This preprint is recommended after a round of reviews by two external reviewers and the recommender and a careful revision of the initial text. The revision addressed all the the concerns raised by the reviewers and myself acting as recommender. I commend the authors for the care taken in the revision process and in addressing all concerns raised by the referees. The preprint is now in a status anabling a very positive recommendation, and I am convinced that PCI friendly journals will be keen to publish it given the quality of the contribution to Forest Pathology and Epidemiology as well as to and Forest Ecology.

Indeed, the preprint adresses an important topic in forest ecology and forest management. Powdery mildew (due to a complex of fungi species of Erysiphe spp.) is a very frequent pathogen affecting oaks and mainly English oak (Quercus robur L.),  a widespread species in Western European forests which bears great ecological and economic interests (see Marçais and Desprez-Loustau, 2014, for a review). Young regenerations are mostly affected by the disease, which infects young, unfoldling leaves and leads to severe reductions in photosynthesis (Hajji et al, 2009) and in some cases to tree dieback in young regenerations, and sometimes in older trees in the case of repeated infestations over several years, or combinations with defoliaitions by processionnary moths (Thaumetopoea processionea L.). Powdery mildew was introduced to Europe at the beginning of the 20th century and caused initially very severe damage in oak stands; currently, damage is much less prevalent, probably due to a co-evolution of the oak host and the pathogen (Desprez-Loustau and Marçais, 2019).

The present investigation adds very interesting and important information to our current knowledge of this disease, and addresses in particular the genetic variability of susceptibility to the disease among oak families and the effect of the disease on the survival of seedlings in the long run. Five main research questions were addressed: i. How does powdery mildew affect juvenile survival; ii. Is the survival rate differing among oak families? iii. Does powdery mildew infection reduce the differences of fitness among oak families? iv. Does powdery mildew impact the genetic diversity of oak populations? v. Are there significant genetic associations between some genetic loci and seedling survival? These questions are important for unerstanding the evolution of a pathosystem like the powdery mildew/English oak system and for explaining the past dynamics of this pathosystem, which resulted in a dicrease in virulence of the disease since its introduction in Europe.

The preprint reports results from a very original and solid experimental design based on the cultivation in the field of 15 oak progenies comprising 1733 indivduals over a quite long time span (9 years) and recurrent observations of growth, survival, infection intensity, ... A control group was protected against the pathogen by application of a fungicide. Moreover, a large number of individuals were genotyped, using single nucleatide polymorphism (SNP) allowing the detection of some candidate loci, and preparing future genome-wide association studies. The results are quite clear, and add very important elements to our understaning of this interesting and evolving pathosystem present in mots of the western European oak forests. 

This preprint is of particular interest since such approaches, which are becoming common in cultivated crops, have only seldom been applied to natural pathosystems despite their importance for the dynamics of forest ecosystems under the increasing impact of climate change. In brief, this is an important preprint that brings a large set of new data and addresses the urgent question of epidemiology of diseases in forest ecosystems.

References

Barrès B, Dutech C, Saint-Jean G, Bodénès C, Burban C, Fiévet V, Lepoittevin C, Garnier-Géré P, Desprez-Loustau M-L (2024) Demographic and genetic impacts of powdery mildew in a young oak cohort. bioRxiv, 2023.06.22.546164, ver. 2 peer-reviewed and recommended by Peer Community in Forest and Wood Science. https://doi.org/10.1101/2023.06.22.546164

Desprez-Loustau ML, Hamelin FM, Marçais B (2019) The ecological and evolutiionary trajectory of oak powdery mildew in Europe. In: Wilson K, Fenton A, Tompkins D, Wildlife Disease Ecology: Linking Theory to Data and Application. Ecological Reviews. Cambridge University Press, 978-1-107-13656-4.
https://doi.org/10.1017/9781316479964.015
 
Hajji M, Dreyer E, Marçais B. (2009) Impact pf Erysiphe alphotoides on transpiration and photosynthesis in Quercus robur leaves. Eur J Plant Pathol, 125, 63-72, 
https://doi.org/10.1007/s10658-009-9458-7
 
Marçais B, Desprez-Loustau ML (2014) European oak powdery mildew: impact on trees, effects of environmental factors, and potential effects of climate change. Ann For Sci, 71, 633-642, 
https://doi.org/10.1007/s13595-012-0252-x