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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

Average size of ER polygons and mitochondria correlates under light and dark growth conditions. (A,B) Representative images from 8 day old plants of RER Arabidopsis transgenics grown in the light (164 μmol m−2s−1) (A) and complete darkness (B) show the visible difference in the size of ER polygons. (C) A comparison of mitochondria and ER size from plants grown in the light and dark. Mitochondria from mito-GFP plants (n = 200 mitochondria per treatment) were significantly longer when plants were grown in the dark than in the light (1.07 ± 0.34 and 0.78 ± 0.15 μm, dark and light, respectively; p < 0.01). The average ER polygon area was also significantly larger in dark grown plants than those grown in the dark (55.07 ± 39.44 and 3.27 ± 2.05 μm, dark and light respectively; n = 120 ER polygons per treatment; p < 0.01). Standard error bars are shown. (D) “Corrals,” regions with small ER polygons formed between large ER polygons (boxed in area) were observed in dark grown plants. Mitochondria enmeshed in these regions were small while mitochondria elsewhere in the cell appeared elongated. The number of small ER polygons increased upon exposure to light and coincided with the increase in population of small mitochondria. Scale bars in (A,B,D) = 10 μm.
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Figure 4: Average size of ER polygons and mitochondria correlates under light and dark growth conditions. (A,B) Representative images from 8 day old plants of RER Arabidopsis transgenics grown in the light (164 μmol m−2s−1) (A) and complete darkness (B) show the visible difference in the size of ER polygons. (C) A comparison of mitochondria and ER size from plants grown in the light and dark. Mitochondria from mito-GFP plants (n = 200 mitochondria per treatment) were significantly longer when plants were grown in the dark than in the light (1.07 ± 0.34 and 0.78 ± 0.15 μm, dark and light, respectively; p < 0.01). The average ER polygon area was also significantly larger in dark grown plants than those grown in the dark (55.07 ± 39.44 and 3.27 ± 2.05 μm, dark and light respectively; n = 120 ER polygons per treatment; p < 0.01). Standard error bars are shown. (D) “Corrals,” regions with small ER polygons formed between large ER polygons (boxed in area) were observed in dark grown plants. Mitochondria enmeshed in these regions were small while mitochondria elsewhere in the cell appeared elongated. The number of small ER polygons increased upon exposure to light and coincided with the increase in population of small mitochondria. Scale bars in (A,B,D) = 10 μm.

Mentions: Our earlier observations had established that while mitochondria in plants grown under light are small, there is a significant increase in the sub-population of elongated mitochondria in the dark (Figure 1). A possible correlation with the ER was sought by comparing mito-GFP-RER seedlings grown under dark and light conditions. In comparison to the meshwork of small ER polygons under light-growth conditions (Figure 4A), the polygons were significantly larger in dark grown seedlings (Figures 4B,C). In general, the increased ER-polygon size correlated well with increased mitochondrial length in the dark (Figure 4C). Therefore, it was perplexing to find some small mitochondria too in dark grown plants. The reason for this apparent discrepancy was traced to the presence of numerous small ER polygons that are formed between large ER-polygons (Figure 4D). Based on our observation of numerous small mitochondria trapped in these small-ER-polygon enriched regions it appeared that elongated mitochondria enmeshed within such pockets, named “corrals,” broke up to form small mitochondria. Time-lapse imaging of dark grown plants following their exposure to light revealed that the formation of ER corrals increased over time so that after a few hours in light, the ER network comprised predominantly of small polygons. Notably there was a concomitant increase in the population of small mitochondria within the cell. Thus, our observations clearly indicated that the length of a mitochondrion in wild type plants depends upon the size of contiguous ER polygons and small polygons correlate with increased mitochondrial fission.


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

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

Average size of ER polygons and mitochondria correlates under light and dark growth conditions. (A,B) Representative images from 8 day old plants of RER Arabidopsis transgenics grown in the light (164 μmol m−2s−1) (A) and complete darkness (B) show the visible difference in the size of ER polygons. (C) A comparison of mitochondria and ER size from plants grown in the light and dark. Mitochondria from mito-GFP plants (n = 200 mitochondria per treatment) were significantly longer when plants were grown in the dark than in the light (1.07 ± 0.34 and 0.78 ± 0.15 μm, dark and light, respectively; p < 0.01). The average ER polygon area was also significantly larger in dark grown plants than those grown in the dark (55.07 ± 39.44 and 3.27 ± 2.05 μm, dark and light respectively; n = 120 ER polygons per treatment; p < 0.01). Standard error bars are shown. (D) “Corrals,” regions with small ER polygons formed between large ER polygons (boxed in area) were observed in dark grown plants. Mitochondria enmeshed in these regions were small while mitochondria elsewhere in the cell appeared elongated. The number of small ER polygons increased upon exposure to light and coincided with the increase in population of small mitochondria. Scale bars in (A,B,D) = 10 μm.
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Figure 4: Average size of ER polygons and mitochondria correlates under light and dark growth conditions. (A,B) Representative images from 8 day old plants of RER Arabidopsis transgenics grown in the light (164 μmol m−2s−1) (A) and complete darkness (B) show the visible difference in the size of ER polygons. (C) A comparison of mitochondria and ER size from plants grown in the light and dark. Mitochondria from mito-GFP plants (n = 200 mitochondria per treatment) were significantly longer when plants were grown in the dark than in the light (1.07 ± 0.34 and 0.78 ± 0.15 μm, dark and light, respectively; p < 0.01). The average ER polygon area was also significantly larger in dark grown plants than those grown in the dark (55.07 ± 39.44 and 3.27 ± 2.05 μm, dark and light respectively; n = 120 ER polygons per treatment; p < 0.01). Standard error bars are shown. (D) “Corrals,” regions with small ER polygons formed between large ER polygons (boxed in area) were observed in dark grown plants. Mitochondria enmeshed in these regions were small while mitochondria elsewhere in the cell appeared elongated. The number of small ER polygons increased upon exposure to light and coincided with the increase in population of small mitochondria. Scale bars in (A,B,D) = 10 μm.
Mentions: Our earlier observations had established that while mitochondria in plants grown under light are small, there is a significant increase in the sub-population of elongated mitochondria in the dark (Figure 1). A possible correlation with the ER was sought by comparing mito-GFP-RER seedlings grown under dark and light conditions. In comparison to the meshwork of small ER polygons under light-growth conditions (Figure 4A), the polygons were significantly larger in dark grown seedlings (Figures 4B,C). In general, the increased ER-polygon size correlated well with increased mitochondrial length in the dark (Figure 4C). Therefore, it was perplexing to find some small mitochondria too in dark grown plants. The reason for this apparent discrepancy was traced to the presence of numerous small ER polygons that are formed between large ER-polygons (Figure 4D). Based on our observation of numerous small mitochondria trapped in these small-ER-polygon enriched regions it appeared that elongated mitochondria enmeshed within such pockets, named “corrals,” broke up to form small mitochondria. Time-lapse imaging of dark grown plants following their exposure to light revealed that the formation of ER corrals increased over time so that after a few hours in light, the ER network comprised predominantly of small polygons. Notably there was a concomitant increase in the population of small mitochondria within the cell. Thus, our observations clearly indicated that the length of a mitochondrion in wild type plants depends upon the size of contiguous ER polygons and small polygons correlate with increased mitochondrial fission.

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