Bacterial Plant Biostimulants: A Sustainable Way towards Improving Growth, Productivity, and Health of Crops

Round 1

Reviewer 1 Report

The authors reviewed the bacterial plant biostimulants as a sustainable way for improving growth, productivity and health of crops. The article is well written and informative, however there are some faults that need attention before the article being published. Please see mu comments and suggestions below.

As a general observation the abstract is too long, maybe the authors can try to shorten it and transfer part of it to Introduction.

Line 83 The authors can introduce one more reference there (DOI: 10.1007/s13762-020-02818-6) that is related to abiotic stresses and the interaction of plant with the environment.

Please present at the end of the introduction the scope of the article and the originality. Also please mention how the articles were search and selected and what is the period covered by the review.

Based on which information Table 1 was created. Shouldn't the authors mention some references?

What is the source of Figure 2? Was created by the authors, of adapted from another study? In the second case the authors need reference and permission to use it. Moreover, in Figure 2, in the part related to abiotic stress “secondary metabolites” should be added. Please see the reference suggested before.

Table 2 please insert one more column at the end and mention the adequate references for each line

Line 148 – please put a reference at the end of the paragraph

Line 183 186 and 219 – please put references at the end of the sentences

Line 315 – put a space in front of ref [94]

Table 3 and Table 4 – the same comment as for Table 2

Line 374 – put a reference (or more) at the end of the paragraph

Line 321 – please mention the role of VOCs in attracting pollinators

Lines 324-327 the authors wrote “These include benzene, cyclohexane, 2-(benzyloxy)-1-ethanamine, methyl, dodecane, decane, 1-(N-phenyl carbamyl)-2 morpholinocyclohexene, benzene (1-methylnonadecyl), dotriacontane 1-chlorooctadecane, tetradecane, and 11-decyldocosane although, their type and quantities released varies among different species [118].” This is not correct, because the mentioned components are not fitting with the classes mentioned before “alcohols, aldehydes, hydrogen cyanide (HCN), sulfides and ketones” (in lines 392-393). For example, cyclohexane, dodecane, decane, dotriacontane, tetradecane, and 11-decyldocosane are alkanes; 2-(benzyloxy)-1-ethanamine is an amine; methyl is just an organic radical that does not exist as an standalone component, HCN is an acid not a class of components, etc. Please revise and correct this part.

Line 427 – please put a reference at the end of the sentence

Line 449 - reference at the end of the sentence

Line 455 - reference at the end of the sentence

In the paragraph between the lines 465-474, please reference every idea, but not the whole paragraph at the end.

Conclusions part is too long. I suggest the authors to condense it.  

Minor comments

Line 30 – put a space before “Plants”

Line 118 – probably is better to put the reference [19] at the end of paragraph.

Line 329 – put a reference at the end of the sentence.

Line 352 – delete the space after [100], and put it in front of “heavy metals”

Probably no free line should be kept between the lines 449-450

Line 463 – put a dot at the end of the sentence

Probably no free line should be kept between the lines 518-519

Probably no free line should be kept between the lines 529-530

Author Response

The authors are thankful to the reviewer for excellent reviewing and valuable suggestion for the improvement of the review article. Please find the response for each query and suggestion. We, the authors have incorporated the changes as recommended by the reviewer.

 

Major Comments

• As a general observation the abstract is too long, maybe the authors can try to shorten it and transfer part of it to Introduction.

Authors’ Response: Agreed and as suggested abstract is shortened to Line 28-48 and some of the part of it is transferred to Introduction at Line 82-86.

.

• Line 83 The authors can introduce one more reference there (DOI: 10.1007/s13762-020-02818-6) that is related to abiotic stresses and the interaction of plant with the environment.

Authors’ Response: The said reference has been cited [Ref. 23] in the text. Line No. 102.

 

• Please present at the end of the introduction the scope of the article and the originality. Also please mention how the articles were search and selected and what is the period covered by the review.

