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Reactive Oxygen Species Signal Chloroplasts to Extend Themselves Maureen R

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Reactive Oxygen Species Signal Chloroplasts to Extend Themselves Maureen R COMMENTARY COMMENTARY Reactive oxygen species signal chloroplasts to extend themselves Maureen R. Hanson1 thaliana, to examine stromule formation Department of Molecular Biology and Genetics, Cornell University, Ithaca, NY 14853 and frequency when tissues were placed under various environmental regimes and stresses. When the photosynthetic electron ’ – When Sam Wildman s group first reported his plant cells (4 7). Probable functions for stro- transport chain was inhibited by exogenously phase-contrast microscopic observations of mules have been hypothesized for many years supplied chemicals, resulting in generation of – chloroplast tubular extensions in 1962 (1), he (4,5,810), but there has been no proof of ROS, stromule frequency in N. benthamiana was greeted with skepticism by some plant bi- function and little has been known about epidermal chloroplasts and in A. thaliana ologists, who dismissed his findings of mem- how they form. In PNAS, Brunkard et al. guard cell chloroplasts significantly increased. brane protrusions as artifacts of stress caused (11) describe their discovery that stromules However, stromule frequency was not altered by long observation of leaf cells under the mi- do not require external structures for their for- in naturally nonphotosynthetic leucoplasts croscope. Following their rediscovery through mation. Furthermore, the authors demonstrate present in A. thaliana epidermal cells, dem- GFP technology (2), it is now known that stress that increase in reactive oxygen species (ROS) onstrating that ROS generated by photosyn- actually can induce the tubular formations (3), by inhibition of photosynthesis induces stro- thesis is responsible for the effect. Brunkard subsequently named stromules (4). But stro- mule formation in chloroplasts. et al. also took advantage of a transient RNA mules are no artifact; instead, they are a feature Brunkard et al. (11) used two model plants, silencing method in N. benthamiana to re- exhibitedbyplastidsinmanydifferenttypesof Nicotiana benthamiana and Arabidopsis duce the expression of the nuclear-encoded chloroplast NADPH-dependent thioredoxin reductase. Following this disruption of redox signal transduction within the chloroplast, stromule frequency more than doubled. No- tably, RNA silencing of a gene involved in plastid gene expression and another involved in tetrapyrrole biosynthesis did not affect stromule frequency, indicating that not all disturbances in chloroplast function lead to an increase in stromules. Treating Arabidopsis cotyledons with an inhibitor that causes ROS generation in mitochondria also did not affect stromule frequency. The experi- ments by Brunkard et al. in PNAS establish that ROS generated within chloroplasts stimulate stromule formation (Fig. 1). These results extend the findings of Caplan et al. (12), who observed that stromule formation is induced in N. benthamiana following ROS generation in chloroplasts during the defense response. Thus, both pathogen ef- fectors and photosynthetic function can lead to production of ROS and the ensuing increase in stromules. By microscopic examination every 4 h for 44 h, Brunkard et al. (11) observed that stro- mule frequency was higher in chloroplasts in the cotyledon epidermis of N. benthamiana during illumination during the day vs. a night- time dark period. Suspecting that increases in Fig. 1. ROS signaling and stromule formation. (A) Light induces stromule formation, presumably because of ROS Author contributions: M.R.H. wrote the paper. generated during photosynthesis. (B) Inhibition of the photosynthetic electron transport chain by DCMU [3-(3,4- The author declares no conflict of interest. dichlorophenyl)-1,1-dimethylurea] or DBMIB (2,5-dibromo-6-isopropyl-3-methyl-1,4-benzoquinone) increases ROS production and promotes stromule formation. (C) When ROS increases because of silencing of thioredoxin reductase, See companion article on page 10044. stromules are induced. 