What plant roots know?

Despite their paramount role in plant life, the study of roots has been largely neglected until recently. Here, I shortly describe a few newly-discovered abilities of plants to undergo adaptive changes and execute developmental decisions based on roots' perception of non-resource information pertaining to imminent challenges and opportunities. Seemingly simple in their morphology and architecture and lacking central information-processing centres, roots are able to sense and integrate complex cues and signals over time and space that allow plants to perform elaborate behaviours analogous, some claim even homologous, to those of intelligent animals. Although our knowledge of root behaviour is rapidly expanding, further understanding of its underlying mechanisms is largely preliminary, calling for detailed investigation of the involved cues, signals and information processing controls, as well as their implications for plant development, growth and reproduction under realistic ecological and agricultural settings.

Interspecific Drought Cuing in Plants.

Plants readily communicate with their pollinators, herbivores, symbionts, and the predators and pathogens of their herbivores. We previously demonstrated that plants could exchange, relay, and adaptively utilize drought cues from their conspecific neighbors. Here, we studied the hypothesis that plants can exchange drought cues with their interspecific neighbors. Triplets of various combinations of split-root Stenotaphrum secundatum and Cynodon dactylon plants were planted in rows of four pots. One root of the first plant was subjected to drought while its other root shared its pot with one of the roots of an unstressed target neighbor, which, in turn, shared its other pot with an additional unstressed target neighbor. Drought cuing and relayed cuing were observed in all intra- and interspecific neighbor combinations, but its strength depended on plant identity and position. Although both species initiated similar stomatal closure in both immediate and relayed intraspecific neighbors, interspecific cuing between stressed plants and their immediate unstressed neighbors depended on neighbor identity. Combined with previous findings, the results suggest that stress cuing and relay cuing could affect the magnitude and fate of interspecific interactions, and the ability of whole communities to endure abiotic stresses. The findings call for further investigation into the mechanisms and ecological implications of interplant stress cuing at the population and community levels.

Plant responsiveness to root-root communication of stress cues.

BACKGROUND AND AIMS: Phenotypic plasticity is based on the organism's ability to perceive, integrate and respond to multiple signals and cues informative of environmental opportunities and perils. A growing body of evidence demonstrates that plants are able to adapt to imminent threats by perceiving cues emitted from their damaged neighbours. Here, the hypothesis was tested that unstressed plants are able to perceive and respond to stress cues emitted from their drought- and osmotically stressed neighbours and to induce stress responses in additional unstressed plants. METHODS: Split-root Pisum sativum, Cynodon dactylon, Digitaria sanguinalis and Stenotaphrum secundatum plants were subjected to osmotic stress or drought while sharing one of their rooting volumes with an unstressed neighbour, which in turn shared its other rooting volume with additional unstressed neighbours. Following the kinetics of stomatal aperture allowed testing for stress responses in both the stressed plants and their unstressed neighbours. KEY RESULTS: In both P. sativum plants and the three wild clonal grasses, infliction of osmotic stress or drought caused stomatal closure in both the stressed plants and in their unstressed neighbours. While both continuous osmotic stress and drought induced prolonged stomatal closure and limited acclimation in stressed plants, their unstressed neighbours habituated to the stress cues and opened their stomata 3-24 h after the beginning of stress induction. CONCLUSIONS: The results demonstrate a novel type of plant communication, by which plants might be able to increase their readiness to probable future osmotic and drought stresses. Further work is underway to decipher the identity and mode of operation of the involved communication vectors and to assess the potential ecological costs and benefits of emitting and perceiving drought and osmotic stress cues under various ecological scenarios.

Is ABA the exogenous vector of interplant drought cuing?

