Dear Rita,

Thank you for submitting your manuscript entitled "Plasmodium NEK1 coordinates MTOC organisation and kinetochore attachment during rapid mitosis in male gamete formation" for consideration as a Research Article by PLOS Biology. I am so sorry for the long wait.

Your manuscript has now been evaluated by the PLOS Biology editorial staff, and I am writing to let you know that we would like to send your submission out for external peer review. However, we have not received the advice yet of an Academic Editor regarding how we will proceed with the submission (going back to the reviewers or not), so it is possible that we will ask the reviewers to evaluate the revision.

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Feel free to email us at plosbiology@plos.org if you have any queries relating to your submission.

Kind regards,

Melissa

Melissa Vazquez Hernandez, Ph.D.

Associate Editor

PLOS Biology

mvazquezhernandez@plos.org

Dear Rita,

Thank you for your patience while we considered your revised manuscript "Plasmodium NEK1 coordinates MTOC organisation and kinetochore attachment during rapid mitosis in male gamete formation" for consideration as a Research Article at PLOS Biology. Your revised study has now been evaluated by the PLOS Biology editors and the Academic Editor. I would first like to apologize for the long delay during this process.

In this case, the Academic Editor has arbitrated the revision and agreed that most reviewers’ concerns were addressed. However, the Academic Editor has still some requests which you can find at the end of this e-mail, such as additional statistical analyses, some adjustments in the text and additional points of discussion. Addressing the concerns and suggestions of the Academic Editor is essential for further consideration of your manuscript for publication in PLOS Biology.

We expect to receive your revised manuscript within 1 month. Please email us (plosbiology@plos.org) if you have any questions or concerns, or would like to request an extension.

At this stage, your manuscript remains formally under active consideration at our journal; please notify us by email if you do not intend to submit a revision so that we withdraw the manuscript.

**IMPORTANT - SUBMITTING YOUR REVISION**

Your revisions should address the specific points made by each reviewer. Please submit the following files along with your revised manuscript:

1. A 'Response to Reviewers' file - this should detail your responses to the editorial requests, present a point-by-point response to all of the reviewers' comments, and indicate the changes made to the manuscript.

*NOTE: In your point-by-point response to the reviewers, please provide the full context of each review. Do not selectively quote paragraphs or sentences to reply to. The entire set of reviewer comments should be present in full and each specific point should be responded to individually.

You should also cite any additional relevant literature that has been published since the original submission and mention any additional citations in your response.

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*Resubmission Checklist*

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https://blogs.plos.org/plos/2019/05/plos-journals-now-open-for-published-peer-review/

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Please note that as a condition of publication PLOS' data policy (http://journals.plos.org/plosbiology/s/data-availability) requires that you make available all data used to draw the conclusions arrived at in your manuscript. If you have not already done so, you must include any data used in your manuscript either in appropriate repositories, within the body of the manuscript, or as supporting information (N.B. this includes any numerical values that were used to generate graphs, histograms etc.). For an example see here: http://www.plosbiology.org/article/info%3Adoi%2F10.1371%2Fjournal.pbio.1001908#s5

*Blot and Gel Data Policy*

We require the original, uncropped and minimally adjusted images supporting all blot and gel results reported in an article's figures or Supporting Information files. We will require these files before a manuscript can be accepted so please prepare them now, if you have not already uploaded them. Please carefully read our guidelines for how to prepare and upload this data: https://journals.plos.org/plosbiology/s/figures#loc-blot-and-gel-reporting-requirements

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To enhance the reproducibility of your results, we recommend that if applicable you deposit your laboratory protocols in protocols.io, where a protocol can be assigned its own identifier (DOI) such that it can be cited independently in the future. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols

Thank you again for your submission to our journal. We hope that our editorial process has been constructive thus far, and we welcome your feedback at any time. Please don't hesitate to contact us if you have any questions or comments.

Sincerely,

Melissa

Melissa Vazquez Hernandez, Ph.D.

