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Open AccessReview
Peer-Review Record

What Makes the Wood? Exploring the Molecular Mechanisms of Xylem Acclimation in Hardwoods to an Ever-Changing Environment

Forests 2019, 10(4), 358; https://doi.org/10.3390/f10040358
Reviewer 1: Anonymous
Reviewer 2: Anonymous
Forests 2019, 10(4), 358; https://doi.org/10.3390/f10040358
Received: 28 February 2019 / Revised: 13 April 2019 / Accepted: 23 April 2019 / Published: 25 April 2019

Round 1

Reviewer 1 Report

Just a few minor comments about this manuscript. This review is focused on vessels and therefore on hardwood (angiosperms). The general concepts described here about environmental control on xylem structure are in general broadly valid for conifers (gymnosperms) as well, however the terminology used here makes necessary to specify since the beginning that this review is focused on angiosperms.

Ln 41-43 I think this statement is more appropriate for conifers species with tracheids. Increased cell wall thickness in vessels certainly happens, but I would say that the risk of cavitation is also (probably mostly)controlled by reducing vessel lumen area (or diameter), a process driven by soil moisture.

Ln 53 “and [13]”?

Ln 59 Again, careful with the language. Depending on what we are talking about, we cannot assume that “tracheids” and “vessels” are the same thing

Ln 68-73 Check the formatting of these lines

Ln 65 Figure 1 does not show gymnosperm wood. Either add a section of gymnosperms to the figure or remove the link to Figure 1 here.

Ln 66-67 Move this sentence earlier in the manuscript

Ln 187-188 This is true even for gymnosperms as well. On the other hand, the statement in Ln 188-190 is valid only for angiosperms.

Ln 371 “…in order to maintain PRIMARILY the hydraulic functionING of the wood.”


Author Response

Thank you for your benevolent review of our manuscript. We have addressed all your suggestions. Please find the details below:


Just a few minor comments about this manuscript. This review is focused on vessels and therefore on hardwood (angiosperms). The general concepts described here about environmental control on xylem structure are in general broadly valid for conifers (gymnosperms) as well, however the terminology used here makes necessary to specify since the beginning that this review is focused on angiosperms.

We totally agree that this review focuses on xylem acclimation in angiosperms. Therefore, we have deleted all references to gymnosperms in the manuscript to not confuse the reader. The title has been changed as well in order to highlight the focus on angiosperms.

 

Ln 41-43 I think this statement is more appropriate for conifers species with tracheids. Increased cell wall thickness in vessels certainly happens, but I would say that the risk of cavitation is also (probably mostly)controlled by reducing vessel lumen area (or diameter), a process driven by soil moisture.

We absolutely agree and have rephrased this sentence accordingly, emphasizing the importance of a reduction in vessel diameter.


Ln 53 “and [13]”?

The scribal error “and” has been deleted

 

Ln 59 Again, careful with the language. Depending on what we are talking about, we cannot assume that “tracheids” and “vessels” are the same thing

Tracheids has been rephrased to xylem vessels.

 

Ln 68-73 Check the formatting of these lines

Formatting has been corrected

 

Ln 65 Figure 1 does not show gymnosperm wood. Either add a section of gymnosperms to the figure or remove the link to Figure 1 here.

As stated above all referrals to gymnosperms have been removed. The reference to Figure 1 has been moved

 

Ln 66-67 Move this sentence earlier in the manuscript

This sentence has been removed as it also referred to gymnosperms.

 

Ln 187-188 This is true even for gymnosperms as well. On the other hand, the statement in Ln 188-190 is valid only for angiosperms.

We believe that due to the removal of all references to gymnosperms there will be no confusion because of this statement.

 

Ln 371 “…in order to maintain PRIMARILY the hydraulic functionING of the wood.”

The sentence has been rephrased


Reviewer 2 Report

The manuscript 'What make the wood?- How xylem acclimates to ever-changing environmental conditions' by Eckert et al. provides a short overview on the effects of environmental stresses (drought, salt stress and nutrient deficiency) on xylogenesis and xylem traits. The review highlights the role of xylem features in the plant adaptation to changing environment. Xylem morphology, cell wall metabolic pathways and molecular biology of wood formation are presented with the aim to provide the current understanding on this important topic in the field of forestry sciences.

Although the topic is very intriguing and deserves with the aims of the journal, there are some crucial shortcomings and minor points that authors need to consider to improve the ms and to make it more interesting for a wide audience.

Main shortcomings:
1) The title is misleading. My feeling is that authors should better focus the content of the manuscript in the title. The review describes the recent advances on the molecular aspects of wood formation in poplar and a few hardwood species and these points should be highlighted (for example conifers are excluded, as well as sugar metabolism).  
2) The terms 'adaptation', 'acclimation' and 'plasticity' are used in confounding way thus I suggest the authors to define these terms in the first chapter and to use them accordingly within the following chapters.
3) The figures are misleading, useless and should be changed. Micrometric bars are not reported in figure 1 and 3. In Figue 1, I was not able to check the region of cell division, expansion and secondary wall formation; in Figure 2, authors should better explain how environmental stimuli act to modulate wood formation. What are the environmental factor(s) determining lumen area and vessel frequency decrease as well as wall thickness increase? The authors should add some figures (like graphical abstract or flowcharts) to better explain the relationship between genes, metabolic pathway, xylem traits and stressors. This could be highly appreciated by potential readers.

4) The mechanisms driven the refilling of embolized vessels were not taken into account. The refilling mechanisms of embolized vessels is a well known process involving sugar metabolism, gene expression and pit morphology (see papers of Secchi et al.,). As the authors try to explain acclimation/adaptation strategies involved in the modulation of hydraulic efficiency in response to drought, this topic should be added to the review.

