Deciduous and evergreen oaks: unravelling the co-occurrence of different functional strategies in Quercus L. species under Mediterranean type climates

El clima mediterráneo presenta inviernos suaves o fríos y húmedos, mientras que el verano está afectado por las altas presiones que traen aire seco y caluroso (aridez estival), siendo esta última, la característica genuina que lo diferencia de otros tipos de clima. De este modo, el periodo vegetativo se ve afectado por la sequía en verano, que, junto con las bajas temperaturas en invierno, pueden limitar el crecimiento vegetativo esencialmente a dos estaciones: primavera y otoño. Aún con estas restricciones, los ecosistemas mediterráneos tienen una alta riqueza de especies que representan la sexta parte de la flora del planeta. Este es el caso del género Quercus, que, con más de 400 especies distribuidas por todo el hemisferio norte, es el elemento dominante de una amplia variedad de hábitats y en especial, del clima mediterráneo.En la actualidad es posible hablar de dos tipos de robles bien diferenciados que coexisten en las regiones mediterráneas: el roble perennifolio esclerófilo con un origen en la Flora Paleotropical y el malacófilo caducifolio de origen Arctoterciario. Estos dos modelos, que influyen en la adecuación de la planta al ambiente, pueden ser muy diferentes a nivel morfológico, fenológico y fisiológico. De este modo, los dos tipos de robles deben constituir dos modelos de funcionamiento muy distintos frente al clima mediterráneo. Es por eso por lo que el principal objetivo de esta tesis es el estudio comparado del funcionamiento de los dos tipos de especies de robles con diferentes hábitos foliares y grado de esclerofilia que coexisten en el clima mediterráneo. Por consiguiente, esta tesis consta de cinco capítulos que corresponden a cinco artículos ya publicados o en fase de revisión que pretenden arrojar luz al tema planteado anteriormente.Así, se realizó una revisión bibliográfica sobre la esclerofilia en el género Quercus para definir los mecanismos que hay detrás y sus consecuencias económicas para la hoja. Pese a al amplio rango de variación en los rasgos funcionales de las hojas y sus estrategias adaptativas contrastantes, no puede explicarse por sí sola por ninguno de los factores ecológicos considerados (sequía, escasez de nutrientes, bajas temperaturas y daño físico). El estudio sugiere que estas restricciones pueden tener un efecto sinérgico, y desde un punto de vista funcional, podemos concluir que, en los robles, el hábito foliar modula en gran medida las implicaciones fisiológicas de la esclerofilia.Usando un enfoque filogenético, se cuantificaron las variables anatómicas, composicionales y climáticas en 85 especies de Quercus caducifolios y perennifolios que mostraron diferencias morfológicas foliares fundamentales revelando una respuesta adaptativa diversa. Mientras que la LMA en los caducifolios parece haberse diversificado en coordinación con el grosor modulado principalmente por la aridez, la diversificación de la LMA en los perennifolios parece depender del grupo infragenérico. Así, en estos últimos, la diversificación en el grosor de la hoja fue modulada tanto por la aridez como por el frío, mientras que la diversificación en la densidad de la hoja es sólo modulada por la aridez.Asimismo, se estudió la importancia relativa de cada característica de la hoja sobre las propiedades mecánicas en 25 especies de Quercus. Se sugiere que las hojas de Quercus esclerófilos son más duras y fuertes debido a la pared externa de su epidermis más gruesa y/o a una mayor concentración de celulosa. Además, las especies de la sección Ilex comparten rasgos comunes independientemente de que ocupen climas bastante diferentes. De modo similar, las especies de hoja perenne que viven en climas de tipo mediterráneo comparten rasgos foliares comunes independientemente de su diferente origen filogenético.Además, se evaluaron los cambios dependientes de la edad foliar en los rasgos morfológicos, anatómicos, químicos y fotosintéticos en Quercus ilex subsp. rotundifolia Lam., un roble perennifolio con hojas de alta longevidad. Se observan disminuciones de todos los rasgos fotosintéticos con el aumento de la edad de la hoja. Los cambios en la anatomía y bioquímica de la hoja fueron responsables de las modificaciones dependientes de la edad en la asimilación neta de CO2 y la conductancia del CO2 a través del mesófilo. Estos hallazgos revelaron un deterioro fisiológico gradual relacionado con el desmantelamiento del aparato fotosintético en hojas más viejas de Q. ilex subsp. rotundifolia.Por último, se analizaron las características fotosintéticas, fotoquímicas e hidráulicas de diferentes órganos de Q. faginea y Q. ilex subsp. rotundifolia bajo condiciones de sequía severa. La fuerte disminución de los rasgos fotosintéticos de Q. faginea estuvo acompañada de una fuerte disminución de la conductancia hidráulica de las hojas en respuesta a la sequía. Este hecho probablemente evitó una embolia xilemática en los tallos (¿segmentación de la vulnerabilidad¿). Por el contrario, las hojas de Q. ilex subsp. rotundifolia mostraron mecanismos fotoprotectores efectivos y alta resistencia a la cavitación inducida por la sequía, lo que estaría relacionado con la mayor longevidad de las hojas de las encinas mediterráneas.<br /

