Potential Application of Genomic Technologies in Breeding for Fungal and Oomycete Disease Resistance in Pea
and Thomas D. Warkentin 1,*Round 1
Reviewer 1 Report
This review on the application of genomic technologies in breeding for resistance to fungal diseases in peas is excellent and very timely, following the recently published first pea genome sequence.
To my knowledge, no study that reviews the science very specifically on this topic is available. This review will be very useful in gaining easy access and a very informative overview on (i) sources of resistance and markers associated with resistance to one or more pea fungal pathogens and (ii) genomic resources eg. the newly described SSRs or functional omics resources, enabled by the pea genome sequence, to accelerate efforts for breeding of future pea varieties resistant to fungal diseases.
The manuscript is very well written, highly and very precisely documented with a high number of references (n=137). The Table 1 reports very exhaustively the studies identifying markers linked to disease resistance loci.
I highly recommend publishing the manuscript, with minor revisions outlined in the attached file.
Best regards
Comments for author File: 
Comments.pdf
Author Response
Responses to the reviewer 1
Note that each of our responses is preceded by TW
Reviewer 1
Comments and Suggestions for Authors
This review on the application of genomic technologies in breeding for resistance to fungal diseases in peas is excellent and very timely, following the recently published first pea genome sequence.
To my knowledge, no study that reviews the science very specifically on this topic is available. This review will be very useful in gaining easy access and a very informative overview on (i) sources of resistance and markers associated with resistance to one or more pea fungal pathogens and (ii) genomic resources eg. the newly described SSRs or functional omics resources, enabled by the pea genome sequence, to accelerate efforts for breeding of future pea varieties resistant to fungal diseases.
The manuscript is very well written, highly and very precisely documented with a high number of references (n=137). The Table 1 reports very exhaustively the studies identifying markers linked to disease resistance loci.
I highly recommend publishing the manuscript, with minor revisions outlined in the attached file.
- Line 92 : « … were identified as resistance sources to F. solani [17]. »
TW: Based on the suggestion of two reviewers, we modified this sentence as “…..were identified as resistance sources of F. solani resistance [17].”
- Line 104 : « …pea accessions originated from 60 countries for E. pisi resistance. »
TW: The sentence was corrected as suggested.
- Line 147 : replace « contain » by « reduce »
TW: As suggested by reviewer 2, the phrase “to contain the impact of disease severity” is replaced with “for disease management”. The sentence now reads as “The level of disease resistance identified in P. sativum accessions is often not sufficient for disease management in natural conditions and against different strains of the pathogens”.
- Line 158 : « Jha et al [48] observed ascochyta resistance, high lodging score… »
TW: The sentence was corrected to add ‘Ascochyta resistance’ as suggested.
- Line 164 : correct « ascochyta »
TW: The spelling of ‘Ascochyta’ is corrected in this sentence.
- Lines 164-165 : please verify references cited, since all of them do not use interspecific populations, with a wild pea as one of the parents
TW: The cited references were verified and only studies based on interspecific populations were retained.
- Lines 165-176 : The pea germplasm lines published in the study [66] were not derived from wild relatives. This whole paragraph should be moved elsewhere in the manuscript, most likely in section 2.1.
TW: The suggestion was accepted. The referred paragraph was moved to section 2.1.
- Line 180 : The title of this section 3 may be replaced by a more appropriate title, for example « Markers associated to fungal disease resistance for accelerated breeding »
TW: The title of section 3 is modified as “Molecular Markers Associated with Fungal Disease Resistance for Accelerated Breeding”
- Lines 199-200 : verify the sentence format
TW: The sentence is corrected to “SNP arrays have been developed based on the identification of genome-wide SNPs from genome and/or transcriptome sequencing of a set of diverse pea lines.”
- Lines 243 and 245 : hyphens are missing for words « meta-analysis » and « Twenty-seven »
TW: Corrections were made as suggested.
- Line 274 : replace « major steps » by « early steps »
TW: ‘major’ is replaced with ‘early’ in this sentence.
- Line 275 : replace « A. euteiches symptoms » by « first disease symptoms »
TW: Replaced “A. euteiches symptoms” with “first disease symptoms” in this sentence.
- Line 279 : rephrase as follows : « … colonization by A. euteiches and delayed appearance of disease symptoms. »
TW: The suggestion to rephrase was accepted.
- Lines 282-283 : rephrase as follows : « … using 175 pea lines evaluated in field infested nurseries in nine environments and for response to inoculation by two isolates of A. euteiches in controlled conditions. »
TW: Thank you, the suggested correction was accepted.
