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Auxin regulates SNARE-dependent vacuolar morphology restricting cell size.

Löfke C, Dünser K, Scheuring D, Kleine-Vehn J - Elife (2015)

Bottom Line: Here, we reveal that the phytohormone auxin impacts on the shape of the biggest plant organelle, the vacuole.Genetic and pharmacological interference with the auxin effect on vacuolar SNAREs interrelates with auxin-resistant vacuolar morphogenesis and cell size regulation.Vacuolar SNARE VTI11 is strictly required for auxin-reliant vacuolar morphogenesis and loss of function renders cells largely insensitive to auxin-dependent growth inhibition.

View Article: PubMed Central - PubMed

Affiliation: Department of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences, Vienna, Austria.

ABSTRACT
The control of cellular growth is central to multicellular patterning. In plants, the encapsulating cell wall literally binds neighbouring cells to each other and limits cellular sliding/migration. In contrast to its developmental importance, growth regulation is poorly understood in plants. Here, we reveal that the phytohormone auxin impacts on the shape of the biggest plant organelle, the vacuole. TIR1/AFBs-dependent auxin signalling posttranslationally controls the protein abundance of vacuolar SNARE components. Genetic and pharmacological interference with the auxin effect on vacuolar SNAREs interrelates with auxin-resistant vacuolar morphogenesis and cell size regulation. Vacuolar SNARE VTI11 is strictly required for auxin-reliant vacuolar morphogenesis and loss of function renders cells largely insensitive to auxin-dependent growth inhibition. Our data suggests that the adaptation of SNARE-dependent vacuolar morphogenesis allows auxin to limit cellular expansion, contributing to root organ growth rates.

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Quantification of epidermal cell length and vacuolar morphology.(A) From the onset of pronounced elongation (atrichoblast cell which is 2.5 times longer than wide), eight atrichoblast cells (depicted in yellow numbers) were counted towards the root tip. At this position, the length of four tricho-/atrichoblast cells (depicted in white numbers) were measured and averaged. Propidium-iodide-stained cell walls (orange). (B) The same positional information was used for quantifying the vacuolar morphology. Longest and widest distance was measured in the largest depicted vacuolar structure in four tricho-/atrichoblast cells per root. Vacuolar morphology was depicted by multiplying the distances (C) or by dividing the cell length by width (D). In this manuscript we mainly used (C) as vacuolar morphology index (vac. morph. index). (E) Three dimensional representation (orthogonal sectioning) of VAMP711-YFP expressing root epidermis; cross-hair depicts the region of optical sections used for all figures. T refers to trichoblast and A to atrichoblast cell file. Scale bar in (A) 50 µm; in (B) 10 µm; in (E) 20 µm.DOI:http://dx.doi.org/10.7554/eLife.05868.004
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fig1s1: Quantification of epidermal cell length and vacuolar morphology.(A) From the onset of pronounced elongation (atrichoblast cell which is 2.5 times longer than wide), eight atrichoblast cells (depicted in yellow numbers) were counted towards the root tip. At this position, the length of four tricho-/atrichoblast cells (depicted in white numbers) were measured and averaged. Propidium-iodide-stained cell walls (orange). (B) The same positional information was used for quantifying the vacuolar morphology. Longest and widest distance was measured in the largest depicted vacuolar structure in four tricho-/atrichoblast cells per root. Vacuolar morphology was depicted by multiplying the distances (C) or by dividing the cell length by width (D). In this manuscript we mainly used (C) as vacuolar morphology index (vac. morph. index). (E) Three dimensional representation (orthogonal sectioning) of VAMP711-YFP expressing root epidermis; cross-hair depicts the region of optical sections used for all figures. T refers to trichoblast and A to atrichoblast cell file. Scale bar in (A) 50 µm; in (B) 10 µm; in (E) 20 µm.DOI:http://dx.doi.org/10.7554/eLife.05868.004

Mentions: We established a vacuolar morphology index in epidermal cells based on the biggest luminal structure to further evaluate the apparent auxin effect on vacuolar shape (Figure 1—figure supplement 1). This analysis revealed that high auxin conditions affect vacuolar structures, particularly in atrichoblasts (Figure 1D,G). Adversely, pharmacological depletion of auxin caused visibly larger vacuolar structures in both cell types, but was more pronounced in trichoblasts (relative to the untreated control) (Figure 1A,C,D).


