Diversity, Ecological Characteristics and Identification of Some Problematic Phytopathogenic Fusarium in Soil: A Review

Round 1

Reviewer 1 Report

Dear Authors,

The article is very important for the management of Fusarium wilt. I would like authors to include few images of Fusarium morphology which indicates how difficult to identify the pathogen with supporting molecular data. If you include these data it will be very useful for the readers and scientist who are actively involved in the research. 

Regards

 

Author Response

Thank you for your recommendations.

We included a Supplementary figure 1 to demonstrate most important morphological features of different Fusarium species and Supplementary table 1 with information about morphology of 8 Fusarium species.

Also we included the link to the article where the most recent Fusarium phylogeny is presented (Lines 83-84).

The link to these supporting files is in Lines 55-57

Reviewer 2 Report

This manuscript aims to present a synthesis of knowledge to date of the diversity and ecological characteristics of the genus Fusarium, an important fungal genus, in terms of both abundance and distribution in the world and in terms of its role in the functioning of agrosystems, and even that of human and animal health. The objective is ambitious and the task colossal knowing that books devoted to this genus  as well as Fusarium laboratory manuals, have already been published with, of course, different inclinations but also a sum of information that is difficult to summarize, a fortiori because new knowledge must participate in this update (most of the books are decades old). I would have liked to be able to salute the initiative of the authors of this manuscript. Unfortunately, the proposed synthesis is too general, does not go deep enough because of both the diversity of the genus Fusarium and the multiplicity of situations in which species of this genus are involved.

The manuscript is structured in six main sections including the conclusion, two of the sections (4- Fusarium control and soil suppressiveness against Fusarium fungi and 5 - Research and diagnostics of phytopathogenic Fusarium) are themselves subdivided into two parts

The first section relating to the systematics of the genus Fusarium is the most interesting, the most complete and the most accomplished of the six sections included in this manuscript. After a brief history retracing the hazards from the first description of the genus to the still vague one proposed today, it highlights with relevance the differences between the different groups of researchers on the real definition of species within the genus, on the concept of species complex and on the necessary complementarity of morphological, metabolomic and genetic approaches to characterize species. The authors rely on a recent and relevant bibliography and in this way invite readers to consult the articles cited to understand the reasons justifying the difficulties encountered.

The section two dedicated to the ecology of Fusarium is very vague and not very informative from lines 85 to 115. (I am not sure of the stenotopic character of F. graminearum but the quoted reference is not accessible). On the other hand, the second part of this section is based on examples and factual data that are much more informative when it comes to the ecological requirements of Fusarium in relation to the production of mycotoxins but also in relation to saprotrophic development in the soil. Table 1 is much too incomplete to be presented in a review of Fusarium. The host spectrum of the Fusarium species presented in this table is much broader (eg the vegetable plants infested by F. oxysporum are not even mentioned) than the restrictive one proposed by the authors. How do the authors justify the choice of these nine species? This table is all the more incongruous as table 2 resumes, with more details as to the host spectra and with a greater number of species, the information provided by this table 1

Section three focuses on the importance of Fusarium in agriculture through the production of mycotoxins by most species of this genus. In citing the main Fusarium diseases (line 213) the authors forget to mention Fusarium Head blight, a disease caused by the most mycotoxin-producing Fusarium species. Table 2 from the excellent review by Munkwold et al., 2021 includes some gaps. As long as you take the information, you might as well make sure they are complete. Thus, for example, the authors cite only four of the eight mycotoxins produced by F. sporotrichioides, five of those produced by F. poae, three of the five produced by F. venenatum,... they limit the habitat of F. proliferatum to tropical regions while this fungus causes serious problems in temperate regions on garlic, asparagus, maize..., the host spectrum of F. oxysporum includes more than 105 plant species (= number of forma speciales currently recognized), the habitat of many Fusarium is the soil...