- Line 284 : rephrase as follows : « …and validated 6 out of 7… »
TW: The phrase is corrected as “…. and validated six out of seven….”
- Line 313-314 : replace « …Fsp-Ps4.1 observed in single… » by « …Fsp-Ps4.1 detected from single..»
TW: ‘observed in’ is replaced with ‘detected from’ in the referred phrase.
- Line 393 : write « defense » like in line 399
TW: ‘defence’ is corrected as ‘defense’ in the referred sentence.
- Line 432 : replace « …of this QTL… » by « …at this QTL… »
TW: The suggested change was made.
- Line 493 : remove « from »
TW: The suggested correction was accepted.
- Line 497 : verify the correct format of the sentence
TW: The sentence is corrected as “… powdery mildew resistance by er1 is due to loss-of-function mutations in PsMLO1, ……”
- Lines 515-516 : replace « …could play an important role … » by « … could be useful… »
TW: The suggested change was made.
Reviewer 2 Report
This manuscript primarily reviews the QTL markers identified in pea for resistance to several root and foliar diseases. Thus, the title is a bit misleading since genomic technologies such as genomic selection are just beginning to be used in pea. Also, the review describes developing resistance to diseases caused by fungal and oomycete pathogens. I recommend that the authors consider revising the title to be more reflective of the contents of the review. I made some English grammar corrections on the attached pdf. Below are additional questions and comments.
Line 29: The accepted family name is Fabaceae.
Line 47: This paragraph needs to be completely revised for accuracy. Note that Aphanomyces euteiches and Peronspora viciae are oomycetes, not fungi. Perhaps a lead sentence would be: Diseases are the most important biotic constraints affecting global pea production [12] causing yield losses that range from a small percentage to complete crop loss depending on location and environmental conditions.
Line 51: Here and throughout the manuscript, pisi should not be capitalized.
Line 83, 89: Need a more complete description of the source of the 2,500 accessions or delete “obtained from the USDA, Pullman, WA”.
Line 112: Clarify which pathogen is being referred to as P. pisi.
Line 135: Here and throughout the paper pisi is italicized.
Line 136: Here and throughout the paper, Ascochyta is capitalized.
Line 143: Replace white rot with white mold.
Line 147: Suggest this edit: …is not sufficient for disease control in natural conditions….
Line 155: Not clear what is meant by "can damage meiosis in hybrids". Meiosis is a process not an object. Suggest …can interfere with meiosis resulting in sterility of the hybrids.
Line 199: Suggest this edit: SNP arrays have been developed based on the identification of genome-wide SNPs from genome and/or transcriptome sequencing of a set of diverse pea lines.
Line 255: Suggest this edit: Due to the co-linearity between the Medicago truncatula and pea genome sequences, inspection of the six main meta-QTL regions in the M. truncatula genome identified 318 candidate genes with 14 to 91 candidates per meta-QTL.
Line 294: The pathogen F. solani f. sp. pisi is abbreviated here as Fsp, but the abbreviation is never used. Suggest using the abbreviation in the remainder of the section referring to this pathogen.
Line 317: Please expand on what is meant by defensive family. Do you mean defensins?
Line 320: Are Mycosphaerella blight and Ascochyta blight the same disease? Please use one name for the disease or clarify that they are the same disease. In this paragraph, the term resistance is often not included. Please revise carefully. For example, Four QTLs for F. solani …. should be revised to Four QTLs for resistance to F. solani…
Line 346: Throughout this section Ascochyta is not capitalized. Because it is a genus name of the fungus, the disease should be capitalized as Ascochyta blight.
Line 469: In this section (and also starting inline 599), because the gene names are italicized indicating that they are genes, the word gene should be deleted but the sentences should not start with er1. In line 470 suggest: Complete resistance was provided by er1 with no visible sign of necrosis….In line 480: The resistance genes er1, er2, and Er3 were located on….
Line 505: Please italicize the alleles in this section such as er1-1, er1-4, etc.
Line 537: Suggest this edit: Until recently, pea had relatively few genomic resources compared to most other crop species.
Comments for author File: Comments.pdf
Author Response
Responses to the reviewer 2
Note that each of our responses is preceded by TW
Reviewer 2
Reviewer: This manuscript primarily reviews the QTL markers identified in pea for resistance to several root and foliar diseases. Thus, the title is a bit misleading since genomic technologies such as genomic selection are just beginning to be used in pea. Also, the review describes developing resistance to diseases caused by fungal and oomycete pathogens. I recommend that the authors consider revising the title to be more reflective of the contents of the review. I made some English grammar corrections on the attached pdf. Below are additional questions and comments.