Living in Drylands: Functional Adaptations of Trees and Shrubs to Cope with High Temperatures and Water Scarcity

Plant functioning and survival in drylands are affected by the combination of high solar radiation, high temperatures, low relative humidity, and the scarcity of available water. Many ecophysiological studies have dealt with the adaptation of plants to cope with these stresses in hot deserts, which are the territories that have better evoked the idea of a dryland. Nevertheless, drylands can also be found in some other areas of the Earth that are under the Mediterranean-type climates, which imposes a strong aridity during summer. In this review, plant species from hot deserts and Mediterranean-type climates serve as examples for describing and analyzing the different responses of trees and shrubs to aridity in drylands, with special emphasis on the structural and functional adaptations of plants to avoid the negative effects of high temperatures under drought conditions. First, we analyze the adaptations of plants to reduce the input of energy by diminishing the absorbed solar radiation through (i) modifications of leaf angle and (ii) changes in leaf optical properties. Afterwards, we analyze several strategies that enhance the ability for heat dissipation through (i) leaf size reduction and changes in leaf shape (e.g., through lobed leaves), and (ii) increased transpiration rates (i.e., water-spender strategy), with negative consequences in terms of photosynthetic capacity and water consumption, respectively. Finally, we also discuss the alternative strategy showed by water-saver plants, a common drought resistance strategy in hot and dry environments that reduces water consumption at the expense of diminishing the ability for leaf cooling. In conclusion, trees and shrubs living in drylands have developed effective functional adaptations to cope with the combination of high temperature and water scarcity, all of them with clear benefits for plant functioning and survival, but also with different costs concerning water use, carbon gain, and/or leaf cooling.This research was funded by Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA) grant number RTA2015-00054-C02-01, by Ministerio de Ciencia e Innovación grant number PID2019-106701RR-I00/AEI/10.13039/501100011033 and INERTIA project (PID-2019-111332-C22), project IMAGINA (Prometeu program/2019/110, GVA) and from Gobierno de Aragón H09_20R research group. Work of D.A.F. is supported by a FPI-INIA contract BES-2017-081208. CEAM is funded by Generalitat Valenciana

Minimum leaf conductance (gmin) is higher in the treeline of Pinus uncinata Ram. in the Pyrenees: Michaelis’ hypothesis revisited

The search for a universal explanation of the altitudinal limit determined by the alpine treeline has given rise to different hypotheses. In this study, we revisited Michaelis’ hypothesis which proposed that an inadequate “ripening” of the cuticle caused a greater transpiration rate during winter in the treeline. However, few studies with different explanations have investigated the role of passive mechanisms of needles for protecting against water loss during winter in conifers at the treeline. To shed light on this, the cuticular transpiration barrier was studied in the transition from subalpine Pinus uncinata forests to alpine tundra at the upper limit of the species in the Pyrenees. This upper limit of P. uncinata was selected here as an example of the ecotones formed by conifers in the temperate mountains of the northern hemisphere. Our study showed that minimum leaf conductance in needles from upper limit specimens was higher than those measured in specimens living in the lower levels of the sub-alpine forest and also displayed lower cuticle thickness values, which should reinforce the seminal hypothesis by Michaelis. Our study showed clear evidence that supports the inadequate development of needle cuticles as one of the factors that lead to increased transpirational water losses during winter and, consequently, a higher risk of suffering frost drought

