Climate change shapes the future evolution of plant metabolism

Abstract Planet Earth has experienced many dramatic atmospheric and climatic changes throughout its 4.5‐billion‐year history that have profoundly impacted the evolution of life as we know it. Photosynthetic organisms, and specifically plants, have played a paramount role in shaping the Earth's atmosphere through oxygen production and carbon sequestration. In turn, the diversity of plants has been shaped by historical atmospheric and climatic changes: plants rose to this challenge by evolving new developmental and metabolic traits. These adaptive traits help plants to thrive in diverse growth conditions, while benefiting humanity through the production of food, raw materials, and medicines. However, the current rapid rate of climate change caused by human activities presents unprecedented new challenges to the future of plants. Here, we discuss the potential effects of modern climate change on plants, with specific attention to plant specialized metabolism. We explore potential avenues of future scientific investigations, powered by cutting‐edge methods such as synthetic biology and genome engineering, to better understand and mitigate the consequences of rapid climate change on plant fitness and plant usage by humans.

Initial Editorial Evaluation 08/12/2020 _____________________________________________________________________________________________ (1) Can you please introduce a sentence about the solutions that genetics and genomics bring to the issue into your abstract? We need to have a solution to the problem in the abstract, and we cannot wander around other disciplines. As you concluded, either that we need genetic markers to breed plants faster or that natural breeding is not fast enough to introduce the traits required and therefore parallel editing is needed -synthetic biology and genome engineering are good approaches!
(2) Please mainly focus on the secondary metabolite synthesis.
(3) How robust of these metabolite synthetic pathways are in response to environmental changes? How are the levels of synthetic enzymes regulated normally or in response to abiotic stress such as climate conditions? Through gene expression and epigenetic alterations?
(4) How are enzymatic activities altered CHEMICALLY in response to abiotic stress? Are there chemical characteristics of synthetic enzymes vulnerable to elevated temperature and other stressors?
(5) How are the alterations of signal transduction pathways in response to environmental changes transmitted to these metabolic pathways?
(6) Since secondary metabolites are synthesized for plant defense, are these mechanisms already installed in plants? For example, plants routinely respond to daily changes of temperature and seasonal changes of temperature. Since elevated CO2 was relatively stable in the past million years, do plants have a mechanism to deal with increasing CO2 and high-levels of carbohydrates? How do sugar levels affect secondary metabolites?

st Reviews, Editor Decision, and Authors' Response
1st Editorial Decision 01/14/2020 Manuscript ID GGN-2019-0009 entitled "Climate change shapes the future evolution of plant metabolism" which you submitted to Genetics & Genomics Next, has been reviewed very favorably and minor revisions have been requested. I invite you to respond to the comments appended below and revise your manuscript.
Editor Comments to Author: Please address all reviewers' comments and add one additional section in the manuscript according to the reviewer 1, "One related topic that I found to be missing here to be clearly stated is the rapid growth of the world's human population and challenges arising from it. The need to drastically increase global food production will require to find ways to fast adapt crops to environmental stresses and to further increase crop yields, which intersects with the challenges posed by climate change. I wonder if the authors might find a place in the manuscript to emphasize this issue with a sentence or two". This content was in fact mentioned in your abstract, but not included in the manuscript, "We explore potential avenues of future scientific investigations, powered by cutting-edge methods such as synthetic biology and genome engineering, to better understand and mitigate the consequences of rapid climate change on plant fitness and plant usage by humans". ________________________________________________________________________________________ Reviewer(s)' Comments to Author:

