Specific PCR primer designed from genome data for rapid detection of Fusarium oxysporum f. sp. cubense tropical race 4 in the Cavendish banana

Shunsuke Nozawa; Dan Charlie Joy Pangilinan; G. Alvindia Dionisio; Kyoko Watanabe

doi:10.1371/journal.pone.0313358

Peer Review History

Original SubmissionJuly 26, 2024
10 Sep 2024 Decision Letter - Ravinder Kumar, Editor PONE-D-24-28376Specific PCR primer designed from genome data for rapid detection of Fusarium oxysporum f. sp. cubense tropical race 4 in the Cavendish bananaPLOS ONE Dear Dr. Watanabe, Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. Please submit your revised manuscript by Oct 25 2024 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file. 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Please include this amended Role of Funder statement in your cover letter; we will change the online submission form on your behalf. [Note: HTML markup is below. Please do not edit.] Reviewers' comments: Reviewer's Responses to Questions Comments to the Author 1. 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 #2: Yes Reviewer #3: Yes ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #2: Yes Reviewer #3: Yes ****** 3. 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 #2: Yes Reviewer #3: Yes ****** 4. 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: No Reviewer #2: Yes Reviewer #3: Yes ****** 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: The research entitled "Specific PCR primer designed from genome data for rapid detection of Fusarium oxysporum f. sp. cubense tropical race 4 in Cavendish banana" is a good research, the authors did an excellent job, however, I recommend some changes to improve the formatting of the manuscript. 1. Expand the introduction, demonstrating the history of Fusarium wilt in bananas, for example, write a history since the discovery of banana wilt in Central America, going through the morphology, phylogenetic analysis (for example, how many lineages are there within Fusarium oxysporum f.sp. cubense). I found the authors' approach interesting, even designing the primers makes it clear that race 4 is a species called Fusarium odoratissimum. 2. I recommend including in the material and methods photos of plants with symptoms of plants with wilt, or were the isolates obtained from a collection? 3. The authors do not mention the other isolates identified in the phylogeny, for example isolate PH 22-981 grouped with Fusarium fabacearum, the isolates grouped with Fusarium elaeidis, however, these results are not valued in the discussion. 4.The authors should value the phylogeny data, at no point do they mention the grouping of the isolates studied, please look at the phylogenetic tree and describe the data obtained. 5. What was the morphology of the isolates? Why not include a figure with the fungus cultures? 6. In the discussion, the authors mention this information: "However, based on our comparison of primer specificities, the primer set 13712F and 13712R may offer better detection, although they are not as perfect as the other primers because some isolates (4 out of 79 non-Foc TR4 strains) that are from fields and not Foc TR4 were detected. Therefore, our primer successfully detected Foc TR4 in diseased plant tissue (Fig 5) and are expected to reduce the time and effort required for diagnosis". This worries me, specific primers should be perfect and the authors mention that they are not so perfect, they should justify this sentence better. 7. Although the research is important, I see that the manuscript needs to be improved.... I noticed that the main focus was only the design of the primers, but in addition, the authors obtained other results and this should be discussed. Reviewer #2: Fusarium oxysporum f. sp. cubense (Foc) tropical race 4 (TR4) causes severely banana wilt. The rapid diagnosis is necessary to monitor the disease outbreaks. Current detection methods, even including race specific primer pairs, have the defects on time consuming or accuracy. The author Kyoko Watanabe developed a new primer pair based on one race specific gene from comparing genome analysis. Application of the new primer pair increased the accuracy and efficiency to investigate the TR4 distribution. The findings has the potential epidemiological significance to increase the level of monitoring TR4 population. My concerns are as follows. 1. Line 130: It’s better to provide a list of the 86 isolates with locations as well as the positive and negative reference strains that would be used during the PCR screening. 2. Line 170: Please make sure Fig.1 legend for Fig. 1 or Fig. 2 (Line 187), and vice versa. Fig.2 just shows the locations of two primer fragments. 