TY - JOUR
AU1 - Mano, Shoji
AU2 - Nakamura, Takanori
AU3 - Kondo, Maki
AU4 - Miwa, Tomoki
AU5 - Nishikawa, Shuh-ichi
AU6 - Mimura, Tetsuro
AU7 - Nagatani, Akira
AU8 - Nishimura, Mikio
AB - Abstract The Plant Organelles Database 2 (PODB2), which was first launched in 2006 as PODB, provides static image and movie data of plant organelles, protocols for plant organelle research and external links to relevant websites. PODB2 has facilitated plant organellar research and the understanding of plant organelle dynamics. To provide comprehensive information on plant organelles in more detail, PODB2 was updated to PODB3 (http://podb.nibb.ac.jp/Organellome/). PODB3 contains two additional components: the electron micrograph database and the perceptive organelles database. Through the electron micrograph database, users can examine the subcellular and/or suborganellar structures in various organs of wild-type and mutant plants. The perceptive organelles database provides information on organelle dynamics in response to external stimuli. In addition to the extra components, the user interface for access has been enhanced in PODB3. The data in PODB3 are directly submitted by plant researchers and can be freely downloaded for use in further analysis. PODB3 contains all the information included in PODB2, and the volume of data and protocols deposited in PODB3 continue to grow steadily. We welcome contributions of data from all plant researchers to enhance the utility and comprehensiveness of PODB3. Introduction In plant biology, a wide variety of databases have been constructed to address specific research aims and to provide global overviews of plant systems. Image-based databases for plant organelles, which compile image and movie data of visualized organelles, have been constructed and used to understand organelle dynamics in plant cells (Cutler et al. 2000, Damme et al. 2004, Brown et al. 2005, Koroleva et al. 2005, Li et al. 2006, Mathur 2007, Mano et al. 2008, Mano et al. 2011, Higaki et al. 2012, Higaki et al. 2013). The Plant Organelles Database (PODB) was launched in 2006 to facilitate our understanding of organelle dynamics, including organelle functions, biogenesis, differentiation, movements and interactions with other cellular components (Mano et al. 2008). Initially, the PODB contained three components: the organellome database, a compilation of static image data; the functional analysis database, a collection of protocols for plant organelle research; and external links to other relevant websites. The creation of PODB presented considerable challenges in comparison with database establishment for text-based information because of the heterogeneity and complexity of the primary data. Since its inception, the volume of data in PODB has increased as a result of generous contributions from many plant researchers, and PODB has been accessed from locations worldwide. In 2009, PODB was updated to a newer version, PODB2, which additionally housed movie data such as time-lapse images and 3D structure rotations (Mano et al. 2011). Using PODB2, users were readily able to examine the temporal and/or spatial organelle dynamics in plant cells. Thus, PODB2 has proved to be a useful tool to aid research on plant organelle dynamics. Plants positively utilize signals that are produced by environmental changes in order to adapt appropriately to the environment. Various external environmental signals, such as light and insect damage, induce changes in the number, size, morphology, movement, subcellular position and cellular interactions of all organelles. Thus, the adaptability of plants is supported by organelle flexibility and organelle sensitivity to environmental signals (Hayashi and Nishimura 2009). For example, chloroplasts exhibit intracellular photorelocation in response to changes in intensity and quality of light (Kadota et al. 2000). Another example is the wounding-induced formation of endoplasmic reticulum-derived structures (ER bodies) (Matsushima et al. 2002). Therefore, it is clearly essential to understand organelle responses to external stimuli in order to comprehend plant dynamics and adaptability. The dynamic nature of organelles is supported by changes at the suborganellar level. In addition, some defects in organelle dynamics are the consequence of mutations that induce alterations in the subcellular and suborganellar structures. Therefore, the ability to visualize cellular and organellar ultrastructures is critical for the understanding of organelle dynamics. Consequently, electron microscopy is a key tool allowing examination of subcellular and suborganellar structures at high resolution. Recent technological advances in electron microscopy and management of large-scale data have facilitated the construction of high-quality electron micrograph databases (Myouga et al. 2013, Orloff et al. 2013). To aid understanding of the response of organelles to external stimuli at the subcellular and suborganellar levels, we reasoned that it would be useful to incorporate information and electron micrographs relating to organelle dynamics into our database. Therefore, we updated PODB2 to a newer version, PODB3. In addition to the four units from PODB2 (organelle movie database, organellome database, functional analysis database and external links), PODB3 houses two new collections: the electron micrograph database and the perceptive organelle database. With the electron micrograph database, users can easily view the ultrastructures of plant cells and organelles and use