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Review
Peer-Review Record

Use of Elicitors and Beneficial Bacteria to Induce and Prime the Stilbene Phytoalexin Response: Applications to Grapevine Disease Resistance

Agronomy 2023, 13(9), 2225; https://doi.org/10.3390/agronomy13092225
by Philippe Jeandet 1,*, Patricia Trotel-Aziz 1, Cédric Jacquard 1, Christophe Clément 1, Chandra Mohan 2, Iwona Morkunas 3, Haroon Khan 4 and Aziz Aziz 1
Reviewer 1:
Reviewer 2: Anonymous
Reviewer 3: Anonymous
Reviewer 4:
Agronomy 2023, 13(9), 2225; https://doi.org/10.3390/agronomy13092225
Submission received: 8 August 2023 / Revised: 20 August 2023 / Accepted: 23 August 2023 / Published: 25 August 2023

Round 1

Reviewer 1 Report

The review of Jeandet et al. tackles an interesting subject for sustainable agricultural applications and it is globally well-written. However, I believe that the text is quite descriptive and that with more deepening the manuscript can be significantly improved. The authors write a list of a series of experimental results by dividing them in categories based on the treatment type, without many points of critical deepening and without proposing novel hypotheses about the existing knowledge gaps in this field. I think there is a lot of room for improvement in this sense and I hope that my comments can be helpful for this.

MAJOR COMMENTS:

The authors list the experiments by categorizing them basing on the resistance inducer type (metal salts, hormones, bioinducers, beneficial microorganisms). It would be interesting to resume the different advantages and disadvantages of each category in relation to field application (e.g. problem of heavy metals accumulation; growth-defense trade-off effects of hormones, difficulty to control beneficial microbial inoculum in open field etc.). Maybe this can be done through a table. In direct link with this, I think it would be important to talk some more about all the potential drawbacks of these treatments in the text, as I find it too much unbalanced towards the positive effects.

In Chapter 2 the authors cite the impact of chemical modifications on stilbenes biocidal activity (hydroxylation, methylation, oligomerization). Is it known what are effects of such modifications on the mechanism of action of stilbenes? Do the authors have some hypotheses to advance in this sense?

- The conclusion part is very long and doesn’t add much to the manuscript. All the text between L 733-792 can be just reduced to a couple of sentences summing up the advantages and disadvantages of the different treatments. On the other hand, there is no mention for further research directions. What questions remains to be answered to achieve effective phytoalexin stimulation in field conditions? What kind of experiments can be designed in this sense? What are the most critical knowledge gaps to be filled?

 MINOR COMMENTS

ABSTRACT

L23-25: Please reformulate this sentence in a clearer manner.

INTRODUCTION

L 52-53: “ferment of activity” is a very weird expression.

L 65: Please replace “no doubt” with “without doubt”

Chapter 2

L 93: Please correct the use of the commas in this sentence.

L 94: Please avoid the use of improper metaphors. Something with a well-defined location, such as a cellular compartment or a defined group of cells, can be compared to a seat, not a molecule.

L 189-190: Far-fetched comparison. The human disease mentioned do not have microbial basis, therefore the molecular mechanisms are unlikely to be comparable with those of plant diseases.

Chapter 3

L257-259: Please correct the use of commas in this sentence.

L275: “In the attempt to…” rather than “In attempting to…”

L292: It is Reactive Burst Oxidase Homolog, and the acronym is RBOH (not Homologue and RbOH). Please correct thoroughly in the text. Authors should also specify that the mentioned “activation” refers to the enzymatic activity and not gene expression, thus making not possible to determine which isoform is responsible for the observed effect. Indeed, the authors should not refer to RBOHs as one protein, given that it is a multigenic family (at least that studies on a specific isoform are mentioned). In general, the paragraph citing RBOHs should be revised. These enzymes have important roles in plant immunity and in the defense priming process and this is not mentioned at all.

L 368: remove point after “leaves”

L 398 and rest of the text: MeJA, not MeJa.

