with a fully developed and functionally differentiated endomembrane system (Step five).

Mentions: Both molecular phylogenetic analyses [51,52,53] and evidence from the fossil record [54,55,56] support the notion that prokaryotes predated eukaryotes. This evidence suggests that the eukaryotic cell must have arisen from a state resembling that of a prokaryote; that is, that the acquisition of organelles and complex cellular machineries in eukaryotes must be explained from a cellular state lacking most membrane organisation. Consequently, most credible scenarios of eukaryotic ES origin start from a prokaryotic stage [53,57,58]. However, important gaps in membrane organisation are still present and have been used to criticize those scenarios [59]. The prediction of a multi-functional TVN as the ancestral eukaryotic ES refines current autogenous theories of eukaryotic ES development and fills the gap between prokaryotes and eukaryotes by providing plausible intermediate organisations (Figure 3).


A multi-functional tubulovesicular network as the ancestral eukaryotic endomembrane system.

González-Sánchez JC, Costa R, Devos DP - Biology (Basel) (2015)

Model for endomembrane system development with TVN as intermediary step. The figure represents schematics of putative intracellular membrane organisations, showcasing the different steps of the proposed hypothesis. Schemas not to scale. DNA is represented as a (wrapped) string. Prokaryotic periplasm is coloured in light grey and cytoplasm in white. Cytoplasmic and inner membranes (IM) are in black, outer membranes (OM) are in light grey. Mitochondrial and nuclear spaces are red and yellow, respectively. (a) diderm prokaryotes (Step one); (b) prokaryotes with IM vesicles (Step two); (c) prokaryotic intracellular membrane organisations, with IM invaginations (Step three); (d) intermediary organism with a multifunctional TVN (Step four); (e) ‘classical’ eukaryote with a fully developed and functionally differentiated endomembrane system (Step five).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4498299&req=5

biology-04-00264-f003: Model for endomembrane system development with TVN as intermediary step. The figure represents schematics of putative intracellular membrane organisations, showcasing the different steps of the proposed hypothesis. Schemas not to scale. DNA is represented as a (wrapped) string. Prokaryotic periplasm is coloured in light grey and cytoplasm in white. Cytoplasmic and inner membranes (IM) are in black, outer membranes (OM) are in light grey. Mitochondrial and nuclear spaces are red and yellow, respectively. (a) diderm prokaryotes (Step one); (b) prokaryotes with IM vesicles (Step two); (c) prokaryotic intracellular membrane organisations, with IM invaginations (Step three); (d) intermediary organism with a multifunctional TVN (Step four); (e) ‘classical’ eukaryote with a fully developed and functionally differentiated endomembrane system (Step five).
Mentions: Both molecular phylogenetic analyses [51,52,53] and evidence from the fossil record [54,55,56] support the notion that prokaryotes predated eukaryotes. This evidence suggests that the eukaryotic cell must have arisen from a state resembling that of a prokaryote; that is, that the acquisition of organelles and complex cellular machineries in eukaryotes must be explained from a cellular state lacking most membrane organisation. Consequently, most credible scenarios of eukaryotic ES origin start from a prokaryotic stage [53,57,58]. However, important gaps in membrane organisation are still present and have been used to criticize those scenarios [59]. The prediction of a multi-functional TVN as the ancestral eukaryotic ES refines current autogenous theories of eukaryotic ES development and fills the gap between prokaryotes and eukaryotes by providing plausible intermediate organisations (Figure 3).

Bottom Line: One of the potential selective advantages provided by this organisation was the capacity to perform endocytosis.This possibility is illustrated by membrane organisations observed in current organisms in the three domains of life.Based on this, we propose a coherent model of autogenous eukaryotic endomembrane system evolution in which mitochondria are involved at a late stage.

View Article: PubMed Central - PubMed

Affiliation: Centro Andaluz de Biologia del Desarollo (CABD), Universidad Pablo de Olavide, Carretera de Utrera km 1, Seville 41013, Spain. jcgonsan@upo.es.

ABSTRACT
The origin of the eukaryotic endomembrane system is still the subject of much speculation. We argue that the combination of two recent hypotheses addressing the eukaryotic endomembrane's early evolution supports the possibility that the ancestral membranes were organised as a multi-functional tubulovesicular network. One of the potential selective advantages provided by this organisation was the capacity to perform endocytosis. This possibility is illustrated by membrane organisations observed in current organisms in the three domains of life. Based on this, we propose a coherent model of autogenous eukaryotic endomembrane system evolution in which mitochondria are involved at a late stage.

No MeSH data available.


Related in: MedlinePlus