Publications

Trees of the genus Prunus produce some of the most widely consumed fruits globally. The combination of climate change-related warming and increased drought stress, scarcity of freshwater resources for irrigation, and increasing demands due to population growth creates a need for increased drought tolerance in these tree species. Recently, we have shown in the field that a native wild pear species performs better under drought than two cultivated pear species. Here, a comparative field study was conducted in Israel to investigate traits associated with drought tolerance in almond (cultivated Prunus dulcis (Mill.) D. A. Webb vs wild Prunus ramonensis Danin) and plum (cultivated Prunus domestica L. vs wild Prunus ursina Kotschy). Measurements of xylem embolism and shoot and root carbon reserves were done along a year, including seasonal drought in the wild and a 35-day drought experiment in the orchards. Synchronous measurements of native xylem embolism and shoot water potential showed that cultivated and wild almond trees lost similar to 50% of hydraulic conductivity at -2.3 and -3.2 MPa, respectively. Micro-CT images confirmed the higher embolism ratio in cultivated versus wild almond, whereas the two plum species were similar. Dynamics of tissue concentrations of nonstructural carbohydrates were mostly similar across species, with higher levels in cultivated versus wild plum. Our results indicate an advantage for the wild almond over its cultivated relative in terms of xylem resistance to embolism, a major risk factor for trees under drought stress. This result is in line with our previous experiment on pear species. However, the opposite trends observed among the studied plum species mean that these trends cannot be generalized. It is possible that the potential for superior drought tolerance in wild tree species, relative to their cultivated relatives, is limited to wild species from dry and hot habitats.

In the published version of this editorial paper, the sentence in the first paragraph should be corrected as shown below.

Forestry at the dry edge of forest existence has been a long-lasting interest to arid land residents. Current land-use and climate changes have broaden this interest to the global society, seeking for improved tree and forest drought resistance across biomes. Within this transition, Israel is a hub for scientific research and testing ground alike. Israel is a small country, spanning over arid, semi-arid, and thermo-Mediterranean environments, with relatively little forest. Nevertheless afforestation efforts have been unprecedented (by percent change in land cover), and many of these forests serve today as a 'living lab' for forest and tree drought resistance research. Considering the ongoing warming and drying, tree physiologists, forest ecologists, and forest managers in Israel are running a race to the unknown. To ensure local forest sustainability for future generations, the gap between the increased drought risk on the one hand, and the rather stationary forest drought resistance on the other hand, must be closed. The aim of this review is to highlight the findings and achievements, as well as challenges, of this contemporary research. Examples from Israel are given at the Middle East, and the wider, global arid land, contexts. In particular, important progress has been made in the following aspects: (1) the physiology of tree drought resistance, including water-use traits and phenology; (2) the genetic approach, advancing from provenance trials, to the application of molecular tools in the identification of tree drought resistance mechanisms; (3) the canopy flux measurement approach, e.g. monitoring the exchange of carbon, water, and energy in water-limited forests; (4) the application of remote sensing tools, such as satellite-based vegetation indices; and (5) the application of adaptive management practices in increasing forest resilience under drought. Taken together, these advances represent a way forward, while indicating important gaps, and open questions to future research. Lessons learnt in forests in Israel should be useful and transferable to other forest ecosystems in the Middle East, the Mediterranean, and additional water-limited regions.

The mutualistic symbiosis between forest trees and ectomycorrhizal fungi (EMF) is among the most ubiquitous and successful interactions in terrestrial ecosystems. Specific species of EMF are known to colonize specific tree species, benefitting from their carbon source, and in turn, improving their access to soil water and nutrients. EMF also form extensive mycelial networks that can link multiple root-tips of different trees. Yet the number of tree species connected by such mycelial networks, and the traffic of material across them, are just now under study. Recently we reported substantial belowground carbon transfer between Picea, Pinus, Larix and Fagus trees in a mature forest. Here, we analyze the EMF community of these same individual trees and identify the most likely taxa responsible for the observed carbon transfer. Among the nearly 1,200 EMF root-tips examined, 50%-70% belong to operational taxonomic units (OTUs) that were associated with three or four tree host species, and 90% of all OTUs were associated with at least two tree species. Sporocarp C-13 signals indicated that carbon originating from labelled Picea trees was transferred among trees through EMF networks. Interestingly, phylogenetically more closely related tree species exhibited more similar EMF communities and exchanged more carbon. Our results show that belowground carbon transfer is well orchestrated by the evolution of EMFs and tree symbiosis.

