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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

The range of mitochondrial forms obtained in Arabidopsis plants under different conditions. (A) Mitochondria in dark grown hypocotyl cells could appear punctate (box), clustered (*), or elongated (e). An elongated mitochondrion could exhibit terminal (arrowheads) or medial matrixules (small arrow). The medial matrixule was often observed just before the fission of an elongated mitochondrion. (B) Elongated mitochondria displayed shape contortions that eventually led to mitochondrial fission. Thin, stretched out regions, as shown in an elongated mitochondrion (single arrowhead) and a possible break-point shown in a sickle-shaped mitochondrion (facing arrowheads) were commonly observed. (C) Elongated mitochondria from dark-grown plants often exhibited a beads-on-a-string form consisting of dilated (d) and narrow intervening regions in the nmt1-2 mutant. Whereas, in elongated mitochondria in the wild type this form often preceded fission, it persisted in the fission-impaired adl2a and nmt1-2 mutants. (D,E) Single, expanded torus-like mitochondrial forms were observed under oxygen-limited conditions. As suggested by the extension in (E) this shape is not fixed and changes over time. (F) Under prolonged hypoxia enlarged mitochondria expanded into flattened discs and sheet-like forms. (G) Hypoxia in a plant expressing mitochondrial targeted mEosFP resulted in expanded mitochondria, some of which (arrowheads) were photo-converted from green to orange-red. (H) A time-lapse image series showed the interaction (frames 1–4) and eventual fusion (frame 5-arrowhead) of a green (g) and a photo-converted, red (r) mitochondrion to produce an even larger giant mitochondrion (frame 5) with an intermediate orange fluorescence. (I,J) A color distribution map of frame1 compared to frame 5 in (H) provided an estimate of redistribution of mitochondrial matrix through the prominent color mixing that occurred upon fusion of the green non-photo-converted with the red, photo-converted mitochondrion. (K) A time-lapse image sequence obtained after irradiating a giant mitochondrion formed under low oxygen conditions (1) with bright light for 6 min initiated a break point (arrowhead in 2), progressive separation of a small fragment (3,4) and its eventual moving away from the large mitochondrion. Size bars = 5 μm.
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Figure 2: The range of mitochondrial forms obtained in Arabidopsis plants under different conditions. (A) Mitochondria in dark grown hypocotyl cells could appear punctate (box), clustered (*), or elongated (e). An elongated mitochondrion could exhibit terminal (arrowheads) or medial matrixules (small arrow). The medial matrixule was often observed just before the fission of an elongated mitochondrion. (B) Elongated mitochondria displayed shape contortions that eventually led to mitochondrial fission. Thin, stretched out regions, as shown in an elongated mitochondrion (single arrowhead) and a possible break-point shown in a sickle-shaped mitochondrion (facing arrowheads) were commonly observed. (C) Elongated mitochondria from dark-grown plants often exhibited a beads-on-a-string form consisting of dilated (d) and narrow intervening regions in the nmt1-2 mutant. Whereas, in elongated mitochondria in the wild type this form often preceded fission, it persisted in the fission-impaired adl2a and nmt1-2 mutants. (D,E) Single, expanded torus-like mitochondrial forms were observed under oxygen-limited conditions. As suggested by the extension in (E) this shape is not fixed and changes over time. (F) Under prolonged hypoxia enlarged mitochondria expanded into flattened discs and sheet-like forms. (G) Hypoxia in a plant expressing mitochondrial targeted mEosFP resulted in expanded mitochondria, some of which (arrowheads) were photo-converted from green to orange-red. (H) A time-lapse image series showed the interaction (frames 1–4) and eventual fusion (frame 5-arrowhead) of a green (g) and a photo-converted, red (r) mitochondrion to produce an even larger giant mitochondrion (frame 5) with an intermediate orange fluorescence. (I,J) A color distribution map of frame1 compared to frame 5 in (H) provided an estimate of redistribution of mitochondrial matrix through the prominent color mixing that occurred upon fusion of the green non-photo-converted with the red, photo-converted mitochondrion. (K) A time-lapse image sequence obtained after irradiating a giant mitochondrion formed under low oxygen conditions (1) with bright light for 6 min initiated a break point (arrowhead in 2), progressive separation of a small fragment (3,4) and its eventual moving away from the large mitochondrion. Size bars = 5 μm.

Mentions: In agreement with earlier reports (Van Gestel and Verbelen, 2002; Logan, 2006a) seedlings with approximately 1.5–2 μm long mitochondria, when kept between a glass slide and coverslip for more than 30 min showed an increase in mitochondrial lengths of up to 5–8 μm (Figures 2A,B). Mitochondrial elongation took place irrespective of whether the seedlings were grown in the dark or light, with or without sucrose. The considerably elongated mitochondria displayed normal motility rates of 1.5 ± 0.4 μms−1 and morphed continuously, coiling, and forming branched and reticulate shapes (Figure 2B). Time-lapse imaging of tubular mitochondria showed sporadic dilations and constrictions forming along their length resulting in a beads-on-a-string appearance (Figure 2C). Exposing the plants to 800 ± 50 μmol m−2s−1 light for approximately 30 s using the bright-field illumination on our upright epi-fluorescence microscope led to the rapid fission of such mitochondria into smaller units. In nearly all cases the beads-on-a-string form preceded a fission event with the actual break occurring at the narrow neck region (Figures 2A,B). Occasionally, single mitochondria displayed thin transient extensions that have been called matrixules (Scott et al., 2007; Figure 2A).