 

Section four : Diseases caused by Fusarium do not only concern cereals and are not all associated with the production of mycotoxins. Fusarium wilt caused by F. oxysporum, root or crown rots caused by F. oxysporum f. sp. radicis ... and by F. solani are examples. Lines 315-320 are not clear enough.

The sub-section devoted to the suppressive soil is interesting, based on several relevant references but contains inaccuracies. Thus, the first line defines the suppressive character of a soil as its ability to eliminate pathogenic agents, then, the next line, the definition of the suppressiveness of a soil specifies that the pathogenic agent is present in the soil but cannot express its pathogenic activity.  Line 382: why cite reference 67 and not have it numbered 54? Line 386: What was shown in Bubici et al., 2019 concerned F. oxysporum f. sp. cubense, not all the Fusarium. Do not generalize too quickly.  Line 408: This is not always true, soil suppressiveness can to a soil-borne disase also be acquired by monoculture. This was the case of take-all decline in wheat (Berendsen et al., 2012 doi: 10.1016/j.tplants.2012.04.001; Schlatter et al., 2017 doi.org/10.1094/PHYTO-03-17-0111- RVW). True, the pathogen is Gaeumannomyces graminis var. tritici and not Fusarium (the same has been observed for beet damping-off caused by Rhizoctonia solani. Mendes et al., 2011 doi: 10.1126/science.1203980) but it should be mentioned that this situation also exists.

Section 5

Line 439:  vegetation experiment ? not clear

I am surprised that it is the ref of Goncharov et al 2020 (11) which is cited for the practical aspects concerning the inoculums whereas this reference is a meta-analysis (admittedly well done) but I would have preferred a reference belonging to laboratory work

Line 485: tef-1-a identifies more species than the eight listed

lines 506-513 are unnecessary in this paragraph

Lines 539-543: Why bring it all back to mycotoxins ?

Table 3 is a partial copy-paste of the table published by Rampersad, 2020. The latter at least had the kindness to cite his sources, i.e. the ref, in his table!!!

line 561: why is the reference not numbered, and not available in the list at the end of the manuscript

 

Conclusion

The initiative of this manuscript is undoubtedly commendable but the realization is not up to the ambitions. The authors cite several recent and relevant references but which are themselves reviews, some of which are very complete but do not seek to cover the entire genus and characteristics of Fusarium. Authors should limit themselves either to a group of Fusarium (such as pathogenic Fusarium of cereals, including the production of mycotoxins), or to a characteristic of this group (such as soil suppressiveness), or to the identification of Fusarium both in complex media (soil, plants,...) and with problematic isolates with analysis of available methods and gaps in this area.

This manuscript is certainly correctly written and has undoubtedly required a lot of redaction work, but it does not really bring new information, it remains very general, like an overview of the question without any real questioning about the role, the place of this fascinating genus in the functioning of agrosystems as the title of the manuscript suggested

 

Author Response

Dear reviewer,

Thank you very much for this comprehensive and detailed revision. We hope that our corrections according to your recommendations improved our manuscript. In our review, we mostly focused on Fusarium pathogens of cereal crops, their ecological features, and potential ways of its identification. Also we aimed to describe the ways to reduce the spread and severity of Fusarium-borne diseases, including soil suppressiveness to Fusarium pathogens. We believe that the information summarized in the manuscript could be valuable for readers that are not yet familiar with complications of Fusarium taxonomy and detection.

R2 The first section relating to the systematics of the genus Fusarium is the most interesting, the most complete and the most accomplished of the six sections included in this manuscript. After a brief history retracing the hazards from the first description of the genus to the still vague one proposed today, it highlights with relevance the differences between the different groups of researchers on the real definition of species within the genus, on the concept of species complex and on the necessary complementarity of morphological, metabolomic and genetic approaches to characterize species. The authors rely on a recent and relevant bibliography and in this way invite readers to consult the articles cited to understand the reasons justifying the difficulties encountered.