Associate Editor

PLOS Biology

mvazquezhernandez@plos.org

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ADDITIONAL COMMENTS FROM THE ACADEMIC EDITOR:

The study is a thorough analysis of the cell biology of the nek1 kinase during the rapid rounds of mitosis preceding exflagellation of male microgametes. It combines high quality light and electron microscopy to detail the development of centriolar plaques and spindles and the relative positions of various components including NEK1. It combines this with inducible knockdown and promoter trap to prove essentiality of NEK1 for mitosis in male gamete development and it also provides some NEK1 deficient transcriptome & phosphoproteome and NEK1 interactome data. This is a very useful analysis of an enigmatic stage in parasite development that will be valuable not only for the characterisation of NEK1 in this process but as a general reference for the process itself.

I don’t believe any additional experiments are required but some of the analyses needed statistical support or re-writing and some points need clarifying.

I found the results relating to relative positions of nek1 and centrin unconvincing. In asexual blood stage schizonts the supposed difference in dna overlap of NEK1 compared to centrin requires a statistical test to prove there is a difference between correlations for overlaps and might be better tested comparing distance between peak fluorescence intensities rather than correlations of overlap, I have provided more details in my comment on the comment from reviewer 2. In male gametes fig 2e timing of division of centrin and nek1 is convincing but their relative orientation to cytoplasm and nucleus looks like it could just be chromatic shift with both centrin 4 spots shifted in the same direction. From the uEXM in fig 2f the nek1 and centriolar MTOC associated centrin are similar distances from dna at 1 min but by 10 min the nek1 is more nuclear and is dissociating through the nucleus. I think this EXM data for nek1 localisation relative to centrin and dna in male gametes is much more convincing than the live microscopy and the claims of relative proximity to dna from the live microscopy in fig 2E are confusing and could be deleted.

Fig 4, mass spec, is missing and there is no fig 5j, please carefully check fig numbering in this revised MS

Line 456 RNASeq, I suggest rephrasing “all replicates were clustered together”, this is a bit ambiguous and could be interpreted to mean that duplicates were pooled prior to diff gene expression analysis when the authors actually mean the replicates were reproducible and similar to each other in a clustering analysis, maybe just say the replicates were reproducible?

I believe that the transcriptome and proteomes are useful information but also that these analyses are difficult to interpret when they compare parasites that have had interrupted development, particularly for the 30 min post activation rnaseq. Would 30 min activated rnaseq be somewhat confounded by the reduced number of male compared to female gametes? Are the genomes actively transcribed in microgametes? Could the data be compared to sex specific transcriptomes/proteomes to exclude the differential kinase transcription and the peptide differences being a consequence of no male microgametes being produced rather than a direct consequence of NEK1 phosphorylating a regulator of these genes/proteins? Perhaps just include some discussion of the potential confounders for these analysis when comparing developmentally different parasites.

The legend for the symbols within fig 6 needs to be aligned

Re reviewers comments

Reviewer 1

I think NDC80 is an OK surrogate for the centromeres at the stages examined. The authors could include a conditional comment though to make it clear that NDC80 is not an integral component of the centromere but has only a centromeric location in their chipseq. I note though that the chipseq is presumably only a single timepoint so may not be representative of the stages in the figures.

Reviewer 2

Major points

2) validating omics. I don’t think this is necessary, the authors were describing the function of nek1, they have done a thorough job by identifying candidate interacting factors, they are useful leads for future work but proving them or investigating them further is really beyond the scope of a study focusing on nek1.

Minor points

2) subtraction of background from imaging.

The reviewer mentions photoshop but I think the program used is irrelevant, ie axiovision might also be used to set a threshold value for background below which everything is zero. This is the same issue raised by reviewer 1. I have not analysed sim or exm myself so I do not know whether maximum intensity projections is acceptable. For widefield or confocal fluorescence microscopy I would not accept the subtraction of "background" below a threshold level as this constitutes removing data. I agree with the reviewers that the presented image should show the full dynamic range of the data with background having a detectable value and maximum signal not being saturating.

10) fig1c, comparison of nek1 centrin distance to dna, quantitation requested.

For figs 1E and F there are more than 30 measures for each plot so the authors should perform a statistical test to support their claim that NEK1 is closer than centrin to dna and ndc is closer than nek1 to dna. Actually I think that correlation is perhaps not the best measure to compare different proteins if the compared measure is "distance from". If a line were drawn through peak fluorescence it is not clear to me from the supplied images that peak centrin would be any further from dna than would nek1.

