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- Plant Signal Behav
- v.1(1); Jan-Feb 2006
- PMC2633694
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Plant Signal Behav. 2006 Jan-Feb; 1(1): 9–14.
PMCID: PMC2633694
PMID: 19521470
M Tafforeau, M C Verdus, V Norris, C Ripoll, and M Thellier
Author information Article notes Copyright and License information PMC Disclaimer
Abstract
Plants are sensitive to stimuli from the environment (e.g., wind, rain, contact, pricking, wounding). They usually respond to such stimuli by metabolic or morphogenetic changes. Sometimes the information corresponding to a stimulus may be “stored” in the plant where it remains inactive until a second stimulus “recalls” this information and finally allows it to take effect. Two experimental systems have proved especially useful in unravelling the main features of these memory-like processes.
In the system based on Bidens seedlings, an asymmetrical treatment (e.g., pricking, or gently rubbing one of the seedling cotyledons) causes the cotyledonary buds to grow asymmetrically after release of apical dominance by decapitation of the seedlings. This information may be stored within the seedlings, without taking effect, for at least two weeks; then the information may be recalled by subjecting the seedlings to a second, appropriate, treatment that permits transduction of the signal into the final response (differential growth of the buds). Whilst storage is an irreversible, all-or-nothing process, recall is sensitive to a number of factors, including the intensity of these factors, and can readily be enabled or disabled. In consequence, it is possible to recall the stored message several times successively.
In the system based on flax seedlings, stimulation such as manipulation stimulus, drought, wind, cold shock and radiation from a GSM telephone or from a 105 GHz Gunn oscillator, has no apparent effect. If, however, the seedlings are subjected at the same time to transient calcium depletion, numerous epidermal meristems form in their hypocotyls. When the calcium depletion treatment is applied a few days after the mechanical treatment, the time taken for the meristems to appear is increased by a number of days exactly equal to that between the application of the mechanical treatment and the beginning of the calcium depletion treatment. This means that a meristem-production information corresponding to the stimulation treatment has been stored in the plants, without any apparent effect, until the calcium depletion treatment recalls this information to allow it to take effect. Gel electrophoresis has shown that a few protein spots are changed (pI shift, appearance or disappearance of a spot) as a consequence of the application of the treatments that store or recall a meristem-production signal in flax seedlings. A SIMS investigation has revealed that the pI shift of one of these spots is probably due to protein phosphorylation. Modifications of the proteome have also been observed in Arabidopsis seedlings subjected to stimuli such as cold shock or radiation from a GSM telephone.
Key Words: memory, environmental signals, meristems, mobile telephone, bud growth, proteome, plants
Introduction
“Do memory processes also occur in plants?” This apparently paradoxical question was raised by one of us and his coworkers1 almost twenty-five years ago. At that time a lot of work had been carried out concerning the memory of insects and other lower animals.2–6 The type of response chosen to detect memorization ability in those animals was always closely related to learning and to the possession of specialised nervous cells. In that definition, clearly the concept of memory would not have been valid for plants, which have no neurons and for which the notion of learning is irrelevant. However, memory can be given a more general definition, i.e., as being an ability to “store” an item of information, to “recall” that information after an interval of time and possibly to use it for determining a response by the system under consideration. In that sense, the concept of memory becomes applicable to any type of nonliving (e.g., a computer) or living system, plants included, but then the memorization process has to be made evident by use of a test other than learning.