> Thank you for the comments. We added the fresh information regarding the Fusarium phylogeny and morphology according to the recommendations of another reviewer

R2 The section two dedicated to the ecology of Fusarium is very vague and not very informative from lines 85 to 115. (I am not sure of the stenotopic character of F. graminearum but the quoted reference is not accessible). On the other hand, the second part of this section is based on examples and factual data that are much more informative when it comes to the ecological requirements of Fusarium in relation to the production of mycotoxins but also in relation to saprotrophic development in the soil. Table 1 is much too incomplete to be presented in a review of Fusarium. The host spectrum of the Fusarium species presented in this table is much broader (eg the vegetable plants infested by F. oxysporum are not even mentioned) than the restrictive one proposed by the authors. How do the authors justify the choice of these nine species? This table is all the more incongruous as table 2 resumes, with more details as to the host spectra and with a greater number of species, the information provided by this table 1

> We decided to remove the Table 1, because the Table 2 also contains the information regarding host plants

Also, we shortened the section from lines 85 to 115 and moved it to the second paragraph of the section

R2 Section three focuses on the importance of Fusarium in agriculture through the production of mycotoxins by most species of this genus. In citing the main Fusarium diseases (line 213) the authors forget to mention Fusarium Head blight, a disease caused by the most mycotoxin-producing Fusarium species. Table 2 from the excellent review by Munkwold et al., 2021 includes some gaps. As long as you take the information, you might as well make sure they are complete. Thus, for example, the authors cite only four of the eight mycotoxins produced by F. sporotrichioides, five of those produced by F. poae, three of the five produced by F. venenatum,... they limit the habitat of F. proliferatum to tropical regions while this fungus causes serious problems in temperate regions on garlic, asparagus, maize..., the host spectrum of F. oxysporum includes more than 105 plant species (= number of forma speciales currently recognized), the habitat of many Fusarium is the soil...

>We added the information regarding Fusarium head blight and also added more information to Table 2.

R2 Section four : Diseases caused by Fusarium do not only concern cereals and are not all associated with the production of mycotoxins. Fusarium wilt caused by F. oxysporum, root or crown rots caused by F. oxysporum f. sp. radicis ... and by F. solani are examples. Lines 315-320 are not clear enough.

>We changed the text in lines 315-320

R2 The sub-section devoted to the suppressive soil is interesting, based on several relevant references but contains inaccuracies. Thus, the first line defines the suppressive character of a soil as its ability to eliminate pathogenic agents, then, the next line, the definition of the suppressiveness of a soil specifies that the pathogenic agent is present in the soil but cannot express its pathogenic activity.

>We changed the text to make it clear. Supression doesn’t mean full elimination.

 R2 Line 382: why cite reference 67 and not have it numbered 54?

>we checked the reference numbers throughout the manuscript

R2 Line 386: What was shown in Bubici et al., 2019 concerned F. oxysporum f. sp. cubense, not all the Fusarium. Do not generalize too quickly. 

>we corrected the text

R2 Line 408: This is not always true, soil suppressiveness can to a soil-borne disase also be acquired by monoculture. This was the case of take-all decline in wheat (Berendsen et al., 2012 doi: 10.1016/j.tplants.2012.04.001; Schlatter et al., 2017 doi.org/10.1094/PHYTO-03-17-0111- RVW). True, the pathogen is Gaeumannomyces graminis var. tritici and not Fusarium (the same has been observed for beet damping-off caused by Rhizoctonia solani. Mendes et al., 2011 doi: 10.1126/science.1203980) but it should be mentioned that this situation also exists.

>we corrected the text to make it clear that the increase of phytopathogens could take place in monocultures in most cases, but not as a general rule

R2 Line 439:  vegetation experiment ? not clear

>corrected to greenhouse or pot experiment

R2 I am surprised that it is the ref of Goncharov et al 2020 (11) which is cited for the practical aspects concerning the inoculums whereas this reference is a meta-analysis (admittedly well done) but I would have preferred a reference belonging to laboratory work

>we added two more relevant references

R2 Line 485: tef-1-a identifies more species than the eight listed

>we corrected the text

R2 lines 506-513 are unnecessary in this paragraph

>we consider it necessary, but still corrected the text

R2 Lines 539-543: Why bring it all back to mycotoxins ?

