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Mitochondrial pleomorphy in plant cells is driven by contiguous ER dynamics.

Jaipargas EA, Barton KA, Mathur N, Mathur J - Front Plant Sci (2015)

Bottom Line: Here, through live-imaging of the entire range of mitochondria pleomorphy we uncover the underlying basis for the predominantly punctate mitochondrial form in plants.We demonstrate that mitochondrial morphology changes in response to light and cytosolic sugar levels in an ER mediated manner.By observing elongated mitochondria in normal plants and fission-impaired Arabidopsis nmt1-2 and drp3a mutants we also establish that thin extensions called matrixules and a beads-on-a-string mitochondrial phenotype are direct consequences of mitochondria-ER interactions.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Plant Development and Interactions, Department of Molecular and Cellular Biology, University of Guelph ON, Canada.

ABSTRACT
Mitochondria are pleomorphic, double membrane-bound organelles involved in cellular energetics in all eukaryotes. Mitochondria in animal and yeast cells are typically tubular-reticulate structures and several micro-meters long but in green plants they are predominantly observed as 0.2-1.5 μm punctae. While fission and fusion, through the coordinated activity of several conserved proteins, shapes mitochondria, the endoplasmic reticulum (ER) has recently been identified as an additional player in this process in yeast and mammalian cells. The mitochondria-ER relationship in plant cells remains largely uncharacterized. Here, through live-imaging of the entire range of mitochondria pleomorphy we uncover the underlying basis for the predominantly punctate mitochondrial form in plants. We demonstrate that mitochondrial morphology changes in response to light and cytosolic sugar levels in an ER mediated manner. Whereas, large ER polygons and low dynamics under dark conditions favor mitochondrial fusion and elongation, small ER polygons result in increased fission and predominantly small mitochondria. Hypoxia also reduces ER dynamics and increases mitochondrial fusion to produce giant mitochondria. By observing elongated mitochondria in normal plants and fission-impaired Arabidopsis nmt1-2 and drp3a mutants we also establish that thin extensions called matrixules and a beads-on-a-string mitochondrial phenotype are direct consequences of mitochondria-ER interactions.

No MeSH data available.