3. Line 181: Even gene 13712 is specific to TR4, aliment of the sequence through NCBI in case of false positive result. No more illustration about the sequence of unique gene 13712 and how to design the sequence. Is there any another better one? 4. Line 242: The legend should mention each line referring to and whether the positive, negative, empty control went together with. Reviewer #3: This study examined the genome data of 93 Fusarium oxysporum strains to identify genes unique to F. oxysporum f. sp. cubense Tropical Race 4 (Foc TR4), ultimately selecting Foc TR4-specific loci as the basis for developing a new PCR primer set. The primers were validated using Foc TR4 and other related strains. Compared to primers designed in previous studies, which either failed to detect Foc TR4 or detected non-TR4 strains, the newly designed primers specifically detected Foc TR4. When tested on 86 isolates from banana fields in the Philippines, the new primer set accurately identified seven strains as Foc TR4, with no false negatives. However, four non-TR4 strains were detected as false positives, potentially due to horizontal gene transfer or shared ancestral genetic regions. Despite these minor false positives, the 13712F and 13712R primers proved more accurate than previously reported primers. The study concludes that the new primers will improve the speed and accuracy of diagnosing Foc TR4 in banana plants. In summary, the authors of the manuscript under review developed a new PCR primer set based on a pathogenicity-related gene, specifically for detecting Fusarium oxysporum f. sp. cubense Tropical Race 4 (Foc TR4). Compared to previous primers, these showed greater specificity in identifying Foc TR4, with no false negatives and minimal false positives when tested on 86 isolates from banana fields. While not perfect, the new primers offer improved accuracy for diagnosing Foc TR4 and are expected to streamline the diagnostic process in banana fields. The paper reports on an experiment conducted to a high technical standard and reports new results that should prove beneficial to the broader scientific community. Therefore, I recommend this manuscript for publication. ****** 6. 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If this link does not appear, there are no attachment files.] While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step. https://doi.org/10.1371/journal.pone.0313358.r001
Revision 1
13 Oct 2024 Author Response RESPONSE TO REVIEWERS Thank you for considering our manuscript (PONE-D-24-28376), now we revised sentences according to the reviewer’s advice. We particularly thank the reviewer for his/her incisive comment, which has helped us to make significant improvements to the scientific aspects of our study. Our responses to the comments are as follows. RESPONSE TO REVIEWE#1 Comments from Reviewer #1: 1. Expand the introduction, demonstrating the history of Fusarium wilt in bananas, for example, write a history since the discovery of banana wilt in Central America, going through the morphology, phylogenetic analysis (for example, how many lineages are there within Fusarium oxysporum f.sp. cubense). I found the authors' approach interesting, even designing the primers makes it clear that race 4 is a species called Fusarium odoratissimum. Response Thank you so much for giving us advice for the introduction. I have followed your advice and made the following corrections. Line 34-38 “However, banana production has been threatened by banana wilt disease caused by Fusarium oxysporum f. sp. cubense (Foc), a soil-borne pathogen. In the 20th century, the disease caused by Foc race 1 eradicated thousands of hectares of the Gros Michel banana in Central America. In response to this, the resistant variety, Cavendish banana was discovered and this variety became the dominant commercial banana worldwide.” Line 49-55 “A recent study showed that although it is difficult to find differences in morphology from other races, Foc TR4 is independent of other lineages including Foc race 1 and Foc subtropical race 4 (STR4), based on phylogenetic analysis using four loci: calmodulin (cmdA), RNA polymerase second largest subunit (rpb2), translation elongation factor 1-alpha (tef1), and β-tubulin 2 (tub2) regions [6]. Therefore, Foc TR4 can be distinguished from other races by phylogenetic analysis.” Comments from Reviewer #1: 2. I recommend including in the material and methods photos of plants with symptoms of plants with wilt, or were the isolates obtained from a collection? 