Peer Review History

Original SubmissionApril 22, 2024
Decision Letter - Awatif Abid Al-Judaibi, Editor

PONE-D-24-16245Genetic drift, historic migration, and limited gene flow contributing to the subpopulation divergence in wild sea beet (Beta vulgaris ssp. maritima)PLOS ONE

Dear Dr. chu,

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Kind regards,

Awatif Abid Al-Judaibi, PhD

Academic Editor

PLOS ONE

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"USDA-ARS CRIS project No. 3060-21000-045-000D, the Beet Sugar Development Foundation (BSDF), and the Sugarbeet Research and Education Board of Minnesota and North Dakota (SBREB)."

  

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

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Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: I Don't Know

**********

3. Have the authors made all data underlying the findings in their manuscript fully available?

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Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

**********

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Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

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5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: First, I extend my gratitude to the authors for their outstanding work and well-constructed text. In this study, authors investigated 599 sea beet (Beta maritima) accessions collected from the north Atlantic Ocean and Mediterranean Sea coasts. It is a comprehensive study about the distribution and origin of sea beet and cultivated beet. The title explains the research properly, and the results are described well in details. I think the manuscript contains a good research question and explains the migration route of wild beet along the north Atlantic Ocean and Mediterranean Sea coasts. In the future, the findings will be useful to identify novel genomic regions related to resistance against abiotic/biotic stress factors in Beta vulgaris. However, I have some comments as follows. I recommend minor revisions.

Here are my comments:

-In Materials and Methods, authors did not describe the growth conditions of beet accessions. Authors should mention how many accessions they used from each of the following: Africa, Asia, northern Europe, southern Europe, western Europe, eastern Europe, and North America.

-In Figures 4 and S3, why did not authors show the location of Cluster 6? That map does not show the locations correctly unless I have missed something. For example, I do not see Greece and Italy in Cluster 2 (please see discussion, line 306). Why do you think the Cluster 2 is the center of origin for sea beet and cultivated beet? You may highlight the experimental results for clearer explanation. In addition, each cluster (1-8) must be briefly described in the legend of figure S3.

Reviewer #2: Correct name: Beta vulgaris subsp. maritima (L.) Arcang.

Adding to the title and in the first citation of the text the authorship of the species -> Verify: www.tropicos.org

I suggest adding the botanical family name to the title or in the keywords.

I suggest adding the scientific name of the causal agents of the diseases mentioned in paragraph 3 of the Introduction.

I congratulate the authors on this present work, of fundamental importance for the establishment or better management of genetic improvement programs, as well as for the conservation of wild species.

Reviewer #3: The origin of cultivated plants and the identification of the most closely related native populations, as well as their crop wild relatives, is a highly topical subject, given its potential for the genetic improvement of crops. Following on from other work that has been carried out on sugar beet, the submitted manuscript analyses more than six hundred samples of Beta maritima from various regions of the world. The results presented are interesting and improve the knowledge of the phylogenetic relationships of the populations, particularly those occurring in the Mediterranean region.

In general, the manuscript is well-written, well-structured, and easy to understand.

Apart from a few minor suggestions/comments (listed below), there is one aspect that I would like to highlight because I think it should be corrected: some of the samples used are from areas where Beta maritima is not native, but naturalised (this is the case with the samples from North America). I think this should be mentioned/analysed throughout the text (material and methods, results and discussion, tables, etc.). This aspect can even add value to the discussion, as hypotheses can be put forward for the origin of the populations in the regions where Beta maritima is naturalised.

Other comments:

Ln. 54 – ‘Sea beet (Beta vulgaris L. ssp. maritima Arcang., referred to as B. maritima hereafter)’ – Currently, some of the world's most important taxonomic databases (e.g. Plants of the World Online - POWO; and World Flora Online - WFO) only accept Beta vulgaris subsp. vulgaris and consider Beta vulgaris subsp. maritima as a synonym. This does not invalidate the work developed, but it can be mentioned in the text that the work carried out used the classification adopted by the US National Plant Germplasm System (NPGS).

ln. 59 – ‘Wild B. maritima populations extend along the Mediterranean basin and the Atlantic coast.’ – This description should be more detailed (see POWO) and the regions where the species is introduced should be indicated.