Related in: MedlinePlus

Contortions and fission of elongated mitochondria occur through physical interactions with the ER mesh. (A) A collapsed confocal image stack shows two elongated and two swollen, oval mitochondria embedded in the ER. Arrowheads indicate ER bands that encircle the tubular mitochondria. (B) Iso-surface volume rendering of boxed-in region 1 in (A) depicts the 3-dimensionality of the mitochondrion-ER spatial relation. An oval mitochondrion is located within an ER-cup while a tubular mitochondria appears threaded between ER polygons. Note the constrictions in the elongated mitochondrion due to encircling ER bands (e.g., arrowhead). (C) 3-D volume rendering of boxed-in region 2 in (A) shows a tubular mitochondrion enmeshed in the channel created by contiguous ER polygons of variable diameter. Increasing the transparency of the green channel has allowed an appreciation of the ER tubules lying behind the mitochondria. (D) Four snapshots selected from a time-lapse series (Supplementary Movie 2) show an elongated mitochondrion (panel 1) with a putative fission site (arrowhead) contorting (panel 2) before breaking (panel 3). The distance between the longer portion of the mitochondria and the broken off segment widens in panels 3 and 4 while another break appears (arrowhead in panel 3) and complete fission of one elongated mitochondria into three is achieved in panel 4. Note that the contiguous ER also stretches and rearranges during this process. (E) An image suggesting that different portions of mitochondria can become enmeshed within different ER polygons and thus get stretched during the dynamic reorganization of the ER reorganizes. The stretching creates dilations (*) and narrow regions (arrows) in the elongated mitochondrion suggesting the beads-on-a-string form. The terminal, thin regions may also be interpreted as matrixules. (F,G) Snapshots acquired from a time-lapse image sequence show the stretching of an elongated mitochondrion and the formation of thin regions (arrowheads in F1) suggesting matrixules. Note that the dilated region (G1; arrowhead) locates to enlarged ER cistern. Panels 2–5 show fission and expanding ER cisternae in G that increase the gap between the different mitochondrial segments. Panels 5–7 suggest a snap-back phenomenon where the mitochondrial segments curl up on themselves as the neighboring ER completes their separation. A single yellow fluorescent peroxisome (*in panel 1) was also observed in this image series. Size bars = 5 μm.
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Figure 3: Contortions and fission of elongated mitochondria occur through physical interactions with the ER mesh. (A) A collapsed confocal image stack shows two elongated and two swollen, oval mitochondria embedded in the ER. Arrowheads indicate ER bands that encircle the tubular mitochondria. (B) Iso-surface volume rendering of boxed-in region 1 in (A) depicts the 3-dimensionality of the mitochondrion-ER spatial relation. An oval mitochondrion is located within an ER-cup while a tubular mitochondria appears threaded between ER polygons. Note the constrictions in the elongated mitochondrion due to encircling ER bands (e.g., arrowhead). (C) 3-D volume rendering of boxed-in region 2 in (A) shows a tubular mitochondrion enmeshed in the channel created by contiguous ER polygons of variable diameter. Increasing the transparency of the green channel has allowed an appreciation of the ER tubules lying behind the mitochondria. (D) Four snapshots selected from a time-lapse series (Supplementary Movie 2) show an elongated mitochondrion (panel 1) with a putative fission site (arrowhead) contorting (panel 2) before breaking (panel 3). The distance between the longer portion of the mitochondria and the broken off segment widens in panels 3 and 4 while another break appears (arrowhead in panel 3) and complete fission of one elongated mitochondria into three is achieved in panel 4. Note that the contiguous ER also stretches and rearranges during this process. (E) An image suggesting that different portions of mitochondria can become enmeshed within different ER polygons and thus get stretched during the dynamic reorganization of the ER reorganizes. The stretching creates dilations (*) and narrow regions (arrows) in the elongated mitochondrion suggesting the beads-on-a-string form. The terminal, thin regions may also be interpreted as matrixules. (F,G) Snapshots acquired from a time-lapse image sequence show the stretching of an elongated mitochondrion and the formation of thin regions (arrowheads in F1) suggesting matrixules. Note that the dilated region (G1; arrowhead) locates to enlarged ER cistern. Panels 2–5 show fission and expanding ER cisternae in G that increase the gap between the different mitochondrial segments. Panels 5–7 suggest a snap-back phenomenon where the mitochondrial segments curl up on themselves as the neighboring ER completes their separation. A single yellow fluorescent peroxisome (*in panel 1) was also observed in this image series. Size bars = 5 μm.

Mentions: Simultaneous imaging of mitochondria and the ER in Arabidopsis transgenic seedlings co-expressing mito-GFP and RER revealed that mitochondria were nestled within polygons created by ER tubules. Time-lapse images showed further that the seemingly erratic movement of mitochondria correlated with the motility and organization patterns of ER tubules (Supplementary Movie 2). Immersion of seedlings in water under a coverslip for 30–45 min allowed mitochondria to elongate without a noticeable change in ER motility. Subsequent exposure to bright light for 30 s triggered mitochondrial fission. Through highly reproducible time-lapse series taken in over 80 different cells from 10 plants and from iso-surface volume rendering of confocal image stacks it became apparent that single elongated mitochondria were encircled by multiple ER tubules at several positions (Figures 3A–C; Supplementary Movie 2). The position of these ER bands around mitochondria often changed during the reorganization of the dynamic ER mesh. Changes in the organization of ER tubules and the consequent narrowing or broadening of ER polygons resulted in the stretching and twisting of enmeshed mitochondria. Whereas, an average time for a fission event could not be estimated due to the rather asynchronous interactions of mitochondria and the ER, a medial narrowing or constriction of the mitochondrion preceded every such event (Figures 3D,E; Supplementary Movie 3). This narrowing usually formed the point of fission (Figures 3F,G). A certain amount of force to separate the mitochondrial fragments was indicated in the way that the two portions of the mitochondrion and the ER pulled away into opposite directions after a fission event (Figures 3F,G). The pulling force often created a thin region between two fragments, very much like a medial matrixule, prior to their actual separation (Figures 3F,G).