L 556-558: If the tagatose-based product induced just a slight increase in stilbenes accumulation (so probably not responsible of the protective effect), then I ask the authors why it is worth to report this study in this review? Perhaps it should be mentioned much more succinctly?

Chapter 4

L 663-673: Remark similar to the one above (L556-558).

CONCLUSION

L 721-724: This is a good critical remark, I think it would be good to develop it bit more as it will give more critical depth to the discussion, e.g. are there some common features between the studies reporting negative and positive correlations between stilbenes accumulation and disease protection?

- I recommend revising the grammar of the first part of this manuscript, notably the introduction and the second chapter. Although the vocabulary is of good quality, the construction of the sentences is not so straightforward and hinders a smooth reading, therefore decreasing the overall attractiveness of the text. Overall, I recommend being more concise and avoid redundancies.

Author Response

Preliminary Remark

First of all, we thank the four reviewers for their in-depth analysis of the manuscript and for their comments done in a very short time.

Reviewer 1

MAJOR COMMENTS:

The authors list the experiments by categorizing them basing on the resistance inducer type (metal salts, hormones, bioinducers, beneficial microorganisms). It would be interesting to resume the different advantages and disadvantages of each category in relation to field application (e.g. problem of heavy metals accumulation; growth-defense trade-off effects of hormones, difficulty to control beneficial microbial inoculum in open field etc.). Maybe this can be done through a table. In direct link with this, I think it would be important to talk some more about all the potential drawbacks of these treatments in the text, as I find it too much unbalanced towards the positive effects.

Answer: a new section dedicated to these questions (section 5) was added.

In Chapter 2 the authors cite the impact of chemical modifications on stilbenes biocidal activity (hydroxylation, methylation, oligomerization). Is it known what are effects of such modifications on the mechanism of action of stilbenes? Do the authors have some hypotheses to advance in this sense?

Answer: some data regarding these aspects were added at the end of section 2.

- The conclusion part is very long and doesn’t add much to the manuscript. All the text between L 733-792 can be just reduced to a couple of sentences summing up the advantages and disadvantages of the different treatments. On the other hand, there is no mention for further research directions. What questions remains to be answered to achieve effective phytoalexin stimulation in field conditions? What kind of experiments can be designed in this sense? What are the most critical knowledge gaps to be filled?

Answer: Some parts of the conclusion were deleted (see the new text lines) and some perspectives were also integrated at the end of the conclusion section.

 MINOR COMMENTS

ABSTRACT

L23-25: Please reformulate this sentence in a clearer manner.

Answer: Correction was done to the manuscript directly.

INTRODUCTION

L 52-53: “ferment of activity” is a very weird expression.

Answer: Correction was done to the manuscript directly.

L 65: Please replace “no doubt” with “without doubt”

Answer: Correction was done to the manuscript directly.

Chapter 2

L 93: Please correct the use of the commas in this sentence.

Answer: Correction was done to the manuscript directly.

L 94: Please avoid the use of improper metaphors. Something with a well-defined location, such as a cellular compartment or a defined group of cells, can be compared to a seat, not a molecule.

Answer: Correction was done to the manuscript directly.

L 189-190: Far-fetched comparison. The human disease mentioned do not have microbial basis, therefore the molecular mechanisms are unlikely to be comparable with those of plant diseases.

Answer: This sentence was deleted.

Chapter 3

L257-259: Please correct the use of commas in this sentence.

Answer: Correction was done to the manuscript directly.

L275: “In the attempt to…” rather than “In attempting to…”

Answer: Correction was done to the manuscript directly.

L292: It is Reactive Burst Oxidase Homolog, and the acronym is RBOH (not Homologue and RbOH). Please correct thoroughly in the text. Authors should also specify that the mentioned “activation” refers to the enzymatic activity and not gene expression, thus making not possible to determine which isoform is responsible for the observed effect. Indeed, the authors should not refer to RBOHs as one protein, given that it is a multigenic family (at least that studies on a specific isoform are mentioned). In general, the paragraph citing RBOHs should be revised. These enzymes have important roles in plant immunity and in the defense priming process and this is not mentioned at all.

