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Key message: Among the variety of leaf defensive strategies to counteract herbivory attacks, the oak species analyzed in this study maximize investment in no more than one, with high-LMA oaks developing very tough leaves and low-LMA oaks favoring between high concentrations of condensed tannins or high growth rates. Context: Plants develop a variety of defense strategies to counteract herbivory attacks, from physical and chemical defenses to tolerance strategies. Tradeoffs between strategies have been widely assessed from a resource allocation perspective, but there is a need to consider eventual interactions among them. Aim: We evaluate the among-species tradeoff between three main constitutive plant defense traits, while considering the leaf mass per area ratio (LMA) as a proxy of leaf construction investment on area basis. Methods: Leaf toughness measured as work of fracture, condensed tannins, and relative growth rate (RGR) were analyzed in a set of 19 Quercus L. species with contrasting LMA. Results: Most species had low values either in two or in the three traits analyzed. Moreover, the highest values of work of fracture appeared in the species with high LMA; the highest values of condensed tannins were found in the species with the lowest LMA; and high values of RGR were measured in species with intermediate or lower values of LMA. Conclusion: Oaks showed a trade-off among leaf defensive strategies influenced by LMA. Oaks with high LMA developed very tough leaves while oaks with low LMA presented lower values of toughness but favored between one of the two other strategies. [ABSTRACT FROM AUTHOR]

Drought is projected to occur more frequently and intensely in the coming decades, and the extent to which it will affect forest functioning will depend on species-specific responses to water stress. Aiming to understand the hydraulic traits and water dynamics behind water-saver and water-spender strategies in response to drought and recovery, we conducted a pot experiment with two species with contrasting physiological strategies, Scots pine (Pinus sylvestris L.) and Portuguese oak (Quercus faginea L.). We applied two cycles of soil drying and recovery and irrigated with isotopically different water to track fast changes in soil and stem water pools, while continuously measuring physiological status and xylem water content from twigs. Our results provide evidence for a tight link between the leaf-level response and the water uptake and storage patterns in the stem. The water-saver strategy of pines prevented stem dehydration by rapidly closing stomata which limited their water uptake during the early stages of drought and recovery. Conversely, oaks showed a less conservative strategy, maintaining transpiration and physiological activity under dry soil conditions, and consequently becoming more dehydrated at the stem level. We interpreted this dehydration as the release of water from elastic storage tissues as no major loss of hydraulic conductance occurred for this species. After soil rewetting, pines recovered pre-drought leaf water potential rapidly, but it took longer to replace the water from conductive tissues (slower labeling speed). In contrast, water-spender oaks were able to quickly replace xylem water during recovery (fast labeling speed), but it took longer to refill stem storage tissues, and hence to recover pre-drought leaf water potential. These different patterns in sap flow rates, speed and duration of the labeling reflected a combination of water-use and storage traits, linked to the leaf-level strategies in response to drought and recovery. [ABSTRACT FROM AUTHOR]

Background and Aims The existence of sclerophyllous plants has been considered an adaptive strategy against different environmental stresses. Given that it literally means 'hard-leaved', it is essential to quantify the leaf mechanical properties to understand sclerophylly. However, the relative importance of each leaf trait for mechanical properties is not yet well established. Methods Genus Quercus is an excellent system to shed light on this because it minimizes phylogenetic variation while having a wide variation in sclerophylly. We measured leaf anatomical traits and cell wall composition, analysing their relationship with leaf mass per area and leaf mechanical properties in a set of 25 oak species. Key Results The upper epidermis outer wall makes a strong and direct contribution to the leaf mechanical strength. Moreover, cellulose plays a crucial role in increasing leaf strength and toughness. The principal component analysis plot based on leaf trait values clearly separates Quercus species into two groups corresponding to evergreen and deciduous species. Conclusions Sclerophyllous Quercus species are tougher and stronger owing to their thicker epidermis outer wall and/or higher cellulose concentration. Furthermore, section Ilex species share common traits, although they occupy different climates. In addition, evergreen species living in mediterranean-type climates share common leaf traits irrespective of their different phylogenetic origin. [ABSTRACT FROM AUTHOR]

