Plants require the capacity for quick and precise recognition of external stimuli within their environment for survival. Upon exposure to biotic (herbivores and pathogens) or abiotic stressors (environmental conditions), plants can activate hydraulic, chemical, or electrical long-distance signals to initiate systemic stress responses. A plant's stress reactions can be highly precise and orchestrated in response to different stressors or stress combinations. To date, an array of information is available on plant responses to single stressors. However, information on simultaneously occurring stresses that represent either multiple, within, or across abiotic and biotic stress types is nascent. Likewise, the crosstalk between hydraulic, chemical, and electrical signaling pathways and the importance of each individual signaling type requires further investigation in order to be fully understood. The overlapping presence and speed of the signals upon plant exposure to various stressors makes it challenging to identify the signal initiating plant systemic stress/defense responses. Furthermore, it is thought that systemic plant responses are not transmitted by a single pathway, but rather by a combination of signals enabling the transmission of information on the prevailing stressor(s) and its intensity. In this review, we summarize the mode of action of hydraulic, chemical, and electrical long-distance signals, discuss their importance in information transmission to biotic and abiotic stressors, and suggest future research directions.

Redistribution of water within plants could mitigate drought stress of roots in zones of low soil moisture. Plant internal redistribution of water from regions of high soil moisture to roots in dry soil occurs during periods of low evaporative demand. Using minirhizotrons, we observed similar lifespans of roots in wet and dry soil for the grapevine 'Merlot' (Vitis vinifera) on the rootstock 101-14 Millardet de Gramanet (Vitis riparia ¥ Vitis rupestris) in a Napa County, California vineyard. We hypothesized that hydraulic redistribution would prevent an appreciable reduction in root water potential and would contribute to prolonged root survivorship in dry soil zones. In a greenhouse study that tested this hypothesis, grapevine root systems were divided using split pots and were grown for 6 months. With thermocouple psychrometers, we measured water potentials of roots of the same plant in both wet and dry soil under three treatments: control (C), 24 h light + supplemental water (LW) and 24 h light only (L). Similar to the field results, roots in the dry side of split pots had similar survivorship as roots in the wet side of the split pots (P = 0.136) in the C treatment. In contrast, reduced root survivorship was directly associated with plants in which hydraulic redistribution was experimentally reduced by 24 h light. Dry-side roots of plants in the LW treatment lived half as long as the roots in the wet soil despite being provided with supplemental water (P < 0.0004). Additionally, pre-dawn water potentials of roots in dry soil under 24 h of illumination (L and LW) exhibited values nearly twice as negative as those of C plants (P = 0.034). Estimates of root membrane integrity using electrolyte leakage were consistent with patterns of root survivorship. Plants in which nocturnal hydraulic redistribution was reduced exhibited more than twice the amount of electrolyte leakage in dry roots compared to those in wet soil of the same plant. Our study demonstrates that besides a number of ecological advantages to protecting tissues against desiccation, internal hydraulic redistribution of water is a mechanism consistent with extended root survivorship in dry soils.