Answer: Corrections were done to the manuscript directly (see lines) and this part was partially re-written including some new elements.

L 368: remove point after “leaves”

Answer: Correction was done to the manuscript directly.

L 398 and rest of the text: MeJA, not MeJa.

Answer: Corrections were done to the manuscript directly

L 556-558: If the tagatose-based product induced just a slight increase in stilbenes accumulation (so probably not responsible of the protective effect), then I ask the authors why it is worth to report this study in this review? Perhaps it should be mentioned much more succinctly?

Answer: Yes, you are right. Mentions to these studies have been kept but resumed.

Chapter 4

L 663-673: Remark similar to the one above (L556-558).

Answer: Yes, you are right. Mention to these studies have been kept but resumed.

CONCLUSION

L 721-724: This is a good critical remark, I think it would be good to develop it bit more as it will give more critical depth to the discussion, e.g. are there some common features between the studies reporting negative and positive correlations between stilbenes accumulation and disease protection?

Answer: The response is not simple. A tentative explanation was added.

 

Comments on the Quality of English Language

- I recommend revising the grammar of the first part of this manuscript, notably the introduction and the second chapter. Although the vocabulary is of good quality, the construction of the sentences is not so straightforward and hinders a smooth reading, therefore decreasing the overall attractiveness of the text. Overall, I recommend being more concise and avoid redundancies.

Answer: We tried to shorten and to modify some sentences especially in the introduction section and the second chapter.

 

Author Response File: Author Response.pdf

Reviewer 2 Report

It is a very exhaustive review on the possible application of phytoalexins in the management of grapevine disease. 

I added just a reference (reference numbers have to be modified accordingly) and made very minor text editings (see attached file) 

Comments for author File: Comments.pdf

The English style is fine

Author Response

Preliminary Remark

First of all, we thank the four reviewers for their in-depth analysis of the manuscript and for their comments done in a very short time.

 

Reviewer 2

I added just a reference (reference numbers have to be modified accordingly) and made very minor text editings (see attached file)

Answer: your comments have been taken into account and the new reference was added.

Author Response File: Author Response.pdf

Reviewer 3 Report

The review that is made in this manuscript is describing the situation for the topic selected, some inappropriate wording is used such as contamination instead of infection and others marked in the enclosed annotate copy of the manuscript. Some other comments should be answered they are all in the manuscript annotated version.

Comments for author File: Comments.pdf

See remarks in the annotated version of the manuscript provided.

Author Response

Preliminary Remark

First of all, we thank the four reviewers for their in-depth analysis of the manuscript and for their comments done in a very short time.

 

Reviewer 3

The review that is made in this manuscript is describing the situation for the topic selected, some inappropriate wording is used such as contamination instead of infection and others marked in the enclosed annotate copy of the manuscript. Some other comments should be answered they are all in the manuscript annotated version.

Answer: Most comments have been addressed (see the revised manuscript). Recommendations made by the Reviewer to delete certain parts regarding the description of stilbene synthesis have not all been taken into account, as we considered them necessary for the understanding of the paper for researchers who are not familiar with stilbene chemistry.

Author Response File: Author Response.pdf

Reviewer 4 Report

The current review entitled “Use of Elicitors and Beneficial Bacteria to Induce and Prime the Stilbene Phytoalexin Response: Main Experiments and Applications to Grapevine Disease Resistance” reviewed the experiments conducted in this realm over the past three decades. It underscores that the observed protective effects against pathogens are typically associated with the induction and priming of grapevine phytoalexin responses, confirming the interest of using, in a more general way, stimulation of the production of phytoalexins in plants as a basis for crop protection.

Comments:

The specific mechanisms governing the induction of stilbene phytoalexin synthesis through both organic and inorganic metallic salts in grapevines need to be thoroughly explored in section 3.1, "Organic and Inorganic Metallic Salts."

