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Review
Peer-Review Record

Deciphering the Role of Virus Receptors in Plant–Virus–Vector Interactions

Receptors 2024, 3(2), 255-279; https://doi.org/10.3390/receptors3020013
by Sumit Jangra 1,†, Senthilraja Chinnaiah 2,†, Sneha Rashtrapal Patil 3, Bhavya Shukla 4, Ragunathan Devendran 5,* and Manish Kumar 6,*
Reviewer 1:
Reviewer 2: Anonymous
Reviewer 3: Anonymous
Receptors 2024, 3(2), 255-279; https://doi.org/10.3390/receptors3020013
Submission received: 8 March 2024 / Revised: 27 April 2024 / Accepted: 22 May 2024 / Published: 3 June 2024

Round 1

Reviewer 1 Report

Comments and Suggestions for Authors

This review focuses on the involvement of virus receptors in plant-virus-vector interactions. It begins with summarizing already documented viral receptors within vectors involved in virus uptake, retention, and transmission. The identification, characterization, and functional relevance of the viral receptors in aphids, planthoppers, leafhoppers, whiteflies and thrips has been described in depth. Authors have also described detailed overview of virus receptors from plants with emphasis on involvement in immune response and signaling.  Overall, review content is novel, well conceptualized and presents significant scientific interest for future research on virus-vector epidemiology. Therefore, I would recommend it suitable for the journal. I have few minor suggestions which could be considered:

1-       Incorporating graphical representation for the molecular and technical aspects utilized for identification and functional characterization of these receptors will increase the impact.

2-       Including flow diagram/schematics for virus receptors from plants will improve understanding and readability for broader audience.

Author Response

Comments and Suggestions for Authors: Reviewer 1

This review focuses on the involvement of virus receptors in plant-virus-vector interactions. It begins with summarizing already documented viral receptors within vectors involved in virus uptake, retention, and transmission. The identification, characterization, and functional relevance of the viral receptors in aphids, planthoppers, leafhoppers, whiteflies and thrips has been described in depth. Authors have also described detailed overview of virus receptors from plants with emphasis on involvement in immune response and signaling.  Overall, review content is novel, well conceptualized and presents significant scientific interest for future research on virus-vector epidemiology. Therefore, I would recommend it suitable for the journal. I have few minor suggestions which could be considered:

Reply to reviewer 1.

Thank you very much, we are pleased with your critical evaluation of our manuscript.

  1. Incorporating graphical representation for the molecular and technical aspects utilized for identification and functional characterization of these receptors will increase the impact.

Response: We are thankful to the reviewer for the generous suggestion, and this is very encouraging. We have generated a graphical representation as suggested by the reviewer. Thank You.

  1. Including flow diagram/schematics for virus receptors from plants will improve understanding and readability for broader audience.

Response: We have made a schematic diagram and incorporated it in our updated MS. Thank you for your critical suggestions.

Author Response File: Author Response.pdf

Reviewer 2 Report

Comments and Suggestions for Authors

The paper evidences the efforts undertaken by some research Centers to investigate on the role of virus receptors in plant‐virus‐vector interactions to offer efficient approaches for the management of viral diseases and associated vectors. This area of research may indicate future application to control or mitigate the diffusion and distribution of virus diseases. Its publication is acceptable, eventually with minor changes improving the readability.

The section concerning vectors is characterized by a more detailed indication of host plants, viruses, and vectors along the text. Whereas the section devoted to receptors in plants is less easy and the real advancement in the identification and characterization of receptors in relation to plant viruses is not fast. I am wonder if adding along the text the host plants and the virus investigated would make fast the connections between host and virus. Some comments on the results summarized in the tables is could be helpful to make more efficient the conclusions.      

Author Response

Comments and Suggestions for Authors: Reviewer 2

The paper evidences the efforts undertaken by some research Centers to investigate on the role of virus receptors in plant‐virus‐vector interactions to offer efficient approaches for the management of viral diseases and associated vectors. This area of research may indicate future application to control or mitigate the diffusion and distribution of virus diseases. Its publication is acceptable, eventually with minor changes improving the readability.