the images to study the dynamic changes in plant organelles in response to stimuli or as a consequence of mutation. Some data in the organellome database and the organelle movie database in PODB2 were obtained under conditions that show organelle dynamics in response to external stimuli. We compiled these movies and static images to construct the perceptive organelles database, which provides organelle dynamics information, such as subcellular location and morphology, in response to external stimuli. Here, we describe the novel features of PODB3 and discuss its improvements with respect to PODB2. PODB3 can be freely accessed online at http://podb.nibb.ac.jp/Organellome. We expect that PODB3 will provide an extended repository of useful data for plant organelle research. Contents of the PODB3 PODB3 is publicly accessible at http://podb.nibb.ac.jp/Organellome/. In addition to containing all the information included in PODB2, such as collections of static images, movies, protocols and external links, PODB3 houses the electron micrograph database and the perceptive organelles database. Therefore, PODB3 consists of six individual units; namely, the electron micrograph database, the perceptive organelles database, the organelles movie database, the organellome database, the functional analysis database and a compilation of external links to pertinent databases and homepages (Fig. 1). The organelles movie database, the organellome database, the functional analysis database and external links have already been described (Mano et al. 2008, Mano et al. 2011), and details will not be reiterated here. PODB3 users can access each database page by clicking on the relevant links on the homepage (red arrows in Fig. 1) and at the top of each page in the database (blue arrow in Fig. 1). Below, we introduce new material in PODB3 and highlight improvements over the previous version. Fig. 1 View largeDownload slide The graphical user interface for the homepage of PODB3. Six individual parts, the electron micrograph database, the perceptive organelles database, the organelles movie database, the organellome database, the functional analysis database and a compilation of external links are included in PODB3. Users can access the five databases and external links by clicking on each term located on the updated homepage (red arrows) and at the top of each page in the database (blue arrow). Fig. 1 View largeDownload slide The graphical user interface for the homepage of PODB3. Six individual parts, the electron micrograph database, the perceptive organelles database, the organelles movie database, the organellome database, the functional analysis database and a compilation of external links are included in PODB3. Users can access the five databases and external links by clicking on each term located on the updated homepage (red arrows) and at the top of each page in the database (blue arrow). The electron micrograph database Like the organelles movie database and the organellome database, the electron micrograph database is fully searchable. All electron micrographs are deposited in high-resolution TIFF format. Users may access specific data via the ‘Search’ page (Fig. 2A) using four query parameters: species, organ, organelle name and keyword. More complex searches can be performed by combining these different search parameters. Currently, the electron micrograph database encompasses the following 15 subcellular structures: apoplast, cell plate, cell wall, endoplasmic reticulum and related structures, endosome, Golgi apparatus, microfilament, microtubule, mitochondrion, nucleus, peroxisome, plasma membrane, plastid and related structures, vacuole and ‘other’. The ‘other’ describes labeling of unidentified structures. Fig. 2 View largeDownload slide The graphical user interface of the electron micrograph database. (A) A search window provides four parameters for queries. Users can select organelle names and/or enter text in the text boxes for other parameters. Leaving the input boxes empty retrieves all entries. (B) A results table consists of thumbnail images as well as annotations. Clicking on the thumbnail allows access to the detailed information page (C). (C) Detailed information on Arabidopsis root cells is shown as a representative data page. The original high-resolution image files can be downloaded by clicking the ‘Original size (.tif)’ message below each image. (D) If the submitter also provided a navigation file, users can see labels of organelles and a brief caption highlighted on an electron micrograph by hovering a cursor over an image. Fig. 2 View largeDownload slide The graphical user interface of the electron micrograph database. (A) A search window provides four parameters for queries. Users can select organelle names and/or enter text in the text boxes for other parameters. Leaving the input boxes empty retrieves all entries. (B) A results table consists of thumbnail images as well as annotations. Clicking on the thumbnail allows access to the detailed information page (C). (C) Detailed information on Arabidopsis root cells is shown as a representative data page. The original high-resolution image files can be downloaded by clicking the ‘Original size (.tif)’ message below each image. (D) If the submitter also provided a navigation file, users can see labels of organelles and a brief caption highlighted on an electron micrograph by hovering a cursor over an image. Entries matching the query are displayed as a table containing an image thumbnail as well as species, organ and the name of the organelle(s) (Fig. 2B). Clicking on an image will open a page with data that relate to the electron micrograph (Fig. 2C), such as the type of plant material, experimental conditions, sample preparation, sample description, the name of the person to contact and the publication (if published). Electron micrographs in each data page can be downloaded as the original high-resolution image files by clicking the ‘Original size (.tif)’ message below each image (Fig. 2C). We incorporated a navigation system into the electron micrograph database to enable users unfamiliar with electron microscopic analysis to recognize the morphology of organelles and identify any changes due to mutation. A navigation file contains labels of each organelle and/or a brief description. If a navigation file is provided with an image, the image will display labels of organelles and a brief description when the cursor is hovered over the relevant region of the image (Fig. 2D). Currently, the electron micrograph database contains data from transmission electron microscopy (TEM), but not scanning electron microscopy. Two types of TEM data are housed: images of wild-type plants with different organs and/or different conditions, and images of mutant plants. Users can query the electron micrograph database to examine the subcellular and/or suborganellar structures in wild-type and mutant cells at various developmental stages in different conditions. The perceptive organelles database Like the electron micrograph database, the perceptive organelles database is searchable according to several criteria. Currently, two types of data are deposited in this database: static images and movies. As in the organelles movie database, all movies are deposited in QuickTime format; therefore, QuickTime Player (Apple Inc.) must be installed on a computer to view the movies. Users can access specific data via the ‘Search’ page (Fig. 3A), using five query parameters: species, stimulus, organelle name, gene accession number and keyword. More complex searches can be performed by combining these different search parameters. Fig. 3 View largeDownload slide The graphical user interface of the perceptive organelles database. (A) A search window provides five parameters for queries. Users can select a stimulus and organelle names from the pull-down menu, and/or enter text in the text boxes for other parameters. (B) A results window consists of a table of thumbnail images of visualized organelles as well as annotations. Clicking on the title in red allows access to the detailed information page (C and D). The perceptive organelles database includes two types of image data: static images (C) and movie data (D). (C) Detailed information on chloroplast movement in response to weak light is shown as a representative static image data page. (D) Detailed information on vacuolar membrane dynamics under high-salt conditions (Hamaji et al. 2009) is shown as a representative movie data page. Clicking on the thumbnail makes a static image to display or a movie to run in the window (E). (E) Clicking the forward and reverse arrow buttons, which are marked by yellow circles, allows users to view the following or previous image or movies without returning on the results page. Fig. 3 View largeDownload slide The graphical user interface of the perceptive organelles database. (A) A search window provides five parameters for queries. Users can select a stimulus and organelle names from the pull-down menu, and/or enter text in the text boxes for other parameters. (B) A results window consists of a table of thumbnail images of visualized organelles as well as annotations. Clicking on the title in red allows access to the detailed information page (C and D). The perceptive organelles database includes two types of image data: static images (C) and movie data (D). (C) Detailed information on chloroplast movement in response to weak light is shown as a representative static image data page. (D) Detailed information on vacuolar membrane dynamics under high-salt conditions (Hamaji et al. 2009) is shown as a representative movie data page. Clicking on the thumbnail makes a static image to display or a movie to run in the window (E). (E) Clicking the forward and reverse arrow buttons, which are marked by yellow circles, allows users to view the following or previous image or movies without returning on the results page. Entries matching the query are displayed as a table containing an image thumbnail and the title, as well as species, stimulus and the name of the organelle(s) (Fig. 3B). Clicking on a title will open a page with data that relate to the static image (Fig. 3C) or the movie (Fig. 3D), such as the plant material, experimental conditions, imaging parameters used and the name of the contact. Users can download the static image as a high-resolution file by clicking the button for the download under the image, or view the movie included on each data page by clicking on a thumbnail at the top of the page. Users can instantly view an image or a movie on the result page by clicking on the thumbnail (Fig. 3E). The forward and reverse arrows (encircled in yellow in Fig. 3E) allow the following and previous movies, respectively, to be displayed without returning to the results page. Currently, 11 stimuli are categorized in the perceptive organelles database: light, water, heat, cold, dehydration, gravity, nutrition, insect damage, senescence, salinity and mechanical stress. If requested by users, we will adjust these