Auxin regulates SNARE-dependent vacuolar morphology restricting cell size.

Löfke C, Dünser K, Scheuring D, Kleine-Vehn J - Elife (2015)

Quantification of epidermal cell length and vacuolar morphology.(A) From the onset of pronounced elongation (atrichoblast cell which is 2.5 times longer than wide), eight atrichoblast cells (depicted in yellow numbers) were counted towards the root tip. At this position, the length of four tricho-/atrichoblast cells (depicted in white numbers) were measured and averaged. Propidium-iodide-stained cell walls (orange). (B) The same positional information was used for quantifying the vacuolar morphology. Longest and widest distance was measured in the largest depicted vacuolar structure in four tricho-/atrichoblast cells per root. Vacuolar morphology was depicted by multiplying the distances (C) or by dividing the cell length by width (D). In this manuscript we mainly used (C) as vacuolar morphology index (vac. morph. index). (E) Three dimensional representation (orthogonal sectioning) of VAMP711-YFP expressing root epidermis; cross-hair depicts the region of optical sections used for all figures. T refers to trichoblast and A to atrichoblast cell file. Scale bar in (A) 50 µm; in (B) 10 µm; in (E) 20 µm.DOI:http://dx.doi.org/10.7554/eLife.05868.004
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4384535&req=5

fig1s1: Quantification of epidermal cell length and vacuolar morphology.(A) From the onset of pronounced elongation (atrichoblast cell which is 2.5 times longer than wide), eight atrichoblast cells (depicted in yellow numbers) were counted towards the root tip. At this position, the length of four tricho-/atrichoblast cells (depicted in white numbers) were measured and averaged. Propidium-iodide-stained cell walls (orange). (B) The same positional information was used for quantifying the vacuolar morphology. Longest and widest distance was measured in the largest depicted vacuolar structure in four tricho-/atrichoblast cells per root. Vacuolar morphology was depicted by multiplying the distances (C) or by dividing the cell length by width (D). In this manuscript we mainly used (C) as vacuolar morphology index (vac. morph. index). (E) Three dimensional representation (orthogonal sectioning) of VAMP711-YFP expressing root epidermis; cross-hair depicts the region of optical sections used for all figures. T refers to trichoblast and A to atrichoblast cell file. Scale bar in (A) 50 µm; in (B) 10 µm; in (E) 20 µm.DOI:http://dx.doi.org/10.7554/eLife.05868.004
Mentions: We established a vacuolar morphology index in epidermal cells based on the biggest luminal structure to further evaluate the apparent auxin effect on vacuolar shape (Figure 1—figure supplement 1). This analysis revealed that high auxin conditions affect vacuolar structures, particularly in atrichoblasts (Figure 1D,G). Adversely, pharmacological depletion of auxin caused visibly larger vacuolar structures in both cell types, but was more pronounced in trichoblasts (relative to the untreated control) (Figure 1A,C,D).

Bottom Line: Here, we reveal that the phytohormone auxin impacts on the shape of the biggest plant organelle, the vacuole.Genetic and pharmacological interference with the auxin effect on vacuolar SNAREs interrelates with auxin-resistant vacuolar morphogenesis and cell size regulation.Vacuolar SNARE VTI11 is strictly required for auxin-reliant vacuolar morphogenesis and loss of function renders cells largely insensitive to auxin-dependent growth inhibition.

View Article: PubMed Central - PubMed

Affiliation: Department of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences, Vienna, Austria.

ABSTRACT
The control of cellular growth is central to multicellular patterning. In plants, the encapsulating cell wall literally binds neighbouring cells to each other and limits cellular sliding/migration. In contrast to its developmental importance, growth regulation is poorly understood in plants. Here, we reveal that the phytohormone auxin impacts on the shape of the biggest plant organelle, the vacuole. TIR1/AFBs-dependent auxin signalling posttranslationally controls the protein abundance of vacuolar SNARE components. Genetic and pharmacological interference with the auxin effect on vacuolar SNAREs interrelates with auxin-resistant vacuolar morphogenesis and cell size regulation. Vacuolar SNARE VTI11 is strictly required for auxin-reliant vacuolar morphogenesis and loss of function renders cells largely insensitive to auxin-dependent growth inhibition. Our data suggests that the adaptation of SNARE-dependent vacuolar morphogenesis allows auxin to limit cellular expansion, contributing to root organ growth rates.

Show MeSH