Cell-level anatomy explains leaf age-dependent declines in mesophyll conductance and photosynthetic capacity in the evergreen Mediterranean oak Quercus ilex subsp. rotundifolia

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

Changes in the Abundance of Monoterpenes from Breathable Air of a Mediterranean Conifer Forest: When Is the Best Time for a Human Healthy Leisure Activity?

The exposure to monoterpenes emitted by plants to the air might provide human health benefits during forest-based leisure activities. However, forests, especially Mediterranean ones, lack studies to relate forest production and the emission of monoterpenes, considering potential human forest exposure. Thus, the aim of this study was to analyze the variation in the abundance of monoterpenes in the human breathable air under the canopy of a Mediterranean conifer forest, evaluating the influence of different factors. For this purpose, from March to November 2018, we monitored the abundance of monoterpenes in the air at nose height, leaf development, air temperature and soil water potential in a mountain Mediterranean forest of Pinus pinaster located in Sierra de Albarracín (Teruel, Spain). We detected six monoterpenes, with a-pinene, ß-pinene and limonene being the three most abundant. Temperature was the main environmental factor driving the abundance of monoterpenes in air, with a maxima of abundance found during summer. Leaf development in spring decreased the abundance, while after a drought period, the abundance increased. Thus, people enjoying forest-based activities in Mediterranean conifer areas would be more exposed to air monoterpenes when the temperature increases during the period after leaf development, as long as the trees are not severely water-stressed. If that is the case, the abundance of monoterpenes in the air would increase after the drought period. © 2022 by the authors. Licensee MDPI, Basel, Switzerland

Vapor pressure deficit constrains transpiration and photosynthesis in holm oak: A comparison of three methods during summer drought.

High rates of vapor pressure deficit (VPD) can severely decrease plant productivity by reducing stomatal conductance, which might be exacerbated during Mediterranean summers due to soil water deficit. In this study, we monitored the response of holm oak, the archetype of Mediterranean trees, to changes in VPD during a summer drought period to evaluate the effects and consequences on gas exchange of the two water stresses (atmospheric and soil). Measurements were performed on trees growing in an experimental plantation over two summers with moderate drought stress by using three different methods: at the leaf level with an infrared gas analyzer, using a whole-plant chamber for short-term monitoring at the tree level, and measuring the canopy temperature for long-term monitoring. The three methods provided negative relationships between leaf conductance and VPD but with discrepancies probably associated with the measurement scale. Overall, the results showed that atmospheric and soil water stress had an additive effect. Under well-watered conditions, an increase in VPD was partially compensated by a reduction in stomatal conductance, resulting in a slight increase in the transpiration rates. With soil water deficit, the response to VPD resulted in a further decrease in stomatal conductance, reducing transpiration as a water saving strategy. The decrease in conductance in response to VPD was transitory, recovering to initial values as soon as the VPD decreased, both under well-watered and drought conditions. Due to this high sensitivity to atmospheric drought, the maximum carbon gain rates of holm oak were restricted to a short environmental window, which might modulate its physiological performance and natural distribution.Publishe

Deciduous and evergreen oaks show contrasting adaptive responses in leaf mass per area across environments

• Increases in leaf mass per area (LMA) are commonly observed in response to environmental stresses and are achieved through increases in leaf thickness and/or leaf density. Here, we investigated how the two underlying components of LMA differ in relation to species native climates and phylogeny, across deciduous and evergreen species. • Using a phylogenetic approach, we quantified anatomical, compositional and climatic variables from 40 deciduous and 45 evergreen Quercus species from across the Northern Hemisphere growing in a common garden. • Deciduous from shorter growing seasons tended to have leaves with lower LMA and leaf thickness than those from longer growing seasons, while the opposite pattern was found for evergreens. For both habits, LMA and thickness increased in arid environments. However, this shift was associated with increased leaf density in evergreens but reduced density in deciduous species. • Deciduous and evergreen oaks showed fundamental leaf morphological differences that revealed a diverse adaptive response. While LMA in deciduous may diversified in tight coordination with thickness mainly modulated by aridity, diversification of LMA within evergreens appears dependent on the infrageneric group, with diversification in leaf thickness modulated by both aridity and cold, while diversification in leaf density only modulated by aridity.Publishe