Ln. 76 – ‘Tehseen et al’ - Tehseen et al. The full stop is missing.

Ln. 108 to 111 – Detail the distribution (native or non-native) in the mentioned regions. In Table 1, mark (e.g. with a *) the accessions collected in regions where the taxa is not native (e.g. North America). Check the values in this table: the total is 601 and not 599 as it should be.

Check the legend of Fig. 1 (ln 524) - references to A and B are missing.

In Results section, I think Fig. 3 (Ln. 208) could be made supplementary and Fig. S3 (ln. 231) be included in the main text. The latter is quite enlightening. However, its graphic presentation could be improved.

ln. 273 – ‘… is influenced by a combination of landscape characteristics.’ - I suggest replacing 'landscape' (which has aesthetic connotations) with environment.

Ln. 300 – In the discussion, this manuscript could also consider the results of the paper Veloso et al. 2021 (Genetic Diversity and Population Structure of Wild Beets (Beta spp.) from the Western Iberian Peninsula and the Azores and Madeira Islands) which also highlights the importance of ocean currents in species dispersal.

Finally, I suggest complementing the discussion by including some conservation proposals, namely the prioritisation of certain populations / regions taking into account their phylogenetic affinities and genetic diversity.

**********

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Reviewer #1: No

Reviewer #2: No

Reviewer #3: No

**********

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Revision 1

Response to Editor:

When submitting your revision, we need you to address these additional requirements.

1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming. The PLOS ONE style templates can be found at

https://journals.plos.org/plosone/s/file?id=wjVg/PLOSOne_formatting_sample_main_body.pdf and

https://journals.plos.org/plosone/s/file?id=ba62/PLOSOne_formatting_sample_title_authors_affiliations.pdf

Response: format was checked and corrected according to the guidelines.

2. We note that the grant information you provided in the ‘Funding Information’ and ‘Financial Disclosure’ sections do not match. When you resubmit, please ensure that you provide the correct grant numbers for the awards you received for your study in the ‘Funding Information’ section.

Response: grant numbers added.

3. Thank you for stating the following financial disclosure:

"USDA-ARS CRIS project No. 3060-21000-045-000D, the Beet Sugar Development Foundation (BSDF), and the Sugarbeet Research and Education Board of Minnesota and North Dakota (SBREB)."

Please state what role the funders took in the study. If the funders had no role, please state: "The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript."

If this statement is not correct you must amend it as needed.

Please include this amended Role of Funder statement in your cover letter; we will change the online submission form on your behalf.

Response: the statement is added.

4. In the online submission form, you indicated that [All relevant data are within the manuscript and its Supporting Information files. Raw data are available per request.].

All PLOS journals now require all data underlying the findings described in their manuscript to be freely available to other researchers, either 1. In a public repository, 2. Within the manuscript itself, or 3. Uploaded as supplementary information.

This policy applies to all data except where public deposition would breach compliance with the protocol approved by your research ethics board. If your data cannot be made publicly available for ethical or legal reasons (e.g., public availability would compromise patient privacy), please explain your reasons on resubmission and your exemption request will be escalated for approval.

Response: All data are available and attached, and the raw marker data is stored at NPGS-GRIN and is publicly available. This information is added in the manuscript.

5. We note that [Figure 4 and S3] in your submission contain [map/satellite] images which may be copyrighted. All PLOS content is published under the Creative Commons Attribution License (CC BY 4.0), which means that the manuscript, images, and Supporting Information files will be freely available online, and any third party is permitted to access, download, copy, distribute, and use these materials in any way, even commercially, with proper attribution. For these reasons, we cannot publish previously copyrighted maps or satellite images created using proprietary data, such as Google software (Google Maps, Street View, and Earth). For more information, see our copyright guidelines: http://journals.plos.org/plosone/s/licenses-and-copyright.