11) similarity of nek1 in liver stages.

I accept the authors’ explanation but they have not amended the original text to clarify this, which they should, because it was not clear to the reviewer and so is also likely to be unclear to multiple readers. I suggest they add the adjective nuclear before the noun foci.

12) video dapi signal saturation.

The authors explain why they saturated dapi but they need to clarify what they have done to alter MS as per the reviewers request, ie how have material or legends been altered to indicate differences in processing?

14) preinduction image of kinesin 8B.

Fig 3A is labelled ndc80, not kinesin 8B, have the authors supplied the pre-induction image of kinesin 8b as requested and as they have stated?

16) NDC80/kinetochores arrayed along spindle

The explanation in the text seems clear that nek1 is in the mtocs and the ndc80/centromeres are organised along the spindle, I dont think this requires further explanation.

Reviewer 3

Major comments

3) validating (phosphor)proteomics

Validating the kinase target is probably beyond the scope of the study, I think the cell biology plus the omics screens is sufficient. The omics analyses are not definitive proof but provide leads for future studies which seems appropriate appropriate to me. I note that another reviewer requested follow-up to the interacting proteome. In light of the multiple omics sets analysed I think following up is beyond the scope of one study.

5) NEK1 in liver stages

I think that analysis of liver stages is beyond the scope of the MS

Dear Rita,

Thank you for your patience while we considered your revised manuscript "Plasmodium NEK1 coordinates MTOC organisation and kinetochore attachment during rapid mitosis in male gamete formation" for consideration as a Research Article at PLOS Biology. Your revised study has now been evaluated by the PLOS Biology editors and the Academic Editor. I would like to apologize once more for the delay.

Although the Academic Editor acknowledged that some of his concerns were properly addressed, he highlighted important issues that must be fully resolved for further consideration. Specifically, please address the concerns regarding the chromatic shift. Additionally, during the discussion, it was noted that some changes claimed to be made in the previous version according to the reviewer's comments were not actually implemented. Please ensure that the manuscript is revised according to the comments and discussions in the rebuttal letter. In your rebuttal letter and the manuscript, please clearly indicate where the changes have been made. This will help us more rapidly assess the revisions. I have pasted the comments from the Academic Editor after my signature.

We expect to receive your revised manuscript within 1 month. Please email us (plosbiology@plos.org) if you have any questions or concerns, or would like to request an extension.

At this stage, your manuscript remains formally under active consideration at our journal; please notify us by email if you do not intend to submit a revision so that we withdraw the manuscript.

**IMPORTANT - SUBMITTING YOUR REVISION**

Your revisions should address the specific points made by each reviewer. Please submit the following files along with your revised manuscript:

1. A 'Response to Reviewers' file - this should detail your responses to the editorial requests, present a point-by-point response to all of the reviewers' comments, and indicate the changes made to the manuscript.

*NOTE: In your point-by-point response to the reviewers, please provide the full context of each review. Do not selectively quote paragraphs or sentences to reply to. The entire set of reviewer comments should be present in full and each specific point should be responded to individually.

You should also cite any additional relevant literature that has been published since the original submission and mention any additional citations in your response.

2. In addition to a clean copy of the manuscript, please also upload a 'track-changes' version of your manuscript that specifies the edits made. This should be uploaded as a "Revised Article with Changes Highlighted " file type.

*Resubmission Checklist*

When you are ready to resubmit your revised manuscript, please refer to this resubmission checklist: https://plos.io/Biology_Checklist

To submit a revised version of your manuscript, please go to https://www.editorialmanager.com/pbiology/ and log in as an Author. Click the link labelled 'Submissions Needing Revision' where you will find your submission record.