Disentangling leaf structural and material properties in relation to their anatomical and chemical compositional traits in oaks (Quercus L.)

The existence of sclerophyllous plants has been considered an adaptive strategy against different environmental stresses. As 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 on mechanical properties is not yet well established. The genus Quercus is an excellent system to shed light on this since it minimizes phylogenetic variation while having a wide variation in sclerophylly. Thus, leaf anatomical traits and cell wall composition were measured, analyzing their relationship with LMA and leaf mechanical properties in a set of 25 oak species. Outer wall contributed strongly to leaf mechanical strength. Moreover, cellulose plays a critical role in increasing leaf strength and toughness. The PCA plot based on leaf trait values clearly separated Quercus species into two groups corresponding to evergreen and deciduous species. Sclerophyllous Quercus species are tougher and stronger due to their thicker epidermis outer wall and/or higher cellulose concentration. Furthermore, section Ilex species share common traits regardless of they occupy quite different climates. In addition, evergreen species living in Mediterranean-type climates share common leaf traits irrespective of their different phylogenetic origin.Unpublishe

Estudi de l'efecte de la salinitat sobre l'activitat respiratòria en Arabidopsis thaliana

La salinitat és un greu problema que afecta sòls de tot el món i per tant a les plantes de manera que redueix el creixement i la producció de molts cultius. Per créixer, la planta necessita tenir un bon estat hídric que es veu afectat per l’estrès salí. Un enzim clau durant l’estrès salí és l'oxidasa alternativa (AOX) que es troba a la cadena respiratòria. La hipòtesi d’aquest estudi és que l'activitat d'AOX estarà relacionada amb l'estat hídric de la planta. S'ha mesurat la capacitat, l'activitat (mitjançant la tècnica del fraccionament d'isòtops d'oxigen) i el contingut hídric relatiu a plantes d'Arabidopsis thaliana wild-type i mutants knockout del gen aox1a (SALK_084897), el qual codifica per AOX. S'ha sotmès a les plantes a una concentració 300 mmol de NaCl durant 24 hores. Com a resultat s'ha observat un augment en l'activitat d'AOX en condicions d'estrès salí i una reducció del contingut hídric relatiu i s'ha comprovat que la capacitat d'AOX no correlaciona amb la seva activitatSalinity is a serious problem that affects soils around the world and therefore the plants, reducing the growth and yield of many crops. For growing, plants need a good hydric status that is affected by salt stress. An important enzyme in salt stress is the alternative oxidase (AOX) of respiration chain. The hypothesis of this study is that AOX activity is related to water status of the plant. AOX capacity, activity (using the oxygen isotope fractionation technique) and relative water content have been measured in Arabidopsis thaliana mutants and wild-type knockout aox1a gene (SALK_084897), which encodes for AOX. Plants have been exposed to a concentration of 300 mmol NaCl for 24 hours. Results show an increase in the activity of AOX in salt stress conditions, a reduction in relative water content and found that the capacity of AOX not correlated with their activit

Trade-offs among leaf toughness, constitutive chemical defense, and growth rates in oaks are influenced by the level of leaf mass per area

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.Este trabajo ha contado con el apoyo de la beca CNS2022-136156 financiada por MCIN/AEI/10.13039/501100011033 y de la Unión Europea Next Generation EU/PRTR, por la subvención PID2019-106701RR-I00/AEI/10.13039/501100011033, y por el Grupo de investigación S74_23R del Gobierno de Aragón.Taninos condensadosRasgos defensivosTasa de crecimiento relativoQuercusTrabajo de fracturaPublishe