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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

Reduced ER dynamics promote mitochondrial fusion to form giant mitochondria. (A) Representative view of the ER organization and assorted mitochondrial size in normal, light-grown hypocotyl cell. (B) Representative view of expanded ER cisternae surrounding almost isotropically expanded mitochondria after 1 h under oxygen-limited conditions. (C) Mitochondrial clusters in ER corrals (e.g., boxed in region) surrounded by relatively large ER polygons were observed in dark-grown plants. (D) A representative image from a dark plant similar to (C) after an hour of oxygen limited conditions shows flat, giant mitochondria that appear to have formed through the fusion of mitochondria caught up in ER corrals. Note that there are no unduly expanded cisternae. (E) Representative image showing rather diffuse, enlarged mitochondria embedded in greatly expanded ER cisternae (cis) and not very well defined ER polygons (pol) in the pah1pah2 double mutant. (F) Snapshots from a time-lapse series of a cell with expanded mitochondria and ER cisternae exposed to light showed the resumption of dynamic behavior for both organelles. Mitochondrial blobs started extending and stretching and eventually breaking up as contiguous ER polygons got reorganized. A matrixule–like projection was extended from an expanded mitochondrion resuming dynamic behavior (arrowhead in panel F5). Size bars (A–E) = 5 μm; (F) = 10 μm.
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Figure 5: Reduced ER dynamics promote mitochondrial fusion to form giant mitochondria. (A) Representative view of the ER organization and assorted mitochondrial size in normal, light-grown hypocotyl cell. (B) Representative view of expanded ER cisternae surrounding almost isotropically expanded mitochondria after 1 h under oxygen-limited conditions. (C) Mitochondrial clusters in ER corrals (e.g., boxed in region) surrounded by relatively large ER polygons were observed in dark-grown plants. (D) A representative image from a dark plant similar to (C) after an hour of oxygen limited conditions shows flat, giant mitochondria that appear to have formed through the fusion of mitochondria caught up in ER corrals. Note that there are no unduly expanded cisternae. (E) Representative image showing rather diffuse, enlarged mitochondria embedded in greatly expanded ER cisternae (cis) and not very well defined ER polygons (pol) in the pah1pah2 double mutant. (F) Snapshots from a time-lapse series of a cell with expanded mitochondria and ER cisternae exposed to light showed the resumption of dynamic behavior for both organelles. Mitochondrial blobs started extending and stretching and eventually breaking up as contiguous ER polygons got reorganized. A matrixule–like projection was extended from an expanded mitochondrion resuming dynamic behavior (arrowhead in panel F5). Size bars (A–E) = 5 μm; (F) = 10 μm.

Mentions: As optimized earlier, the immersion of seedlings in water for about 45 min to an hour resulted in a general expansion of mitochondria. For light grown seedlings the simultaneous visualization of the ER and mitochondria at this stage showed a gradual reduction in the motility of both organelles with concomitant expansion of ER cisternae and single mitochondria (Figure 5A vs. Figure 5B; arrowheads in Figure 5B). For dark grown plants with small mitochondria clustered in ER corrals (Figure 5C-box) the expanded ER cisternae did not become as apparent as in light-grown plants. However, ER motility and the rearrangement of ER polygons did slow down and enlarged, flattened mitochondria became evident within the same duration as light grown plants (Figure 5D). Time-lapse observations suggested that reduced ER dynamics increased interaction time between mitochondria and promoted their fusion. These observations were tested in the nmt1-2/elm1-1 mutant transformed with RER. While the mutant has characteristically elongated mitochondria we were able to observe punctate mitochondria, by growing plants on 3% sugar containing MS medium and exposing them to light for 6 h before subjecting them to hypoxia. Punctate mitochondria clustered rapidly, fused and converted into long tubules within 15 min (Supplementary Movie 5). While the fusion in nmt1-2/elm1-1 mutant took place quickly and the ER appeared slightly diffuse and gave the impression of having expanded cisternae we used another mutant to reinforce this point. An Arabidopsis double mutant pah1pah2 in the phosphatidic acid phosphohydrolase1 and 2 contains over-expanded ER cisternal membranes (Eastmond et al., 2010) and was used to address this question. RER and mito-GFP dual probe expression in the pah1pah2 double mutant background showed expanded mitochondria with a diffuse outline in regions with large cisternae (Figure 5E).