Mitochondrial pleomorphy in plant cells is driven by contiguous ER dynamics.

Jaipargas EA, Barton KA, Mathur N, Mathur J - Front Plant Sci (2015)

Contortions and fission of elongated mitochondria occur through physical interactions with the ER mesh. (A) A collapsed confocal image stack shows two elongated and two swollen, oval mitochondria embedded in the ER. Arrowheads indicate ER bands that encircle the tubular mitochondria. (B) Iso-surface volume rendering of boxed-in region 1 in (A) depicts the 3-dimensionality of the mitochondrion-ER spatial relation. An oval mitochondrion is located within an ER-cup while a tubular mitochondria appears threaded between ER polygons. Note the constrictions in the elongated mitochondrion due to encircling ER bands (e.g., arrowhead). (C) 3-D volume rendering of boxed-in region 2 in (A) shows a tubular mitochondrion enmeshed in the channel created by contiguous ER polygons of variable diameter. Increasing the transparency of the green channel has allowed an appreciation of the ER tubules lying behind the mitochondria. (D) Four snapshots selected from a time-lapse series (Supplementary Movie 2) show an elongated mitochondrion (panel 1) with a putative fission site (arrowhead) contorting (panel 2) before breaking (panel 3). The distance between the longer portion of the mitochondria and the broken off segment widens in panels 3 and 4 while another break appears (arrowhead in panel 3) and complete fission of one elongated mitochondria into three is achieved in panel 4. Note that the contiguous ER also stretches and rearranges during this process. (E) An image suggesting that different portions of mitochondria can become enmeshed within different ER polygons and thus get stretched during the dynamic reorganization of the ER reorganizes. The stretching creates dilations (*) and narrow regions (arrows) in the elongated mitochondrion suggesting the beads-on-a-string form. The terminal, thin regions may also be interpreted as matrixules. (F,G) Snapshots acquired from a time-lapse image sequence show the stretching of an elongated mitochondrion and the formation of thin regions (arrowheads in F1) suggesting matrixules. Note that the dilated region (G1; arrowhead) locates to enlarged ER cistern. Panels 2–5 show fission and expanding ER cisternae in G that increase the gap between the different mitochondrial segments. Panels 5–7 suggest a snap-back phenomenon where the mitochondrial segments curl up on themselves as the neighboring ER completes their separation. A single yellow fluorescent peroxisome (*in panel 1) was also observed in this image series. Size bars = 5 μm.
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Figure 3: Contortions and fission of elongated mitochondria occur through physical interactions with the ER mesh. (A) A collapsed confocal image stack shows two elongated and two swollen, oval mitochondria embedded in the ER. Arrowheads indicate ER bands that encircle the tubular mitochondria. (B) Iso-surface volume rendering of boxed-in region 1 in (A) depicts the 3-dimensionality of the mitochondrion-ER spatial relation. An oval mitochondrion is located within an ER-cup while a tubular mitochondria appears threaded between ER polygons. Note the constrictions in the elongated mitochondrion due to encircling ER bands (e.g., arrowhead). (C) 3-D volume rendering of boxed-in region 2 in (A) shows a tubular mitochondrion enmeshed in the channel created by contiguous ER polygons of variable diameter. Increasing the transparency of the green channel has allowed an appreciation of the ER tubules lying behind the mitochondria. (D) Four snapshots selected from a time-lapse series (Supplementary Movie 2) show an elongated mitochondrion (panel 1) with a putative fission site (arrowhead) contorting (panel 2) before breaking (panel 3). The distance between the longer portion of the mitochondria and the broken off segment widens in panels 3 and 4 while another break appears (arrowhead in panel 3) and complete fission of one elongated mitochondria into three is achieved in panel 4. Note that the contiguous ER also stretches and rearranges during this process. (E) An image suggesting that different portions of mitochondria can become enmeshed within different ER polygons and thus get stretched during the dynamic reorganization of the ER reorganizes. The stretching creates dilations (*) and narrow regions (arrows) in the elongated mitochondrion suggesting the beads-on-a-string form. The terminal, thin regions may also be interpreted as matrixules. (F,G) Snapshots acquired from a time-lapse image sequence show the stretching of an elongated mitochondrion and the formation of thin regions (arrowheads in F1) suggesting matrixules. Note that the dilated region (G1; arrowhead) locates to enlarged ER cistern. Panels 2–5 show fission and expanding ER cisternae in G that increase the gap between the different mitochondrial segments. Panels 5–7 suggest a snap-back phenomenon where the mitochondrial segments curl up on themselves as the neighboring ER completes their separation. A single yellow fluorescent peroxisome (*in panel 1) was also observed in this image series. Size bars = 5 μm.
Mentions: Simultaneous imaging of mitochondria and the ER in Arabidopsis transgenic seedlings co-expressing mito-GFP and RER revealed that mitochondria were nestled within polygons created by ER tubules. Time-lapse images showed further that the seemingly erratic movement of mitochondria correlated with the motility and organization patterns of ER tubules (Supplementary Movie 2). Immersion of seedlings in water under a coverslip for 30–45 min allowed mitochondria to elongate without a noticeable change in ER motility. Subsequent exposure to bright light for 30 s triggered mitochondrial fission. Through highly reproducible time-lapse series taken in over 80 different cells from 10 plants and from iso-surface volume rendering of confocal image stacks it became apparent that single elongated mitochondria were encircled by multiple ER tubules at several positions (Figures 3A–C; Supplementary Movie 2). The position of these ER bands around mitochondria often changed during the reorganization of the dynamic ER mesh. Changes in the organization of ER tubules and the consequent narrowing or broadening of ER polygons resulted in the stretching and twisting of enmeshed mitochondria. Whereas, an average time for a fission event could not be estimated due to the rather asynchronous interactions of mitochondria and the ER, a medial narrowing or constriction of the mitochondrion preceded every such event (Figures 3D,E; Supplementary Movie 3). This narrowing usually formed the point of fission (Figures 3F,G). A certain amount of force to separate the mitochondrial fragments was indicated in the way that the two portions of the mitochondrion and the ER pulled away into opposite directions after a fission event (Figures 3F,G). The pulling force often created a thin region between two fragments, very much like a medial matrixule, prior to their actual separation (Figures 3F,G).