1Email: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1512645112 PNAS | August 11, 2015 | vol. 112 | no. 32 | 9799–9800 Downloaded by guest on September 25, 2021 leucoplasts might be a result of the provision recoil or flip when the attachment is bro- locations rather than communication among of sucrose from mesophyll cells, the au- ken (6, 15, 16). Therefore, although the au- plastids. The current work (11), along with thors examined the effect of sucrose treat- thors have shown that chloroplasts are able that of Caplan et al. (12), implicates ROS as ment on stromule formation in A. thaliana. to form stromules in the absence of the molecules that may emanate from stromules As previously observed by Schattat and intact cell, it remains possible that within to other components of the cell. Brunkard Klösgen (13), Brunkard et al. (11) docu- the living cell, close interactions or attach- et al. (11) provide the first published images mented a large increase in stromules on ment to external structures affects the loca- of stromules acquired by superresolution leucoplasts in sucrose-treated epidermal tion on the plastid body they form and play microscopy; such methods should facili- cells. However, whereas the previous study a complementary role in their formation tate further probing of the interactions of detected an increase in stromule frequency and maintenance. stromules and other parts of the cell. in Arabidopsis mesophyll cells upon sucrose TheworkbyBrunkardetal.(11)provides There is no reason to believe that stromules treatment (13), Brunkard et al. (11) found further clues to the possible functions of stro- have a single function, nor that their function no effect of sucrose on either guard cell or mules. The observation that ROS generated mesophyll stromule frequency. internally induces stromules raises the possi- is identical in different cell types, on different An important observation made by Brunk- bility that one purpose is to increase contact types of plastid, or under different environ- ard et al. (11) is the formation of stromules with nuclei and thereby signal their oxidative mental conditions. As well as involvement in on cell-free chloroplasts, even after purifica- stress. Stromules have previously been docu- ROS signaling from chloroplasts and sucrose tion on a density gradient. Although many mented to border nuclei or other organelles signaling on nonphotosynthetic plastids, both investigators have routinely examined the (4, 12, 18), leading to the hypothesis that they implicated in the present study (11), prior quality of their chloroplast preparations by may facilitate exchange of signaling mole- work has suggested that stromules might phase or differential interference contrast mi- cules or metabolites. During the innate im- break off—releasing small vesicles that enter croscopy, the presence of stromules would mune response, Caplan et al. (12) observed the vacuole—to allow autophagic recycling of typicallyhavegoneunnoticedwithoutspe- stromules in close proximity to nuclei and a portion of the protein content of a chloro- cific labeling. To determine whether isolated that H2O2 increased within nuclei at the plast during times of nutrient limitation (20). chloroplasts could form stromules, Brunkard point of contact with the stromules. Proteins Brunkard et al.’s (11) finding of increased stro- et al. used transgenic plants expressing chlo- are known to flow through stromules, so mule formation following inhibition of the roplast-targeted GFP or stained wild-type small molecules undoubtedly are distributed photosynthetic electron transport chain sug- chloroplasts with carboxyfluorescein diace- through them as well (2, 19). Whereas two gests another possible new function for the tate. Being able to observe stromule forma- plastid bodies have occasionally been ob- “tip-shedding” of stromules that has some- tion on isolated chloroplasts opens a way to served to be joined together through stro- times been observed (6): perhaps toxic ROS examine what factors affect stromule forma- mules and to exchange molecules (2, 19), tion in vitro. Furthermore, this discovery in- GFP photobleaching experiments performed are released from the chloroplast to disperse dicates that cytoskeletal elements outside the soon after their rediscovery (4) demonstrated them or to detoxify them elsewhere in the cell. chloroplast are not required for formation of that there is no network of interconnected ACKNOWLEDGMENTS. Recent work on stromules in stromules. A remaining riddle is the identity plastids in those cells that were examined. M.R.H.’s laboratory was supported by grants from the of the structure within the chloroplast that is Thus, stromules are more likely to function Chemical Sciences, Geosciences, and Biosciences Di- vision, Office of Basic Energy Sciences, Office of Sci- responsible for extending the narrow tubular in reducing diffusion distance of mole- ence, and US Department of Energy Grant DE-FG02- structures, sometimes to considerable length. cules between plastids and other subcellular 09ER16070 (to M.R.H.). A general pressure from within the plastid would not be adequate to form thin stro- mules; a constriction of the envelope mem- 1 Wildman SG, Hongladarom T, Honda SI (1962) Chloroplasts and 11 Brunkard JO, Runkel AM, Zambryski PC (2015) Chloroplasts mitochondria in living plant cells—Cinephotomicrographic studies. Science extend stromules independently and in response to internal redox brane is also necessary for the tubules to 138(3538):434–436. signals. Proc Natl Acad Sci USA 112:10044–10049. remain narrow as
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