The section concerning vectors is characterized by a more detailed indication of host plants, viruses, and vectors along the text. Whereas the section devoted to receptors in plants is less easy and the real advancement in the identification and characterization of receptors in relation to plant viruses is not fast. I am wonder if adding along the text the host plants and the virus investigated would make fast the connections between host and virus. Some comments on the results summarized in the tables is could be helpful to make more efficient the conclusions.  

Reply to reviewer 2.

Response: We are grateful to reviewer 2 for their praise and constructive feedback, which has been instrumental in further improving the quality of the manuscript. Thank you for the positive response and encouragement. The authors agreed reviewer’s concern regarding the information on recent advances in the characterization and identification of receptors. This is due to word limitation authors limited the information related to characterization. However, we summarized the plant receptors and their role as a schematic diagram which is included in the revised MS. We believe that our MS will be very interesting for the Receptors Journal, MDPI, and you could accept it for publication. Thank You.

Author Response File: Author Response.pdf

Reviewer 3 Report

Comments and Suggestions for Authors

 

Manuscript receptors-2931725 reviews the literature on receptors of plant viruses in hemiptera vectors and plant hosts. It describes major findings in the field of virus-vector-host interactions. As such it is of interest. However, it clearly lacks in-depth critical assessments of the findings. Similarly, it lacks future directions in the field. Therefore, the interest of the review is limited. In addition, the section on virus receptors in insect vectors is more compelling than the section on virus receptors in plants. This is because it seems that plant receptors are narrowly considered by the authors as synonymous to R genes and other genes involved in antiviral immune reactions. This is unfortunate. To strengthen the section of the article on plant receptors, it would be desirable for authors to better link paragraphs 3.1 and subparagraphs 3.1.1.-3.1.4 with paragraph 3 by explaining, for example, how the examples listed fit the zig-zag model of virus-plant interactions for immunity. Furthermore, the section of the article on virus receptors in insect vectors could be strengthen by clearly describing the mode of transmission of the different viruses in relation to the tissue tropism of receptors. Together, manuscript receptors-2931725 is recommended for publication after major revisions.

 

Specific comments:

Lines 16-17: This sentence needs to be re-written. As written, it indicates that plant immunity acts as a first layer of defense. This is obviously incorrect.

Line 18: What is a successful pathogen?

Line 19: Intriguingly, RLKs are also known …

Line 20: … against viruses …

Line 22: … domains located extracellularly or intracellularly to …

Line 35: … receptors are proteins on the cellular surface that transmit a …

Line 37: The ligands can be …

Line 38 and throughout the manuscript: replace life cycle by infectious cycle

Line 44: … viruses, plant receptors are not the principal …

Line 47: replace keynotes by features

Lines 52-55: … plant viruses. This review aims at summarizing progress on the identification of viral receptors in vectors that are critical for transmission and in plants that sense viruses and mount antiviral defense strategies.

Line 68: Aphid-associated …

Line 72: … vectors. Virus overly and immunoblot assays …

Lines 78-79: … efficiencies of BYDV-GA by both aphid vectors was observed …

Figures 1-4: Increase the size of the figures.

Line 81: … putative proteins corresponding …

Lines 82-86: Viruses are not shown; instead, viral receptors in the aphid are shown.

Line 86: The presence of viral receptors is shown …

Line 88: Spell out ASG

Lines 92 and throughout the manuscript, including the tables: virus names should not be capitalized. For example, Beet western yellows virus should read beet western yellows virus

Line 99: … encoded HCPro was used as …

Line 114: … with the CP of cucumber …

Line 122: italicize in planta

Line 130: … to a few other luteoviruses. Immunoprecipitations …

Line 136-137: … infected with CMV enabled …

Line 142-143: Eliminate this sentence

Line 150: … (genus Oryzavirus) …

Line 163: … diagram of a planthopper showing the putative proteins corresponding …

Lines 164-168: Viruses are not shown; instead, viral receptors in the aphid are shown.

Line 168: The presence of viral receptors is shown …

Line 198: … RNA polymerase (RdRP) …

Line 219: … (T. palmi), suggesting …

Line 222: … diagram of a thrips showing the putative proteins corresponding …

Lines 223-226: Viruses are not shown; instead, viral receptors in the aphid are shown.

Line 226: The presence of viral receptors is shown …

Line 227: Receptors of TSWV …

Line 234: How was this finding validated? Some explanation would be welcome.

