Cytoneme-Mediated Contact-Dependent Transport of the
            <i>Drosophila</i>
            Decapentaplegic Signaling Protein

Roy, Sougata; Huang, Hai; Liu, Song-Mei; Kornberg, Thomas B.

doi:10.1126/science.1244624

Cited by 204 publications

(345 citation statements)

References 53 publications

(114 reference statements)

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“…2 and 5), future work will need to carefully consider the biological context of stromule activity. With the discovery that stromules extend from chloroplasts independently of external structures, analogies to cytonemes could help reveal the roles of stromules, because cytonemes are comparable thin, tubular projections that extend from animal cells to facilitate intercellular communication during development (35,36). Although the function of stromules remains unknown, it may be speculated that they similarly facilitate signal transduction between organelles, given that stromules have been observed associating with the nucleus, plasma membrane, endoplasmic reticulum, and other plastids (10,11,30).…”

Section: Resultsmentioning

confidence: 99%

Chloroplasts extend stromules independently and in response to internal redox signals

Brunkard

Runkel

Zambryski

2015

Proc. Natl. Acad. Sci. U.S.A.

144

137

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A fundamental mystery of plant cell biology is the occurrence of "stromules," stroma-filled tubular extensions from plastids (such as chloroplasts) that are universally observed in plants but whose functions are, in effect, completely unknown. One prevalent hypothesis is that stromules exchange signals or metabolites between plastids and other subcellular compartments, and that stromules are induced during stress. Until now, no signaling mechanisms originating within the plastid have been identified that regulate stromule activity, a critical missing link in this hypothesis. Using confocal and superresolution 3D microscopy, we have shown that stromules form in response to light-sensitive redox signals within the chloroplast. Stromule frequency increased during the day or after treatment with chemicals that produce reactive oxygen species specifically in the chloroplast. Silencing expression of the chloroplast NADPH-dependent thioredoxin reductase, a central hub in chloroplast redox signaling pathways, increased chloroplast stromule frequency, whereas silencing expression of nuclear genes related to plastid genome expression and tetrapyrrole biosynthesis had no impact on stromules. Leucoplasts, which are not photosynthetic, also made more stromules in the daytime. Leucoplasts did not respond to the same redox signaling pathway but instead increased stromule formation when exposed to sucrose, a major product of photosynthesis, although sucrose has no impact on chloroplast stromule frequency. Thus, different types of plastids make stromules in response to distinct signals. Finally, isolated chloroplasts could make stromules independently after extraction from the cytoplasm, suggesting that chloroplast-associated factors are sufficient to generate stromules. These discoveries demonstrate that chloroplasts are remarkably autonomous organelles that alter their stromule frequency in reaction to internal signal transduction pathways.chloroplasts | stromules | redox signaling | light signaling | leucoplasts

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Section: Resultsmentioning

confidence: 99%

Chloroplasts extend stromules independently and in response to internal redox signals

Brunkard

Runkel

Zambryski

2015

Proc. Natl. Acad. Sci. U.S.A.

144

137

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“…Imaging of fixed samples was performed with a point laser confocal microscope (Leica SPE). GRASP analysis was conducted as described in Roy et al (2014).…”

Section: Drosophila Wing Disc Culture and Imagingmentioning

confidence: 99%

Essential basal cytonemes take up Hedgehog in the Drosophila wing imaginal disc

et al. 2017

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Morphogen concentration gradients that extend across developmental fields form by dispersion from source cells. In the Drosophila wing disc, Hedgehog (Hh) produced by posterior compartment cells distributes in a concentration gradient to adjacent cells of the anterior compartment. We monitored Hh:GFP after pulsed expression, and analyzed the movement and colocalization of Hh, Patched (Ptc) and Smoothened (Smo) proteins tagged with GFP or mCherry and expressed at physiological levels from bacterial artificial chromosome transgenes. Hh:GFP moved to basal subcellular locations prior to release from posterior compartment cells that express it, and was taken up by basal cytonemes that extend to the source cells. Hh and Ptc were present in puncta that moved along the basal cytonemes and formed characteristic apical-basal distributions in the anterior compartment cells. The basal cytonemes required diaphanous, SCAR, Neuroglian and Synaptobrevin, and both the Hh gradient and Hh signaling declined under conditions in which the cytonemes were compromised. These findings show that in the wing disc, Hh distributions and signaling are dependent upon basal release and uptake, and on cytoneme-mediated movement. No evidence for apical dispersion was obtained.

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“…Cell-based transport requires the endocytosis of ligand, and dynamin has indeed been shown to be important for morphogen spreading 5 . Internalized ligand can then be transported either by transcytosis 5 , a process by which macromolecules are transported across the interior of a cell, or by cytonemes, that is, by specialized filopodia that mediate long-distance signalling during development 6,7 . Diffusion of morphogens, either freely or hindered 3 , is well documented, but the relative contributions of the different transport mechanisms have remained controversial.…”

mentioning

confidence: 99%

Dynamic scaling of morphogen gradients on growing domains

Fried

Iber

2014

Nat Commun

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Developmental mechanisms are highly conserved, yet act in embryos of very different sizes. How scaling is achieved has remained elusive. Here we identify a generally applicable mechanism for dynamic scaling on growing domains and show that it quantitatively agrees with data from the Drosophila wing imaginal disc. We show that for the measured parameter ranges, the Dpp gradient does not reach steady state during Drosophila wing development. We further show that both, pre-steady-state dynamics and advection of cell-bound ligand in a growing tissue can, in principle, enable scaling, even for non-uniform tissue growth. For the parameter values that have been established for the Dpp morphogen in the Drosophila wing imaginal disc, we show that scaling is mainly a result of the pre-steady-state dynamics. Pre-steady-state dynamics are pervasive in morphogen-controlled systems, thus making this a probable general mechanism for dynamic scaling of morphogen gradients in growing developmental systems.

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Cytoneme-Mediated Contact-Dependent Transport of the Drosophila Decapentaplegic Signaling Protein

Cited by 204 publications

References 53 publications

Chloroplasts extend stromules independently and in response to internal redox signals

Chloroplasts extend stromules independently and in response to internal redox signals

Essential basal cytonemes take up Hedgehog in the Drosophila wing imaginal disc

Dynamic scaling of morphogen gradients on growing domains

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