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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

Effects of light, dark and sugar on mitochondria length. (A–E) Pie diagram showing the relative percentage of small (less than 0.85 μm) vs. elongated (longer than 0.85 μm) mitochondria in a cellular population for under different conditions. Data based on Arabidopsis mito-GFP transgenics grown for 7 days in light (70 μmol m−2 s−1) and dark on MS medium with no sucrose (A1,A2,B,C) and with 3% sucrose (A3,A4,D,E). Mitochondria in seedlings grown in the dark were predominantly elongated (B,D) as compared to the punctate mitochondria in plants grown in light (C,E). (F,G) Dark grown plants grown without sucrose were transferred to light (70 μmol m−2s−1) for 1 h (F) and 12 h (G) without sucrose. Putative fission sites on tubular mitochondria are indicated (arrows).
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Figure 1: Effects of light, dark and sugar on mitochondria length. (A–E) Pie diagram showing the relative percentage of small (less than 0.85 μm) vs. elongated (longer than 0.85 μm) mitochondria in a cellular population for under different conditions. Data based on Arabidopsis mito-GFP transgenics grown for 7 days in light (70 μmol m−2 s−1) and dark on MS medium with no sucrose (A1,A2,B,C) and with 3% sucrose (A3,A4,D,E). Mitochondria in seedlings grown in the dark were predominantly elongated (B,D) as compared to the punctate mitochondria in plants grown in light (C,E). (F,G) Dark grown plants grown without sucrose were transferred to light (70 μmol m−2s−1) for 1 h (F) and 12 h (G) without sucrose. Putative fission sites on tubular mitochondria are indicated (arrows).

Mentions: Photosynthesis in green plant cells causes cytosolic sugar levels to fluctuate considerably between cells and during the day and night cycle (Azcón-Bieto and Osmond, 1983; Azcón-Bieto et al., 1983). This was the rationale behind our using a more controlled, in vitro, exogenous sugar-feeding approach. Arabidopsis mito-GFP seeds were sown on MS medium with and without sucrose and kept in the dark to first assess if exogenous sugar in the MS medium actually altered cytosolic sugar levels in seedlings. Cytosolic sugar estimations (Figure 1; Supplementary Information) for 7 day old plants using a phenol-sulfuric acid colorimetric method (Buysse and Merckx, 1993) established that plants grown on MS medium with 3% sucrose had higher soluble sugar levels [10.14 ± 1.10 μg/mg of fresh weight (f.w.)] as compared to plants grown without sucrose in the medium (1.92 ± 0.77 μg/mg f.w.).


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

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

Effects of light, dark and sugar on mitochondria length. (A–E) Pie diagram showing the relative percentage of small (less than 0.85 μm) vs. elongated (longer than 0.85 μm) mitochondria in a cellular population for under different conditions. Data based on Arabidopsis mito-GFP transgenics grown for 7 days in light (70 μmol m−2 s−1) and dark on MS medium with no sucrose (A1,A2,B,C) and with 3% sucrose (A3,A4,D,E). Mitochondria in seedlings grown in the dark were predominantly elongated (B,D) as compared to the punctate mitochondria in plants grown in light (C,E). (F,G) Dark grown plants grown without sucrose were transferred to light (70 μmol m−2s−1) for 1 h (F) and 12 h (G) without sucrose. Putative fission sites on tubular mitochondria are indicated (arrows).
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4585081&req=5

Figure 1: Effects of light, dark and sugar on mitochondria length. (A–E) Pie diagram showing the relative percentage of small (less than 0.85 μm) vs. elongated (longer than 0.85 μm) mitochondria in a cellular population for under different conditions. Data based on Arabidopsis mito-GFP transgenics grown for 7 days in light (70 μmol m−2 s−1) and dark on MS medium with no sucrose (A1,A2,B,C) and with 3% sucrose (A3,A4,D,E). Mitochondria in seedlings grown in the dark were predominantly elongated (B,D) as compared to the punctate mitochondria in plants grown in light (C,E). (F,G) Dark grown plants grown without sucrose were transferred to light (70 μmol m−2s−1) for 1 h (F) and 12 h (G) without sucrose. Putative fission sites on tubular mitochondria are indicated (arrows).
Mentions: Photosynthesis in green plant cells causes cytosolic sugar levels to fluctuate considerably between cells and during the day and night cycle (Azcón-Bieto and Osmond, 1983; Azcón-Bieto et al., 1983). This was the rationale behind our using a more controlled, in vitro, exogenous sugar-feeding approach. Arabidopsis mito-GFP seeds were sown on MS medium with and without sucrose and kept in the dark to first assess if exogenous sugar in the MS medium actually altered cytosolic sugar levels in seedlings. Cytosolic sugar estimations (Figure 1; Supplementary Information) for 7 day old plants using a phenol-sulfuric acid colorimetric method (Buysse and Merckx, 1993) established that plants grown on MS medium with 3% sucrose had higher soluble sugar levels [10.14 ± 1.10 μg/mg of fresh weight (f.w.)] as compared to plants grown without sucrose in the medium (1.92 ± 0.77 μg/mg f.w.).

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