TW: We revised the title as follows: Potential Application of Genomic Technologies in Breeding for Fungal and Oomycete Disease Resistance in Pea
Line 29: The accepted family name is Fabaceae.
TW: We accepted the suggestion.
Line 47: This paragraph needs to be completely revised for accuracy. Note that Aphanomyces euteiches and Peronspora viciae are oomycetes, not fungi. Perhaps a lead sentence would be: Diseases are the most important biotic constraints affecting global pea production [12] causing yield losses that range from a small percentage to complete crop loss depending on location and environmental conditions.
TW: We accepted the suggestion and referred to Aphanomyces euteiches and Peronospora viciae as oomycetes.
Line 51: Here and throughout the manuscript, pisi should not be capitalized.
TW: We made the correction throughout the manuscript.
Line 83, 89: Need a more complete description of the source of the 2,500 accessions or delete “obtained from the USDA, Pullman, WA”.
TW: We accepted the suggestion and deleted “obtained from the USDA, Pullman, WA”.
Line 112: Clarify which pathogen is being referred to as P. pisi.
TW: We changed P. pisi to Peronospora pisa (P. viciae f. sp. pisi) which are synonyms.
Line 135: Here and throughout the paper pisi is italicized.
TW: We italicized “pisi” throughout.
Line 136: Here and throughout the paper, Ascochyta is capitalized.
TW: ‘Ascochyta’ is capitalized throughout in the revision.
Line 143: Replace white rot with white mold.
TW: ‘white rot’ is replaced with ‘white mold’ as suggested.
Line 147: Suggest this edit: …is not sufficient for disease control in natural conditions….
TW: Suggestion accepted to revise the sentence.
Line 155: Not clear what is meant by "can damage meiosis in hybrids". Meiosis is a process not an object. Suggest …can interfere with meiosis resulting in sterility of the hybrids.
TW: Suggestion accepted and sentence was revised using the suggested wording.
Line 199: Suggest this edit: SNP arrays have been developed based on the identification of genome-wide SNPs from genome and/or transcriptome sequencing of a set of diverse pea lines.
TW: Sentence was edited as suggested.
Line 255: Suggest this edit: Due to the co-linearity between the Medicago truncatula and pea genome sequences, inspection of the six main meta-QTL regions in the M. truncatula genome identified 318 candidate genes with 14 to 91 candidates per meta-QTL.
TW: Sentence was edited as suggested.
Line 294: The pathogen F. solani f. sp. pisi is abbreviated here as Fsp, but the abbreviation is never used. Suggest using the abbreviation in the remainder of the section referring to this pathogen.
TW: The abbreviation Fsp was used throughout the section in the revised draft.
Line 317: Please expand on what is meant by defensive family. Do you mean defensins?
TW: We changed the term to ‘defensin gene family’
Line 320: Are Mycosphaerella blight and Ascochyta blight the same disease? Please use one name for the disease or clarify that they are the same disease. In this paragraph, the term resistance is often not included. Please revise carefully. For example, Four QTLs for F. solani …. should be revised to Four QTLs for resistance to F. solani…
TW: We used Ascochyta blight throughout the revised draft. The referred sentence was modified as “Four QTLs for resistance to Fsp…”
Line 346: Throughout this section Ascochyta is not capitalized. Because it is a genus name of the fungus, the disease should be capitalized as Ascochyta blight.
TW: We accepted the suggestion and used ‘Ascochyta’ in the revised draft.
Line 469: In this section (and also starting inline 599), because the gene names are italicized indicating that they are genes, the word gene should be deleted but the sentences should not start with er1. In line 470 suggest: Complete resistance was provided by er1 with no visible sign of necrosis….In line 480: The resistance genes er1, er2, and Er3 were located on….
TW: We accepted the suggestion and removed the word gene after the gene names.
Line 505: Please italicize the alleles in this section such as er1-1, er1-4, etc.
TW: Alleles were italicized in the revised draft.
Line 537: Suggest this edit: Until recently, pea had relatively few genomic resources compared to most other crop species.
TW: The sentence was edited as suggested.
Reviewer 3 Report
The manuscript entitled "Application of Genomic Technologies in Breeding for Fungal Disease Resistance in Pea" submitted for review in Agronomy MDPI, is well written. This paper presents an analysis of available results on pea disease resistance. I believe that some important threads have been omitted.
- Ascochyta blight of pea is caused by a complex of fungal pathogens. The ascochyta complex has traditionally included: Peyronellaea pinodes, Didymella pisi and Peyronellaea pinodella. Davidson et al. (2009) characterized a fourth causal agent, Phoma koolunga. This pathogen and other species such as Phoma herbarum and Phoma glomerata were both shown to be pathogenic on pea and have been associated with ascochyta blight in Australia. I think a thread related to Ascochyta blight should include these important pathogens. In line 594, the authors provide information about Phoma koolunga infection on pea plants? I believe that Table 1 should be expanded to include these pathogens.
