When we launched the multidisciplinary PCI Forest and Wood Sciences, we were well aware that this PCI devoted to a broad object (forests represent 1/3 of the emerged land area) and gathering multiple disciplines (from biology to social sciences), would be confronted with some challenges with respect to the range of pre-prints we would have to consider. Among the first ones submitted to the new PCI was this very interesting one (Lang et al, 2021) in the area of tree genomics and tree population genetics with a strong background in bioinformatics. This could well have been submitted to the PCI in Genomics, or the PCI in Evolutionary Biology, but finally fits very well in PCI Forest and Wood Sciences due to its finality: provide reliable genomic resources to tackle questions that are central to our understanding of the dynamics of forest ecosystems and the adaptation of trees to local conditions.
The phylogenetic status of the two sympatric oak species Quercus robur L. and Q. petraea Matt. Liebl. is an important question that was the center of in depth investigations by the BioGeCo research group at Bordeaux in cooperation with many European groups. The two species are major forest tree species in western Europe, structuring important ecosystems and providing high quality wood and other important ecosystem services. These species are considered to build up what is now called a “syngameon” together with a few other western European white oaks (Cannon and Petit, 2019). A syngameon is a complex of species exchanging genes, while still maintaining some degree of interspecific diversity enabling to differentiate, on the basis of leaf morphology for instance, the originally described species (Kremer et al, 2002 among many others dealing with the identification of oak species on the basis of their phenotype). The full sequencing of the genome of Q. robur (Plomion et al, 2018) opened an avenue for the development of new genomic tools to investigate the concept of species in this syngameon and to identify gene flows between populations and species. To date, whole genome sequencing and annotation is completed for Q. robur, Q. lobata Née, Q. suber L., and Fagus sylvatica L. (Plomion and Martin, 2020).
The preprint of Lang et al (2021) builds up on this background and provides a very interesting and important contribution to this area. First, it provides access to a very large data base of genomic sequences, based on 800 gene fragments and identified 12500 Single Nucleotide Polymorphisms (SNPs) as well as 1500 insertions deletions. 11 individuals assigned to the species Q. robur, 13 assigned to Q. petraea and 1 to Q. ilex L. were used to establish this data base. This is an important asset for developing future research on species identification based on their genomes. In full agreement to the policy of all PCIs about data availability, full access is provided to the data under a free use license CC-BY.
The manuscript has already a long history as a preprint and it was not that easy to find reviewers willing to do the job of reviewing such a large amount of information with a lot of technical details. At the end, we succeeded and obtained three very enthusiastic and positive reviews (attached to this recommendation). All reviewers agreed that this was an important contribution in the field, insisted on the quality of the writing and of the provided data, and finally agreed that the manuscript was to be recommended after a careful revision. The revision was readily done by the authors. One of the reviewers found that the preprint is close to a “data paper”, i.e., a paper providing the required information to enable (and advertise) the reuse of an important data set, which is only partly true. Indeed, the authors nicely used their data to address one of the most debated questions about the population genetics: how comes that in this syngameon, with inter-fertile individuals, clearly distinguishable species (from the phenotype at least) have been maintained?
The main result of the preprint is that indeed there are some (only few) genomic differences among the two species in the patterns of distribution of the SNPs, but also that the patterns reveal a clear introgression of the genome of one of the species into the other one. This was based on a Bayesian clustering analysis reported figure 3, evidencing that 2 individuals displaying an unambiguous Q. petraea phenotype could not be assigned to any of the species. The usual hypothesis postulates an introgression of the Q. robur genome, the pioneer species able to colonize open areas during the post-glacial recolonization into that of Q. petraea, due to hybridization and successive events of back gross with inflowing Q. petraea pollen. Such an introgression was hypothesized decades ago, and receives here some degree of confirmation. Recent findings showed the importance of such an introgression for the adaptation of local oak populations to altitudinal gradients (Leroy et al, 2020).
Given the importance of the contribution (both from the point of view of the development of new genomic tools and from that of our understanding of the population genetics in the oak syngameon, I do recommend this preprint in the frame of the PCI Forest and Wood Sciences after an insightful peer reviewing and a very careful revision leading to the current version 4 of this preprint.
 