Leaves of Mediterranean evergreen tree species experience a reduction in net CO2 assimilation (A N) and mesophyll conductance to CO2 (g m) during aging and senescence, which would be influenced by changes in leaf anatomical traits at cell level. Anatomical modifications can be accompanied by the dismantling of photosynthetic apparatus associated to leaf senescence, manifested through changes at the biochemical level (i.e. lower nitrogen investment in photosynthetic machinery). However, the role of changes in leaf anatomy at cell level and nitrogen content in g m and A N decline experienced by old non-senescent leaves of evergreen trees with long leaf lifespan is far from being elucidated. We evaluated age-dependent changes in morphological, anatomical, chemical and photosynthetic traits in Quercus ilex subsp. rotundifolia Lam. an evergreen oak with high leaf longevity. All photosynthetic traits decreased with increasing leaf age. The relative change in cell wall thickness (T cw) was less than in chloroplast surface area exposed to intercellular air space (S c/ S), and S c/ S was a key anatomical trait explaining variations in g m and A N among different age classes. The reduction of S c/ S was related to ultrastructural changes in chloroplasts associated to leaf aging, with a concomitant reduction in cytoplasmic nitrogen. Changes in leaf anatomy and biochemistry were responsible for the age-dependent modifications in g m and A N. These findings revealed a gradual physiological deterioration related to the dismantling of the photosynthetic apparatus in older leaves of Q. ilex subsp. rotundifolia. [ABSTRACT FROM AUTHOR]

Nowadays, evergreen sclerophyllous and winter-deciduous malacophyllous oaks with different paleogeographical origins coexist under Mediterranean-type climates, such as the mixed forests of the evergreen Quercus ilex subsp. rotundifolia Lam. and the winter-deciduous Quercus faginea Lam. Both Mediterranean oaks constitute two examples of contrasting leaf habit, so it could be expected that they would have different functional strategies to cope with summer drought. In this study, we analysed photosynthetic, photochemical and hydraulic traits of different organs for Q. faginea and Q. ilex subsp. rotundifolia under well-watered conditions and subjected to very severe drought. The coordinated response between photosynthetic and hydraulic traits explained the higher photosynthetic capacity of Q. faginea under well-watered conditions, which compensated its shorter leaf life span at the expense of higher water consumption. The progressive imposition of water stress evidenced that both types of Mediterranean oaks displayed different functional strategies to cope with water limitations. Specifically, the decrease in mesophyll conductance associated with edaphic drought seems to be the main factor explaining the differences found in the dynamics of net CO2 assimilation throughout the drought period. The sharp decline in photosynthetic traits of Q. faginea was coupled with a strong decrease in shoot hydraulic conductance in response to drought. This fact probably avoided extensive xylem embolism in the stems (i.e. 'vulnerability segmentation'), which enabled new leaf development after drought period in Q. faginea. By contrast, leaves of Q. ilex subsp. rotundifolia showed effective photoprotective mechanisms and high resistance to drought-induced cavitation, which would be related with the longer leaf life span of the evergreen Mediterranean oaks. The co-occurrence of both types of Mediterranean oaks could be related to edaphic conditions that ensure the maintenance of soil water potential above critical values for Q. faginea , which can be severely affected by soil degradation and climate change. [ABSTRACT FROM AUTHOR]

Resprouting is an ancestral trait in angiosperms that confers resilience after perturbations. As climate change increases stress, resprouting vigor is declining in many forest regions, but the underlying mechanism is poorly understood. Resprouting in woody plants is thought to be primarily limited by the availability of non‐structural carbohydrate reserves (NSC), but hydraulic limitations could also be important. We conducted a multifactorial experiment with two levels of light (ambient, 2–3% of ambient) and three levels of water stress (0, 50 and 80 percent losses of hydraulic conductivity, PLC) on two Mediterranean oaks (Quercus ilex and Q. faginea) under a rain‐out shelter (n = 360). The proportion of resprouting individuals after canopy clipping declined markedly as PLC increased for both species. NSC concentrations affected the response of Q. ilex, the species with higher leaf construction costs, and its effect depended on the PLC. The growth of resprouting individuals was largely dependent on photosynthetic rates for both species, while stored NSC availability and hydraulic limitations played minor and non‐significant roles, respectively. Contrary to conventional wisdom, our results indicate that resprouting in oaks may be primarily driven by complex interactions between hydraulics and carbon sources, whereas stored NSC play a significant but secondary role. Here we show that root non‐structural carbohydrate reserves only play a minor role as drivers of basal resprouting in Mediterranean oaks. The probability of resprouting was mostly driven by the degree of antecedent hydraulic limitations and the growth of the resprouts depended largely on photosynthetic C uptake. [ABSTRACT FROM AUTHOR]