>in our review we aimed to consider all ways of Fusarium identification, and mycotoxins or genes encoding them could be used for diagnostics.

R2 Table 3 is a partial copy-paste of the table published by Rampersad, 2020. The latter at least had the kindness to cite his sources, i.e. the ref, in his table!!!

>We included references in our table

R2 line 561: why is the reference not numbered, and not available in the list at the end of the manuscript

>we corrected the references throughout the manuscript

Reviewer 3 Report

Dear authors,

This review manuscript systematically presented the diversity, ecological characteristics and identification of phytopathogenic Fusarium in soil. The topic is interesting but some aspects in the manuscript should be clarified.

Line 259, "4. Fusarium control and soil suppressiveness against Fusarium fungi" It is suggested that this part should describe how to control and alleviate phytopathogenic Fusarium from different perspectives (subtitles), so that readers can quickly get the information they want to know and are interested in.

Please modify the format of Tables 1 and 2.

The references do not appear to be in the correct format. 

Author Response

Thank you for your recommendations

Line 259, "4. Fusarium control and soil suppressiveness against Fusarium fungi" It is suggested that this part should describe how to control and alleviate phytopathogenic Fusarium from different perspectives (subtitles), so that readers can quickly get the information they want to know and are interested in.

> Subsections were added

Please modify the format of Tables 1 and 2.

> The table 2 format was modified; the Table 1 was removed after the comments from another reviewer

The references do not appear to be in the correct format. 

> References were checked throughout the manuscript and corrected

Round 2

Reviewer 2 Report

Progress has been made, and I thank the authors for this effort, but I remain convinced that a review article cannot cover the extent of the genus Fusarium, which the title suggests. This is why I propose to make a small change in this title to restrict the focus of this review “Diversity, ecological characteristics and identification of some problematic phytopathogenic Fusarium in soil: a review”

However, there are still a few errors to be corrected and clarifications to be made.

Line 233. I'm sorry but Fusarium oxysporum is not a pathogen of barley. In the worst case, it disrupts nitrogen assimilation by the plant (under controlled conditions - Mostafa et al 2019, doi: 10.1016/j.apgeochem.2019.04.019). It is certainly pathogenic of soybeans (F. oxysporum f.sp adzuki) but as long as we take an example giving a good idea of the economic problem for which this species is responsible, I would rather mention bananas, cotton, or tomatoes (Ploetz 2006 doi:10.1094/phyto-96-0653, Karangwa et al 2018 doi:10.1094/PDIS-02-17-0282-RE Bell et al 2019 DOI10.1094/PDIS-09-18-1624-RE McGovern 2015 doi : 10.1016/j.cropro.2015.02.021.

 

Table 1 : I am embarrassed by the examples of host habitats/plants given by the authors concerning F. oxysporum. It is true that F. oxysporum is ubiquitous but it is not a proven pathogen of cereals, Munkvold et al 2021 pointed this out. I don't have articles relating F. oxysporum as a pathogen of pears, hazelnuts or apples or citrus fruits, but I have articles relating to F. oxysporum on garden market plants, ornamental plants, cotton, banana or the date palm, (Edel-Hermann and Lecomte 2019 doi:10.1094/phyto-08-18-0320-rvw) and I would expect to find such examples, or at least the word “vegetables” in column two of Table 1

Similarly, a little bibliographic research would have shown that, beside wheat and soybean, F. proliferatum is becoming a real pathological and economic problem in Europe because of its damage to garlic (Gálvez and Palmero 2022 doi: 10.3390/horticulturae8070628) and asparagus (Seefelder et al 2002 DOI: 10.1021/jf0115037).