Authors Response: The suggestion has been incorporated as

The present review describes the recent knowledge concerning the beneficial BPBs and their role in improving the crop health through various mechanisms. The article concludes by highlighting the main findings of an in-depth analysis of research articles published between 2015 and 2020, sorted using different data bases like Google Scholar, Science direct, Pub Med, Web of Science etc. Line No. 112-116.

 

• Based on which information Table 1 was created. Shouldn't the authors mention some references?

Authors Response: Table 1 was compiled based on the information obtained from various websites of some major bioformulation making companies and markets. As suggested the pertinent references have been cited in the caption of Table 1. Line No. 137.

 

• What is the source of Figure 2? Was created by the authors, of adapted from another study? In the second case the authors need reference and permission to use it. Moreover, in Figure 2, in the part related to abiotic stress “secondary metabolites” should be added. Please see the reference suggested before.

Authors Response: The figure has been conceptualized and created by authors after in-depth literature survey and has not been adopted from any other source. Also, the fig. 2 has been updated, in the part related to abiotic stress “secondary metabolites” has been added and suggested reference has been added.

 

• Table 2 please insert one more column at the end and mention the adequate references for each line

Authors Response: The table has been edited as recommend by the reviewer and one more column has been inserted at the end and the adequate references have been mentioned.

 

• Line 148 – please put a reference at the end of the paragraph

Authors Response: Reference [Ref.  44] has been incorporated at the end of paragraph. Line. 171

 

• Line 183 186 and 219 – please put references at the end of the sentences

  Authors Response:  As suggested, references [Refs. 62, 63 and 73] have been cited at the Line 202, 208 and 241.

 

• Line 315 – put a space in front of Ref [94]

   Response: A space has been added in front of reference 111 (earlier No. 94). Line 337.

 

• Table 3 and Table 4 – the same comment as for Table 2

Authors Response:  One column of references has been inserted in and pertinent references have been placed in the reference column of Table 3 and Table 4

 

• Line 374 – put a reference (or more) at the end of the paragraph

   Response: Reference [No.129] has been incorporated. Line 395

 

• Line 321 – please mention the role of VOCs in attracting pollinators

Authors Response:  The role of VOCs in attracting pollinators has been incorporated. Lines 422-424.

 

• Lines 324-327 the authors wrote “These include benzene, cyclohexane, 2-(benzyloxy)-1-ethanamine, methyl, dodecane, decane, 1-(N-phenyl carbamyl)-2 morpholinocyclohexene, benzene (1-methylnonadecyl), dotriacontane 1-chlorooctadecane, tetradecane, and 11-decyldocosane although, their type and quantities released varies among different species [118].” This is not correct, because the mentioned components are not fitting with the classes mentioned before “alcohols, aldehydes, hydrogen cyanide (HCN), sulfides and ketones” (in lines 392-393). For example, cyclohexane, dodecane, decane, dotriacontane, tetradecane, and 11-decyldocosane are alkanes; 2-(benzyloxy)-1-ethanamine is an amine; methyl is just an organic radical that does not exist as an standalone component, HCN is an acid not a class of components, etc. Please revise and correct this part.

Authors Response:  This part has been revised. Lines 413-417

 

• Line 427 – please put a reference at the end of the sentence

   Authors Response:  Reference [No. 148] has been incorporated. Line No.449

 

• Line 449 - reference at the end of the sentence

   Authors Response:  Reference [No. 154] has been incorporated. Line No.478

• Line 455 - reference at the end of the sentence

Authors Response:  Reference [No. 155] has been incorporated. Line No.478

 

• In the paragraph between the lines 465-474, please reference every idea, but not the whole paragraph at the end.

Authors Response: The whole section has been modified as suggested by Reviewer 3, every idea has been cited with a relevant reference.

 

• Conclusions part is too long. I suggest the authors to condense it.

Authors Response:  Conclusion part is re-written as suggested by Reviewer 3, and now condensed.

 

Minor comments

• Line 30 – put a space before “Plants”

   Authors Response:  A space has been incorporated before “Plants”.