We require you to either (1) present written permission from the copyright holder to publish these figures specifically under the CC BY 4.0 license, or (2) remove the figures from your submission:

a. You may seek permission from the original copyright holder of Figure 4 and S3 to publish the content specifically under the CC BY 4.0 license.

We recommend that you contact the original copyright holder with the Content Permission Form (http://journals.plos.org/plosone/s/file?id=7c09/content-permission-form.pdf) and the following text:

“I request permission for the open-access journal PLOS ONE to publish XXX under the Creative Commons Attribution License (CCAL) CC BY 4.0 (http://creativecommons.org/licenses/by/4.0/). Please be aware that this license allows unrestricted use and distribution, even commercially, by third parties. Please reply and provide explicit written permission to publish XXX under a CC BY license and complete the attached form.”

Please upload the completed Content Permission Form or other proof of granted permissions as an "Other" file with your submission.

In the figure caption of the copyrighted figure, please include the following text: “Reprinted from [ref] under a CC BY license, with permission from [name of publisher], original copyright [original copyright year].”

b. If you are unable to obtain permission from the original copyright holder to publish these figures under the CC BY 4.0 license or if the copyright holder’s requirements are incompatible with the CC BY 4.0 license, please either i) remove the figure or ii) supply a replacement figure that complies with the CC BY 4.0 license. Please check copyright information on all replacement figures and update the figure caption with source information. If applicable, please specify in the figure caption text when a figure is similar but not identical to the original image and is therefore for illustrative purposes only.

The following resources for replacing copyrighted map figures may be helpful:

USGS National Map Viewer (public domain): http://viewer.nationalmap.gov/viewer/

The Gateway to Astronaut Photography of Earth (public domain): http://eol.jsc.nasa.gov/sseop/clickmap/

Maps at the CIA (public domain): https://www.cia.gov/library/publications/the-world-factbook/index.html and https://www.cia.gov/library/publications/cia-maps-publications/index.html

NASA Earth Observatory (public domain): http://earthobservatory.nasa.gov/

Landsat: http://landsat.visibleearth.nasa.gov/

USGS EROS (Earth Resources Observatory and Science (EROS) Center) (public domain): http://eros.usgs.gov/#

Natural Earth (public domain): http://www.naturalearthdata.com/

Response: the figures were reproduced using NASA world map (https://data.nasa.gov/), and ocean current direction was manually added according to the reference listed.

6. Please include captions for your Supporting Information files at the end of your manuscript, and update any in-text citations to match accordingly. Please see our Supporting Information guidelines for more information: http://journals.plos.org/plosone/s/supporting-information.

Response: added.

7. Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

Response: all references were checked.

Responses to Reviewers' comments:

Reviewer #1:

First, I extend my gratitude to the authors for their outstanding work and well-constructed text. In this study, authors investigated 599 sea beet (Beta maritima) accessions collected from the north Atlantic Ocean and Mediterranean Sea coasts. It is a comprehensive study about the distribution and origin of sea beet and cultivated beet. The title explains the research properly, and the results are described well in details. I think the manuscript contains a good research question and explains the migration route of wild beet along the north Atlantic Ocean and Mediterranean Sea coasts. In the future, the findings will be useful to identify novel genomic regions related to resistance against abiotic/biotic stress factors in Beta vulgaris. However, I have some comments as follows. I recommend minor revisions.

Here are my comments:

- In Materials and Methods, authors did not describe the growth conditions of beet accessions.

Response: information was added.

- Authors should mention how many accessions they used from each of the following: Africa, Asia, northern Europe, southern Europe, western Europe, eastern Europe, and North America.

Response: number of accessions were added for each region. The region ‘eastern Europe’ is deleted since the two lines have not good marker data and were not included in the analysis.

-In Figures 4 and S3, why did not authors show the location of Cluster 6?

Response: it has two reasons: 1) the cluster 6 is corresponding to cultivated beet that selected worldwide, not a specific location is assigned; and 2) B. maritima accessions in the cluster 6 are spread similarly in several other clusters with no dominant amount from a specific region, it is impossible to assign a location for those accessions.

