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Drought stress represents a particularly great environmental challenge for plants. A decreased water availability can severely limit growth, and this jeopardizes the organism's primary goal—to survive and sustain growth long enough to ensure the plentiful production of viable seeds within the favorable growth season. It is therefore vital for a growing plant to sense oncoming drought as early as possible, and to respond to it rapidly and appropriately in all organs. A typical, fast energy-saving response is the arrest of growth in young organs, which is likely mediated by root-derived signals. A recent publication indicates that three plant hormones (abscisic acid, ethylene and gibberellic acid) mediate the adaptation of leaf growth in response to drought, and that they act at different developmental stages. Abscisic acid mainly acts in mature cells, while ethylene and gibberellic acid function in expanding and dividing leaf cells. This provides the plant with a means to differentially control the developmental zones of a growing leaf, and to integrate environmental signals differently in sink and source tissues. Here we discuss the biological implications of this discovery in the context of long-distance xylem and phloem transport.
Plants have developed an inter-organ communication system to rapidly and dynamically orchestrate developmental changes in response to environmental cues.1,2 Phloem sap contains vast amounts of proteins, mRNAs, hormones, sucrose and other small molecules, all of which have the potential to convey specific information to sink tissues, and many of which are defense- or stress-related.3,4 A well-known example of inter-organ communication that occurs in response to the perception of environmental change is floral induction: lengthening of the photoperiod is perceived in leaves, and this induces the expression of the FT protein in the leaf vasculature. After transport, FT subsequently acts to transform the shoot apical meristem into a floral meristem.5 Lake et al.6 showed that mature leaves are also the source of environment-induced phloemmobile information to young leaves: when only the mature leaves of a plant are exposed to e.g., increased CO2 concentrations, its young leaves will develop with a reduced stomatal index, even though they have not experienced the changed conditions themselves. Long-distance communication between root and shoot is exemplified by the BYPASS1-dependent signal in Arabidopsis. This carotenoid-derived signal molecule, whose identity and mode-of-action remain elusive, is transported from root to shoot through the xylem, and limits the growth of young leaves by acting on both cell division and expansion.7–9 These examples show that xylem and phloem are central circuits for the exchange of information between the different plant organs, with the potential to override the developmental program of the target organ in response to the perception of environmental cues.
Because a major physiological effect of drought is decreased photosynthesis, e.g., due to stomatal closure10 and inhibition of the photosynthetic machinery (Memmi et al., in preparation), the plant's autotrophic production of energy and carbon is threatened. An “appropriate response” to drought—beneficial for growth and survival in the long run—is therefore the immediate conservation of energy, followed by a gradual adaptation to the suboptimal conditions.29 The most prominent sinks are growing organs, in which dividing and expanding cells demand large amounts of energy and resources. A typical response to stress is hence the transient cessation of organ growth until the plant has adapted its energy homeostasis. This growth arrest occurs as rapidly as stomatal closure in leaves (Skirycz A and Inzé D, unpublished results), and long before the water potential in aerial plant parts decreases.11 The responsible signals must therefore originate in the root,12 and they enable the plant to exert tight control over organ growth, depending on the plant's energy status and the environmental challenges it encounters. A recent paper by Skirycz and co-workers13 lifts a tip of the veil, by providing unique information from the receiving end of the signal: the growing leaf itself. Their experiments suggest that the plant systemically sends out three distinct hormonal signals to a young leaf, which each act at different developmental stages to instruct the adaptation to stress.