 

• Line 118 – probably is better to put the reference [19] at the end of paragraph.

Authors Response:  Reference is not fitting with meaning of whole sentence but needful insertion has been made to keep the coherence. Line No.146

 

• Line 329 – put a reference at the end of the sentence.

Authors Response:  References [No. 44,114] have been added at the end of the sentence. Line 351

 

• Line 352 – delete the space after [100], and put it in front of “heavy metals”

Authors Response:  Space has been deleted. Line No.373

 

• Probably no free line should be kept between the lines 449-450

   Authors Response:  The free space has been deleted and this section has been modified as suggested by reviewer 3.

 

• Line 463 – put a dot at the end of the sentence

 Authors Response:  This section has been modified as suggested by reviewer 3.

 

 

• Probably no free line should be kept between the lines 518-519

  Authors Response: This section has been modified as suggested by reviewer 3 and unnecessary free spaces have been deleted.

 

• Probably no free line should be kept between the lines 529-530

Authors Response:  This section has been modified as suggested by reviewer 3 and unnecessary free spaces have been deleted.

Author Response File: Author Response.docx

Reviewer 2 Report

The Review entitled "Bacterial plant biostimulants: A sustainable way towards improving growth, productivity and health of crops" features as a review of the many demonstrate that the inoculation of PGPR improve the plant development grown and health under biotic and abiotic stress conditions by via physiological, biochemical and molecular. As the authors describe, the literature reports many information’s on the role of this PGPR in multiple functional roles. Hence the importance of the review which reports in a very well manner some molecular aspects of the role of this mechanisms. The figures and schemes show a good review and are very well descriptive; the language is clear and the text is well structured. The purpose of the review is to lay the foundations for future understandings of the resource for research focused on the development of biochemical and genetic of growth and tolerance mechanisms to combat adverse conditions. The review, however, must be improved in terms of writing since some grammar and syntax errors are present in the manuscript. They should address the subject and critically review the information from the literature.

Main textual comments:

In the introduction, I suggest insertion a paragraph, reporting the constant changes in the environment (with emphasis on rising temperatures and scarcity of rain).

When dealing with abiotic stresses, change "resistance" to "tolerance" when dealing with water stress. i.e. It is impossible to have a plant that survives in the total absence of water (resistance).

The authors need to make it very clear, what are the adverse conditions that can lead to resistance and those that can cause tolerance. Items 3.6; 3.6.1; 3.6.2 are very confused.

In my opinion, the authors do not report anything about mitigating abiotic conditions, which can lead the plant to develop an induced systemic tolerance (IST). Please discuss induced systemic tolerance.

The manuscript does not mention that after inoculation of plants by PGPR, induction of systemic resistance was already described by Alquéres et al. in MPMI 26(8):937-945, 2013. As kind of elicitor of this plant response, N-acyl-homoserine lactones, produced by PGPR, are possible candidates, because these bacterial signalling compounds are able to induce systemic tolerance (IST) responses in colonized plants.

Changes under drought conditions have already been observed, since it has already been shown that PGPR can induce systemic tolerance (IST) in rice. The N-acyl-homoserine lactones (AHLs), produced by PGPR, may mediate this plant response to abiotic stress, since AHLs alone induce systemic tolerance towards anti-stress responses. (review and quote: Filgueiras, L.; Silva, R.; Almeida, I.; Vidal, M.; Baldani, JI; Meneses, CHSG. Gluconacetobacter diazotrophicus mitigates drought stress in Oryza sativa L.. Plant Soil 451, 57–73 (2020). https://doi.org/10.1007/s11104-019-04163-1.

