Chloroplasts and Mitochondria in Living Plant Cells: Cinephotomicrographic Studies

Wildman, S. G.; Hongladarom, Tasani; Honda, Shigeru

doi:10.1126/science.138.3538.434

Cited by 151 publications

(104 citation statements)

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“…In cinephotomicrographic and video microscopic studies, chloroplast protuberances have been observed to segment into vesicular structures (Wildman et al, 1962;Gunning, 2005). The release of bodies approximately 1.5 mm in diameter from the ends of stromules has been observed (Gunning, 2005).…”

Section: Discussionmentioning

confidence: 93%

Mobilization of Rubisco and Stroma-Localized Fluorescent Proteins of Chloroplasts to the Vacuole by anATGGene-Dependent Autophagic Process

et al. 2008

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During senescence and at times of stress, plants can mobilize needed nitrogen from chloroplasts in leaves to other organs. Much of the total leaf nitrogen is allocated to the most abundant plant protein, Rubisco. While bulk degradation of the cytosol and organelles in plants occurs by autophagy, the role of autophagy in the degradation of chloroplast proteins is still unclear. We have visualized the fate of Rubisco, stroma-targeted green fluorescent protein (GFP) and DsRed, and GFP-labeled Rubisco in order to investigate the involvement of autophagy in the mobilization of stromal proteins to the vacuole. Using immunoelectron microscopy, we previously demonstrated that Rubisco is released from the chloroplast into Rubisco-containing bodies (RCBs) in naturally senescent leaves. When leaves of transgenic Arabidopsis (Arabidopsis thaliana) plants expressing stroma-targeted fluorescent proteins were incubated with concanamycin A to inhibit vacuolar H 1 -ATPase activity, spherical bodies exhibiting GFP or DsRed fluorescence without chlorophyll fluorescence were observed in the vacuolar lumen. Double-labeled immunoelectron microscopy with anti-Rubisco and anti-GFP antibodies confirmed that the fluorescent bodies correspond to RCBs. RCBs could also be visualized using GFP-labeled Rubisco directly. RCBs were not observed in leaves of a T-DNA insertion mutant in ATG5, one of the essential genes for autophagy. Stroma-targeted DsRed and GFP-ATG8 fusion proteins were observed together in autophagic bodies in the vacuole. We conclude that Rubisco and stroma-targeted fluorescent proteins can be mobilized to the vacuole through an ATG gene-dependent autophagic process without prior chloroplast destruction.

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Section: Discussionmentioning

confidence: 93%

Mobilization of Rubisco and Stroma-Localized Fluorescent Proteins of Chloroplasts to the Vacuole by anATGGene-Dependent Autophagic Process

et al. 2008

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“…Stromules were first observed in spinach cells (12), and have since been observed in every cell type and land plant species investigated to date (13). Several studies have identified conditions that can induce or decrease stromule formation (14)(15)(16)(17)(18), concluding that stromule frequency can change in response to abiotic stress, phytohormone signaling, and massive disruption of cellular function (e.g., strong inhibition of cytosolic translation or of actin microfilament dynamics).…”

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confidence: 99%

Chloroplasts extend stromules independently and in response to internal redox signals

Brunkard

Runkel

Zambryski

2015

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

166

145

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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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“…In the living higher plant cell, chloroplasts consist of a grantular, chlorophyllouis, stationary lamellar component suirrounded and, presumably, interpenetrated by a pleomorphic mobile phase containing stroma (4,6,21,22). In chloroplasts viewed in situ by electron microscopy ( 14), the stationary lamellar component together with the mobile phase is enclosed by a structural membrane.…”

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“…Individual chloroplasts cotuld be swollen and contracted repeatedly throtugh as many as 4 cycles. The relationsh p between the capacity for osmotic behavior and chloroplast appearaince in cell extracts is dliscuissed.In the living higher plant cell, chloroplasts consist of a grantular, chlorophyllouis, stationary lamellar component suirrounded and, presumably, interpenetrated by a pleomorphic mobile phase containing stroma (4,6,21,22 …”

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Reversible Swelling and Contraction of Isolated Spinach Chloroplasts

Hongladarom

Honda

1966

Plant Physiol.

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Sunwiary. Bly uise of a micro technique for prodtucing extracts of spiInach mesophyll cells, chloroplasts were isolated in a state wherein they dlisplaye(l microscopically visible, reversible osmotic properties. Swollein spherical chloroplasts treatedl with hypertonic sucrose or mannitol media, bUt not NaCl, couild be shruinken to a state resembling their disk appearance in livinig cells. Reversible osmotic behavior was more easily demonstratedl when the chloroplasts were initially-isolated from cells in a relatively low osmolar concentration in contrast to uising 0.25 m1 suicrose or more concentrated media. Individual chloroplasts cotuld be swollen and contracted repeatedly throtugh as many as 4 cycles. The relationsh p between the capacity for osmotic behavior and chloroplast appearaince in cell extracts is dliscuissed.In the living higher plant cell, chloroplasts consist of a grantular, chlorophyllouis, stationary lamellar component suirrounded and, presumably, interpenetrated by a pleomorphic mobile phase containing stroma (4,6,21,22

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Chloroplasts and Mitochondria in Living Plant Cells: Cinephotomicrographic Studies

Cited by 151 publications

References 2 publications

Mobilization of Rubisco and Stroma-Localized Fluorescent Proteins of Chloroplasts to the Vacuole by anATGGene-Dependent Autophagic Process

Mobilization of Rubisco and Stroma-Localized Fluorescent Proteins of Chloroplasts to the Vacuole by anATGGene-Dependent Autophagic Process

Chloroplasts extend stromules independently and in response to internal redox signals

Reversible Swelling and Contraction of Isolated Spinach Chloroplasts

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