Plants prevent uncontrolled water loss by synthesizing, depositing and maintaining a hydrophobic layer over their primary aerial organs—the plant cuticle. Quercus coccifera L. can plastically respond to environmental conditions at the cuticular level. When exposed to hot summer conditions with high vapour-pressure deficit (VPD) and intense solar radiation (Mediterranean atmospheric conditions; MED), this plant species accumulates leaf cuticular waxes even over the stomata, thereby decreasing transpirational water loss. However, under mild summer conditions with moderate VPD and regular solar radiation (temperate atmospheric conditions; TEM), this effect is sharply reduced. Despite the ecophysiological importance of the cuticular waxes of Q. coccifera , the wax composition and its contribution to avoiding uncontrolled dehydration remain unknown. Thus, we determined several leaf traits for plants exposed to both MED and TEM conditions. Further, we qualitatively and quantitatively investigated the cuticular lipid composition by gas chromatography. Finally, we measured the minimum leaf conductance (gmin) as an indicator of the efficacy of the cuticular transpiration barrier. The MED leaves were smaller, stiffer and contained a higher load of cuticular lipids than TEM leaves. The amounts of leaf cutin and cuticular waxes of MED plants were 1.4 times and 2.6 times higher than that found for TEM plants, respectively. In detail, MED plants produced higher amounts of all compound classes of cuticular waxes, except for the equivalence of alkanoic acids. Although MED leaves contained higher cutin and cuticular wax loads, the gmin was not different between the two habitats. Our findings suggest that the qualitative accumulation of equivalent cuticular waxes might compensate for the higher wax amount of MED plants, thereby contributing equally to the efficacy of the cuticular transpirational barrier of Q. coccifera. In conclusion, we showed that atmospheric conditions profoundly affect the cuticular lipid composition of Q. coccifera leaves, but do not alter its transpiration barrier properties. [ABSTRACT FROM AUTHOR]

Vapour pressure deficit is a major driver of seasonal changes in transpiration, but photoperiod also modulates leaf responses. Climate warming might enhance transpiration by increasing atmospheric water demand and the length of the growing season, but photoperiod‐sensitive species could show dampened responses. Here, we document that day length is a significant driver of the seasonal variation in stomatal conductance. We performed weekly gas exchange measurements across a common garden experiment with 12 oak species from contrasting geographical origins, and we observed that the influence of day length was of similar strength to that of vapour pressure deficit in driving the seasonal pattern. We then examined the generality of our findings by incorporating day‐length regulation into well‐known stomatal models. For both angiosperm and gymnosperm species, the models improved significantly when adding day‐length dependences. Photoperiod control over stomatal conductance could play a large yet underexplored role on the plant and ecosystem water balances. We demonstrate that photoperiod exerts a major control on the seasonal pattern of stomatal conductance, being as important as the effects of varying VPD. Inclusion of photoperiod regulation in stomatal models led to significant improvements in model fit across angiosperm and gymnosperm species. [ABSTRACT FROM AUTHOR]

Phylogenetic analysis by maximum likelihood (PAML) has become the standard approach to study positive selection at the molecular level, but other methods may provide complementary ways to identify amino acid replacements associated with particular conditions. Here, we compare results of the decision tree (DT) model method with ones of PAML using the key photosynthetic enzyme RuBisCO as a model system to study molecular adaptation to particular ecological conditions in oaks (Quercus). We sequenced the chloroplast rbcL gene encoding RuBisCO large subunit in 158 Quercus species, covering about a third of the global genus diversity. It has been hypothesized that RuBisCO has evolved differentially depending on the environmental conditions and leaf traits governing internal gas diffusion patterns. Here, we show, using PAML, that amino acid replacements at the residue positions 95, 145, 251, 262 and 328 of the RuBisCO large subunit have been the subject of positive selection along particular Quercus lineages associated with the leaf traits and climate characteristics. In parallel, the DT model identified amino acid replacements at sites 95, 219, 262 and 328 being associated with the leaf traits and climate characteristics, exhibiting partial overlap with the results obtained using PAML. [ABSTRACT FROM AUTHOR]

'White oaks'—one of the main groups of the genus Quercus L.—are represented in western Eurasia by the 'roburoid oaks', a deciduous and closely related genetic group that should have an Arcto-Tertiary origin under temperate-nemoral climates. Nowadays, roburoid oak species such as Quercus robur L. are still present in these temperate climates in Europe, but others are also present in southern Europe under Mediterranean-type climates, such as Quercus faginea Lam. We hypothesize the existence of a coordinated functional response at the whole-shoot scale in Q. faginea under Mediterranean conditions to adapt to more xeric habitats. The results reveal a clear morphological and physiological segregation between Q. robur and Q. faginea, which constitute two very contrasting functional types in response to climate dryness. The most outstanding divergence between the two species is the reduction in transpiring area in Q. faginea, which is the main trait imposed by the water deficit in Mediterranean- type climates. The reduction in leaf area ratio in Q. faginea should have a negative effect on carbon gain that is partially counteracted by a higher inherent photosynthetic ability of Q. faginea when compared with Q. robur, as a consequence of higher mesophyll conductance, higher maximum velocity of carboxylation and much higher stomatal conductance (gs). The extremely high gs of Q. faginea counteracts the expected reduction in gs imposed by the stomatal sensitivity to vapor pressure deficit, allowing this species to diminish water losses maintaining high net CO2 assimilation values along the vegetative period under nonlimiting soil water potential values. In conclusion, the present study demonstrates that Q. faginea can be regarded as an example of adaptation of a deciduous oak to Mediterranean-type climates. [ABSTRACT FROM AUTHOR]