Reviewer: 1
Comments to the Author This review discusses possible impacts of climate change on plants and how plant science can mitigate negative effects on crop productivity. The authors start by describing the general significance of plants and plant products for human life. They point out several plant secondary metabolites with medical uses. A short overview of earth's climate history within the 500 million years, where evolution of land plants took place, makes clear that Earth's flora had to adapt many times to drastic environmental changes. Yet, recent human activity caused a very fast rise in CO2. The increase in CO2 impacts the climate, which poses a challenge to plant growth. Temperature, humidity, ground ozone and UV radiation are identified as major factors that change rapidly and have an effect on plant growth. The balance between growth and defense, which humans have changed in crops to make them more useful, is majorly disturbed. The change in climate has a noticeable Influence on quality and flavor of crop plants adapted to specific environments.
While there is a positive impact of increased CO2 levels on plant growth, negative impacts of climate change might outweigh these in many cases. To be able to better address these issues, it is of increasing interest to better understand the growth-defense antagonism in crop plants, which is being disturbed. Also, to be able to adapt crops to climate change, it might be important to further study and harness existing plant diversity in order to identify mechanisms for adaptation that could be transferred to crop plants. The authors point out that some of the less understood fields of research relevant to adaptations of plants to changing environment are epigenetic mechanisms and RNA secondary structure and their impact on gene expression. The authors conclude in highlighting recent technologies in biochemical and molecular analytics, genome editing and synthetic biology as tools that can be used to better understand the biology of the plants that humanity relies on in order to address the challenges that climate change poses. Altogether the manuscript is a well written overview of the current understanding of the impacts of climate change on plants humans rely on for food and many other uses. It is a good reference leading the reader into current topics in plant science that might be important to answer the challenges.
One related topic that I found to be missing here to be clearly stated is the rapid growth of the world's human population and challenges arising from it. The need to drastically increase global food production will require to find ways to fast adapt crops to environmental stresses and to further increase crop yields, which intersects with the challenges posed by climate change. I wonder if the authors might find a place in the manuscript to emphasize this issue with a sentence or two.

Reviewer: 2
Comments to the Author This perspective review provides an overview of the impact of climate change on crop physiology, metabolism and productivity. The authors also briefly discuss the prospects that synthetic biology has to offer to alleviate some of the corresponding negative effects. Overall, the review is well written. It is intended for a layman -though scientifically literate-audience rather than to experts on the topic. The manuscript does not address any concepts or opinions that one hasn't already read or heard about, but the references are appropriate and up to date. In short, this is a decent summary of the mainstream opinions on this subject.
A few points to consider though: p6: It seems odd to start the section describing climate change as preceding mass extinction of plant species and endangering human existence by 'The good news is that [...] plants have certainly tolerated and overcome more extreme challenges than present day temperatures and CO2 levels'. I suggest to remove 'The good news is that'.
p7: I would remove 'Luckily' (there is nothing 'lucky' or to be proud of in having humans contributing to the current climate crisis; science and technological advances have a major responsibility in such a crisis). Also, there is not one human society, but some human societies.
p7: Not all phenylpropanoids are specialized metabolites. For instance t-cinnamate and p-coumarate are vital to plant life (e.g. null mutants of cinnamate-4-hydroxylase are lethal); they are primary metabolites.
p15: The last sentence of the paper is odd too ['Although this seems like a sound plan to cope with the changing climate and to keep up with the exponential growth of the human society, we must ask ourselves, is this where we really want to go? The choice in our hands [sic].'].
Since climate change is already happening, what choices does humanity has other than breeding and engineering plants with corresponding desirable traits?
Panels a, b, c, d of Figure 1 are not called in the text in the order they are presented (e.g. 1C is called before a and b). Although this eventually remains an editorial choice, I suggest to re-order the panels in Figure 1, so those match the text.
Panel 1d is non-informative (and the drawings not publication grade); I would delete it _____________________________________________________________________________________________ impacts the climate, which poses a challenge to plant growth. Temperature, humidity, ground ozone and UV radiation are identified as major factors that change rapidly and have an effect on plant growth. The balance between growth and defense, which humans have changed in crops to make them more useful, is majorly disturbed. The change in climate has a noticeable Influence on quality and flavor of crop plants adapted to specific environments. While there is a positive impact of increased CO2 levels on plant growth, negative impacts of climate change might outweigh these in many cases. To be able to better address these issues, it is of increasing interest to better understand the growth-defense antagonism in crop plants, which is being disturbed. Also, to be able to adapt crops to climate change, it might be important to further study and harness existing plant diversity in order to identify mechanisms for adaptation that could be transferred to crop plants. The authors point out that some of the less understood fields of research relevant to adaptations of plants to changing environment are epigenetic mechanisms and RNA secondary structure and their impact on gene expression. The authors conclude in highlighting recent technologies in biochemical and molecular analytics, genome editing and synthetic biology as tools that can be used to better understand the biology of the plants that humanity relies on in order to address the challenges that climate change poses. Altogether the manuscript is a well written overview of the current understanding of the impacts of climate change on plants humans rely on for food and many other uses. It is a good reference leading the reader into current topics in plant science that might be important to answer the challenges.
One related topic that I found to be missing here to be clearly stated is the rapid growth of the world's human population and challenges arising from it. The need to drastically increase global food production will require to find ways to fast adapt crops to environmental stresses and to further increase crop yields, which intersects with the challenges posed by climate change. I wonder if the authors might find a place in the manuscript to emphasize this issue with a sentence or two.
We thank Reviewer 1 for her/his thoughtful content suggestions. We found it a relevant consideration for future work and have added a sentence in that section.