- That map does not show the locations correctly unless I have missed something. For example, I do not see Greece and Italy in Cluster 2 (please see discussion, line 306).

Response: Thank you so much for pointing this out. When making the figure, we only thought to find regions and try to make them distinct, but clusters 2 and 4 are very close and their regions are largely overlapped. We thus enlarged the region of the cluster 2 to let it covers Italy and Greece, and it is more consistent with our results. Great thanks!

- Why do you think the Cluster 2 is the center of origin for sea beet and cultivated beet? You may highlight the experimental results for clearer explanation.

Response: Cluster 2 is the center of origin for sea beet simply because it contains accessions collected from almost all regions, the location of regions for Cluster 2 is determined based on the location that majority of the accessions were collected. Accessions in Cluster 2 but collected from the other regions are indication of they were migrated from the region we defined, indicating regions assigned to major accessions in Cluster 2 at Mediterranean Sea coast likely to be the center of sea beet. However, the sea beet accessions close to Cluster 6 that equivalent to cultivated beet were largely collected in Greece, indicating Greece might be the center of cultivated beet domesticated from sea beet.

- In addition, each cluster (1-8) must be briefly described in the legend of figure S3.

Response: Great thanks for this suggestion, cluster descriptions were added accordingly. We appreciate your comments to improve the manuscript.

Reviewer #2:

- Correct name: Beta vulgaris subsp. maritima (L.) Arcang. Adding to the title and in the first citation of the text the authorship of the species -> Verify: www.tropicos.org I suggest adding the botanical family name to the title or in the keywords.

Response: Great thanks, the scientific name was corrected in the title and in the text.

- I suggest adding the scientific name of the causal agents of the diseases mentioned in paragraph 3 of the Introduction.

Response: the causal agents of the diseases were added.

- I congratulate the authors on this present work, of fundamental importance for the establishment or better management of genetic improvement programs, as well as for the conservation of wild species.

Response: great thanks and appreciate your comments for improving the manuscript.

Reviewer #3:

The origin of cultivated plants and the identification of the most closely related native populations, as well as their crop wild relatives, is a highly topical subject, given its potential for the genetic improvement of crops. Following on from other work that has been carried out on sugar beet, the submitted manuscript analyses more than six hundred samples of Beta maritima from various regions of the world. The results presented are interesting and improve the knowledge of the phylogenetic relationships of the populations, particularly those occurring in the Mediterranean region.

In general, the manuscript is well-written, well-structured, and easy to understand.

Apart from a few minor suggestions/comments (listed below), there is one aspect that I would like to highlight because I think it should be corrected: some of the samples used are from areas where Beta maritima is not native, but naturalised (this is the case with the samples from North America). I think this should be mentioned/analysed throughout the text (material and methods, results and discussion, tables, etc.). This aspect can even add value to the discussion, as hypotheses can be put forward for the origin of the populations in the regions where Beta maritima is naturalised.

Response: We agree the location of some accessions not the location they were collected, as you indicated that accessions from North America may be donated by some institution oversea. Since the number of such accessions are small and they didn’t affect the results much, we didn’t mention about them in the discussion. Actually, we just started a new project using conserved gene sequence to investigate the evolution of B. maritima accessions as well as cultivated beets, which will be better to differentiate B. maritima accessions and then narrow down region of the origin.

Other comments:

Ln. 54 – ‘Sea beet (Beta vulgaris L. ssp. maritima Arcang., referred to as B. maritima hereafter)’ – Currently, some of the world's most important taxonomic databases (e.g. Plants of the World Online - POWO; and World Flora Online - WFO) only accept Beta vulgaris subsp. vulgaris and consider Beta vulgaris subsp. maritima as a synonym. This does not invalidate the work developed, but it can be mentioned in the text that the work carried out used the classification adopted by the US National Plant Germplasm System (NPGS).