ABSTRACT The adaptive benefit of stomatal crypts remains a matter of controversy. This work studies the effect on gas exchange of cuticular rims that overarch the stomatal pore in the Mediterranean species Quercus coccifera L. growing under Mediterranean (lower relative humidities and high summer temperatures) or oceanic conditions (higher daily relative humidities and mild temperatures). After microscopic assessment of the leaf surfaces and stomatal architecture, the impact of the cuticular 'cup' on gas exchange was evaluated by employing three-dimensional finite element models. Here, we provide evidence for a high plasticity of the Q. coccifera cuticular cup, with much larger vents under oceanic conditions compared to small vents under Mediterranean conditions. This structure adds a substantial fixed resistance thereby strongly decreasing gas exchange under Mediterranean conditions. The cuticular cup, which also increases leaf internal humidity, might buffer the rapid changes in vapour pressure deficit ( VPD) often observed under Mediterranean conditions. Since water loss of guard and adjacent epidermal cells regulates stomatal aperture, we suggest that this structure allows an efficient regulation of stomatal conductance and optimum use of resources under high VPD. This study provides evidence that plasticity of stomatal architecture can be an important structural component of hydraulic adaptation to different climate conditions. [ABSTRACT FROM AUTHOR]

The ability of three Mediterranean oaks (Quercus cocciferaL., Quercus ilexssp. ballota(Desf.) Samp and Quercus suberL.) to cope with intense drought was investigated. Water stress reduced stomatal conductance and photosynthesis in these species. Drought-mediated changes in photosynthetic-related parameters allowed the characterisation of the specific photo-protective mechanisms. Specifically, Q. suberdownregulated photosynthetic electron transport rates (ETR) closing PSII reaction centres (i.e. decreasing photochemical quenching) and through an antheraxanthin (A)+zeaxanthin (Z)-mediated diminished intrinsic PSII efficiency (Φexc.). These changes were lower in Q. cocciferaand Q. ilexssp. ballota, which decreased further ETR photo-inactivating PSII centres (evidenced by their low predawn Fv/Fmratios at high water stress). The predawn Fv/Fmratio decreased in Q. cocciferalargely due to Fmdecreases, whereas in Q. ilexssp. ballota Fv/Fmdecreases were due to F0increases, below –4MPa. These Fv/Fmdecreases were well correlated with increases in the A+Z photo-protective pigments. An analysis of dark respiration and photorespiration as alternative electron sinks under intense drought stress also revealed interspecific differences. The largest imbalance between electrons generated and consumed increased potentially oxidative damage in Q. suber. Subsequently, only Q. subershowed loss of chlorophyll, which is one of the main targets of oxidative damage. Data suggest that Q. cocciferaand Q. ilexssp. ballotaseem more able than Q. suberto withstand highly xeric conditions. Therefore, our results question the consideration of Mediterranean evergreen oaks as a homogeneous physiological group. [ABSTRACT FROM AUTHOR]

[Display omitted] • Leaf vein density was independent from photosynthetic rates in oaks. • Leaf vein density was related to leaf vascular redundancy. • Cuticular or nocturnal conductances increased with leaf venation. • Leaf venation could enhance drought-induced mortality by increasing water leaks. Predicting plant growth from functional traits has been a long-term goal of experimental botany. Early studies considered that resource traits align across a single axis, from high to low growth rates. The drivers of nocturnal and cuticular leaf conductances have received much recent attention, but how they align with other functional traits along axes of resource use remains to be investigated. Here we examined correlated evolution of secondary growth, leaf economic, stomatal, venation and gas exchange traits across 12 Quercus species growing in a common garden. Variation in growth correlated with variation in assimilation and nocturnal conductance (g n). Our observations are consistent with the hypothesis of a negative relationship between SLA and leaf vein density (VLA all) within oaks, indicating that increased VLA all is a strategy to enhance leaf vascular redundancy against stress or perturbation as the degree of sclerophylly increases. g n was negatively correlated with growth and decoupled from daytime conductance and photosynthesis. g n seemed to be a passive process in this genus, apparently driven by enhanced water supply that results from increased VLA all. We also observed a positive relationship between leaf vein density and cuticular conductance, indicating that increasing VLA all may incur significant water costs under strong drought. [ABSTRACT FROM AUTHOR]