Special Online Collection – Database Paper
The Plant Organelles Database 3 (PODB3) Update 2014:
Integrating Electron Micrographs and New Options for
Plant Organelle Research
Shoji Mano1,2,*, Takanori Nakamura3, Maki Kondo1, Tomoki Miwa3, Shuh-ichi Nishikawa4,
Tetsuro Mimura5, Akira Nagatani6 and Mikio Nishimura1,2,*
1
Department of Cell Biology, National Institute for Basic Biology, Okazaki, 444-8585 Japan
Department of Basic Biology, School of Life Science, The Graduate University for Advanced Studies, Okazaki, 444-8585 Japan
3
Data Integration and Analysis Facility, National Institute for Basic Biology, Okazaki, 444-8585 Japan
4
Department of Biology, Graduate School of Science, Niigata University, Niigata, 950-2181 Japan
5
Department of Biology, Graduate School of Science, Kobe University, Kobe, 657-8501 Japan
6
Department of Botany, Graduate School of Science, Kyoto University, Kyoto, 606-8502 Japan
*Corresponding authors: Shoji Mano, E-mail, [email protected]; Fax, +81-564-53-7400; Mikio Nishimura, E-mail, [email protected];
Fax, +81-564-53-7400
(Received August 26, 2013; Accepted September 18, 2013)
2
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.
Keywords: Database Electron micrograph Organelle
dynamics Perception PODB.
Abbreviations: FTS, File Transmission System; PODB,
Plant Organelles Database; TEM, transmission electron
microscope.
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 Cell Physiol. 55(1): e1(1–9) (2014) doi:10.1093/pcp/pct140, available online at www.pcp.oxfordjournals.org
! The Author 2013. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists.
All rights reserved. For permissions, please email: [email protected]
Plant Cell Physiol. 55(1): e1(1–9) (2014) doi:10.1093/pcp/pct140 ! The Author 2013.
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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.
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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.
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.
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
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The perceptive organelles database
Fig. 1 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).
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.
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.
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
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Fig. 2 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.
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Fig. 3 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.
‘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).
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Fig. 4 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
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system has been described previously (Mano et al. 2008,
Mano et al. 2011).
For submission of electron micrographs, contributors should
send data directly to [email protected]. 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 [email protected].
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 [email protected] in these cases.
Discussion
The electron micrograph database
Although several databases other than PODB3 contain plant
organelle image data, most gather only fluorescence-based
Plant Cell Physiol. 55(1): e1(1–9) (2014) doi:10.1093/pcp/pct140 ! The Author 2013.
Plant Organelles Database 3
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
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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
[email protected].
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.
8
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.
Disclosures
The authors have no conflicts of interest to declare.
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