Response: Thanks. We made the change accordingly.

ln. 59 – ‘Wild B. maritima populations extend along the Mediterranean basin and the Atlantic coast.’ – This description should be more detailed (see POWO) and the regions where the species is introduced should be indicated.

Response: More details were added according to POWO, but we are not sure if it’s correct for mentioning accessions were introduced. I heard that few B. maritima accessions from California, USA might be natively collected, but no further information to indicate if it’s true.

Ln. 76 – ‘Tehseen et al’ - Tehseen et al. The full stop is missing.

Response: Corrected. Thanks!

Ln. 108 to 111 – Detail the distribution (native or non-native) in the mentioned regions. In Table 1, mark (e.g. with a *) the accessions collected in regions where the taxa is not native (e.g. North America). Check the values in this table: the total is 601 and not 599 as it should be.

Response: Detailed information was added, accordingly. It should be 599 accessions. The two accessions from eastern Europe have not good marker data and were removed from analysis later, but we forget to change the table, accordingly.

Check the legend of Fig. 1 (ln 524) - references to A and B are missing.

Response: Thanks for finding this. We changed the figure but forget to change the figure legends. It’s now corrected.

In Results section, I think Fig. 3 (Ln. 208) could be made supplementary and Fig. S3 (ln. 231) be included in the main text. The latter is quite enlightening. However, its graphic presentation could be improved.

Response: Thanks for this comment. We originally put Figure S3 in the main text, but considered the figure was published, we then move it as supplemental file. This did flag out by academic editor and the journal. We have to redo the figure but still think it’s better to put it as the supplementary.

ln. 273 – ‘… is influenced by a combination of landscape characteristics.’ - I suggest replacing 'landscape' (which has aesthetic connotations) with environment.

Response: Thanks. We changed it as suggested.

Ln. 300 – In the discussion, this manuscript could also consider the results of the paper Veloso et al. 2021 (Genetic Diversity and Population Structure of Wild Beets (Beta spp.) from the Western Iberian Peninsula and the Azores and Madeira Islands) which also highlights the importance of ocean currents in species dispersal.

Response: Thanks. The reference is cited.

Finally, I suggest complementing the discussion by including some conservation proposals, namely the prioritisation of certain populat

Attachments
Attachment
Submitted filename: response to reviewers.docx
Decision Letter - Awatif Abid Al-Judaibi, Editor

Genetic drift, historic migration, and limited gene flow contributing to the subpopulation divergence in wild sea beet (Beta vulgaris ssp. maritima (L.) Arcang)

PONE-D-24-16245R1

Dear Dr. Chenggen Chu,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

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Kind regards,

Awatif Abid Al-Judaibi, PhD

Academic Editor

PLOS ONE

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: (No Response)

Reviewer #3: All comments have been addressed

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2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #3: (No Response)

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3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #3: (No Response)

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4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #3: (No Response)

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5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #3: (No Response)

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6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: The authors have improved the manuscript based on the reviewers' comments, I congratulate them for this comprehensive study. I recommend acceptance.

Reviewer #3: (No Response)

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7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: Yes: Seher Yolcu

Reviewer #3: No

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Formally Accepted
Acceptance Letter - Awatif Abid Al-Judaibi, Editor

PONE-D-24-16245R1

PLOS ONE

Dear Dr. Chu,

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now being handed over to our production team.

At this stage, our production department will prepare your paper for publication. This includes ensuring the following:

* All references, tables, and figures are properly cited

* All relevant supporting information is included in the manuscript submission,

* There are no issues that prevent the paper from being properly typeset

If revisions are needed, the production department will contact you directly to resolve them. If no revisions are needed, you will receive an email when the publication date has been set. At this time, we do not offer pre-publication proofs to authors during production of the accepted work. Please keep in mind that we are working through a large volume of accepted articles, so please give us a few weeks to review your paper and let you know the next and final steps.

Lastly, if your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

If we can help with anything else, please email us at customercare@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Professor Awatif Abid Al-Judaibi

Academic Editor

PLOS ONE

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