We have recently demonstrated that root cuing from drought-stressed plants increased the survival time of neighboring plants under drought, which came at performance costs under benign conditions. The involvement of abscisic acid (ABA) was implicated from additional experiments in which interplant drought cuing was greatly diminished in ABA-deficient plants. Here, we tested the hypothesis that ABA is the exogenous vector of interplant drought cuing. Pisum sativum plants were grown in rows of three split-root plants. One of the roots of the first plant was subjected to either drought of benign conditions in one rooting vial, while its other root shared its rooting vial with one of the roots of an unstressed neighbor, which in turn shared its other rooting vial with an additional unstressed neighbor. One hour after subjecting one of the roots of the first plant to drought, ABA concentrations were 106% and 145% higher around its other root and the roots of its unstressed neighbor, compared to their respective unstressed controls; however, the absolute concentrations of ABA found in the rooting media were substantially low. The results may indicate that despite its involvement in interplant drought and the commonly observed exchange of ABA between drought-stressed plants and their rhizospheres, ABA is not directly involved in exogenous interplant drought cuing. However, previous studies have shown that even minute concentrations of ABA in the rhizosphere can prevent ABA leakage from roots and thus to significantly increase endogenous ABA levels. In addition, under drought conditions, plants tend to accumulate ABA, which could markedly increase internal ABA concentrations over time and ABA concentrations in close proximity to the root surface might be significantly greater than estimated from entire rooting volumes. Finally, phaseic acid, an ABA degradation product, is known to activate various ABA receptors, which could enhance plant drought tolerance. It is thus feasible that while the role of ABA is limited, its more stable degradation products could play a significant role in interplant drought cuing. Our preliminary findings call for an extensive investigation into the identity and modes of operation of the exogenous vectors of interplant drought cuing.

Ontogenetic contingency of tolerance mechanisms in response to apical damage.

BACKGROUND AND AIMS: Plants are able to tolerate tissue loss through vigorous branching which is often triggered by release from apical dominance and activation of lateral meristems. However, damage-induced branching might not be a mere physiological outcome of released apical dominance, but an adaptive response to environmental signals, such as damage timing and intensity. Here, branching responses to both factors were examined in the annual plant Medicago truncatula. METHODS: Branching patterns and allocation to reproductive traits were examined in response to variable clipping intensities and timings in M. truncatula plants from two populations that vary in the onset of reproduction. Phenotypic selection analysis was used to evaluate the strength and direction of selection on branching under the damage treatments. KEY RESULTS: Plants of both populations exhibited an ontogenetic shift in tolerance mechanisms: while early damage induced greater meristem activation, late damage elicited investment in late-determined traits, including mean pod and seed biomass, and supported greater germination rates. Severe damage mostly elicited simultaneous development of multiple-order lateral branches, but this response was limited to early damage. Selection analyses revealed positive directional selection on branching in plants under early- compared with late- or no-damage treatments. CONCLUSIONS: The results demonstrate that damage-induced meristem activation is an adaptive response that could be modified according to the plant's developmental stage, severity of tissue loss and their interaction, stressing the importance of considering these effects when studying plastic responses to apical damage.

Picking battles wisely: plant behaviour under competition.

Plants are limited in their ability to choose their neighbours, but they are able to orchestrate a wide spectrum of rational competitive behaviours that increase their prospects to prevail under various ecological settings. Through the perception of neighbours, plants are able to anticipate probable competitive interactions and modify their competitive behaviours to maximize their long-term gains. Specifically, plants can minimize competitive encounters by avoiding their neighbours; maximize their competitive effects by aggressively confronting their neighbours; or tolerate the competitive effects of their neighbours. However, the adaptive values of these non-mutually exclusive options are expected to depend strongly on the plants' evolutionary background and to change dynamically according to their past development, and relative sizes and vigour. Additionally, the magnitude of competitive responsiveness is expected to be positively correlated with the reliability of the environmental information regarding the expected competitive interactions and the expected time left for further plastic modifications. Concurrent competition over external and internal resources and morphogenetic signals may enable some plants to increase their efficiency and external competitive performance by discriminately allocating limited resources to their more promising organs at the expense of failing or less successful organs.

Ecological implications of the determination of branch hierarchies.