categories and add new ones. At present, 28 records are deposited in this database. Half of them are movies, and the remainder are static images, which show organelle dynamics in leaf, root, stem and cultured cells. As examples, via this database, users can observe vacuolar membrane dynamics in Arabidopsis cells cultured in high-salt conditions, (http://podb.nibb.ac.jp/Organellome/bin/browseMovie.php?ID=Movie-omiwa_port.kobe-u.ac.jp-20100107161943; Hamaji et al. 2009), and clearly understand the dynamics of autophagosomes in response to changes in nutritional conditions in Arabidopsis root cells (http://podb.nibb.ac.jp/Organellome/bin/browseImage.php?ID=Image-k-yoshi_psc.riken.jp-20090310173318; Yoshimoto et al. 2004). Users can similarly query the perceptive organelles database to examine the dynamics of organelles, such as movement and behavior, in response to external stimuli at various developmental stages in different plant species. Redesign of pages in PODB3 PODB2 was substantially updated and improved in the development of PODB3. We improved almost all of the pages by redesigning the layout, debugging programs and adding links to relevant databases. As stated above, the addition of new ‘Electron Micrograph Database’ and ‘Perceptive Organelles Database’ links at the top of every page included in PODB3 allows users to access the ‘Search page’ of the electron micrograph database and the perceptive organelles database directly (blue arrow in Fig. 4). In addition, links to two Arabidopsis gene expression profile databases were added in the ‘Gene accession number’ field on each data page of the organellome database (red arrow in Fig. 4). Selection of ‘AVT’ will lead users to the AtGenExpress Visualization Tool (http://jsp.weigelworld.org/expviz/expviz.jsp), and ‘ATTED-II’ will guide users to ATTED-II (http://atted.jp; Obayashi et al. 2009, Obayashi et al. 2011). Fig. 4 View largeDownload slide The updated graphical user interface of the organellome database. A detailed information page on At3g10572 (Goto et al. 2011) is shown as a representative data page. Clicking on the word ‘NCBI’, ‘AVT’ or ‘ATTED-II’ opens a result window that shows the result using the accession number from each website. Fig. 4 View largeDownload slide The updated graphical user interface of the organellome database. A detailed information page on At3g10572 (Goto et al. 2011) is shown as a representative data page. Clicking on the word ‘NCBI’, ‘AVT’ or ‘ATTED-II’ opens a result window that shows the result using the accession number from each website. Data submission Critically, PODB3 consists of experimentally determined data submitted by plant researchers. All additional submissions are welcomed in order to expand and develop the database. For submission to the perceptive organelles database, contributors should submit static image files (except for electron micrographs) and/or movie files via the web-based data submission system. As in PODB2, only registered users are able to log in to the submission site. The username and password needed are common to the organellome database and the organelles movie database. Data in the perceptive organelles database are compatible with those in the organellome database and the organelles movie database, and submitters are able to submit the data to the perceptive organelles database using the same submission system as for PODB2. Information on how to obtain a username and password and use the submission system has been described previously (Mano et al. 2008, Mano et al. 2011). For submission of electron micrographs, contributors should send data directly to podb@nibb.ac.jp. We would like contributors to submit high-resolution TIFF-format images, basic information for each electron micrograph, a navigation file and contributor contact information. Example submissions are provided on the submission page. Basic information in this context includes information about the biological source (plant material, organ, developmental stage, experimental condition, organelles, wild-type or mutant plants) and how electron microscopy was performed and analyzed (fixation, use of osmium and type of resin) and should be submitted using the Excel template downloadable from the PODB3 homepage. The navigation file will be used to provide organelle information on the micrograph when a cursor hovers over relevant regions of the image. The navigation file must therefore relate to the submitted electron micrograph, and should be provided as an independent JPEG image file containing organelle labels and brief descriptions. If difficulties are encountered when sending large files, we will arrange access rights to the File Transmission System (FTS) in the National Institute for Basic Biology. Queries about data submission can be sent to podb@nibb.ac.jp. Data quality and accuracy are primarily determined by the contributor. However, to maintain the integrity of the database, submitted data are evaluated for sufficient quality prior to addition to the database, including whether peer-reviewed papers have been published that contain the submitted data, and/or whether appropriate measurements, such as immunocytochemical analysis using organellar proteins whose localization has been characterized, are included in the submitted data. We ask the submitter to make revisions and resubmit when the submitted data are considered not to be of sufficient quality. In addition to submissions to the perceptive organelles database and the electron micrograph database, PODB3 continuously welcomes