 

Section 4.1 is titled "Mitigation strategies towards Fusarium, sub-section 4.1.2. is titled Fusarium control and its limitation then the following sub-sections discuss chemical, agrotechnological approaches, allude to invertebrates (line 322). I think that it would be relevant in this section to propose a sub-section "Biocontrol". This sub-section, by presenting examples of biological control agents selected and inoculated with success or failure (and why?) would not be redundant with the following one (soil suppressiveness ) which reports mechanisms highlighted in microbe-microbe interactions in suppressive soil even if it is true that suppressive soils are often the source of biocontrol agents as suggested by comparative molecular analyses of the biodiversity of suppressive and conducive soils to Fusarium wilt (Manikandan et al 2017 doi:10.1016/j.pmpp.2017.10.001; Siegel-Hertz et al. al 2018 doi:10.3389/fmicb.2018.00568). The part relating to mycorrhizae (lines 427-440) could be moved to this "biocontrol" sub-section

 

section 4.1.3 If this manuscript is intended to be a synthesis relating to the genus Fusarium, it should not be limited to the case of cereals. Authors should mention other advances in genetics in this section. Say, for example, resistance genes have been identified in many host plants of Fusarium sp. (cotton, banana, tomato, melon, peas, …) (Taken and Rep 2010 doi: 10.1111/j.1364-3703.2009.00605.x; Murray et al 2021 doi: 10.21273/HORTSCI16186-21; Epstein et al 2022 doi: 10.3389/ fpls.2022.921516; ...). Unfortunately, these genes have often been bypassed by the Fusarium, which has made it possible to identify races within the special forms but which forces breeders to use more complex selection strategies such as genetic pyramiding.

 

4.2 Soil suppressiveness

degree of suppression/elimination?

I will keep only the word "suppression" and I will discard the word "elimination". Suppression implies the notion of control i.e. prevention of development, limitation of growth and repression of activity including pathogenic activity, but it also implies that this prevention leads to death. And it is this concept involving an impediment including that of living that is behind the words disease suppression and disease suppressiveness (or soil suppressiveness to disease).

The review published by Alabouvette on the work this author conducted to demonstrate the role of biotic (and transmissible), and abiotic factors in soil naturally resistant to Fusarium wilt in the Chateaurenard region of France deserves to be quoted in this § for example about lines 363-365 (Alabouvette 1986 doi:10.1051/agro:19860307) as well as the reference to Cook and Baker (Cook, R. J., & Baker, K. F. (1983). The Nature and Practice of Biological Control of Plant Pathogens. St. Paul, MN: American Phytopathological Society), who proposed the concept of soil suppressiveness to disease.

 

Author Response

>Response to the reviewer

Progress has been made, and I thank the authors for this effort, but I remain convinced that a review article cannot cover the extent of the genus Fusarium, which the title suggests. This is why I propose to make a small change in this title to restrict the focus of this review “Diversity, ecological characteristics and identification of some problematic phytopathogenic Fusarium in soil: a review”

>Thank you very much for that recommendation. We thought about changing the name of the manuscript, but we didn’t come to such a good correction.

However, there are still a few errors to be corrected and clarifications to be made.

Line 233. I'm sorry but Fusarium oxysporum is not a pathogen of barley. In the worst case, it disrupts nitrogen assimilation by the plant (under controlled conditions - Mostafa et al 2019, doi: 10.1016/j.apgeochem.2019.04.019). It is certainly pathogenic of soybeans (F. oxysporum f.sp adzuki) but as long as we take an example giving a good idea of the economic problem for which this species is responsible, I would rather mention bananas, cotton, or tomatoes (Ploetz 2006 doi:10.1094/phyto-96-0653, Karangwa et al 2018 doi:10.1094/PDIS-02-17-0282-RE Bell et al 2019 DOI10.1094/PDIS-09-18-1624-RE McGovern 2015 doi : 10.1016/j.cropro.2015.02.021.

