Stromules: a characteristic cell-specific feature of plastid morphology

Natesan, Senthil Kumar; Sullivan, Jerome L.; Gray, John C.

doi:10.1093/jxb/eri088

Cited by 147 publications

(124 citation statements)

References 53 publications

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“…One putative function of stromules may be to increase the surface area of chloroplasts to aid in the transport to and from the cytosol or organelles (Natesan et al, 2005). Although it was suggested that stromules may therefore be of importance in the low-phosphateresponse-related exchange of galactolipids and phospholipids, the results of our lipid measurements did not show an effect of the different SF in the wild type, max2-1, and max3-9 and phospholipid exchange.…”

Section: Galactolipid-phospholipid Exchange Under Low Pi Not Affectedcontrasting

confidence: 55%

Low-Phosphate Induction of Plastidal Stromules Is Dependent on Strigolactones But Not on the Canonical Strigolactone Signaling Component MAX2

et al. 2016

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Stromules are highly dynamic protrusions of the plastids in plants. Several factors, such as drought and light conditions, influence the stromule frequency (SF) in a positive or negative way. A relatively recently discovered class of plant hormones are the strigolactones; strigolactones inhibit branching of the shoots and promote beneficial interactions between roots and arbuscular mycorrhizal fungi. Here, we investigate the link between the formation of stromules and strigolactones. This research shows a strong link between strigolactones and the formation of stromules: SF correlates with strigolactone levels in the wild type and strigolactone mutants (max2-1 max3-9), and SF is stimulated by strigolactone GR24 and reduced by strigolactone inhibitor D2.

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Section: Galactolipid-phospholipid Exchange Under Low Pi Not Affectedcontrasting

confidence: 55%

Low-Phosphate Induction of Plastidal Stromules Is Dependent on Strigolactones But Not on the Canonical Strigolactone Signaling Component MAX2

et al. 2016

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“…Previous reports have investigated stromules using a variety of plastid types in a broad range of species and tissues, generally assuming that stromules act similarly in all cells (9)(10)(11)(12)(13)(14)(15)(16)(17)(18)(19). In light of the clear differences in signals that influence leucoplast and chloroplast stromule formation (Figs.…”

Section: Discussionmentioning

confidence: 99%

“…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).…”

mentioning

confidence: 99%

Chloroplasts extend stromules independently and in response to internal redox signals

Brunkard

Runkel

Zambryski

2015

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

142

136

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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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“…5B). Many stromules (stroma-filled tubules that extend from the surface of plastids; for review, see Kwok and Hanson, 2004a;Natesan et al, 2005) appeared in mesophyll cells after incubation irrespective of the addition of concanamycin A (Fig. 5, B-E).…”

Section: Involvement Of An Atg-dependent Autophagic Process In the Acmentioning

confidence: 99%

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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Stromules: a characteristic cell-specific feature of plastid morphology

Cited by 147 publications

References 53 publications

Low-Phosphate Induction of Plastidal Stromules Is Dependent on Strigolactones But Not on the Canonical Strigolactone Signaling Component MAX2

Low-Phosphate Induction of Plastidal Stromules Is Dependent on Strigolactones But Not on the Canonical Strigolactone Signaling Component MAX2

Chloroplasts extend stromules independently and in response to internal redox signals

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

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