title: Chloroplasts extend stromules independently and in response to internal redox signals.
abstract: 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.
authors.affiliation: Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720.
authors.forename: Jacob O
authors.initials: JO
authors.lastname: Brunkard
authors.affiliation: Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720.
authors.forename: Anne M
authors.initials: AM
authors.lastname: Runkel
authors.affiliation: Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720 zambrysk@berkeley.edu.
authors.forename: Patricia C
authors.initials: PC
authors.lastname: Zambryski
mesh_terms: D001483:Base Sequence; D016227:Benzoquinones / Q000494:pharmacology; D002736:Chloroplasts / Q000378:metabolism* / Q000648:ultrastructure; D002940:Circadian Rhythm / Q000187:drug effects; D004237:Diuron / Q000494:pharmacology; D020868:Gene Silencing / Q000187:drug effects; D049452:Green Fluorescent Proteins / Q000378:metabolism; D008954:Models, Biological; D008969:Molecular Sequence Data; D009249:NADP / Q000378:metabolism; D010084:Oxidation-Reduction / Q000187:drug effects; D010788:Photosynthesis / Q000187:drug effects; D010802:Phylogeny; D019441:Plant Epidermis / Q000187:drug effects / Q000378:metabolism; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D017382:Reactive Oxygen Species / Q000378:metabolism; D015398:Signal Transduction / Q000187:drug effects; D013395:Sucrose / Q000494:pharmacology; D013880:Thioredoxin-Disulfide Reductase / Q000378:metabolism; D059008:Time-Lapse Imaging; D014026:Nicotiana / Q000187:drug effects / Q000378:metabolism*
chemical_list: D016227:Benzoquinones; D010940:Plant Proteins; D017382:Reactive Oxygen Species; D049452:Green Fluorescent Proteins; D009249:NADP; D013395:Sucrose; D004237:Diuron; D013880:Thioredoxin-Disulfide Reductase
keywords: chloroplasts; leucoplasts; light signaling; redox signaling; stromules