Seed physiology, which was a little forgotten in forest ecology since several decades, needs be revitalized as a research area given the many open questions about population dynamics and demography in rapidly changing environments (and not only for endangered species). 

Indeed, seed physiology was long mobilized mainly to optimize seed conservation and germination for the production of plant material in a range of tree species used for afforestation/plantation. In the case of back poplar (which by the way is the male genitor of the multiple hybrid Populus x euramerica poplar cultivars), the focus is rather on the conservation ecology of this riparian species, and mainly on in situ conservation (Lefèvre et al, 1998). Indeed, the protection of populations of Populus nigra L requires an improved understanding of the ecology of this species with a focus on reproduction. Indeed, black poplar seeds need to be rapidly disseminated, to germinate as soon as the conditions are favourable (with rather small time windows) and establish seedlings with access to water in the rather harsh environment of mobile and sandy river banks submitted to alternating periods of flooding and of severe water deficits during low river flows in summer (Imbert and Lefèvre, 2003; Corenblit et al, 2014; Tinschert et al, 2020).

This process is therefore central to the propagation/maintenance of these populations that are threatened by the destruction of river banks and by introgression by either genes from the widespread “Italica” cultivar of black poplar, of from other poplar species leading to a variety of natural hybrids (Smulders et al, 2008).

Many questions remain open about seeds of black poplar (Michalak et al, 2015). One of the most intriguing one is to what extent seed properties and physiology differ within and among local populations from different river catchments. This question was addressed in this preprint by Lefebvre et al. (2021) that provides a very detailed and comparative analysis of two populations from central and southern France, each represented by 10 half sib families (i.e., seed collected separately from 10 adult individuals after open pollination).

Investigated properties were mainly seed biomass, anatomy, germination rate, root growth, lipid and sugar contents, protein content (with identification of some major protein families).

The within populations variability was indeed quite large, but nevertheless there were significant differences between the two populations in several traits, like seed weight, lipid content, and starch content. Storage proteins differed among families, but only slightly between the two populations. However, the main conclusion was that intrinsic qualities of the seeds were not critical for early stage establishment in the two populations, despite some significant differences in mean seed biomass, in lipid and in soluble sugars contents.

The preprint nicely analyses these differences, brings a large set of new observations about the seed physiology of Populus nigra. The referees found the data produced during this research quite important and original. This is why, despite the fact that the number of tested groups of populations remains rather small and the link with seedling establishment remains rather weak, this study is an important contribution to conservation ecology. This research (and that of many other groups) needs be further developed with an emphasis on inter and intra population variation and on demogenetics of forest tree species.

References

Corenblit D., Steiger J., González, E et al. (2014), The biogeomorphological life cycle of poplars during the fluvial biogeomorphological succession: a special focus on Populus nigra L.. Earth Surf. Process. Landforms, 39: 546-563. doi: https://doi.org/10.1002/esp.3515

Imbert E. and Lefèvre F. (2003) Dispersal and geneflow of Populus nigra (Salicaceae) along a dynamic river system. Journal of Ecology  91: 447-456. doi: https://doi.org/10.1046/j.1365-2745.2003.00772.x

Lefebvre M., Villar M., Boizot N., Delile A., Dimouro B., Lomelech A.-M. and Teyssier, C. (2021) Variability in seeds’ physicochemical characteristics, germination and seedling growth within and between two French Populus nigra populations. arXiv, 2008.05744, ver 3 peer-reviewed and recommended by Peer community in Forest and Wood Sciences. https://arxiv.org/abs/2008.05744

Lefèvre F., Légionnet A., de Vries S. and Turok J. (1998) Strategies for the conservation of a pioneer tree species, Populus nigra L., in Europe. Genetics, Selection, Evolution 30, S181-196. doi: https://doi.org/10.1186/1297-9686-30-S1-S181

Michalak M., Plitta B.P., Tylkowski T. et al. (2015) Desiccation tolerance and cryopreservation of seeds of black poplar (Populus nigra L.), a disappearing tree species in Europe. European Journal of Forest Research 134, 53–60. doi: https://doi.org/10.1007/s10342-014-0832-4

Smulder M.J.M., Beringen R., Volosyanchuk R. et al. (2008) Natural hybridisation between Populus nigra L. and P. x canadensis Moench. Hybrid offspring competes for niches along the Rhine river in the Netherlands. Tree Genetics & Genomes 4, 663–675. doi: https://doi.org/10.1007/s11295-008-0141-5

Tinschert E., Egger G., Wendelgass J. et al. (2020) Alternate reproductive strategies of Populus nigra influence diversity, structure and successional processes within riparian woodlands along the Allier River, France. Journal of Hydro-environment research 30, 100-108. doi: https://doi.org/10.1016/j.jher.2020.03.004

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