Line 241: change undertaken by selected

Line 241: … validation. Protein Obst was found …

Line 248: 2.4. Whiteflies-associated virus receptors

Line 250: … serious diseases of …

Lines 253-254: … interact with tomato yellow leaf curl Sardinia virus (TYLCSV)-CP and are involved …

Line 258: … diagram of a whitefly showing the putative proteins corresponding …

Lines 258-268: Viruses are not shown; instead, viral receptors in the aphid are shown.

Line 268: The presence of viral receptors is shown …

Line 271: In vitro interactions …

Line 276: … against the CP of tomato …

Line 278: … midgut protein (MGP) was identified as a putative …

Lines 289-290: … specifically interact with the collagen …

Lines 300-301: Eliminate this sentence

Line 366: 3. Viral receptors in plants

Line 370: … beneficial microbes, called Pathogen or …

Line 374: It becomes evident that …

Line 388: Change Zig-Zag to zig-zag

Line 391: Change Coat to coat

Line 392: Change Replication to replication

Line 392: Change Movement to movement

Lines 392-393: … genome to be translated in the plant …

Line 397: Change Receptor to receptor

Line 406: … (Table 2). Subsequently …

Line 414: … and nucleus. The N protein …

Line 415: … of the TMV replicase …

Line 429: … and other potexviruses. In addition, …

Line 433: … recognizes the CP of PVX …

Line 471: Two dominant loci, RCY1 and HRT, that belong to …

Line 472: … proteins, confer resistance …

Line 475: Change Jasmonic to jasmonic …

Line 484: Change plum pox potyvirus to plum pox virus

Line 486: It sense the CP and thereby …

Line 531: … (ORNV), PPV, and turnip …

Line 565: Since plant viruses are …

Line 568: … antiviral strategy. Plant receptors play an important role in plant defense …

Comments on the Quality of English Language

Suggestions for language improvements have been made. See specific comments listed in the evaluation report

Author Response

Comments and Suggestions for Authors: Reviewer 3

Manuscript receptors-2931725 reviews the literature on receptors of plant viruses in hemiptera vectors and plant hosts. It describes major findings in the field of virus-vector-host interactions. As such it is of interest. However, it clearly lacks in-depth critical assessments of the findings. Similarly, it lacks future directions in the field. Therefore, the interest of the review is limited. In addition, the section on virus receptors in insect vectors is more compelling than the section on virus receptors in plants. This is because it seems that plant receptors are narrowly considered by the authors as synonymous to R genes and other genes involved in antiviral immune reactions. This is unfortunate. To strengthen the section of the article on plant receptors, it would be desirable for authors to better link paragraphs 3.1 and subparagraphs 3.1.1.-3.1.4 with paragraph 3 by explaining, for example, how the examples listed fit the zig-zag model of virus-plant interactions for immunity. Furthermore, the section of the article on virus receptors in insect vectors could be strengthen by clearly describing the mode of transmission of the different viruses in relation to the tissue tropism of receptors. Together, manuscript receptors-2931725 is recommended for publication after major revisions.

Reply to reviewer 3.

Response: Thank you very much for your critical and detailed evaluation of our manuscript. The authors appreciate the reviewers' constructive feedback throughout the MS. The revised version of the manuscript has diligently considered and incorporated all the reviewer’s suggestions. Although several reviews have been published recently on plant receptors, we were trying to distinguish the R-gene receptors and other receptors (co-receptors) based on protein domains in different sub-sections. However, as per the reviewers’ suggestion, the authors linked the paragraphs by adding and rephrasing text. An example of a zig-zag model is discussed clearly as per the reviewers’ suggestion. In addition, A point-by-point response to the reviewers' comments is indicated in the blue text below. We have done our best to ensure that the manuscript is correct in terminology, form, language, grammar, and content. All changes in the text are highlighted in yellow colour.

Specific comments:

Lines 16-17: This sentence needs to be re-written. As written, it indicates that plant immunity acts as a first layer of defense. This is obviously incorrect.

Response: The text is rephrased as per the reviewer’s suggestion. In short “basal defense”. Thank You.

Line 18: What is a successful pathogen?

Response: Authors mean that a pathogen that overcomes the basal defense to cause successful infection. We have rephrased the sentence. Thanks.