• The performance of the whole plant is largely dependent on its ability to allocate limited resources to branches that perform best throughout its life. Here, the hypothesis that the fate of young branches is determined by their growth rates and not merely by their relative physical sizes or net photosynthetic outputs was tested. • The development of asymmetrical two-branch plants was followed after either one or both of the branches were restrained for short periods. • The larger branch was invariably dominant in unrestrained or bilaterally restrained plants. However, when the larger branch was restrained while the smaller branch was not, the branch hierarchy inverted despite the pronounced photosynthetic advantage of the larger branch over its smaller counterpart. • It is suggested that growth rates are more important than physical size or photosynthetic output in young plants, where they could serve as better predictors of the overall future performance of the branch. It is speculated that rate-sensitivity has been selected for when plastic responses cannot adequately track environmental changes in real time.

Developmental responses of portulaca seedlings to conflicting spectral signals.

Portulaca oleracea seedlings avoid growing in the direction of neighbouring plants even when they are very small or remote. The present study was designed to determine the relative effect on the development of Portulaca seedlings of light availability (i.e. the resource level) as compared with spectral composition (i.e. the signal of future competition for the resource). The plants were subjected to various intensities of photosynthetic light and red/far-red (R/FR) ratios from opposite directions. The seedlings became recumbent preferentially towards the direction with the lower FR light, even when this meant growing towards plastic that absorbed 20 times more photosynthetic light. A preference for the direction with higher photosynthetic light over lower FR was also found, though only under extreme light differences. The response of the seedlings was not absolute: the orientation chosen depended on the light received from other alternative directions.

How portulaca seedlings avoid their neighbours.

Portulaca oleracea L. seedlings do not develop in the direction of neighbours, even when these neighbours are small and distant. Neighbouring plants could be simulated by small rectangles of a plastic that resembled leaves in its spectral characteristics. Unlike seedlings, mature plants did not respond to objects that do not influence photosynthetic light. When light of equal intensity was received from all directions, Portulaca seedlings avoided the direction with higher far-red light. Portulaca is thus able to use spectral composition and direction of light as clues for the probability of the direction of future shade.

Say it with flowers: flowering acceleration by root communication.

The timing of reproduction is a critical determinant of fitness, especially in organisms inhabiting seasonal environments. Increasing evidence suggests that inter-plant communication plays important roles in plant functioning. Here, we tested the hypothesis that flowering coordination can involve communication between neighboring plants. We show that soil leachates from Brassica rapa plants growing under long-day conditions accelerated flowering and decreased allocation to vegetative organs in target plants growing under non-inductive short-day conditions. The results suggest that besides endogenous signaling and external abiotic cues, flowering timing may involve inter-plant communication, mediated by root exudates. The study of flowering communication is expected to illuminate neglected aspects of plant reproductive interactions and to provide novel opportunities for controlling the timing of plant reproduction in agricultural settings.

Architectural plasticity in a Mediterranean winter annual.

Size variability in plants may be underlain by overlooked components of architectural plasticity. In annual plants, organ sizes are expected to depend on the availability and reliability of resources and developmental time. Given sufficient resources and developmental time, plants are expected to develop a greater number of large branches, which would maximize fitness in the long run. However, under restrictive growth conditions and environmental reliability, developing large branches might be risky and smaller branches are expected to foster higher final fitness. Growth and architecture of Trifolium purpureum (Papilionaceae) plants from both Mediterranean (MED) and semi-arid (SAR) origins were studied, when plants were subjected to variable water availability, photoperiod cues and germination timing. Although no clear architectural plasticity could be found in response to water availability, plants subjected to photoperiod cuing typical to late spring developed fewer basal branches. Furthermore, plants that germinated late were significantly smaller, with fewer basal branches, compared with plants which grew for the same time, starting at the beginning of the growing season. The results demonstrate an intricate interplay between size and architectural plasticities, whereby size modifications are readily induced by environmental factors related to prevalent resource availability but architectural plasticity is only elicited following the perception of reliable anticipatory cues.

The effect of steepness of temporal resource gradients on spatial root allocation.