The role of root systems in drought tolerance is a subject of very limited information compared with above-ground responses. Adjustments to the ability of roots to supply water relative to shoot transpiration demand is proposed as a major means for woody perennial plants to tolerate drought, and is often expressed as changes in the ratios of leaf to root area (AL:AR). Seasonal root proliferation in a directed manner could increase the water supply function of roots independent of total root area (AR) and represents a mechanism whereby water supply to demand could be increased. To address this issue, seasonal root proliferation, stomatal conductance (gs) and whole root system hydraulic conductance (kr) were investigated for a drought-tolerant grape root system (Vitis berlandieri×V. rupestris cv. 1103P) and a non-drought-tolerant root system (Vitis riparia×V. rupestris cv. 101-14Mgt), upon which had been grafted the same drought-sensitive clone of Vitis vinifera cv. Merlot. Leaf water potentials (ψL) for Merlot grafted onto the 1103P root system (–0.91±0.02 MPa) were +0.15 MPa higher than Merlot on 101-14Mgt (–1.06±0.03 MPa) during spring, but dropped by approximately –0.4 MPa from spring to autumn, and were significantly lower by –0.15 MPa (–1.43±0.02 MPa) than for Merlot on 101-14Mgt (at –1.28±0.02 MPa). Surprisingly, gs of Merlot on the drought-tolerant root system (1103P) was less down-regulated and canopies maintained evaporative fluxes ranging from 35–20 mmol vine−1 s−1 during the diurnal peak from spring to autumn, respectively, three times greater than those measured for Merlot on the drought-sensitive rootstock 101-14Mgt. The drought-tolerant root system grew more roots at depth during the warm summer dry period, and the whole root system conductance (kr) increased from 0.004 to 0.009 kg MPa−1 s−1 during that same time period. The changes in kr could not be explained by xylem anatomy or conductivity changes of individual root segments. Thus, the manner in which drought tolerance was conveyed to the drought-sensitive clone appeared to arise from deep root proliferation during the hottest and driest part of the season, rather than through changes in xylem structure, xylem density or stomatal regulation. This information can be useful to growers on a site-specific basis in selecting rootstocks for grape clonal material (scions) grafted to them.

Summary• Linkages between plant growth rate and root responses to soil moisture heterogeneity were investigated.• Root dynamics were studied using genetically identical shoots (Vitis vinifera cv. Merlot) with genetically distinct root systems that promote higher (HSV) and lower (LSV) shoot growth rates (1103P and 101-14 Mgt, respectively). Three quantities of irrigation replenished different amounts of evapotranspiration (0, 40 and 100% ET c ) in a California vineyard.• Roots of HSV vines exhibited more plasticity, as indicated by greater preferential growth in irrigated soil during the summer, and a larger shift in root diameter with a change in soil moisture than LSV vines. Higher tolerance of low soil moisture was not observed in LSV roots -root survivorship was similar for the two rootstocks. LSV vines produced a large fraction of its roots during the winter months and increased root density over the study, while HSV vines produced roots mainly in summer and only exhibited a high initial peak in root biomass in the first year.• These results demonstrated that a plant of higher vigor has greater morphological plasticity in response to lateral heterogeneity in soil moisture but similar tolerance to moisture stress as indicated by root survivorship in dry soil.

Forest ecosystems play a central role in global water and carbon cycles, yet the impact of global climate change, in particular drought, on trees and forests is poorly understood. Therefore, there is an urgent need for forest-scale experiments in improving our understanding of trees' responses to extreme drought events and subsequent recovery under field conditions. Here, we present the design and efficacy of a novel throughfall exclusion experiment with retractable roofs in a mature forest allowing for flexible drought and recovery periods. A total of 12 plots (144 AE 26 m 2 on average) with 3-7 European beech and Norway spruce trees each were established by root trenching to a depth of one meter, four years prior to the experiment. Subsequent installation of roofs (n = 6) allowed for the removal of throughfall precipitation and almost a complete non-availability of soil water in the upper 70 cm during five subsequent growing seasons, that is, 2014-2018. This reduction in available soil water resulted in pre-dawn leaf water potentials down to −1.8 MPa in mature trees. Stem diameter growth decreased by 30% in beech and 70% in spruce, and fine root abundance was reduced by 57% in beech and 73% in spruce compared with controls. After only one growing season, the mycorrhizal community composition changed in response to drought. Careful watering of hydrophobic forest soils in early summer of 2019 resulted in recovered pre-dawn leaf water potentials of drought-stressed trees within one week. Recovery of stem diameter growth, however, did not occur within the same growing season and remained reduced by 33% in beech and 69% in spruce compared with controls. The implemented throughfall exclusion system imposed recurrent seasonal drought events on a mature beech/spruce forest with high efficacy. Shifts in community composition of mycorrhizae in parallel to tree growth decline advocate for a more holistic view on forest-scale drought and watering experiments, particularly in light of more frequently predicted drought events in future. The perennial nature of mature trees and their subsequent slow recovery from drought, that is, over multiple growing seasons, argues for more long-term experiments that span several years.