Bottom Line: Here, through live-imaging of the entire range of mitochondria pleomorphy we uncover the underlying basis for the predominantly punctate mitochondrial form in plants.We demonstrate that mitochondrial morphology changes in response to light and cytosolic sugar levels in an ER mediated manner.By observing elongated mitochondria in normal plants and fission-impaired Arabidopsis nmt1-2 and drp3a mutants we also establish that thin extensions called matrixules and a beads-on-a-string mitochondrial phenotype are direct consequences of mitochondria-ER interactions.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Plant Development and Interactions, Department of Molecular and Cellular Biology, University of Guelph ON, Canada.

ABSTRACT
Mitochondria are pleomorphic, double membrane-bound organelles involved in cellular energetics in all eukaryotes. Mitochondria in animal and yeast cells are typically tubular-reticulate structures and several micro-meters long but in green plants they are predominantly observed as 0.2-1.5 μm punctae. While fission and fusion, through the coordinated activity of several conserved proteins, shapes mitochondria, the endoplasmic reticulum (ER) has recently been identified as an additional player in this process in yeast and mammalian cells. The mitochondria-ER relationship in plant cells remains largely uncharacterized. Here, through live-imaging of the entire range of mitochondria pleomorphy we uncover the underlying basis for the predominantly punctate mitochondrial form in plants. We demonstrate that mitochondrial morphology changes in response to light and cytosolic sugar levels in an ER mediated manner. Whereas, large ER polygons and low dynamics under dark conditions favor mitochondrial fusion and elongation, small ER polygons result in increased fission and predominantly small mitochondria. Hypoxia also reduces ER dynamics and increases mitochondrial fusion to produce giant mitochondria. By observing elongated mitochondria in normal plants and fission-impaired Arabidopsis nmt1-2 and drp3a mutants we also establish that thin extensions called matrixules and a beads-on-a-string mitochondrial phenotype are direct consequences of mitochondria-ER interactions.

No MeSH data available.


Related in: MedlinePlus