Please make sure to read the following important policies and guidelines while preparing your revision:

*Published Peer Review*

Please note while forming your response, if your article is accepted, you may have the opportunity to make the peer review history publicly available. The record will include editor decision letters (with reviews) and your responses to reviewer comments. If eligible, we will contact you to opt in or out. Please see here for more details:

https://blogs.plos.org/plos/2019/05/plos-journals-now-open-for-published-peer-review/

*PLOS Data Policy*

Please note that as a condition of publication PLOS' data policy (http://journals.plos.org/plosbiology/s/data-availability) requires that you make available all data used to draw the conclusions arrived at in your manuscript. If you have not already done so, you must include any data used in your manuscript either in appropriate repositories, within the body of the manuscript, or as supporting information (N.B. this includes any numerical values that were used to generate graphs, histograms etc.). For an example see here: http://www.plosbiology.org/article/info%3Adoi%2F10.1371%2Fjournal.pbio.1001908#s5

*Blot and Gel Data Policy*

We require the original, uncropped and minimally adjusted images supporting all blot and gel results reported in an article's figures or Supporting Information files. We will require these files before a manuscript can be accepted so please prepare them now, if you have not already uploaded them. Please carefully read our guidelines for how to prepare and upload this data: https://journals.plos.org/plosbiology/s/figures#loc-blot-and-gel-reporting-requirements

*Protocols deposition*

To enhance the reproducibility of your results, we recommend that if applicable you deposit your laboratory protocols in protocols.io, where a protocol can be assigned its own identifier (DOI) such that it can be cited independently in the future. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols

Thank you again for your submission to our journal. We hope that our editorial process has been constructive thus far, and we welcome your feedback at any time. Please don't hesitate to contact us if you have any questions or comments.

Sincerely,

Melissa

Melissa Vazquez Hernandez, Ph.D.

Associate Editor

PLOS Biology

mvazquezhernandez@plos.org

----------------------------------------------------------------

COMMENTS FROM THE ACADEMIC EDITOR:

The authors have addressed most of my comments.

They have not addressed the issue of chromatic shift in live fluorescence. The distance between peak fluorescence analysis is more convincing except that the live fluorescence does not appear to have controlled for chromatic shift. It isn’t a clear problem in fig s2a or fig 2 but is obviously a problem in fig 1B mature schizonts merge where the centrin can be seen on top of the NDC80 staining in the nuclei on the right hand perimeter of the infected red blood cell at 1 oclock but ndc80 moves progressively down and to the left away from the centrin4 as you move clockwise around the infected rbc perimeter from 1 oclock through to 11 oclock. This is clearly chromatic shift and unless it has been controlled for by eg using beads fluorescing at multiple wave lengths to align the images post acquisition, it is not really possible to infer anything about the relative distances between the red and green fluorescing proteins. Clearly for this image, measuring the distance between ndc80 and centrin4 will be different on the left and right hand sides of the cell. For the actual measured distances in figs 1 e and f the provided images in figs 1C look ok but fig 1 d middle schizont looks left shifted. The authors need to provide images showing nuclei oriented in all directions eg as in fig 1c to convincingly show that the chromatic shift is not confounding their distance analysis. As the shift is clearly a problem in fig1b it must be assumed to affect all the live fluorescence and so it would be easiest for the authors to remove distance based analyses based on live microscopy, unless they have in some way controlled for chromatic shift.

In their response to my comment on their omics analyses the authors finish with the statement

“These results suggest that downregulation of NEK1 does not modulate the transcriptome, and depletion of NEK1 does not result in detectable differences in the phosphoproteome during gametogenesis. The slight changes in transcriptome could be due to a reduced number of male gametes.”

From their response it is unclear whether the authors have modified the MS to discuss the possible confounding effect of reduced male gams on the omics analysis. Could the authors please provide explicit details of what and where they have altered the MS to address comments from the reviewers or editor.

Dear Rita,

Thank you for your patience while we considered your revised manuscript "Plasmodium NEK1 coordinates MTOC organisation and kinetochore attachment during rapid mitosis in male gamete formation" for publication as a Research Article at PLOS Biology. This revised version of your manuscript has been evaluated by the PLOS Biology editors.