Line 19: Intriguingly, RLKs are also known …

Response: The brackets have been removed. Thank you!

Line 20: … against viruses …

Response: ‘the’ has been deleted. Thanks.

Line 22: … domains located extracellularly or intracellularly to …

Response: ‘to’ has been replaced with ‘or’. Thanks.

Line 35: … receptors are proteins on the cellular surface that transmit a …

Response:  The sentence has been revised as suggested. Thank you.

Line 37: The ligands can be …

Response:  ligand has been formatted to ligands. Thank you. 

Line 38 and throughout the manuscript: replace life cycle by infectious cycle.

Response: As suggested life cycle has been replaced with infectious cycle throughout the manuscript. Thank you for pointing out this!

Line 44: … viruses, plant receptors are not the principal …

Response: ‘the’ has been deleted. Thanks.

Line 47: replace keynotes by features

Response: edited as suggested! Thanks.

Lines 52-55: … plant viruses. This review aims at summarizing progress on the identification of viral receptors in vectors that are critical for transmission and in plants that sense viruses and mount antiviral defense strategies.

Response: The sentence has been reframed. Thank you!

Line 68: Aphid-associated …

Response: Revised as suggested. Thanks.

Line 72: … vectors. Virus overly and immunoblot assays …

Response: ‘and are discussed in this review’ These words have been deleted from the sentence as per the reviewers' suggestion. Thanks.

Lines 78-79: … efficiencies of BYDV-GA by both aphid vectors was observed …

Response: Sentence has been revised as suggested. Thank you!

Figures 1-4: Increase the size of the figures.

Response: We sincerely appreciate your pointing out the size of the figures. We have increased the length and width of the images and tried to keep them uniform for better visualization. Thank You.

Line 81: … putative proteins corresponding …

Response: The word interacting has been deleted as suggested by the reviewer. Thanks.

Lines 82-86: Viruses are not shown; instead, viral receptors in the aphid are shown.

Response: The figure legend has been revised as suggested. Thank you!

Line 86: The presence of viral receptors is shown …

Response: Revised as suggested. Thanks.

Line 88: Spell out ASG

Response: ASG abbreviation has been used for “accessory salivary gland (ASG)”, as we mentioned in line no. 75., Page no. 2. Thank You.

Lines 92 and throughout the manuscript, including the tables: virus names should not be capitalized. For example, Beet western yellows virus should read beet western yellows virus

Response: We appreciate the suggestion for writing virus name. We have corrected it throughout the manuscript. Thank You!

Line 99: … encoded HCPro was used as …

Response: Corrected, Thanks

Line 114: … with the CP of cucumber …

Response: We revised the sentence. Thank you.

Line 122: italicize in planta

Response: in planta has been italicized. Thanks.

Line 130: … to a few other luteoviruses. Immunoprecipitations …

Response: Revised as suggested.

Line 136-137: … infected with CMV enabled …

Response: Reframed the sentence. Thank You.

Line 142-143: Eliminate this sentence

Response: The sentence has been deleted. Thanks.

Line 150: … (genus Oryzavirus) …

Response: Corrected as suggested. Thank You.

Line 163: … diagram of a planthopper showing the putative proteins corresponding …

Response: The word interacting has been deleted. Thank you.

Lines 164-168: Viruses are not shown; instead, viral receptors in the aphid are shown.

Response: The figure legend has been revised. Thank you for your suggestion.

Line 168: The presence of viral receptors is shown …

Response: ‘is’ has been added in place of ‘was’ in the revised MS. Thanks.

Line 198: … RNA polymerase (RdRP) …

Response: ‘RdRp’ has been formatted to ‘RdRP’.

Line 219: … (T. palmi), suggesting …

Response: Comma added after (T. palmi). Thank you.

Line 222: … diagram of a thrips showing the putative proteins corresponding …

Response: The word interacting has been deleted as suggested by the reviewer. Thanks.

Lines 223-226: Viruses are not shown; instead, viral receptors in the aphid are shown.

Response: The figure legend has been revised as suggested by the reviewer. Thank you!

Line 226: The presence of viral receptors is shown …

Response: ‘is’ has been added instead of ‘was’ in the revised MS.

Line 227: Receptors of TSWV …

Response: Revised as suggested.

Line 234: How was this finding validated? Some explanation would be welcome.