- The second very important and completely omitted in the paper is Fusarium wilt of pea by F. oxysporum. I think this should be considered.
- The root rot of pea also causes other Fusarium species that should be included like F. culmorum, F. graminearum, F. tricinctum and others.
I believe that the manuscript should be supplemented with the listed elements, therefore, I request that it be accepted for publication with major revision.
Specific comments:
l25-Keywords. The term - pea is in the paper's title there is no point in repeating it. I suggest replacing it with e.g. Fusarium or root rot.
l88- F. solani f. sp. Pisi - there is a writing mistake here.
l135- F. solani f. sp. pisi. Please write pisi in italics. Podobnie w wierszach: 294, 302, 307, 312.
l322- Mycosphaerella should be write in italics.
l345- Remove the comma after F. solani.
L459- Aphanomyces should be write in italics. Aphanomyces root rot of pea is the name of the disease, and in that case the notation without the italics may be used.
Author Response
Responses to the reviewer 3
Note that each of our responses is preceded by TW
Reviewer 3
The manuscript entitled "Application of Genomic Technologies in Breeding for Fungal Disease Resistance in Pea" submitted for review in Agronomy MDPI, is well written. This paper presents an analysis of available results on pea disease resistance. I believe that some important threads have been omitted.
- Ascochyta blight of pea is caused by a complex of fungal pathogens. The ascochyta complex has traditionally included: Peyronellaea pinodes, Didymella pisi and Peyronellaea pinodella. Davidson et al. (2009) characterized a fourth causal agent, Phoma koolunga. This pathogen and other species such as Phoma herbarum and Phoma glomerata were both shown to be pathogenic on pea and have been associated with ascochyta blight in Australia. I think a thread related to Ascochyta blight should include these important pathogens. In line 594, the authors provide information about Phoma koolunga infection on pea plants? I believe that Table 1 should be expanded to include these pathogens.
TW: We accepted the suggestion. In the revised draft, we have described all the causal agents of Ascochyta blight complex as suggested.
Line 594: The study by Tran et al. refers to the infection on pea plants.
Table 1: Some studies exclusively are based on Peyronellaea pinodes infection and others are based on field evaluation of Ascochyta blight (there could be one or more causal agents in addition to P. pinodes and we added the same information as a footnote).
- The second very important and completely omitted in the paper is Fusarium wilt of pea by F. oxysporum. I think this should be considered.
TW: We included Fusarium wilt of pea in the revised draft.
- The root rot of pea also causes other Fusarium species that should be included like F. culmorum, F. graminearum, F. tricinctum and others.
TW: Fusarium solani and F. avanaceum are the key pathogens of root rot in pea. Though several other Fusarium spp. are often isolated from pea roots, they are relatively non to weakly aggressive and most often are opportunistic pathogens. The genetic basis of disease resistance against these other Fusarium spp. has hardly been studied. For the purpose of the current review article we focused on F. solani and F. avanaceum.
In the revised draft, we added the sentence “Several other Fusarium spp. that can colonize pea roots are non to weakly aggressive (Sisic et al. 2018)”.
Specific comments:
l25-Keywords. The term - pea is in the paper's title there is no point in repeating it. I suggest replacing it with e.g. Fusarium or root rot.
TW: In the keywords section, we replaced ‘pea’ with ‘Fusarium’
l88- F. solani f. sp. Pisi - there is a writing mistake here.
l135- F. solani f. sp. pisi. Please write pisi in italics. Podobnie w wierszach: 294, 302, 307, 312.
TW: We corrected the fungus name throughout the manuscript. ‘pisi’ is mentioned in italics and the first letter is not capitalized (which was an error of auto capitalization in the previous draft).
l322- Mycosphaerella should be write in italics.
TW: We replaced ‘Mycosphaerella’ with ‘M. pinodes’ as also suggested by reviewer 2.
l345- Remove the comma after F. solani.
TW: Correction was made in the revised draft accordingly.
L459- Aphanomyces should be write in italics. Aphanomyces root rot of pea is the name of the disease, and in that case the notation without the italics may be used.
TW: Correction was made in the revised draft accordingly.
Round 2
Reviewer 2 Report
The authors addressed the questions and suggestions from the previous review.
Reviewer 3 Report
The manuscript has been revised. I recommend that the paper be accepted for publication in its present form.