Table 3: Review and quote: Silva, R.; Filgueiras, L.; Santos, B.; Coelho, M.; Silva, M.; Estrada-Bonilla, G.; Vidal, M.; Baldani, JI; Meneses, C., 2020. Gluconacetobacter diazotrophicus changes the molecular mechanisms of root development in Oryza sativa L. growing under water stress. Int. J. Mol. Sci. 21, 333. https://doi.org/10.3390/ijms21010333

 

Table 3: Review and quote: Filgueiras, L.; Silva, R.; Almeida, I.; Vidal, M.; Baldani, JI; Meneses, CHSG. Gluconacetobacter diazotrophicus mitigates drought stress in Oryza sativa L.. Plant and Soil 451, 57–73 (2020). https://doi.org/10.1007/s11104-019-04163-1

 

Table 3: Review and quote: Moreno-Galván, A.; Romero-Perdomo, F.A.; Estrada-Bonilla, G.; Meneses, C.H.S.G.; Bonilla, R.R. Dry-Caribbean Bacillus spp. Strains Ameliorate Drought Stress in Maize by a Strain-Specific Antioxidant Response Modulation. Microorganisms 2020, 8, 823. https://doi.org/10.3390/microorganisms8060823

There are several current works showing the effect of the PGPR ameliorates the effects of abiotic stress. I suggest updating the references with current references.

Nothing for proline, Glycine-betaine and trehalose? There are several studies reporting the activity of this compounds in mitigating abiotic stress.

Rewrite the conclusion! It needs to be much improved.

There are several other responses mitigated by PGPR in plants that were not mentioned in the review. Authors should make a great effort to leave the review complete.

Author Response

Excellent review on Biologicals - the most important subject in global agriculture.  Very comprehensive and detailed on bacteria species, modes of action and physiological impact on crop production. This review also impacts global soil health, critical for sustainable crop production. Literature review very comprehensive.

 

Authors’ Response: The authors are thankful to the reviewer for excellent reviewing and appreciation

Author Response File: Author Response.docx

Reviewer 3 Report

Excellent review on Biologicals - the most important subject in global agriculture.  Very comprehensive and detailed on bacteria species, modes of action and physiological impact on crop production. This review also impacts global soil health, critical for sustainable crop production. Literature review very comprehensive.

Author Response

The authors are thankful to the reviewer for excellent reviewing and valuable suggestion for the improvement of the review article. Please find the response for each query and suggestion. We, have incorporated the changes as recommended by the reviewer.

 

Major textual comments

• In the introduction, I suggest insertion a paragraph, reporting the constant changes in the environment (with emphasis on rising temperatures and scarcity of rain).

 

Authors Response: Agreed and as suggested, a paragraph reporting the constant changes in the environment (with emphasis on rising temperatures and scarcity of rain) has been inserted in the introduction. Line No. 51-72.

 

• When dealing with abiotic stresses, change "resistance" to "tolerance" when dealing with water stress. i. e. It is impossible to have a plant that survives in the total absence of water (resistance).

 

Authors Response: Agreed and as suggested, necessary changes have been made. Line No. 296, 309.

 

• The authors need to make it very clear, what are the adverse conditions that can lead to resistance and those that can cause tolerance. Items 3.6; 3.6.1; 3.6.2 are very confused.

 

Authors Response: As suggested the comment has been addressed and all the necessary changes have been incorporated. The sections 3.6; 3.6.1; 3.6.2 has been entirely modified. Line No. 458-536.

 

4)      In my opinion, the authors do not report anything about mitigating abiotic conditions, which can lead the plant to develop an induced systemic tolerance (IST). Please discuss induced systemic tolerance.

                            

Authors Response:  As suggested the comment has been reported and IST has been discussed in separate Section 3.6.3. Line No. 539-569.

 

5)       The manuscript does not mention that after inoculation of plants by PGPR, induction of   systemic resistance was already described by Alquéres et al. in MPMI 26(8):937-945, 2013. As kind of elicitor of this plant response, N-acyl-homoserine lactones, produced by PGPR, are possible candidates, because these bacterial signalling compounds are able to induce systemic tolerance (IST) responses in colonized plants.

 

Authors Response: As suggested the comment has been addressed and the pertinent reference [178] has been cited in Section 3.6.2. Line No. 535.