Many examples of storage (and possible recall) of a variety of environmental signals have been explicitly or implicitly shown to exist in plants or micro-organisms, and possibly at molecular level. This includes persistence of alternative states of the lac operon in growing cultures of Escherichia coli,7 hypocotyl growth inhibition,8 thigmomorphogenetic sensitivity,9 control of the relative growth of the cotyledonary buds of Bidens pilosa,10 seed germination,11 epigenetic inheritance,12 information storage about previous phosphate fluctuations in cyanobacteria,13–15 meristem induction,16 response to hypoosmotic shock,17 memory and imprinting effects in multienzyme complexes,18 drought-induced calcium signalling,19 cell cycle progress20 and “historicity” of microbial interactions.21
Several of those processes are related to plant responses to environmental stimuli such as wind, touch, rain or wounding. It is well known that the transduction of these signals22 involves rapid stimulation of polysome formation,23 changes in gene expression24 and ultimately modification of plant growth and morphogenesis. To assess the possible existence of memorization processes in these responses, it was thus logical to investigate (1) whether information generated by the plant in response to environmental signals could be stored and subsequently recalled and (2) which biochemical or other cellular modifications were specifically associated with the storage and recall functions. Two experimental systems have been especially useful to such studies by our group and coworkers: the breaking of the symmetry of bud growth in juvenile Bidens plants and the induction of meristems in the hypocotyls of flax seedlings.
The Breaking of the Growth Symmetry of the Cotyledonary Buds of Bidens Seedlings
As a consequence of severing the terminal (also termed “apical”) bud of Bidens seedlings (seedling “decapitation”), the buds at the axil of the two opposite cotyledons (cotyledonary buds) can start to grow (release of apical dominance). They grow at approximately the same rate when the seedlings are grown under optimal conditions of mineral nutrition and photosynthesis (the plants thus remaining bilaterally symmetrical), while under nonoptimal conditions one of the cotyledonary buds usually starts to grow significantly faster than the other (breaking of the symmetry of bud growth). Stimulating one of the seedling cotyledons gives a statistical advantage to the axillary bud of the opposite cotyledon (the “distal” bud) relative to the bud at the axil of the stimulated cotyledon (the “proximal” bud). In fact, it is not known whether the asymmetrical stimulus tends to stimulate the growth of the distal bud or to inhibit that of the proximal bud (or both), but the resulting effect for the whole seedling is the same.25 This relative advantage of one bud upon the other can be measured by use of a parameter, g, the values of which range from 0 (the two buds have equal chances to be the first to start to grow) to − 1 or + 1 (total asymmetry in favour of the proximal or the distal bud, respectively) (Fig. 1). Moreover, in their processing of the stimulating signal, the seedlings reveal basic storage and recall functions, the characteristics of which have been described in detail in e.g., Desbiez et al.10,20,26 and already reviewed in Thellier et al.27
Figure 1
Experimenting with Bidens seedlings. (A) Normal Bidens seedling exhibiting bilateral symmetry. TB = terminal (or “apical”) bud, C1 and C2 = (opposite) cotyledons, AB1 and AB2 = axillary (i.e., “cotyledonary”) buds of cotyledons C1 and C2, H = hypocotyl, R = root. (B) When the terminal bud was removed (seedling “decapitation”), the axillary buds of the cotyledons started to grow (release of apical dominance). They grew at approximately the same rate under optimal conditions of mineral nutrition and photosynthesis. One of them started to grow significantly faster that the other under nonoptimal conditions (not shown). (C) Under nonoptimal conditions, a few needle pricks, P, were applied to one of the cotyledons of nondecapitated seedlings. (D) This gave (after release of apical dominance) a statistical advantage to the axillary bud of the opposite cotyledon (distal bud) to be the first to start to grow. This advantage was measured using an index, g, with − 1 ≤ g ≤ + 1. If, in a set of Bidens seedlings, it was always the distal bud which was the first to start to grow, then g = + 1. In a case in which the bud at the axil of the pricked cotyledon (proximal bud) would always be the first to start to grow, then g would be equal to − 1 (not shown). In a case in which there would be an approximately equal number of seedlings where it was the proximal or the distal bud which was the first to start to grow, then g # 0 (not shown). Substituting an asymmetrical nonwounding treatment (such as gently rubbing one of the cotyledons) for the asymmetrical pricking treatment would not change the result as measured by the g-value (not shown). Note that, at a given time, the length of a growing bud can be very different from one seedling to another; only the relative growth of the two cotyledonary buds of each seedling thus has to be taken into consideration in these experiments. (Figure modified from Thellier et al.27).