Plants are able to discriminately allocate greater biomass to organs that grow under higher resource levels. Recent evidence demonstrates that split-root plants also discriminately allocate more resources to roots that grow under dynamically improving nutrient levels, even when their other roots grow in richer patches. Here, we further tested whether, besides their responsiveness to the direction of resource gradients, plants are also sensitive to the steepness of environmental trajectories. Split-root Pisum sativum plants were grown so that one of their roots developed under constantly-high nutrient levels and the other root was subjected to dynamically improving nutrient levels of variable steepness. As expected, plants usually allocated a greater proportion of their biomass to roots that developed under constantly high resource availability; however, when given a choice, they allocated greater biomass to roots that initially experienced relatively low but steeply improving nutrient availabilities than to roots that developed under continuously-high nutrient availability. Such discrimination was not observed when the roots in the poor patch experienced only gentler improvements in nutrient availability. The results are compatible with the notion that responsiveness to the direction and steepness of environmental gradients could assist annual plants to increase their performance by anticipating resource availabilities foreseeable before the end of their growing season. The results exemplify the ability of plants to integrate and utilize environmental information and execute adaptive behaviours which, until recently, were attributed only to animals with central nervous systems.

Rumor has it...: relay communication of stress cues in plants.

Recent evidence demonstrates that plants are able not only to perceive and adaptively respond to external information but also to anticipate forthcoming hazards and stresses. Here, we tested the hypothesis that unstressed plants are able to respond to stress cues emitted from their abiotically-stressed neighbors and in turn induce stress responses in additional unstressed plants located further away from the stressed plants. Pisum sativum plants were subjected to drought while neighboring rows of five unstressed plants on both sides, with which they could exchange different cue combinations. On one side, the stressed plant and its unstressed neighbors did not share their rooting volumes (UNSHARED) and thus were limited to shoot communication. On its other side, the stressed plant shared one of its rooting volumes with its nearest unstressed neighbor and all plants shared their rooting volumes with their immediate neighbors (SHARED), allowing both root and shoot communication. Fifteen minutes following drought induction, significant stomatal closure was observed in both the stressed plants and their nearest unstressed SHARED neighbors, and within one hour, all SHARED neighbors closed their stomata. Stomatal closure was not observed in the UNSHARED neighbors. The results demonstrate that unstressed plants are able to perceive and respond to stress cues emitted by the roots of their drought-stressed neighbors and, via 'relay cuing', elicit stress responses in further unstressed plants. Further work is underway to study the underlying mechanisms of this new mode of plant communication and its possible adaptive implications for the anticipation of forthcoming abiotic stresses by plants.

Anticipating future conditions via trajectory sensitivity.

Plants are known to be highly responsive to environmental heterogeneity and normally allocate more biomass to organs which grow in richer patches. However, recent evidence demonstrates that plants can discriminately allocate more resources to roots that develop in patches with increasing nutrient levels, even when their other roots develop in richer patches. Responsiveness to the direction and steepness of spatial and temporal trajectories of environmental variables might enable plants to increase their performance by improving their readiness to anticipated resource availabilities in their immediate proximity. Exploring the ecological implications and mechanisms of trajectory- sensitivity in plants is expected to shed new light on the ways plants learn their environment and anticipate its future challenges and opportunities.

The effects of nutrient dynamics on root patch choice.

Plants have been recognized to be capable of allocating more roots to rich patches in the soil. We tested the hypothesis that in addition to their sensitivity to absolute differences in nutrient availability, plants are also responsive to temporal changes in nutrient availability. Different roots of the same Pisum sativum plants were subjected to variable homogeneous and heterogeneous temporally - dynamic and static nutrient regimes. When given a choice, plants not only developed greater root biomasses in richer patches; they discriminately allocated more resources to roots that developed in patches with increasing nutrient levels, even when their other roots developed in richer patches. These results suggest that plants are able to perceive and respond to dynamic environmental changes. This ability might enable plants to increase their performance by responding to both current and anticipated resource availabilities in their immediate proximity.