Water availability is becoming a limiting factor with increasing world population that challenges global food security. Thus, we need to enhance cultivation in increasingly drier and hotter climate and prepare fruit trees for the ongoing climate change. Wild tree species might offer vital information and plant material in face of these challenges.A year-long comparative field study was conducted to investigate the mechanisms underlying drought tolerance in pear species (cultivated Pyrus communis and Pyrus pyrifolia vs. the wild Pyrus syriaca).We confirmed the hypothesis of higher drought tolerance in wild pear compared to its cultivated relative. P. syriaca xylem had fewer, narrower vessels, and lower vulnerability to embolism. It showed higher intrinsic water-sue efficiency and more robust seasonal patterns of photosynthesis, hydraulic conductivity, and PIP (plasma intrinsic protein) aquaporin expression. Across species, we identified a ubiquitous gene (PIP1:5/1:6), nine drought-inhibited genes, and two drought-induced genes (PIP1:4 and 2:6/2:7, confirming previous studies).Our study highlights the potential of using wild relatives of fruit tree species to prepare key crops to a drier and hotter future. The study of PIPS leads the way to a more focused research of the role of these cellular water channels in minimizing tree water loss under drought, while ensuring hydration of specific tissues.

The response of tree leaf gas exchange to elevated CO2 concentrations has been investigated in numerous experiments along the past 30 years. Stomatal regulation is a major plant control over leaf gas exchange, and the response to the increasing CO2 will shape the biological activity of forests in the future. Here, we collected 144 records from 57 species on stomatal conductance in CO2 manipulation experiments on trees (340-980 ppm CO2). CO2-induced stomatal downregulation was calculated as the slope of the linear regression between stomatal conductance and [CO2]. Among tree species, the slope (a) of change in stomatal conductance per 100 ppm CO(2 )increase ranged between 0 and -151, indicating stomatal downregulation, and only four species showed upregulation. There was a significant divergence between evergreen gymnosperms (a = -3.6 +/- 1.0), deciduous angiosperms (a = -16.3 +/- 3.1) and evergreen angiosperms (a = -32.8 +/- 7.1). Gymnosperms were less sensitive to CO2 changes than deciduous angiosperms even when considering only field experiments. The significant role of tree functional group in predicting CO2-induced stomatal downregulation was detected in multiple mixed-effect models, with p values ranging between 0.0002 and 0.0295. The significantly higher stomatal sensitivity to CO2 of angiosperms versus gymnosperms might be related to the overall higher stomatal conductance of angiosperms; their thinner leaves, in turn losing water faster; and the decreasing atmospheric [CO2] at the time of their taxa diversification. We conclude that species differences must be taken into account in forecasting future forest fluxes. A plain language summary is available for this article.

Drought-related tree mortality had become a widespread phenomenon in forests around the globe. This process leading to these events and its complexity is not fully understood. Trees in the dry timberline are exposed to ongoing drought, and the available water for transpiration in the soil can determine their survival chances. Recent drought years led to 5%–10% mortality in the semi-arid pine forest of Yatir (Israel). The distribution of dead trees was, however, highly heterogeneous with parts of the forest showing >80% dead trees (D plots) and others with mostly live trees (L plots). At the tree level, visible stress was associated with low pre-dawn leaf water potential at the dry season (−2.8 MPa vs. −2.3 MPa in non-stressed trees), shorter needles (5.5 vs. 7.7 mm) and lower chlorophyll content (0.6 vs. 1 mg/g dw). Trends in tree-ring widths reflected differences in stress intensity (30% narrower rings in stressed compared with unstressed trees), which could be identified 15–20 years prior to mortality. At the plot scale, no differences in topography, soil type, tree age or stand density could explain the mortality difference between the D and L plots. It could only be explained by the higher surface rock cover and in stoniness across the soil profile in the L plots. Simple bucket model simulations using the site’s long-term hydrological data supported the idea that these differences could result in higher soil water concentration (m 3 /m 3 ) in the L plots and extend the time above wilting point by several months across the long dry season. Accounting for subsurface heterogeneity may therefore critical to assessing stand-level response to drought and projecting tree survival, and can be used in management strategies in regions undergoing drying climate trends. 