the submission of static image data to the organellome database, movie data to the organelles movie database, and protocols to the functional analysis database. Since its inception in 2006, the volume of static image data, movie data and protocols submitted to these databases has increased substantially. However, the addition of additional data will assist plant organelle research and enhance the value of our database. Therefore, we would appreciate continued contribution of data and protocols from all plant researchers. As in the previous version, corrections, revisions or updates of submitted data can be made at any time; however, users will not be able to correct, revise or update the data by themselves and should contact podb@nibb.ac.jp in these cases. Discussion The electron micrograph database Although several databases other than PODB3 contain plant organelle image data, most gather only fluorescence-based images and not electron micrographs (Cutler et al. 2000, Damme et al. 2004, Brown et al. 2005, Koroleva et al. 2005, Li et al. 2006, Mathur 2007, Mano et al. 2008, Mano et al. 2011, Higaki et al. 2012, Higaki et al. 2013). Fluorescence image-based databases have played a crucial role in organizing and structuring information in modern informatics tools, but cannot be used for the suborganellar analyses level due to resolution limitations. Although electron microscopic analysis is technically challenging, it is a powerful tool for subcellular and suborganellar studies; accordingly, databases containing electron micrograph images began to be established in the early 1990s (Hewan-Lowe 1992). However, because electron micrograph file sizes are much larger than fluorescence images, electron microscopy databases are more challenging to host and manage, and so the number of electron micrograph databases is small in comparison with the number of fluorescence-based databases. Nevertheless, advances in information technology such as the increase in mass storage and the improving rapidity of database access have accelerated the construction of databases holding large files. For example, the Cell Centered Database (CCDB) houses several types of image data including electron micrographs from various kinds of organisms including plants (Martone et al. 2002, Martone et al. 2007, Orloff et al. 2013). A specifically organellar example is the Chloroplast Function Database II, which is dedicated to chloroplast morphology and its function, and this also collects electron micrographs (Myouga et al. 2013). The electron micrograph database in PODB3 was designed for the collection of subcellular and/or suborganellar information from tissue and cultured cells, regardless of plant species and the type of tissue being studied. PODB3 has a number of unique features that are not found in CCDB or the Chloroplast Function Database II: (i) PODB3 contains electron micrographs of various plant cells at different developmental stages, such as epidermis, parenchyma, pollen, and seed; (ii) PODB3 has data pertaining to various organelles; (iii) PODB3 contains mutant data as well as data from wild-type plants; and (iv) PODB3 incorporates a navigation system, which assists users who are not familiar with electron microscopic analysis to interpret the data. At present, the electron micrograph database contains 69 images, and the majority of data are derived from Arabidopsis thaliana and a few additional species, such as Ocimum basilicum, Nicotiana tabacum, Hordeum vulgare, Ricinus communis and Cucubita species. We think it important to increase the number of electron micrographs from other plant species in the database. The perceptive organelles database Organelle responses to external signals are indicative of the key roles that organelles play in the adaptation of plants to environmental changes. The joint research project ‘Environmental sensing of plants: signal perception, processing and cellular responses’, which was initially implemented with a Grant-in-Aid for Scientific Research on Innovative Areas, aims to clarify the molecular mechanisms underlying the perception of environmental signals, cellular response and adaption of individual plants (http://esplant.net/index.html). Some images and movies contain information on organelle dynamics in response to external stimuli such as high-light irradiation or chemical treatment. We therefore considered that the perceptive organelles database would contribute to understanding the mechanisms of environmental sensing of plants as one part of the above joint research project. To the best of our knowledge, although many databases host gene expression profiles under various conditions, no other image databases are currently specialized for studying organelle dynamics in response to external stimuli. Therefore, the perceptive organelles database is a valuable platform for studying the relationships between organelle dynamics and external stimuli. The movies and static images in this database were taken using A. thaliana, Physcomitrella patens and Spinacia sp. We would appreciate contributions of data from other plant species. Interaction with other databases and websites PODB3 data are linked to the AtGenExpress Visualization Tool (AVT) and ATTED-II (Obayashi et al. 2009, Obayashi et al. 2011) databases; this was developed to facilitate the examination of gene expression profiles and co-regulation data pertaining to the PODB3 data of interest (Fig. 4). Creating these linkages for biological data presents a major challenge to the informatics