Comparing Norway spruce and Scots pine, two species separated by a deep evolutionary divergence, it is shown that the genes whose co-expression is most broadly conserved between the species are also those under the strongest purifying selection on their protein-coding sequences.
Abstract
Norway spruce (Picea abies) and Scots pine (Pinus sylvestris) are dominant boreal forest species with globally important contributions to carbon capture and storage and sustain an extensive forestry industry. Both species have adapted to cold and episodic drought, yet each occupies a distinct ecological niche. How conserved their stress responses are, which features are lineage-specific, and how far mechanisms known from herbaceous angiosperms apply, remain open questions of importance in the face of ongoing climate change. We profiled roots and needles of both species under drought and cold, combining differential expression with an orthology-aware comparative co-expression framework that places each gene on a conservation–divergence gradient. Differential expression was largely organ- and stress-specific, yet cross-species overlap at the orthogroup level was extensive and increased with stress intensity. Comparative co-expression recovered a further conserved regulatory backbone that per-timepoint differential expression did not resolve, enriched for abscisic-acid-centred signalling, oxidative and osmotic-stress responses and growth suppression, and containing canonical stress response transcription-factor families including NAC, WRKY and bZIP/ABF. The breadth of co-expression conservation for a gene was coupled to purifying selection on its coding sequence and to network connectivity. Additionally, segmental duplicates shared between the species were enriched among conserved drought circuits, whereas lineage-specific duplicates were enriched among genes lacking conserved co-expression. Regulatory conservation and genome architecture thus describe a single conservation–divergence axis, providing an evolution-anchored criterion that helps separate candidate core regulators (which are conserved, network-central and constrained) from reactive change that differential expression alone cannot resolve. Significance statement Cold and drought are recurring threats to boreal forests, yet how conifers coordinate their responses, and how much of that response is evolutionarily conserved, has been difficult to establish. Comparing Norway spruce and Scots pine, two species separated by a deep evolutionary divergence, we show that the genes whose co-expression is most broadly conserved between the species are also those under the strongest purifying selection on their protein-coding sequences. As these two species diverged so long ago, this conserved regulatory core stands out as an evolutionary signal that simple comparisons of differentially expressed genes fail to capture. The approach provides an evolution-anchored way to distinguish genes central to the stress response from lineage-specific or reactive change.
• Climate change is reducing the boreal snowpack that insulates soils, exposing tree roots to more frequent freezing. The molecular cold response of roots is poorly characterised, and its conservation across the angiosperm–gymnosperm divide is unknown. We asked how much of the root cold response is shared among divergent boreal trees. • We profiled fine-root transcriptomes of four boreal trees (Picea abies, Pinus sylvestris, Betula pendula and Populus tremula) and two Arabidopsis thaliana ecotypes during a ten-day 5 °C treatment by RNA sequencing, and used comparative co-expression to detect conserved regulation independently of response timing. • Expressed genes were largely shared, but the genes differentially expressed, and the timing of their response, diverged between species. Despite this, a core of orthologues retained conserved co-expression neighbourhoods across more than 300 million years, enriched for growth regulation, metabolism and stress signalling, including a gibberellin-related metabolic component of the growth response. • The root cold response is therefore species specific in identity and timing, yet underlain by a conserved co-expression core.
Tuuli Aro, Elena M. van Zalen, Alexander Vergara et al.· bioRxiv· 0 citations
Maritime pine (
Pinus pinaster
Aiton) is a key conifer in southwestern Europe showing ecological plasticity and economic importance. Understanding molecular interactions between above- and below-ground organs is essential for improving forest resilience and management under changing environmental conditions. Previous transcriptomic analyses of a full-sib family using progenitors from contrasting precipitation regions identified differences between drought-tolerant and drought-sensitive genotypes. Grafting experiments further indicated that rootstocks can modulate transcriptomes in aerial tissues. Here, we analyse truTranscriptomes were influenced by scion origin in a rootstock-dependent manner. In tolerant rootstocks, scions from an arid-region promoted transcriptional patterns related to resource conservation and root remodelling. Scions from a wetter region triggered transcriptional patterns related to broader metabolic adjustments. Sensitive rootstocks showed greater transcriptional responsiveness to scion identity, particularly in pathways related to primary metabolism, osmolyte synthesis and growth. A shared set of genes was consistently regulated across graft combinations, suggesting conserved components of scion–root communication. These findings provide the first comprehensive description of root transcriptomic variation in grafted maritime pine and advance a whole-plant framework for understanding molecular integration in conifers.
Irene Cobo-Simón, L. F. Manjarrez, N. de María et al.· Scientific Reports· 0 citations
In the context of climate change plants have to cope with adverse conditions, among which water scarcity is a major threat for their survival. They have developed diverse regulatory processes to face drought that may differ depending on their ecological niche. The two sympatric oaks species (Quercus robur L. and Quercus petraea (Matt.). Liebl) have different levels of drought tolerance. We have investigated their strategies to face drought stress by analysing the transcriptome, small RNAome and methylome dynamics of young plants grown under control and drought stress conditions. Data indicate that cell wall remodeling is most likely involved in the better tolerance Q. petraea than of Q. robur. Furthermore, major methylation differences were identified between both oak species that were in part associated to their difference in drought stress responses. Integration of the three datasets revealed genomic co-locations of potential importance for forest tree adaptation to drought stress. Our data are consistent with species-specific molecular responses of oak to drought stress related to their ecological niches.