Physiologically-Mediated Self/Non-Self Root Discrimination in Trifolium repens has Mixed Effects on Plant Performance.

Recent studies suggest that plant roots can avoid competition with other roots of the same plant, but the mechanism behind this behavior is yet largely unclear and their effects on plant performance hardly studied. We grew combinations of two ramets of Trifolium repens in a single pot that were either intact, disconnected for a shorter or longer time, or that belonged to different genotypes. Interconnected ramets developed lower root length and mass than any other combination of ramets, supporting the notion that self/non-self discrimination in T. repens was based entirely on physiological coordination between different roots that develop on the same plant, rather than biochemical allorecognition. These responses were consistent among eight field-collected genotypes, suggesting that self/non-self discrimination is a common feature in wild populations of white clover. There were no significant treatment x genotype interactions suggesting that genetic variation for self/non-self discrimination may be limited. Self-interactions resulted in lower to similar shoot biomass and number of ramets, but higher flowering probabilities, compared to non-self interactions. Thus, our results demonstrated that the performance consequences of self/non-self discrimination may be more complicated than previously thought.

Physiologically mediated self/non-self discrimination in roots.

Recent evidence suggests that self/non-self discrimination exists among roots; its mechanisms, however, are still unclear. We compared the growth of Buchloe dactyloides cuttings that were grown in the presence of neighbors that belonged to the same physiological individual, were separated from each other for variable periods, or originated from adjacent or remote tillers on the same clone. The results demonstrate that B. dactyloides plants are able to differentiate between self and non-self neighbors and develop fewer and shorter roots in the presence of other roots of the same individual. Furthermore, once cuttings that originate from the very same node are separated, they become progressively alienated from each other and eventually relate to each other as genetically alien plants. The results suggest that the observed self/non-self discrimination is mediated by physiological coordination among roots that developed on the same plant rather than allogenetic recognition. The observed physiological coordination is based on an as yet unknown mechanism and has important ecological implications, because it allows the avoidance of competition with self and the allocation of greater resources to alternative functions.

The effect of mean and variance in resource supply on survival of annuals from Mediterranean and desert environments.

Resource availability is often characterized by mean annual amounts, while ignoring the spatial variation within habitats and the temporal variation within a year. Yet, temporal and spatial variation may be especially important for identifying the source of stress in low productivity environments such as deserts where resources are often pulsed and resource renewal events are separated by long periods of low resource availability. Therefore, the degree of stress will be determined in part by the length of time between recharge events. Here, we investigated the effect of timing and total amount of water application on two congeneric pairs, each with a population from a low (desert) and a high (Mediterranean) productivity habitat. As expected, highest survival and greatest growth were found at low or intermediate recharge intervals, and the magnitude of response to increases in total seasonal amounts was greater for Mediterranean species than desert species. The species that had greater survival switched in the hierarchy under high total water depending on interval length. These results demonstrate that temporal variation in resource availability can be as important as annual total amounts for plant performance and that response to temporal dynamics can vary between species. This has implications for community-level processes, as competitive hierarchies may switch based on resource dynamics rather than only total availability.

Resource pulses, species interactions, and diversity maintenance in arid and semi-arid environments.

Arid environments are characterized by limited and variable rainfall that supplies resources in pulses. Resource pulsing is a special form of environmental variation, and the general theory of coexistence in variable environments suggests specific mechanisms by which rainfall variability might contribute to the maintenance of high species diversity in arid ecosystems. In this review, we discuss physiological, morphological, and life-history traits that facilitate plant survival and growth in strongly water-limited variable environments, outlining how species differences in these traits may promote diversity. Our analysis emphasizes that the variability of pulsed environments does not reduce the importance of species interactions in structuring communities, but instead provides axes of ecological differentiation between species that facilitate their coexistence. Pulses of rainfall also influence higher trophic levels and entire food webs. Better understanding of how rainfall affects the diversity, species composition, and dynamics of arid environments can contribute to solving environmental problems stemming from land use and global climate change.