References

Cannon CH, Petit RJ (2020) The oak syngameon: more than the sum of its parts. New Phytologist, 226, 978–983. https://doi.org/10.1111/nph.16091
 
Kremer A, Dupouey JL, Deans JD, Cottrell J, Csaikl U, Finkeldey R, Espinel S, Jensen J, Kleinschmit J, Dam BV, Ducousso A, Forrest I, Heredia UL de, Lowe AJ, Tutkova M, Munro RC, Steinhoff S, Badeau V (2002) Leaf morphological differentiation between Quercus robur and Quercus petraea is stable across western European mixed oak stands. Annals of Forest Science, 59, 777–787. https://doi.org/10.1051/forest:2002065
 
Lang T, Abadie P, Léger V, Decourcelle T, Frigerio J-M, Burban C, Bodénès C, Guichoux E, Provost GL, Robin C, Tani N, Léger P, Lepoittevin C, Mujtar VAE, Hubert F, Tibbits J, Paiva J, Franc A, Raspail F, Mariette S, Reviron M-P, Plomion C, Kremer A, Desprez-Loustau M-L, Garnier-Géré P (2021) High-quality SNPs from genic regions highlight introgression patterns among European white oaks (Quercus petraea and Q. robur). bioRxiv, 388447, version 4 peer-reviewed and recommended by PCI Forest and Wood Sciences. https://doi.org/10.1101/388447
 
Leroy T, Louvet J-M, Lalanne C, Provost GL, Labadie K, Aury J-M, Delzon S, Plomion C, Kremer A (2020) Adaptive introgression as a driver of local adaptation to climate in European white oaks. New Phytologist, 226, 1171–1182. https://doi.org/10.1111/nph.16095
 
Plomion C, Aury J-M, Amselem J, Leroy T, Murat F, Duplessis S, Faye S, Francillonne N, Labadie K, Le Provost G, Lesur I, Bartholomé J, Faivre-Rampant P, Kohler A, Leplé J-C, Chantret N, Chen J, Diévart A, Alaeitabar T, Barbe V, Belser C, Bergès H, Bodénès C, Bogeat-Triboulot M-B, Bouffaud M-L, Brachi B, Chancerel E, Cohen D, Couloux A, Da Silva C, Dossat C, Ehrenmann F, Gaspin C, Grima-Pettenati J, Guichoux E, Hecker A, Herrmann S, Hugueney P, Hummel I, Klopp C, Lalanne C, Lascoux M, Lasserre E, Lemainque A, Desprez-Loustau M-L, Luyten I, Madoui M-A, Mangenot S, Marchal C, Maumus F, Mercier J, Michotey C, Panaud O, Picault N, Rouhier N, Rué O, Rustenholz C, Salin F, Soler M, Tarkka M, Velt A, Zanne AE, Martin F, Wincker P, Quesneville H, Kremer A, Salse J (2018) Oak genome reveals facets of long lifespan. Nature Plants, 4, 440–452. https://doi.org/10.1038/s41477-018-0172-3
 
Plomion C, Martin F (2020) Oak genomics is proving its worth. New Phytologist, 226, 943–946. https://doi.org/10.1111/nph.16560