5) The role of hormones in the xylogenesis is exhaustively reported but major attention should be payed to the link between free and conjugates forms. This point is crucial to highlight the involvement of the hormones in the regulation of vessel morphology.
6) The name of the species have to be in italics.
7) In the conclusion chapter, authors should highlight how the use of new molecular technologies could improve the studies of regulatory mechanisms in developing xylem. This part could represent a useful track for the readers.

Other points:
line 45: delete 'regular';
line 56: an...[13 ]?;
lines 64-65: figure 1..this is not referred to gymnosperms;
lines 65-66: please add at least a paper reporting this state;
line 72: ..paratracheal parenchyma..please added in which species;
line 110: see point 3;
lines 147-148: please insert the sources of monolignol biosynthesis;
lines 216-218: Under water stress sugars accumulation across the cambial region and phloem plays a major osmotic role than K+ in the maintaining of the turgor pressure. The role of sugars as osmotic molecules as well as the sucrose molecular pathways within the stem should be discussed in this chapter;  
line 330: change water conductance in hydraulic efficiency;
line 370: define 'plastic adjustment';

Author Response

We are grateful for your in-depth review of our manuscript and the valuable suggestions how to improve it. We have addressed all of your remarks.


Main shortcomings:
1) The title is misleading. My feeling is that authors should better focus the content of the manuscript in the title. The review describes the recent advances on the molecular aspects of wood formation in poplar and a few hardwood species and these points should be highlighted (for example conifers are excluded, as well as sugar metabolism).  

We have rephrased the title to “What makes the wood? – Exploring the molecular mechanisms of xylem acclimation in hardwoods to an ever-changing environment” to highlight the focus on the molecular aspect of angiosperm xylem acclimation.


2) The terms 'adaptation', 'acclimation' and 'plasticity' are used in confounding way thus I suggest the authors to define these terms in the first chapter and to use them accordingly within the following chapters. 

We have rephrased the according passages and use the word acclimation consistently throughout the manuscript, since the word adaptation is commonly referring to changes on an evolutionary scale and not on short term responses.


3) The figures are misleading, useless and should be changed. Micrometric bars are not reported in figure 1 and 3. In Figue 1, I was not able to check the region of cell division, expansion and secondary wall formation; in Figure 2, authors should better explain how environmental stimuli act to modulate wood formation. What are the environmental factor(s) determining lumen area and vessel frequency decrease as well as wall thickness increase? The authors should add some figures (like graphical abstract or flowcharts) to better explain the relationship between genes, metabolic pathway, xylem traits and stressors. This could be highly appreciated by potential readers.

We have replaced Figure 1 with a new version, which shows the different zones of xylem development by an intensification of purple color illustrating lignification due to Phosphoglucinol/HCl staining.

We also added micrometric bars to Figure 1 and 3. Thank you for bringing this flaw to our attention. We also followed up your idea and added a graphical abstract to the manuscript which should attract the readers´ interest. Detailed information is then given in Figure 2, which is unchanged.

 

4) The mechanisms driven the refilling of embolized vessels were not taken into account. The refilling mechanisms of embolized vessels is a well known process involving sugar metabolism, gene expression and pit morphology (see papers of Secchi et al.,). As the authors try to explain acclimation/adaptation strategies involved in the modulation of hydraulic efficiency in response to drought, this topic should be added to the review.

We have added a whole paragraph in the “Drought leads to major transcriptional remodelling” section of the manuscript describing and discussing the mechanism of embolism recovery with focus on the molecular processes, sugar metabolism in particular, and gene regulation in vessel-associated cells.

 

5) The role of hormones in the xylogenesis is exhaustively reported but major attention should be payed to the link between free and conjugates forms. This point is crucial to highlight the involvement of the hormones in the regulation of vessel morphology.

We have specified which specific phytohormone form has been used in which study and discuss the necessity to gain further insight in the switch between active and inactive forms of certain phytohormones.


6) The name of the species have to be in italics.

This has been corrected throughout the whole manuscript


7) In the conclusion chapter, authors should highlight how the use of new molecular technologies could improve the studies of regulatory mechanisms in developing xylem. This part could represent a useful track for the readers. 

We have added to the conclusions according to your suggestions a paragraph highlighting the technical advances that will help researchers investigating candidate genes more efficiently.

Other points:
line 45: delete 'regular';

"regular" has been deleted


line 56: an...[13 ]?;

"an…" has been deleted


lines 64-65: figure 1..this is not referred to gymnosperms;

All references to gymnosperms have been removed from the manuscript and the reference to the figure is now moved to an appropriate place.


line 72: ..paratracheal parenchyma..please added in which species;

We have added species names to this sentence


line 110: see point 3;

Please see our answer to point 3


lines 147-148: please insert the sources of monolignol biosynthesis;

The sources of monolignols biosynthesis has been added and the text rephrased


lines 216-218: Under water stress sugars accumulation across the cambial region and phloem plays a major osmotic role than K+ in the maintaining of the turgor pressure. The role of sugars as osmotic molecules as well as the sucrose molecular pathways within the stem should be discussed in this chapter;  

We have added a paragraph about the role of sugar, sucrose in particular, in cambial development and cell expansion


line 330: change water conductance in hydraulic efficiency;

Water conductance has been changed to hydraulic efficiency


line 370: define 'plastic adjustment';

We have removed the term “plastic” since we haven´t used it in the manuscript before and we do not want to introduce a novel term at the very end of the manuscript, because it might confuse the reader.

In addition we would like to point out that the lingual quality of the manuscript has been significantly improved as can be seen by numerous rephrasing throughout the manuscript.

 


Round 2

Reviewer 2 Report

Figure 1 has a very low resolution. Please change it.

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