Reviewer: 2
Comments to the Author This perspective review provides an overview of the impact of climate change on crop physiology, metabolism and productivity. The authors also briefly discuss the prospects that synthetic biology has to offer to alleviate some of the corresponding negative effects. Overall, the review is well written. It is intended for a layman -though scientifically literate-audience rather than to experts on the topic. The manuscript does not address any concepts or opinions that one hasn't already read or heard about, but the references are appropriate and up to date. In short, this is a decent summary of the mainstream opinions on this subject.
A few points to consider though: p6: It seems odd to start the section describing climate change as preceding mass extinction of plant species and endangering human existence by 'The good news is that [...] plants have certainly tolerated and overcome more extreme challenges than present day temperatures and CO2 levels'. I suggest to remove 'The good news is that'.
We have revised accordingly.
p7: I would remove 'Luckily' (there is nothing 'lucky' or to be proud of in having humans contributing to the current climate crisis; science and technological advances have a major responsibility in such a crisis). Also, there is not one human society, but some human societies.
We have revised accordingly.
p7: Not all phenylpropanoids are specialized metabolites. For instance t-cinnamate and p-coumarate are vital to plant life (e.g. null mutants of cinnamate-4-hydroxylase are lethal); they are primary metabolites.
Regarding the light-induced phenylpropanoids (p7), we have adjusted the wording to refer more accurately reflect the specialized phenylpropanoids discussed in the two references.
p15: The last sentence of the paper is odd too ['Although this seems like a sound plan to cope with the changing climate and to keep up with the exponential growth of the human society, we must ask ourselves, is this where we really want to go? The choice in our hands [sic].'].
Since climate change is already happening, what choices does humanity has other than breeding and engineering plants with corresponding desirable traits?
Thanks for the suggestion. We have revised the last sentence to "Existing, preliminary, planned and future efforts to understand and augment our repertoire of plants and their mechanisms of resilience will continue to serve humanity into future generations." Panels a, b, c, d of Figure 1 are not called in the text in the order they are presented (e.g. 1C is called before a and b). Although this eventually remains an editorial choice, I suggest to re-order the panels in Figure 1, so those match the text.
Panel 1d is non-informative (and the drawings not publication grade); I would delete it.
Regarding Figure 1, we see the point that Panel D did not add anything to the figure, and have implemented your suggestions to remove that panel and rearranged the order of Panels A, B and C.
2 nd Editorial Decision 02/06/2020 We recommend adding a table with the secondary metabolites and their related regulatory pathways in the tradeoff between the production and defense in response to various climate change conditions. You discussed about them in the text, and a Thank you for revising your manuscript. It reads great! Before sending it to our production team, we recommend some minor edits in the text (see the track changes in the attached manuscript). Please also use numbers for your cited references in the text to fit our journal style, following our guide for authors.
We have adjusted our references accordingly.
We recommend adding a table with the secondary metabolites and their related regulatory pathways in the tradeoff between the production and defense in response to various climate change conditions. You discussed about them in the text, and a table can help strengthen your points. We suggest that you organize four main classes of specialized metabolite compounds, terpenoids, phenolic compounds, alkaloids, and sulphur-containing compounds, using internationally recognized chemical identifiers (INCHI or SMILE) or ontological terms. Ontology supports for chemical entities, molecular functions and interactions and plant environmental conditions: https://www.ebi.ac.uk/ols/index, http://www.ontobee.org, https://bioportal.bioontology.org https://pubchem.ncbi.nlm.nih.gov, https://www.ebi.ac.uk/chebi/ While we see that a visual reference in the form of a table might be a useful tool for readers to better understand the material, we believe that including such a table in the present manuscript will not add value, and in fact, may mislead readers. To elaborate: a closer inspection of the growth-defense balance section reveals that we mentioned only three plant hormones, which seems insufficient to build a table around. If, instead, the request was for us to include all metabolites from the entire paper to be included in the table, we believe that such a compilation would be better left for a more thorough review, such as in Annual Reviews. This is because, in our manuscript, we discuss only scattered studies, and presenting this in a table may give the misimpression that the contents are a holistic review of the field, which is not true.