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

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

Reduced ER dynamics promote mitochondrial fusion to form giant mitochondria. (A) Representative view of the ER organization and assorted mitochondrial size in normal, light-grown hypocotyl cell. (B) Representative view of expanded ER cisternae surrounding almost isotropically expanded mitochondria after 1 h under oxygen-limited conditions. (C) Mitochondrial clusters in ER corrals (e.g., boxed in region) surrounded by relatively large ER polygons were observed in dark-grown plants. (D) A representative image from a dark plant similar to (C) after an hour of oxygen limited conditions shows flat, giant mitochondria that appear to have formed through the fusion of mitochondria caught up in ER corrals. Note that there are no unduly expanded cisternae. (E) Representative image showing rather diffuse, enlarged mitochondria embedded in greatly expanded ER cisternae (cis) and not very well defined ER polygons (pol) in the pah1pah2 double mutant. (F) Snapshots from a time-lapse series of a cell with expanded mitochondria and ER cisternae exposed to light showed the resumption of dynamic behavior for both organelles. Mitochondrial blobs started extending and stretching and eventually breaking up as contiguous ER polygons got reorganized. A matrixule–like projection was extended from an expanded mitochondrion resuming dynamic behavior (arrowhead in panel F5). Size bars (A–E) = 5 μm; (F) = 10 μm.
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Figure 5: Reduced ER dynamics promote mitochondrial fusion to form giant mitochondria. (A) Representative view of the ER organization and assorted mitochondrial size in normal, light-grown hypocotyl cell. (B) Representative view of expanded ER cisternae surrounding almost isotropically expanded mitochondria after 1 h under oxygen-limited conditions. (C) Mitochondrial clusters in ER corrals (e.g., boxed in region) surrounded by relatively large ER polygons were observed in dark-grown plants. (D) A representative image from a dark plant similar to (C) after an hour of oxygen limited conditions shows flat, giant mitochondria that appear to have formed through the fusion of mitochondria caught up in ER corrals. Note that there are no unduly expanded cisternae. (E) Representative image showing rather diffuse, enlarged mitochondria embedded in greatly expanded ER cisternae (cis) and not very well defined ER polygons (pol) in the pah1pah2 double mutant. (F) Snapshots from a time-lapse series of a cell with expanded mitochondria and ER cisternae exposed to light showed the resumption of dynamic behavior for both organelles. Mitochondrial blobs started extending and stretching and eventually breaking up as contiguous ER polygons got reorganized. A matrixule–like projection was extended from an expanded mitochondrion resuming dynamic behavior (arrowhead in panel F5). Size bars (A–E) = 5 μm; (F) = 10 μm.
Mentions: As optimized earlier, the immersion of seedlings in water for about 45 min to an hour resulted in a general expansion of mitochondria. For light grown seedlings the simultaneous visualization of the ER and mitochondria at this stage showed a gradual reduction in the motility of both organelles with concomitant expansion of ER cisternae and single mitochondria (Figure 5A vs. Figure 5B; arrowheads in Figure 5B). For dark grown plants with small mitochondria clustered in ER corrals (Figure 5C-box) the expanded ER cisternae did not become as apparent as in light-grown plants. However, ER motility and the rearrangement of ER polygons did slow down and enlarged, flattened mitochondria became evident within the same duration as light grown plants (Figure 5D). Time-lapse observations suggested that reduced ER dynamics increased interaction time between mitochondria and promoted their fusion. These observations were tested in the nmt1-2/elm1-1 mutant transformed with RER. While the mutant has characteristically elongated mitochondria we were able to observe punctate mitochondria, by growing plants on 3% sugar containing MS medium and exposing them to light for 6 h before subjecting them to hypoxia. Punctate mitochondria clustered rapidly, fused and converted into long tubules within 15 min (Supplementary Movie 5). While the fusion in nmt1-2/elm1-1 mutant took place quickly and the ER appeared slightly diffuse and gave the impression of having expanded cisternae we used another mutant to reinforce this point. An Arabidopsis double mutant pah1pah2 in the phosphatidic acid phosphohydrolase1 and 2 contains over-expanded ER cisternal membranes (Eastmond et al., 2010) and was used to address this question. RER and mito-GFP dual probe expression in the pah1pah2 double mutant background showed expanded mitochondria with a diffuse outline in regions with large cisternae (Figure 5E).

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