The first sensing of drought typically occurs underground: roots sense a decrease in water availability, and rapidly send an ABA-signal to the shoot, using the xylem as conduit.14 In mature leaves this ABA signal then activates a cascade of responses that enable the plant to successfully deal with the effects of the oncoming drought, such as rapid stomatal closure and the induction of adaptive molecular mechanisms.15,16
Skirycz et al.13 studied the transcriptome of growing Arabidopsis leaves under mild, growth-limiting osmotic stress conditions. In their assay seedlings were subjected to 25 mM mannitol, and this treatment ultimately led to a 50% reduction in final leaf size. A typical biphasic stress response could be observed in young leaves: a rapid reduction in growth rate, followed by complete recovery and adaptation. An important novelty in this experiment was that the authors managed to separately profile the transcriptome of dividing, expanding and mature leaf cells, thus preventing dilution of developmental-stage-specific transcripts and preserving important developmental information. This approach convincingly demonstrated that there is hardly any overlap in the molecular response of dividing and mature cells to decreased water availability. Remarkably, the ABA-dependent stress response that has been so well characterized in mature cells seems to operate at a much lesser extent in expanding cells, and not at all in dividing cells. Instead, gibberellic acid (GA)- and ethylene-dependent pathways are activated in dividing and expanding cells, in response to stress.
Although it had previously been reported that ABA, ethylene and GA are all involved in the adaptive response of plant growth to stress,16–18 this study thus revealed that the action of these hormones is in fact developmentally separated in a growing leaf: stress-induced ABA appears to target only mature cells, whereas GA and ethylene act in expanding and dividing cells. The rapidity with which a leaf stops growing upon drought perception suggests that—rather than being synthesized de novo in the leaf itself—the hormonal signals are being imported directly from another tissue, to ensure an immediate response. The fact that the genes encoding ethylene and GA biosynthetic enzymes are not upregulated in dividing cells by stress13 supports this view.
All three mentioned phytohormones are certainly amenable to long-distance transport.19 ABA is easily transported from root to shoot in the xylem,20 and it also trafficks in the phloem.21 GAs are translocated via both phloem and xylem, as inactive conjugates which can probably be activated at an appropriate time and location.22,23 The ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC) is known to be exported from the root in the xylem24 and it is also present in phloem sap.25
Keeping in mind the biphasic nature of the growth response to drought, it is tempting to speculate that leaf growth is controled by a complex integration of different long-distance signals, sent out by the roots and the mature leaves. This would ensure a dynamic and appropriate growth response to both current water availability and photosynthetic productivity. The rapid cessation of growth is almost certainly dictated by root-derived signals (ABA, ACC, the BYPASS1-dependent molecule, etc.,), which selectively target dividing, expanding or mature cells. During the subsequent recovery of growth, however, we can suspect that also the mature leaves partake in determining the new, adapted growth rate of the sink organs, through a set of phloem-mobile signals. This would give them the potential to limit the sinks' strenght (e.g., reduce the energy demand of dividing cells by reversibly inhibiting the cell cycle) until environmental conditions become stable again to ensure a reliable output from photosynthesis. The nature of this putative phloem-borne signal derived from mature leaves is currently unknown. Apart from ABA, ACC and GAs, mature leaves appear to load a multitude of proteins and transcripts into the phloem sap stream, which results in a highly complex leaf-derived signal.3,4,26,27 At this stage, we can therefore not exclude that proteins or mRNAs in the phloem sap are also involved in the long-distance growth control in response to stress.
Phloem-mobile signals would not only reach young, growing leaves, but also other sinks. This way the root—as initial source of the signal—also receives feedback from the mature leaves, such that the response to drought can be systemically coordinated, and organ growth can resume at an adapted rate as soon as possible. Figure 1 illustrates how interorgan communication is organized in a plant under drought stress. It will be a very interesting challenge to further dissect the complex long-distance signals with which a plant controls the growth rate of young organs. The experiments of Skirycz et al.13 have provided exciting insight into the molecular adaptations that occur in dividing and expanding cells in response to these signals. Repeating these experiments in e.g., a bps1 mutant background (lacking a functional BYPASS1 gene) could uncover the specific molecular response to the BYPASS1-dependent signal, while the use of ethylene and GA mutants could shed a light upon the role of these hormones in the adaptation of immature cells to stress.
Previously published online: www.landesbioscience.com/journals/psb/article/11421