community, achieving the integration of biological information across scales and disciplines (Mano et al. 2009, Mochida and Shinozaki 2010, Mochida and Shinozaki 2011). Therefore, we aim to continue working with other biological databases and colleagues in plant research and bioinformatics fields for the interoperation of our data. We are beginning to collaborate with the Data Citation Index project in Thomson Reuters (http://wokinfo.com//products_tools/multidisciplinary/dci/about/), which aims to create a platform to support discovery, access, citation and attribution of digital resources. By developing partnerships with other databases and websites, PODB3 and later versions of our database will be a valuable platform for imaging analysis in the field of plant biology. This will, in time, enhance our understanding of organelle dynamics in plants. Future perspectives Databases such as PODB3 can make maximal use of rich data by making the data sets available for additional analyses. PODB3 also harbors potentially rich data sources for computational analyses. As stated above, the data in PODB3 are freely downloadable, so users can download the data and use them for quantitative analysis. However, at present, PODB3 does not provide the means to download automatically a large data set containing static images, movies and electron micrographs along with the relevant information. This will be implemented in the future. To facilitate the extraction of biological information from image data, we are currently collaborating with mathematical morphologists in establishing organelle-specific algorithm(s) for statistical analysis (Kimori et al. 2007, Kimori et al. 2010, Kimori 2011, Kimori et al. 2011, Mano et al. 2013). The information extracted from image data by this method, together with other information such as expression data, will be useful for the construction of simulation models of plants in systems biology. As part of our maintenance of PODB3, we continuously update records of electron micrographs, movie data, static images, protocols and links to other websites. To facilitate the ongoing expansion of information, the organization and layout of PODB3 have been modified to be of wider use. We will therefore continue to modify the layout of pages and to develop the compatibility with new operating systems and web browsers. A website, Plant Organelles World (http://podb.nibb.ac.jp/Organellome/PODBworld/en/index.html), which is based on PODB2, was launched in 2010. Plant Organelles World uses non-technical language and was developed as a resource for members of the non-scientific community such as students and schoolteachers. After updating to PODB3, we intend to continue our efforts to reflect the data in PODB3 in Plant Organelles World. We believe that PODB3 and Plant Organelles World are easily accessible platforms for those who wish to explore the basics of plant organelles research. We welcome comments and suggestions from users to assist our continued improvement and development of PODB3. Design and implementation PODB3 operates on a CentOS system under an Apache web server and uses MySQL as the database management system. The MySQL database system is used to store the collected data with information of each datum file. The web interface was designed in the PHP server-side scripting language (version 5.3.3) and in Web-based JavaScript. Availability PODB3 can be accessed at the website http://podb.nibb.ac.jp/Organellome at the National Institute for Basic Biology. All data in PODB3 are free for educational and academic use. We request that the submitter of data/protocols and PODB3 be given proper credit in scientific publications that use these data/tools. Please direct all technical questions and concerns, such as comments, suggestions, revisions and updates of data, to podb@nibb.ac.jp. Like the previous version PODB2, PODB3 provides biological information only and does not collect, generate or distribute genetic resources, such as the DNA, seeds, mutants and transgenic plants that were used to produce the data. To request these resources, users should contact the submitter directly. Funding This work was supported by the Ministry of Education, Culture, Sports, Science and Technology (MEXT) of Japan KAKENHI [Grants-in-Aid for Scientific Research in Priority Areas (‘Organelle differentiation as the Strategy for environmental adaptation in plants’; No. 16085101) and Grant-in-Aid for Scientific Research on Innovative Areas (‘Environmental sensing of plants: signal perception, processing and cellular responses’; No. 22120001)]; Japan Society for the Promotion of Science (JSPS) KAKENHI [Grant-in-Aid for the Publication of Scientific Research Results (Nos. 218060 and 228052)]. Acknowledgments We would like to thank Ms. Chizuru Ueda at the Division of Cell Mechanisms, Department of Cell Biology, and Dr. Tomoko Kurata and Mr. Colin Kawaguchi at the Office of Public Relations and International Cooperation of the National Institute for Basic Biology for their assistance in proofing the English language and maintaining the website. 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TI - The Plant Organelles Database 3 (PODB3) Update 2014: Integrating Electron Micrographs and New Options for Plant Organelle Research
JF - Plant and Cell Physiology
DO - 10.1093/pcp/pct140
DA - 2013-11-07
UR - https://www.deepdyve.com/lp/oxford-university-press/the-plant-organelles-database-3-podb3-update-2014-integrating-electron-hu37fMPspT
SP - e1
EP - e1
VL - 55
IS - 1
DP - DeepDyve
ER -