Understanding which species are able to recover from drought, under what conditions, and the mechanistic processes involved, will facilitate predictions of plant mortality in response to global change. In response to drought, some species die because of embolism-induced hydraulic failure, whilst others are able to avoid mortality and recover, following rehydration. Several tree species have evolved strategies to avoid embolism, whereas others tolerate high embolism rates but can recover their hydraulic functioning upon drought relief. Here, we focus on structures and processes that might allow some plants to recover from drought stress via embolism reversal. We provide insights into how embolism repair may have evolved, anatomical and physiological features that facilitate this process, and describe possible trade-offs and related costs. Recent controversies on methods used for estimating embolism formation/repair are also discussed, providing some methodological suggestions. Although controversial, embolism repair processes are apparently based on the activity of phloem and ray/axial parenchyma. The mechanism is energetically demanding, and the costs to plants include metabolism and transport of soluble sugars, water and inorganic ions. We propose that embolism repair should be considered as a possible component of a hydraulic efficiency-safety' spectrum. We also advance a framework for vegetation models, describing how vulnerability curves may change in hydrodynamic model formulations for plants that recover from embolism.

Green roofs provide many ecosystem services such as regulation of building temperatures, reducing urban heat-island effects and draining rainwater. In addition, they are expected to reduce the high levels of CO2 concentrations in big cities. Previous CO2 fixation studies on green roofs were done by taking long-timeperiod samples using expensive equipment and with limited replication. To plan green roofs for optimal CO2 reduction, a simple method to quantify CO2 fixation rate in relation to plant species-composition is required. The method we tested is direct measurement of CO2 concentrations with a portable air-quality meter, which allows a large number of samples. Here we focus on differences in the photosynthetic effect between plots containing the local Mediterranean succulent, Sedum sediforme and plots containing various annuals. In a factorial design (presence or absence of Sedum crossed with presence or absence of annuals), we tested the effect of sedum and annual treatments on CO2 concentrations. To compare our results with a commonly used method, and to evaluate the role of the different species, we examined the photosynthetic activity at the single plant level under these treatments by using a portable gas-exchange measuring system. We found that our method can detect the effect of different green roof plots and can be used as a simple and reliable tool for green-roof planers. We found that annuals reduced CO2 concentrations, but only in the absence of Sedum. Sedum alone had no effect on CO2 concentrations. This emphasizes the importance of integrating plots with annual plants in Sedum-based green roofs. (C) 2017 Elsevier GmbH. All rights reserved.

Climate change is expected to exacerbate drought for many plants, making drought tolerance a key driver of species and ecosystem responses. Plant drought tolerance is determined by multiple traits, but the relationships among traits, either within individual plants or across species, have not been evaluated for general patterns across plant diversity. We synthesized the published data for stomatal closure, wilting, declines in hydraulic conductivity in the leaves, stems, and roots, and plant mortality for 262 woody angiosperm and 48 gymnosperm species. We evaluated the correlations among the drought tolerance traits across species, and the general sequence of water potential thresholds for these traits within individual plants. The trait correlations across species provide a framework for predicting plant responses to a wide range of water stress from one or two sampled traits, increasing the ability to rapidly characterize drought tolerance across diverse species. Analyzing these correlations also identified correlations among the leaf and stem hydraulic traits and the wilting point, or turgor loss point, beyond those expected from shared ancestry or independent associations with water stress alone. Further, on average, the angiosperm species generally exhibited a sequence of drought tolerance traits that is expected to limit severe tissue damage during drought, such as wilting and substantial stem embolism. This synthesis of the relationships among the drought tolerance traits provides crucial, empirically supported insight into representing variation in multiple traits in models of plant and ecosystem responses to drought.