Key message Under severe drought, growth of Norway spruce suffered much more than European beech. Norway spruce benefited from growing in the environment of beech, and both species acclimated slightly to 5 years of experimentally extended drought. Abstract Recent studies show that the detrimental effects of drought on stand growth are mitigated when the stand contains mixed tree species. We analysed the growth responses of Norway spruce and European beech to episodic and experimentally extended drought in intra-and inter-specific mature stands. We used annual diameter growth records dating back to 1998 to determine the impact of the natural episodic drought in 2003 and 2015. To analyse extended drought, spruce and beech trees were exposed to extreme drought under automatic throughfall exclusion roofs from 2014 to 2018. The growth of spruce in an inter-specific environment with beech was 20-50% less affected by natural episodic drought compared with an intraspecific constellation. When beech grew in an inter-specific environment, it was by 23% more affected by drought compared to intra-specific conditions, but seemed to recover faster. The induced drought from 2014 to 2018 resulted in a strong growth reduction in the first year particularly for spruce, followed by a slight acclimation to the dry conditions. Beech acclimated and recovered faster than spruce across all growing conditions, while spruce only acclimatized faster in the environment of beech. Both species showed a higher mortality under induced drought compared with the controls; for spruce, the mortality rate was fivefold higher compared to the long-term mortality. The long-term moderate-growth stabilization and the growth increase after the 5-year exposure to drought suggest a gradual acclimation to drought by beech. The resistance and acclimation to drought of spruce when growing in mixture should be considered when designing resource efficient and productive mixed conifer-broadleaved stands for future climates.

Summary1. Root herbivores and pathogens interfere with basic below-ground plant function, and can thereby affect plant fitness and spatial and temporal patterns in natural plant communities. However, there has been little development of concepts and theories on below-ground plant defence, a deficit that is in contrast to the abundance of theorizing for above-ground plant parts. 2. A review of the past 10 years of research on below-ground plant-herbivore interactions has revealed that, similar to above-ground tissues, root defences can be expressed constitutively or induced upon herbivore attack, and can be classified into direct and indirect traits, tolerance, and escape. Indeed, it has been shown that roots tolerate herbivory by outgrowing or re-growing lost tissues, or resist it by producing secondary metabolites that are toxic to herbivores or attract natural enemies of herbivores. 3. We propose that, similar to above-ground plant-herbivore theories, the partition of abiotic and biotic factors over ecological succession can serve as the basis for predicting investment in defence strategies below-ground. 4. Investigation of herbivore pressure and root responses along primary and secondary successional gradients suggests that: (i) roots are often fast growing, thinner and softer in early compared to later succession. (ii) Insect and nematode herbivore pressure increases until midsuccession and later decreases. (iii) Mycorrhizal abundance increases with succession, and the composition of fungal species changes through succession, often shifting from arbuscular mycorrhizae to ecto-mycorrhizae. 5. Based on these findings, and on classical (above-ground) plant defence theory, we suggest the following set of testable hypotheses for below-ground plant defence: (i) During succession, early plants invest most of their resources in growth and less in defences (associated with a general lack of herbivores and pathogens, and with limited availability of resources in the system), therefore relying more on re-growth (tolerance) strategies. (ii) During mid-succession, a buildup of herbivore pressure facilitates replacement by plant species that exhibit greater direct and indirect defence strategies. (iii) Constitutive and inducible levels of defences may trade-off, and early successional plants should rely more on induction of defences after herbivore attack, whereas late successional plants will increasingly rely on constitutively produced levels of physical and chemical defence. (iv) Successional changes in microbial associations have consequences for root defence by improving plant nutrition and defence expression as well as directly competing for root space; however, toxic or impenetrable root defences may also limit association with root symbionts, and so may constrain the expression of root defence.

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