 >We edited this text and added the recommended references

Table 1 : I am embarrassed by the examples of host habitats/plants given by the authors concerning F. oxysporum. It is true that F. oxysporum is ubiquitous but it is not a proven pathogen of cereals, Munkvold et al 2021 pointed this out. I don't have articles relating F. oxysporum as a pathogen of pears, hazelnuts or apples or citrus fruits, but I have articles relating to F. oxysporum on garden market plants, ornamental plants, cotton, banana or the date palm, (Edel-Hermann and Lecomte 2019 doi:10.1094/phyto-08-18-0320-rvw) and I would expect to find such examples, or at least the word “vegetables” in column two of Table 1

Similarly, a little bibliographic research would have shown that, beside wheat and soybean, F. proliferatum is becoming a real pathological and economic problem in Europe because of its damage to garlic (Gálvez and Palmero 2022 doi: 10.3390/horticulturae8070628) and asparagus (Seefelder et al 2002 DOI: 10.1021/jf0115037).

 >we added this missing information in the table with the references. Also we added the information from the recommended references throughout the manuscript

Section 4.1 is titled "Mitigation strategies towards Fusarium, sub-section 4.1.2. is titled Fusarium control and its limitation then the following sub-sections discuss chemical, agrotechnological approaches, allude to invertebrates (line 322). I think that it would be relevant in this section to propose a sub-section "Biocontrol". This sub-section, by presenting examples of biological control agents selected and inoculated with success or failure (and why?) would not be redundant with the following one (soil suppressiveness ) which reports mechanisms highlighted in microbe-microbe interactions in suppressive soil even if it is true that suppressive soils are often the source of biocontrol agents as suggested by comparative molecular analyses of the biodiversity of suppressive and conducive soils to Fusarium wilt (Manikandan et al 2017 doi:10.1016/j.pmpp.2017.10.001; Siegel-Hertz et al. al 2018 doi:10.3389/fmicb.2018.00568). The part relating to mycorrhizae (lines 427-440) could be moved to this "biocontrol" sub-section

 >we added the section regarding biocontrol agents, moved a part of the text from “soil suppressiveness” there and added some more relevant information with references.

section 4.1.3 If this manuscript is intended to be a synthesis relating to the genus Fusarium, it should not be limited to the case of cereals. Authors should mention other advances in genetics in this section. Say, for example, resistance genes have been identified in many host plants of Fusarium sp. (cotton, banana, tomato, melon, peas, …) (Taken and Rep 2010 doi: 10.1111/j.1364-3703.2009.00605.x; Murray et al 2021 doi: 10.21273/HORTSCI16186-21; Epstein et al 2022 doi: 10.3389/ fpls.2022.921516; ...). Unfortunately, these genes have often been bypassed by the Fusarium, which has made it possible to identify races within the special forms but which forces breeders to use more complex selection strategies such as genetic pyramiding.

 >we added these references and text

4.2 Soil suppressiveness

degree of suppression/elimination?

I will keep only the word "suppression" and I will discard the word "elimination". Suppression implies the notion of control i.e. prevention of development, limitation of growth and repression of activity including pathogenic activity, but it also implies that this prevention leads to death. And it is this concept involving an impediment including that of living that is behind the words disease suppression and disease suppressiveness (or soil suppressiveness to disease).

>we corrected the name and the text according to the recommendations

The review published by Alabouvette on the work this author conducted to demonstrate the role of biotic (and transmissible), and abiotic factors in soil naturally resistant to Fusarium wilt in the Chateaurenard region of France deserves to be quoted in this § for example about lines 363-365 (Alabouvette 1986 doi:10.1051/agro:19860307) as well as the reference to Cook and Baker (Cook, R. J., & Baker, K. F. (1983). The Nature and Practice of Biological Control of Plant Pathogens. St. Paul, MN: American Phytopathological Society), who proposed the concept of soil suppressiveness to disease.

>we added these references

Round 3

Reviewer 2 Report

Thanks to the authors for the significant edits and clarification to the title that make this review acceptable for publication. Small detail to check,  reference73 also appears in 87.