We are likely to accept this manuscript for publication, provided you satisfactorily address the remaining editorial points. Please also make sure to address the following data and other policy-related requests.

a) You may be aware of the PLOS Data Policy, which requires that all data be made available without restriction: http://journals.plos.org/plosbiology/s/data-availability. For more information, please also see this editorial: http://dx.doi.org/10.1371/journal.pbio.1001797

Please supply the numerical values either in the a supplementary file or as a permanent DOI’d deposition for the following figures:

Figure 1EF, 4, 5ABCDFGHI, S1EFGH, S4GHJ, S5C

NOTE: the numerical data provided should include all replicates AND the way in which the plotted mean and errors were derived (it should not present only the mean/average values).

b) Please cite the location of the data clearly in all relevant main and supplementary Figure legends, e.g. “The data underlying this Figure can be found in S1 Data” or “The data underlying this Figure can be found in https://doi.org/10.5281/zenodo.XXXXX”

c) We require the original, uncropped and minimally adjusted images supporting all blot and gel results reported in the Figures S1BC, S4BCF

We will require these files before a manuscript can be accepted so please prepare and upload them now. Please carefully read our guidelines for how to prepare and upload this data: https://journals.plos.org/plosbiology/s/figures#loc-blot-and-gel-reporting-requirements

d) Thank you for providing the raw data on NCBI and ProteomeXChange. However, we were not able to access the data at ProteomeXChange; please make it publicly available in the next submission.

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Please note that we cannot accept sole deposition of code in GitHub, as this could be changed after publication. However, you can archive this version of your publicly available GitHub code to Zenodo. Once you do this, it will generate a DOI number, which you will need to provide in the Data Accessibility Statement (you are welcome to also provide the GitHub access information). See the process for doing this here: https://docs.github.com/en/repositories/archiving-a-github-repository/referencing-and-citing-content

As you address these items, please take this last chance to 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 cover letter that accompanies your revised manuscript.

We expect to receive your revised manuscript within two weeks.

To submit your revision, please go to https://www.editorialmanager.com/pbiology/ and log in as an Author. Click the link labelled 'Submissions Needing Revision' to find your submission record. Your revised submission must include the following:

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*Published Peer Review History*

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*Protocols deposition*

To enhance the reproducibility of your results, we recommend that if applicable you deposit your laboratory protocols in protocols.io, where a protocol can be assigned its own identifier (DOI) such that it can be cited independently in the future. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols

Please do not hesitate to contact me should you have any questions.

Sincerely,

Melissa

Melissa Vazquez Hernandez, Ph.D.

Associate Editor

mvazquezhernandez@plos.org

PLOS Biology

------------------------------------------------------------------------

Dear Rita,

Thank you for the submission of your revised Research Article "Plasmodium NEK1 coordinates MTOC organisation and kinetochore attachment during rapid mitosis in male gamete formation" for publication in PLOS Biology. On behalf of my colleagues and the Academic Editor, Michael Duffy, I am pleased to say that we can in principle accept your manuscript for publication, provided you address any remaining formatting and reporting issues. These will be detailed in an email you should receive within 2-3 business days from our colleagues in the journal operations team; no action is required from you until then. Please note that we will not be able to formally accept your manuscript and schedule it for publication until you have completed any requested changes.

Thank you once more for your patience.

Please take a minute to log into Editorial Manager at http://www.editorialmanager.com/pbiology/, click the "Update My Information" link at the top of the page, and update your user information to ensure an efficient production process.

PRESS

We frequently collaborate with press offices. If your institution or institutions have a press office, please notify them about your upcoming paper at this point, to enable them to help maximise its impact. If the press office is planning to promote your findings, we would be grateful if they could coordinate with biologypress@plos.org. If you have previously opted in to the early version process, we ask that you notify us immediately of any press plans so that we may opt out on your behalf.

We also ask that you take this opportunity to read our Embargo Policy regarding the discussion, promotion and media coverage of work that is yet to be published by PLOS. As your manuscript is not yet published, it is bound by the conditions of our Embargo Policy. Please be aware that this policy is in place both to ensure that any press coverage of your article is fully substantiated and to provide a direct link between such coverage and the published work. For full details of our Embargo Policy, please visit http://www.plos.org/about/media-inquiries/embargo-policy/.

Thank you again for choosing PLOS Biology for publication and supporting Open Access publishing. We look forward to publishing your study. 

Sincerely, 

Melissa

Melissa Vazquez Hernandez, Ph.D., Ph.D.

Associate Editor

PLOS Biology

mvazquezhernandez@plos.org