Response: The findings were validated using surface plasma resonance and GST pull-down and this has been added in the revised version of the MS. Thank You.

Line 241: change undertaken by selected

Response: Revised as suggested. Thanks.

Line 241: … validation. Protein Obst was found …

Response: Corrected, Thanks.

Line 248: 2.4. Whiteflies-associated virus receptors

Response: The section heading has been revised as suggested by the reviewer. Thank You.

Line 250: … serious diseases of …

Response: Reframed as suggested. Thanks.

Lines 253-254: … interact with tomato yellow leaf curl Sardinia virus (TYLCSV)-CP and are involved …

Response: The words ‘of begomoviruses’ has been deleted from the sentence as suggested.

Line 258: … diagram of a whitefly showing the putative proteins corresponding …

Response: The word interacting has been deleted as suggested by the reviewer.

Lines 258-268: Viruses are not shown; instead, viral receptors in the aphid are shown.

Response: The figure legend has been revised as suggested earlier. Thank You.

Line 268: The presence of viral receptors is shown …

Response: ‘is’ has been added in place of ‘was’ in the revised MS. Thanks.

Line 271: In vitro interactions …

Response: Done as suggested. Thank You.

Line 276: … against the CP of tomato …

Response: ‘the’ added before CP as per reviewers’ suggestions.

Line 278: … midgut protein (MGP) was identified as a putative …

Response: ‘was identified’ added after (MGP) as suggested. Thank You

Lines 289-290: … specifically interact with the collagen …

Response: The line has been revised as suggested.

Lines 300-301: Eliminate this sentence

Response: As suggested the sentence has been deleted in the revised version of the MS. Thanks.

Line 366: 3. Viral receptors in plants

Response: The subheading has been revised as suggested by the reviewer. Thank you.

Line 370: … beneficial microbes, called Pathogen or …

Response: The sentence has been revised as suggested.

Line 374: It becomes evident that …

Response: The sentence has been modified as per the reviewer's comment. Thanks.

Line 388: Change Zig-Zag to zig-zag

Response: Zig-Zag has been changed to zig-zag.

Line 391: Change Coat to coat

Response: Coat has been changed to “coat”.

Line 392: Change Replication to replication

Response: Replication has been changed to replication.   

Line 392: Change Movement to movement

Response: Revised as suggested. Thanks.

Lines 392-393: … genome to be translated in the plant …

Response: Reframed the sentence. Thank you.

Line 397: Change Receptor to receptor

Response: Receptor has been changed to “receptor”

Line 406: … (Table 2). Subsequently …

Response: The has been reframed as suggested. Thanks

Line 414: … and nucleus. The N protein …

Response: ‘The’ added at the start of the sentence. Thanks for correcting.

Line 415: … of the TMV replicase …

Response: TMV has been added as suggested by the reviewer. Thanks

Line 429: … and other potexviruses. In addition, …

Response: Corrected as suggested. Thank You.

Line 433: … recognizes the CP of PVX …

Response: The extended form of CP has been deleted in the revised MS. Thank You.

Line 471: Two dominant loci, RCY1 and HRT, that belong to …

Response: Revised as suggested, Thanks.

Line 472: … proteins, confer resistance …

Response: ‘are’ deleted as suggested, Thanks.

Line 475: Change Jasmonic to jasmonic …

Response: Jasmonic has been changed to “jasmonic”

Line 484: Change plum pox potyvirus to plum pox virus

Response: plum pox potyvirus has been changed to plum pox virus. Thank You.

Line 486: It sense the CP and thereby …

Response: Revised as suggested, Thanks.

Line 531: … (ORNV), PPV, and turnip …

Response: Done as suggested, Thank You!

Line 565: Since plant viruses are …

Response: ‘Since the species of plant viruses are’ has been changed to ‘Since the plant viruses are’

Line 568: … antiviral strategy. Plant receptors play an important role in plant defense …

Response: The sentence has been revised as per reviewers' suggestions. Thank You.

Author Response File: Author Response.pdf

Round 2

Reviewer 2 Report

Comments and Suggestions for Authors

The revisions have improved the understanding and readability of the paper. The plants receptors is now more clear and easy to follow. 

Reviewer 3 Report

Comments and Suggestions for Authors

Revisions are satisfactory

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