Insight into the Role of Epigenetic Processes in Abiotic and Biotic Stress Response in Wheat and Barley

Round 1

Reviewer 1 Report

The review manuscript by Kong, Liu et al. provides a well researched overview in the topic of biotic and abiotic stress responses in wheat and barley.

I have some points of criticism and shortcomings that the authors should address in their article.

1) General:

 - I miss at least one summarizing or concluding figure - The table is not ‘handy’ enough.

 - The manuscript’s title suggests a review on “epigenetic regulation”. The majority of the manuscript, however, does not detail any aspect of regulation. Although everything the authors’ write is correct, they miss - at least for my understanding - to put the regulatory aspect at center stage. Most of the paragraphs stay enumerative, which is o.k. in a field where only little information is there. But at least some of the more conclusive processes - probably taken in analogy from Arabidopsis should be included.

Therefore, the manuscript in its present form is nice, but I feel, that the authors’ review manuscript does not perfectly match with the title.

 - It should explicitly be mentioned that most of the mechanisms described in the section are based on Arabidopsis research - -which is not wrong, but should be highlighted in the light in a review article on crop cereals.

 - I would like to read a much more general section on stress responses, stress response genes and epigenetic regulation. e.g. The expression of many stress responsive genes is repressed under non-stress condition, but are rapidly induced upon stress. Are these genes epigenetically repressed during ambient conditions? Is this repression lifted rapidly at stress alarm responses? How fast?

How come that there is a common alarm stress response that is rapid and conserved in many plants, but rather unspecific (e.g. Kilian et al., Biochim Biophys Acta 2011) - is this the lag time, which is required to lift the epigenetic repression from the specific response genes?

 - I miss a section on stress memory, priming, acclimation and tollerance

2) Introduction is imbalanced. As the review is on general stress responses, the paragraph on heave metal stress and accumulation is too long compared to other, equally or even more important threats for these Poaceae. Either this section is condensed, or (my favor) the other sections of the introduction are extended. Especially, in the light of climate change debate, a more elaborate introduction to drought, heat, salinity or flooding stresses would be appropriate.

3) DNA-methylation

The stress responsive ABC-transporters were noted before (Wanke & Kolukisaoglu, Plant Biology 2010).

The authors miss the very important article about transcription factor binding dependency and DNA-methylation:
O'Malley et al: Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape. Cell. 2016

4) Histone modification

The authors put emphasis on the GCN5-mechanism. As acetylation and methylation of histones goes hand-in-hand in every condition, the mechanism behind methylation should be mentioned likewise. e.g. The repressive H3K27me3 modification is mediated by recruiters, DNA-binding proteins that guide the Histone methyl-transferase complexes PRC1 and PRC2 to the correct genomic loci. The first recruiters in plants are the members of the BBR/BPC family that were shown responsible to establish the silencing mark (Hecker et al., Plant Phys 2015; Xiao et al., Nat Genetics 2017).

H3K36me3 and Trx is proposed to be an important link to plant (stress) memory.

But also purely stress related literature is missing, e.g. Rymen et al., Histone acetylation orchestrates wound-induced transcriptional activation and cellular reprogramming in Arabidopsis. Commun Biol. 2019

5)  The section on chromatin remodeling is an absolute shortcoming to me. Even though I understand that there is little report from barley or wheat, the authors should have included an equally broad introductory paragraph to this epigenetic mechanism. I would like to encourage the authors to be more speculative on the possible roles of chromatin remodeling during stress responses!

6) Non-coding RNAs

I miss a full paragraph, including a mechanistic introduction, on RdDM as a feedback of the ncRNAs to the other levels of epigenetic regulation.

The section should be condensed. The authors describe in very detail all the data, which I feel is not fully satisfying, because it looses track of the stress responses. I think that condensation and focusing on the similarities would enhance the clarity of this part of the manuscript.

Author Response

Please see the attachment

Author Response File: Author Response.pdf

Reviewer 2 Report

This manuscript is described that plants employ sophisticated epigenetic mechanisms to fine-tune their responses to environmental stresses. The authors provide an overview of epigenetic processes and elements, such as DNA methylation, histone modification, chromatin remodeling, and non-coding RNAs, that contribute to the regulation of plant responses to abiotic and biotic stresses in wheat and barley. Besides DNA methylation and histone modifications, chromatin structure and non-coding RNAs expression may also be affected in response to abiotic/biotic stresses.

The authors explained that Short-chain non-coding RNAs, such as microRNAs (miRNA) and small interfering RNAs (siRNAs), participate in both transcriptional and post-transcriptional regulation of gene expression. NCRNAs play an important role mainly in "the target-specific post-transcriptional gene silencing" (PTGS). However, additional considerations should be given to whether it is appropriate to handle them in "Epigenetic regulation". So far, several subclasses of siRNAs have been identified, some of which function in PTGS and others function in transcriptional gene silencing (TGS). Or rather, focusing on other mechanism without non-coding RNAs might make the review more meaningful.

The explanation of epigenetic regulation in response to abiotic and biotic stress is quite lacking in the aspect of "Chromatin remodeling". Apparently it appears to be listed the explanation, which is done by arranging the research contents in each part, so the overall consideration is very weak. Therefore, it is necessary to present additional sessions that collectively describe four mechanisms or three mechanisms except at least non-coding RNAs.

Author Response

Review 2 # Comments and Suggestions for Authors

This manuscript is described that plants employ sophisticated epigenetic mechanisms to fine-tune their responses to environmental stresses. The authors provide an overview of epigenetic processes and elements, such as DNA methylation, histone modification, chromatin remodeling, and non-coding RNAs, that contribute to the regulation of plant responses to abiotic and biotic stresses in wheat and barley. Besides DNA methylation and histone modifications, chromatin structure and non-coding RNAs expression may also be affected in response to abiotic/biotic stresses.

- Thank you for the comments!  

The authors explained that Short-chain non-coding RNAs, such as microRNAs (miRNA) and small interfering RNAs (siRNAs), participate in both transcriptional and post-transcriptional regulation of gene expression. NCRNAs play an important role mainly in "the target-specific post-transcriptional gene silencing" (PTGS). However, additional considerations should be given to whether it is appropriate to handle them in "Epigenetic regulation". So far, several subclasses of siRNAs have been identified, some of which function in PTGS and others function in transcriptional gene silencing (TGS). Or rather, focusing on other mechanism without non-coding RNAs might make the review more meaningful.

- Response: Many thanks! We have rewritten the Non-coding RNAs section and extended introduction on NcRNAs-regulated epigenetic processes, including RdDM, histone modification as well as genome topology changes.

The explanation of epigenetic regulation in response to abiotic and biotic stress is quite lacking in the aspect of "Chromatin remodeling". Apparently it appears to be listed the explanation, which is done by arranging the research contents in each part, so the overall consideration is very weak.

- Response: Yes, the section on chromatin remodeling has been extended and more speculation on the possible roles of chromatin remodeling during stress responses in wheat and barley are discussed in the new version.

Therefore, it is necessary to present additional sessions that collectively describe four mechanisms or three mechanisms except at least non-coding RNAs.

- Response: Many thanks. We have collectively described and summarized the role of epigenetic mechanisms in abiotic and biotic stress responses in wheat and barley as a concluding figure in the revised version.

Round 2

Reviewer 2 Report

I think that what I pointed out was properly reflected.