 

6)       Changes under drought conditions have already been observed, since it has already been shown that PGPR can induce systemic tolerance (IST) in rice. The N-acyl-homoserine lactones (AHLs), produced by PGPR, may mediate this plant response to abiotic stress, since AHLs alone induce systemic tolerance towards anti-stress responses. (review and quote: Filgueiras, L.; Silva, R.; Almeida, I.; Vidal, M.; Baldani, JI; Meneses, CHSG. Gluconacetobacter diazotrophicus mitigates drought stress in Oryza sativa L.. Plant Soil 451, 57–73 (2020). https://doi.org/10.1007/s11104-019-04163-1

        

           Authors Response: As suggested the pertinent reference has been reviewed and quoted in Section 3.6.3. Recent references for AHLs elicited IST (in abiotic stress) and ISR (in biotic stress) has also been incorporated in sections 3.6.3 [Ref. 182] and 3.6.2 [Ref. 174], respectively. Line No. 563, 524.

 

7)      Table 3: Review and quote: Silva, R.; Filgueiras, L.; Santos, B.; Coelho, M.; Silva, M.; Estrada-Bonilla, G.; Vidal, M.; Baldani, JI; Meneses, C., 2020. Gluconacetobacter diazotrophicus changes the molecular mechanisms of root development in Oryza sativa L. growing under water stress. Int. J. Mol. Sci. 21, 333. https://doi.org/10.3390/ijms21010333.

          

            Authors Response: As suggested, the pertinent reference has been reviewed and quoted in Table 3.

8)        Table 3: Review and quote: Filgueiras, L.; Silva, R.; Almeida, I.; Vidal, M.; Baldani, JI; Meneses, CHSG. Gluconacetobacter diazotrophicus mitigates drought stress in Oryza sativa L.. Plant and Soil 451, 57–73 (2020). https://doi.org/10.1007/s11104-019-04163-1 4)

           Authors Response: As suggested, the relevant reference has been reviewed and quoted in Table 3.

 

• Table 3: Review and quote: Moreno- Galván, A.; Romero-Perdomo, F.A.; Estrada-Bonilla, G.; Meneses, C.H.S.G.; Bonilla, R.R. Dry-Caribbean Bacillus Strains Ameliorate Drought Stress in Maize by a Strain-Specific Antioxidant Response Modulation. Microorganisms 2020, 8, 823. https://doi.org/10.3390/microorganisms8060823

 

            Authors Response: As suggested, the relevant reference has been reviewed and quoted in Table 3.

 

• There are several current works showing the effect of the PGPR ameliorates the effects of abiotic stress. I suggest updating the references with current references.

 

       Authors Response: A suggested, the references [Ref no. 23, 29-31,62,63,73, 92-96, 151-153, 159-161, 172-174, 179-184] of current works have been updated in the manuscript. Line No. 102, 33, 206, 208, 241, 304, 464, 467, 471, 490, 493, 496, 515, 520, 524, 551, 554, 561, 563, 564, 569.

 

• Nothing for proline, Glycine-betaine and trehalose? There are several studies reporting the activity of this compounds in mitigating abiotic stress.

 

Authors Response: As suggested, the necessary comment has been addressed and incorporated in Table 3

 

• Rewrite the conclusion! It needs to be much improved.

 

        Authors Response: As suggested, the conclusion has been rewritten. Line No. 570-599.

 

• There are several other responses mitigated by PGPR in plants that were not mentioned in the review. Authors should make a great effort to leave the review complete.

 

     Authors Response: As suggested, the necessary comment has been addressed.

Author Response File: Author Response.docx

Round 2

Reviewer 1 Report

The authors addressed all my requirements, and justified reasonable all their answers. The manuscript is considerably improved and clearer. I suggest to be accepted in the present form.

Reviewer 2 Report

Thanks for attending all the suggestions. The manuscript has been significantly improved. In view of the above, I believe that the review presents robust and consolidated content, bringing to light new information on changes Induced by bacterial plant biostimulants in crops plants. I consider that the work has enough quality to be considered for publication in Sustainability (MDPI).