In deciduous trees growing in temperate forests, bud break and growth in spring must rely on intrinsic carbon (C) reserves. Yet it is unclear whether growth and C storage occur simultaneously, and whether starch C in branches is sufficient for refoliation. To test in situ the relationships between growth, phenology and C utilization, we monitored stem growth, leaf phenology and stem and branch nonstructural carbohydrate (NSC) dynamics in three deciduous species: Carpinus betulus L., Fagus sylvatica L. and Quercus petraea (Matt.) Liebl. To quantify the role of NSC in C investment into growth, a C balance approach was applied. Across the three species, >95% of branchlet starch was consumed during bud break, confirming the importance of C reserves for refoliation in spring. The C balance calculation showed that 90% of the C investment in foliage (7.0-10.5 kg tree(-1) and 5-17 times the C needed for annual stem growth) was explained by simultaneous branchlet starch degradation. Carbon reserves were recovered sooner than expected, after leaf expansion, in parallel with stem growth. Carpinus had earlier leaf phenology (by similar to 25 days) but delayed cambial growth (by similar to 15 days) than Fagus and Quercus, the result of a competitive strategy to flush early, while having lower NSC levels.

Short-term, intense heat waves (hamsins) are common in the eastern Mediterranean region and provide an opportunity to study the resilience of forests to such events that are predicted to increase in frequency and intensity. The response of a 50-yr-old Aleppo pine (Pinus halepensis) forest to hamsin events lasting 1-7d was studied using 10yr of eddy covariance and sap flow measurements. The highest frequency of heat waves was c. four per month, coinciding with the peak productivity period (March-April). During these events, net ecosystem carbon exchange (NEE) and canopy conductance (gc ) decreased by c. 60%, but evapotranspiration (ET) showed little change. Fast recovery was also observed with fluxes reaching pre-stress values within a day following the event. NEE and gc showed a strong response to vapor pressure deficit that weakened as soil moisture decreased, while sap flow was primarily responding to changes in soil moisture. On an annual scale, heat waves reduced NEE and gross primary productivity by c. 15% and 4%, respectively. Forest resilience to short-term extreme events such as heat waves is probably a key to its survival and must be accounted for to better predict the increasing impact on productivity and survival of such events in future climates.

A chloroplast protein disulfide isomerase (PDI) was previously proposed to regulate translation of the unicellular green alga Chlamydomonas reinhardtii chloroplast psbA mRNA, encoding the D1 protein, in response to light. Here we show that AtPDI6, one of 13 Arabidopsis thalianaPDI genes, also plays a role in the chloroplast. We found that AtPDI6 is targeted and localized to the chloroplast. Interestingly, AtPDI6 knockdown plants displayed higher resistance to photoinhibition than wild-type plants when exposed to a tenfold increase in light intensity. The AtPDI6 knockdown plants also displayed a higher rate of D1 synthesis under a similar light intensity. The increased resistance to photoinhibition may not be rationalized by changes in antenna or non-photochemical quenching. Thus, the increased D1 synthesis rate, which may result in a larger proportion of active D1 under light stress, may led to the decrease in photoinhibition. These results suggest that, although the D1 synthesis rates observed in wild-type plants under high light intensities are elevated, repair can potentially occur faster. The findings implicate AtPDI6 as an attenuator of D1 synthesis, modulating photoinhibition in a light-regulated manner.

We review observational, experimental, and model results on how plants respond to extreme climatic conditions induced by changing climatic variability. Distinguishing between impacts of changing mean climatic conditions and changing climatic variability on terrestrial ecosystems is generally underrated in current studies. The goals of our review are thus (1) to identify plant processes that are vulnerable to changes in the variability of climatic variables rather than to changes in their mean, and (2) to depict/evaluate available study designs to quantify responses of plants to changing climatic variability. We find that phenology is largely affected by changing mean climate but also that impacts of climatic variability are much less studied, although potentially damaging. We note that plant water relations seem to be very vulnerable to extremes driven by changes in temperature and precipitation and that heatwaves and flooding have stronger impacts on physiological processes than changing mean climate. Moreover, interacting phenological and physiological processes are likely to further complicate plant responses to changing climatic variability. Phenological and physiological processes and their interactions culminate in even more sophisticated responses to changing mean climate and climatic variability at the species and community level. Generally, observational studies are well suited to study plant responses to changing mean climate, but less suitable to gain a mechanistic understanding of plant responses to climatic variability. Experiments seem best suited to simulate extreme events. In models, temporal resolution and model structure are crucial to capture plant responses to changing climatic variability. We highlight that a combination of experimental, observational, and/or modeling studies have the potential to overcome important caveats of the respective individual approaches.