Section 3.1 extensively discusses various studies related to the induction of stilbene phytoalexin synthesis using chemicals linked to grapevine disease resistance. However, it's important to address not only the connection between these chemicals and stilbene production but also the practical application of these chemicals in terms of their protective effects.

Section 3.2. This section discussed the relationship between phytohormone derivatives and the enhancement of grapevine disease resistance through stilbene phytoalexin synthesis. It is acknowledged that phytohormone derivatives have multifaceted mechanisms for stimulating grapevine's natural defense systems. To provide clarity, the initial part of this section should specify which pathways will be considered.

Tables 1-4 consider the most strength points of the current review which summarized the primary objectives of inducing stilbene phytoalexin synthesis through chemicals associated with grapevine disease resistance, enhancing grapevine disease resistance via phytohormone derivative-induced stilbene phytoalexin synthesis, utilizing bio-elicitors for grapevine protection and fostering phytoalexin responses, and managing grapevine diseases through beneficial organisms that trigger phytoalexin synthesis. However, the authors should consider most of the published papers over the past three decades within these tables.

Some paragraphs were thoroughly written as text Bold. All text should be written based on the journal guideline.

Minor editing of English language required

Author Response

Preliminary Remark

First of all, we thank the four reviewers for their in-depth analysis of the manuscript and for their comments done in a very short time.

 

Reviewer 4

The specific mechanisms governing the induction of stilbene phytoalexin synthesis through both organic and inorganic metallic salts in grapevines need to be thoroughly explored in section 3.1, "Organic and Inorganic Metallic Salts."

Answer: These mechanisms have been thoroughly discussed in the light of the recent work of Wang et al. (Hort. Res., 2022). See section 3.1.

Section 3.1 extensively discusses various studies related to the induction of stilbene phytoalexin synthesis using chemicals linked to grapevine disease resistance. However, it's important to address not only the connection between these chemicals and stilbene production but also the practical application of these chemicals in terms of their protective effects.

Answer: I think this has been done for all eliciting treatments: we considered both the effects of this treatment on responsive defense genes including the phytoalexin response and in parallel, the levels of protection of the treatments towards the pathogens were given, generally expressed as percentages of reduction of the diseases both in the text and the tables.

Section 3.2. This section discussed the relationship between phytohormone derivatives and the enhancement of grapevine disease resistance through stilbene phytoalexin synthesis. It is acknowledged that phytohormone derivatives have multifaceted mechanisms for stimulating grapevine's natural defense systems. To provide clarity, the initial part of this section should specify which pathways will be considered.

Answer: Yes, you are perfectly right. The specific pathways considered were briefly notified at the beginning of section 3.2.

Tables 1-4 consider the most strength points of the current review which summarized the primary objectives of inducing stilbene phytoalexin synthesis through chemicals associated with grapevine disease resistance, enhancing grapevine disease resistance via phytohormone derivative-induced stilbene phytoalexin synthesis, utilizing bio-elicitors for grapevine protection and fostering phytoalexin responses, and managing grapevine diseases through beneficial organisms that trigger phytoalexin synthesis. However, the authors should consider most of the published papers over the past three decades within these tables.

Answer: You are right. We deleted two references from Table 2 which did not mention about phytoalexin production in their studies. However, old works on fosetyl-Al which date back 1980 and 1989 were conserved as they constitute important studies in this area.

Some paragraphs were thoroughly written as text Bold. All text should be written based on the journal guideline.

Answer: This was probably due to a conversion of the original word doc during submission. Corrections were made directly to the text.

 

Author Response File: Author Response.pdf

Round 2

Reviewer 1 Report

I would like to thank the authors for taking into account my suggestions, I believe that the manuscript has greatly benefited from this round of revision and I'm happy to have been of help.  

The English is of good quality. I recommend to go through the text once again to detect potential typos before the publication.

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