Climate change challenges the adaptive capacity of several forest tree species in the face of increasing drought and rising temperatures. Therefore, understanding the mechanistic connections between genetic diversity and drought resilience is highly valuable for conserving drought-sensitive forests. Nonetheless, the post-drought recovery in trees from a transcriptomic perspective has not yet been studied by comparing contrasting phenotypes. Here, experimental drought treatments, gas-exchange dynamics, and transcriptomic analysis (RNA-seq) were performed in the relict and drought-sensitive fir Abies pinsapo to identify gene expression differences over immediate (24 hours) and extended drought (20 days). Post-drought responses were investigated to define resilient and sensitive phenotypes. Single nucleotide polymorphisms (SNPs) were also studied to characterize the genomic basis of A. pinsapo drought resilience. Weighted gene co-expression network analysis showed an activation of stomatal closing and an inhibition of plant growth-related genes during the immediate drought, consistent with an isohydric dynamic. During the extended drought, transcription factors, as well as cellular damage and homeostasis protection-related genes prevailed. Resilient individuals activate photosynthesis-related genes and inhibit aerial growth-related genes, suggesting a shifting shoot/root biomass allocation to improve water uptake and whole-plant carbon balance. 152 fixed SNPs were found between resilient and sensitive seedlings, which were mostly located in RNA-activity-related genes, including epigenetic regulation. Contrasting gene expression and SNPs were found between different post-drought resilience phenotypes for the first time in a forest tree, suggesting a transcriptomic and genomic basis for drought resilience. The obtained drought-related transcriptomic profile and drought-resilience candidate genes may guide conservation programs for this threatened tree species.

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Forest tree species are highly vulnerable to the effects of climate change. As sessile organisms with long generation times, their adaptation to a local changing environment may rely on epigenetic modifications when allele frequencies are not able to shift fast enough. However, the current lack of knowledge on this field is remarkable, due to many challenges that researchers face when studying this issue. Huge genome sizes, absence of reference genomes and annotation, and having to analyze huge amounts of data are among these difficulties, which limit the current ability to understand how climate change drives tree species epigenetic modifications. In spite of this challenging framework, some insights on the relationships among climate change-induced stress and epigenomics are coming. Advances in DNA sequencing technologies and an increasing number of studies dealing with this topic must boost our knowledge on tree adaptive capacity to changing environmental conditions. Here, we discuss challenges and perspectives in the epigenetics of climate change-induced forests decline, aiming to provide a general overview of the state of the art.

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The frequency and intensity of drought events are increasing worldwide, challenging the adaptive capacity of several tree species. Here, we evaluate tree growth patterns and climate sensitivity to precipitation, temperature, and drought in the relict Moroccan fir Abies marocana. We selected two study sites, formerly stated as harboring contrasting A. marocana taxa (A. marocana and A. tazaotana, respectively). For each tree, dendrochronological methods were applied to quantify growth patterns and climate–growth sensitivity. Further, ddRAD-seq was performed on the same trees and close saplings to obtain single nucleotide polymorphisms (SNPs) and related genotype–phenotype associations. Genetic differentiation between the two studied remnant populations of A. marocana was weak. Growth patterns and climate–growth relationships were almost similar at the two sites studied, supporting a negative effect of warming. Growth trends and tree size showed associations with SNPs, although there were no relationships with phenotypes related to climatic sensitivity. We found significant differences in the SNPs subjected to selection in the saplings compared to the old trees, suggesting that relict tree populations might be subjected to genetic differentiation and local adaptation to climate dryness. Our results illustrate the potential of tree rings and genome-wide analysis to improve our understanding of the adaptive capacity of drought-sensitive forests to cope with ongoing climate change.