3. The authors do not mention the other isolates identified in the phylogeny, for example isolate PH 22-981 grouped with Fusarium fabacearum, the isolates grouped with Fusarium elaeidis, however, these results are not valued in the discussion. Response We appreciate your suggestion that symptoms be shown. However, we do not have a picture of the original symptoms. So, instead of that, we added a result of the pathogenicity test against the Cavendish banana as supplemental data (S2 Fig) to show that 2718M strain is Foc TR4. The text below was added accordingly. Line 111-112 “Foc TR4 isolates (2718M; S1 Fig) that confirmed its pathogenicity against the Cavendish variety and (S2 Fig),…” Comments from Reviewer #1: 4.The authors should value the phylogeny data, at no point do they mention the grouping of the isolates studied, please look at the phylogenetic tree and describe the data obtained. Response Thank you so much for the valuable advice on the phylogeny of isolates. We agreed with your suggestion and added descriptions of the phylogenetic positions of our isolates in addition to that of Foc TR4 as below. Line 226-233 “Other isolates were clustered with F. elaeidis (5 isolates; ML/NJ/MP = 73%/71%/84%), F. fabacearum (one isolate; ML/NJ/MP = -/-/78%), F. trachichlamydosporum (two isolates; ML/NJ/MP = 98%/98%/99%), and F. triseptatum (two isolates; ML/NJ/MP = 99%/99%/99%). Four isolates are independent of known species and closely related to F. glycines. One isolate, PH22-1069, of those, and three isolates, PH22-1006, PH22-1011, and PH22-1023, from other species complexes (not determined; Fig. 3) were detected using this primer set were not Foc TR4 (Figs 3 and 4, S4 Fig).” Comments from Reviewer #1: 5. What was the morphology of the isolates? Why not include a figure with the fungus cultures? Response Thank you so much for your suggestion about the morphologies of the fungi. For 2718M, which was used for verification, we have included a photo of the isolate as supplemental data for reference (S1 Fig; Line 111). However, we did not include other isolates. This is because FocTR4 has been reported to be monophyletic in phylogenetic analysis, and it is sufficient to show the phylogenetic relationship to validate the primers. Comments from Reviewer #1: 6. In the discussion, the authors mention this information: "However, based on our comparison of primer specificities, the primer set 13712F and 13712R may offer better detection, although they are not as perfect as the other primers because some isolates (4 out of 79 non-Foc TR4 strains) that are from fields and not Foc TR4 were detected. Therefore, our primer successfully detected Foc TR4 in diseased plant tissue (Fig 5) and are expected to reduce the time and effort required for diagnosis". This worries me, specific primers should be perfect and the authors mention that they are not so perfect, they should justify this sentence better. Response Thank you very much for the advice on the justification for the utilization of the developed primer set. We agree with your suggestion. The primers we developed would detect some other strains. However, they have proven to give better results when compared to primers developed previously. Therefore, we have revised the sentences as follows. Line 287-291 “However, based on our comparison of primer specificities by PCR trials including other formae speciales, the primer set 13712F and 13712R offered better detection (Table 1; S1 Fig), although not complete because some isolates (4 out of 79 non-Foc TR4 strains) that are from fields and not Foc TR4 were detected. Furthermore, our primers successfully detected Foc TR4 in diseased plant tissue (Fig 5) and are expected to reduce the time and effort required for diagnosis.” Comments from Reviewer #1: 7. Although the research is important, I see that the manuscript needs to be improved.... I noticed that the main focus was only the design of the primers, but in addition, the authors obtained other results and this should be discussed. Response We appreciate your suggestion. We agree with your advice. Without changing the main trend of validating the usefulness of the developed primers, we added to the results the phylogenetic relationships of the isolates obtained by phylogenetic analysis. As described in the responses to suggestions 3 and 4, we added sentences as below. Line 226-233 “Other isolates were clustered with F. elaeidis (5 isolates; ML/NJ/MP = 73%/71%/84%), F. fabacearum (one isolate; ML/NJ/MP = -/-/78%), F. trachichlamydosporum (two isolates; ML/NJ/MP = 98%/98%/99%), and F. triseptatum (two isolates; ML/NJ/MP = 99%/99%/99%). Four isolates are independent of known species and closely related to F. glycines. One isolate, PH22-1069, of those, and three isolates, PH22-1006, PH22-1011, and PH22-1023, from other species complexes (not determined; Fig. 3) were detected using this primer set were not Foc TR4 (Figs 3 and 4, S4 Fig).” RESPONSE TO REVIEWE#2 Comments from Reviewer #2: 1. Line 130: It’s better to provide a list of the 86 isolates with locations as well as the positive and negative reference strains that would be used during the PCR screening. Response Line 251 We appreciate your suggestion. We agree with that we add the list of 86 isolates. We added a table (Table 3) which contains the result of detection from collected isolates, and their locations, and their phylogenetic positions. Comments from Reviewer #2: 2. Line 170: Please make sure Fig.1 legend for Fig. 1 or Fig. 2 (Line 187), and vice versa. Fig.2 just shows the locations of two primer fragments. Response Thank you so much for your correction. We replaced Fig. 1 and Fig. 2 in the proper place. Line 177-180 Fig 1 Line 198-199 Fig 2 Comments from Reviewer #2: 3. Line 181: Even gene 13712 is specific to TR4, aliment of the sequence through NCBI in case of false positive result. No more illustration about the sequence of unique gene 13712 and how to design the sequence. Is there any another better one? Response Thank you so much for your suggestion about the sequence of the target of the specific primers. Line 192 We added the sequence data of the target region as supplemental data (S1 Data). Line 193-195 We added the following sentence as the information on the primer set's design. “For a forward primer 13712F, GC content is 40%, and the annealing temperature is 53.2℃. For a reverse primer13712R, GC content is 26.9%, and the annealing temperature is 54.6℃.” Comments from Reviewer #2: 4. Line 242: The legend should mention each line referring to and whether the positive, negative, empty control went together with. Response We appreciate your correction. We have reflected on this comment and we changed the explanation of Figure 5 about the positive and negative control as follows. Line 260-265 Fig 5. Detection in plant tissues by PCR amplification. a Diseased (left) and healthy (right) corms of dwarf cavendish banana with and without inoculation of Foc TR4 (2718M). b Extracted DNA from healthy and diseased tissues. Lane M: 1 kb DNA ladder; Lane D: genome DNA from diseased tissue; Lane H: genome DNA from healthy tissue. c Detection of PCR amplicons using DNA templates from healthy and diseased tissues and mycelia of Foc TR4 (2718M). Lane M: 100 bp DNA ladder. Lane D: PCR amplicon from diseased tissue. Lane H: PCR amplicon from healthy tissue. Lane My: PCR amplicon from mycelia. Lane W: Negative control with ddH2O. RESPONSE TO REVIEWE#3 Response to Reviewer #3 Thank you very much for recommending our paper for publication. We have revised the content of the paper in accordance with the advice of reviewers 1 and 2. Attachments Attachment Submitted filename: Responce.docx https://doi.org/10.1371/journal.pone.0313358.r002
23 Oct 2024 Decision Letter - Ravinder Kumar, Editor Specific PCR primer designed from genome data for rapid detection of Fusarium oxysporum f. sp. cubense tropical race 4 in the Cavendish banana PONE-D-24-28376R1 Dear Dr. Watanabe, 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. An invoice will be generated when your article is formally accepted. Please note, if your institution has a publishing partnership with PLOS and your article meets the relevant criteria, all or part of your publication costs will be covered. 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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: All comments have been addressed Reviewer #3: All comments have been addressed ******** 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: Yes ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: Yes Reviewer #3: Yes ****** 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: Yes ****** 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: Yes ****** 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 responded to all the questions and suggestions requested, and therefore I recommend that the manuscript be accepted for publication. Obviously, the primer for the detection of TR4 is an important diagnostic methodology. Reviewer #3: The authors appear to have carefully considered the many helpful comments expressed by the expert reviews upon preparing an improved manuscript suitable for publication. ****** 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: No Reviewer #3: No ******** https://doi.org/10.1371/journal.pone.0313358.r003
Formally Accepted
19 Nov 2024 Acceptance Letter - Ravinder Kumar, Editor PONE-D-24-28376R1 PLOS ONE Dear Dr. Watanabe, 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 Dr. Ravinder Kumar Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0313358.r004

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