B. Rubio, G. Le Provost, B. Brachi et al.· Tree Physiology· 0 citations
Understanding intraspecific variation in drought tolerance is essential for predicting the adaptive capacity of forest species under climate change. Yet, the molecular basis of this variation remains poorly understood in ecologically and economically important conifers. We integrated high-throughput phenotyping with metabolomics and transcriptomics under standardised soil drying to investigate drought responses across nine climatically distinct provenances of the conifer Pinus nigra. We tested whether drought tolerance-measured as decline in maximum quantum yield of the photosystem II (Fv/Fm)-varies among provenances, follows a climatic cline, and involves trade-off with growth. To identify the underlying molecular basis, we performed metabolomics and transcriptomics in four provenances representing contrasting drought tolerance. Drought tolerance varied significantly among provenances and was decoupled from growth, yet showed no differentiation along the climatic cline. Drought-tolerant provenances differed from sensitive ones in both constitutive abundance and drought-induced accumulation of the flavonoid pinostrobin and the diterpene hydroxydehydroabietic acid. Transcriptomic profiles further highlighted provenance-specific differences in gene expression related to flavonoids. Overall, these findings link phenotypic drought responses to molecular variation among provenances, providing insight into the molecular basis of drought responses in an important conifer species.
Muhammad Ahmad, A. Hammerbacher, Clara Priemer et al.· Plant, Cell and Environment· 0 citations
Plants are increasingly exposed to simultaneous warming, drought, and herbivory, yet how invasive and native species regulate carbon allocation under these interacting stressors remains poorly understood. We conducted a full-factorial greenhouse experiment manipulating temperature (+3 °C), soil water availability, and herbivory to compare carbon allocation responses in the invasive Solidago canadensis and its native congener S. decurrens. Drought emerged as the dominant driver of carbon reallocation, shifting investment away from biomass production and photosynthetic function toward belowground allocation, osmotic adjustment, defense, and structural reinforcement. Herbivory imposed additional carbon demands and modified drought-induced responses, particularly by constraining phenolic accumulation under combined stress, whereas warming had comparatively weaker and largely context-dependent effects. Our results showed that the two species differed in how carbon was distributed under stress: S. canadensis maintained greater biomass, chlorophyll, soluble sugars, and hemicellulose, whereas S. decurrens showed stronger investment in structural components. Structural equation models further revealed contrasting pathways linking physiological, defensive, and structural traits to biomass, supporting species-specific strategies of carbon allocation under multiple stressors. These findings suggest that the greater carbon-allocation flexibility observed in S. canadensis may contribute to maintaining performance under increasingly variable environmental conditions. However, because S. canadensis was raised directly from field-collected seeds without a refresher generation, potential maternal environmental effects cannot be completely excluded. Overall, our findings identify coordinated redistribution of carbon among competing functional pools as a potential mechanism underlying contrasting stress responses in these two congeneric species.
J. Okundi, Ling Yuan, Guan-Lin Li et al.· Plants· 0 citations
Photorespiration and drought-induced stomatal closure are two important physiological constraints that reduce carbon assimilation and productivity in C3 forest trees under Mediterranean climatic conditions. Türkiye’s two dominant commercial pine species, Pinus brutia Ten. (Calabrian pine) and Pinus nigra J.F. Arnold subsp. pallasiana (Anatolian black pine), together cover approximately 8.15 million hectares. This study integrated published gas-exchange measurements, radiation-use efficiency estimates from MODIS, official forest inventory data, and dendrochronological growth records into a counterfactual accounting framework and propagated parameter uncertainty by Monte Carlo simulation (N = 40,000 draws). The two constraints jointly reduced weighted-mean net primary productivity (NPP) from a radiation-limited potential of 5.61 to an actual 3.46 Mg C ha−1 yr−1, a reduction of 37.9% (95% CI 32.2–43.4%). Decomposition shows that 47.7% of this loss is the obligate metabolic cost of C3 carboxylation, which no silvicultural intervention can address, while 52.3%—20.1 of the 37.9 percentage points—is drought-attributable. Nationally, the deficit corresponds to 64.3 Mt CO2 yr−1 of forgone sequestration (47.8–81.2) and 34.4 Mm3 yr−1 of forgone stemwood-volume equivalent (24.9–44.5), of which approximately 20.6 Mm3 would be merchantable, giving an annual economic deficit of USD 3.37 billion (2.40–6.48). Filtering the drought-attributable component for eligible area, recovery efficiency, additionality, leakage, and permanence yields approximately 1.0 Mt CO2 yr−1 of potentially issuable credits, fewer than two per cent of the headline figure. Eco-physiological suppression of this magnitude is currently invisible in national forest carbon accounting, and its recognition bears directly on dynamic baseline design and on the credibility of offsets generated from Mediterranean conifer forests.
Emre Yazar, Bülent Akgün, E. Babur· Plants· 0 citations
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