Range limits of forest species are frequently imposed by spatial gradients in climatic variables. Tolerance to maximum and minimum temperatures, including short-term extremes, and tolerance to desiccation are crucial limiting factors for plant survival and often appear interrelated (Box 1995; Choat et al. 2018). Increasing temperatures, more frequent and extreme droughts and late frost events associated with global climate change will affect the dynamics of forest ecosystems and have the potential to dramatically increase plant mortality and accelerate species range shifts if plants are not able to adapt in situ to the novel climate regimes (Parmesan 2006; Choat et al., 2012). This is particularly important at species range edges, where climatic conditions may not be sufficient to impose mortality on individuals directly, but trees experience greater physiological stress, which influences such factors as dispersal, habitat selection, and subsequent reproductive fitness (Parmesan 2006). In such marginal situations, where gene flow may be also restricted (López de Heredia et al. 2010), the effectiveness of adjustment through natural selection is limited resulting in increased vulnerability to extreme climatic events and to a higher risk of mortality of trees.
Tree responses to drought and frost have been extensively studied at many scales from ecophysiology to molecular biology across a large range of species inhabiting diverse biomes (Sakai and Larcher 1987; Bréda et al. 2006). Avoiding dehydration of tissues to maintain cellular viability and function is at the basis of the plant strategy to deal with both constraints as shown by Charrier et al. (2020). These authors go one step further and discuss the impact of the interaction of drought and frost on tree water status and carbon metabolism with special emphasis on the temporal context. Plants from temperate and boreal regions show changes in their resistance to freezing temperature throughout the year (Bower and Aitken 2006) and xylem becomes more resistant to cavitation with cambial age (Rodríguez-Zaccaro et al. 2019). Including timing in this framework involves incorporating phenology. This will be a fundamental step to model species distribution limits in the face of climate change since most observations of climate-change responses have involved alterations of species’ phenologies (Parmesan et al. 2006). For example, the onset of the growing season of trees in temperate Europe is 2.3 days ahead per decade during the last 40 years (Parmesan et al. 2006). Moreover, some studies have shown that climatic constraints limit species distribution mainly because of their impact in phenology rather than their impact on drought and frost mortality (Morin et al. 2007). However, longer growing seasons along with more frequent extreme events increase the probability of long-lived organisms such as trees to experience frosts and drought during the same growing season or one of them after uncompleted recovery of the other in some latitudes. Over the last decade much attention has been devoted to the recovery of growth and ecological function after stressful events (Lloret et al. 2011). Some dendroecological studies have shown for example that resilience to extreme droughts might be constrained by having experienced more frequent droughts, thus exceeding the potential for acclimation of the tree (Bose et al. 2020). Drought can result in chronic hydraulic impairment which can last moths to years (Anderegg et al. 2015) and for some species also in cavitation fatigue, i.e. a progressive increase in vulnerability to cavitation (Hacke et al. 2001), thus increasing vulnerability to subsequent drought and frost events.
Models have proved to be useful tools for synthetizing and integrating climate and soil properties with key functional traits in order to determine desiccation dynamics, carbon metabolism and plant survival during drought of frost (Martin-StPaul et al., 2017; Charrier et al. 2018; Blackman et al., 2019). However, models are currently limited by gaps in our understanding of the fundamental physiological mechanisms that constrain species ranges. Most common approaches to studying species range shifts are related to climatic niches and overlook the processes and traits involved in drought or frost tolerance (Cheaib et al. 2012). Process-based models based on plant hydraulics seem promising providing the link between environmental cues and plant responses, although disregarding carbon metabolism will not give us predictive understanding of system changes such as those due to climate fluctuations (Mackay et al. 2015). New modeling approaches need to be developed not only for better drought prediction performance but for the interaction of drought with other factors. Charrier et al. (2020) offer a framework for improving process-based models with the aim to provide better prediction of carbon and water economy, organ development and ultimately species distribution limits in the face of warmer winters and more frequent winter droughts at high altitudes and late frosts events.

References

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Blackman CJ, Li X, Choat B, Rymer PD, De Kauwe MG, Duursma RA, Tissue DT, Medlyn BE (2019) Desiccation time during drought is highly predictable across species of Eucalyptus from contrasting climates. New Phytologist 224: 632-643. doi: https://doi.org/10.1111/nph.16042
Box EO (1995) Factors determining distributions of tree species and plant functional types. Vegetatio 121, 101–116 (1995). doi: https://doi.org/10.1007/BF00044676
Bower AD, Aitken SN (2006) Geographic and seasonal variation in cold hardiness of whitebark pine. Can J For Res 36:1842–1850. doi: https://doi.org/10.1139/x06-067
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Charrier G, Lacointe A, Améglio T (2018) Dynamic modeling of carbon metabolism during the dormant period accurately predicts the changes in frost hardiness in walnut trees Juglans regia L. Frontiers in Plant Science, 9: 1746. doi: https://doi.org/10.3389/fpls.2018.01746
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