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

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

The range of mitochondrial forms obtained in Arabidopsis plants under different conditions. (A) Mitochondria in dark grown hypocotyl cells could appear punctate (box), clustered (*), or elongated (e). An elongated mitochondrion could exhibit terminal (arrowheads) or medial matrixules (small arrow). The medial matrixule was often observed just before the fission of an elongated mitochondrion. (B) Elongated mitochondria displayed shape contortions that eventually led to mitochondrial fission. Thin, stretched out regions, as shown in an elongated mitochondrion (single arrowhead) and a possible break-point shown in a sickle-shaped mitochondrion (facing arrowheads) were commonly observed. (C) Elongated mitochondria from dark-grown plants often exhibited a beads-on-a-string form consisting of dilated (d) and narrow intervening regions in the nmt1-2 mutant. Whereas, in elongated mitochondria in the wild type this form often preceded fission, it persisted in the fission-impaired adl2a and nmt1-2 mutants. (D,E) Single, expanded torus-like mitochondrial forms were observed under oxygen-limited conditions. As suggested by the extension in (E) this shape is not fixed and changes over time. (F) Under prolonged hypoxia enlarged mitochondria expanded into flattened discs and sheet-like forms. (G) Hypoxia in a plant expressing mitochondrial targeted mEosFP resulted in expanded mitochondria, some of which (arrowheads) were photo-converted from green to orange-red. (H) A time-lapse image series showed the interaction (frames 1–4) and eventual fusion (frame 5-arrowhead) of a green (g) and a photo-converted, red (r) mitochondrion to produce an even larger giant mitochondrion (frame 5) with an intermediate orange fluorescence. (I,J) A color distribution map of frame1 compared to frame 5 in (H) provided an estimate of redistribution of mitochondrial matrix through the prominent color mixing that occurred upon fusion of the green non-photo-converted with the red, photo-converted mitochondrion. (K) A time-lapse image sequence obtained after irradiating a giant mitochondrion formed under low oxygen conditions (1) with bright light for 6 min initiated a break point (arrowhead in 2), progressive separation of a small fragment (3,4) and its eventual moving away from the large mitochondrion. Size bars = 5 μm.
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Figure 2: The range of mitochondrial forms obtained in Arabidopsis plants under different conditions. (A) Mitochondria in dark grown hypocotyl cells could appear punctate (box), clustered (*), or elongated (e). An elongated mitochondrion could exhibit terminal (arrowheads) or medial matrixules (small arrow). The medial matrixule was often observed just before the fission of an elongated mitochondrion. (B) Elongated mitochondria displayed shape contortions that eventually led to mitochondrial fission. Thin, stretched out regions, as shown in an elongated mitochondrion (single arrowhead) and a possible break-point shown in a sickle-shaped mitochondrion (facing arrowheads) were commonly observed. (C) Elongated mitochondria from dark-grown plants often exhibited a beads-on-a-string form consisting of dilated (d) and narrow intervening regions in the nmt1-2 mutant. Whereas, in elongated mitochondria in the wild type this form often preceded fission, it persisted in the fission-impaired adl2a and nmt1-2 mutants. (D,E) Single, expanded torus-like mitochondrial forms were observed under oxygen-limited conditions. As suggested by the extension in (E) this shape is not fixed and changes over time. (F) Under prolonged hypoxia enlarged mitochondria expanded into flattened discs and sheet-like forms. (G) Hypoxia in a plant expressing mitochondrial targeted mEosFP resulted in expanded mitochondria, some of which (arrowheads) were photo-converted from green to orange-red. (H) A time-lapse image series showed the interaction (frames 1–4) and eventual fusion (frame 5-arrowhead) of a green (g) and a photo-converted, red (r) mitochondrion to produce an even larger giant mitochondrion (frame 5) with an intermediate orange fluorescence. (I,J) A color distribution map of frame1 compared to frame 5 in (H) provided an estimate of redistribution of mitochondrial matrix through the prominent color mixing that occurred upon fusion of the green non-photo-converted with the red, photo-converted mitochondrion. (K) A time-lapse image sequence obtained after irradiating a giant mitochondrion formed under low oxygen conditions (1) with bright light for 6 min initiated a break point (arrowhead in 2), progressive separation of a small fragment (3,4) and its eventual moving away from the large mitochondrion. Size bars = 5 μm.
Mentions: In agreement with earlier reports (Van Gestel and Verbelen, 2002; Logan, 2006a) seedlings with approximately 1.5–2 μm long mitochondria, when kept between a glass slide and coverslip for more than 30 min showed an increase in mitochondrial lengths of up to 5–8 μm (Figures 2A,B). Mitochondrial elongation took place irrespective of whether the seedlings were grown in the dark or light, with or without sucrose. The considerably elongated mitochondria displayed normal motility rates of 1.5 ± 0.4 μms−1 and morphed continuously, coiling, and forming branched and reticulate shapes (Figure 2B). Time-lapse imaging of tubular mitochondria showed sporadic dilations and constrictions forming along their length resulting in a beads-on-a-string appearance (Figure 2C). Exposing the plants to 800 ± 50 μmol m−2s−1 light for approximately 30 s using the bright-field illumination on our upright epi-fluorescence microscope led to the rapid fission of such mitochondria into smaller units. In nearly all cases the beads-on-a-string form preceded a fission event with the actual break occurring at the narrow neck region (Figures 2A,B). Occasionally, single mitochondria displayed thin transient extensions that have been called matrixules (Scott et al., 2007; Figure 2A).

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