Briefly, cotyledon stimulation can be carried out by pricking or gently rubbing the treated cotyledon, or else by deposition of a droplet of different types of solution on this cotyledon. When cotyledon stimulation was carried out on nondecapitated seedlings, this had no externally apparent effect on plant morphogenesis; however, if the apical bud was finally removed, the cotyledonary buds started to grow with the same g-values as when cotyledon stimulation was carried out simultaneously to seedling decapitation (all the other experimental conditions being alike). This means that a “symmetry breaking signal” initiated by cotyledon stimulation has been stored within the seedlings, without taking effect, during the time lapse between cotyledon stimulation and seedling decapitation. According to all available experimental data, this signal storage is both all-or-nothing and irreversible. However, depending on the conditions of seedling decapitation and on various other possible treatments (e.g., thermal treatment, water stress, symmetrical or nonsymmetrical stimulation of the seedlings) the observed g-values were close to, or significantly different from zero. This means that, apart from the storage function, the seedlings posses a “recall” function that can be reversibly switched “on” or “off” as a consequence of the above treatments, thus rendering it possible for the stored symmetry-breaking signal to take effect when the recall function is “on”. By successively switching the recall function, “off”, then “on” then “off” again, etc., the observed g-values were close to zero, significantly above zero, close to zero again, etc. This shows that the stored symmetry-breaking signal can be repeatedly solicited, which is strikingly equivalent to the possibility of evoking several times a memorized piece of information in a human or animal.
The overall functioning of this plant memory has been successfully interpreted by means of theoretical modelling, using both continuous28 and discrete25 formalisms. However, since the quiescent cotyledonary buds are very small and embedded in the stem tissues, it was extremely difficult to try to use the conventional means of biochemistry and molecular biology to study the mechanisms involved. Using the memory processes implicated in the growth inhibition of Bidens hypocotyls after stimuli similar to those for the breaking of the symmetry of bud growth,8 Henry-Vian et al.29–30 have shown that the transcription and the translation of genes such as tch1 and hsp70, and the association of mRNA with polysomes, were likely to be involved in the final biochemical events causing the observed morphogenetic effects. But the specific mechanisms for the initial storage and the recall of the symmetry-breaking signal remained largely nonunderstood, except perhaps for the fact that the storage function may be associated in some way with cell cycle control (Fig. 2).20 This was the reason why now our group has turned to another, more convenient experimental system, as explained below.
Figure 2
DNA content (expressed as histograms of percentage of cells) of cell nuclei from the meristems of cotyledonary buds of Bidens seedlings subjected to an asymmetrical, pricking stimulus. The date when seedling germination began was termed day 0. On day 15, the seedlings were pricked four times at the base of one of their two cotyledons. The seedlings were not decapitated (i.e., the cotyledonary buds remained quiescent). Symbols “P” and “D” represent the proximal and distal buds and symbols “T” and “C” the seedlings subjected to the pricking treatment and the non-pricked controls. The DNA measurements were made on day 16 (left row of histograms) and day 20 (right row of histograms) in the buds of nonpricked controls (C16 and C20) and in the proximal (P-T16 and P-T20) and the distal (D-T16 and D-T20) buds of pricked seedlings. The DNA contents were expressed in arbitrary units (AU). In a few cells undergoing cell division, the DNA content was approximately 45 AU in metaphase cell nuclei and 22 AU at each pole of cell nuclei in telophase. In each histogram, the cells on the left and on the right of the vertical, dashed lines at 32 AU may thus be considered to be in (or close to) the G1 and G2 phases of the cell cycle, respectively. In the nonpricked controls (C16 and C20) there were an appreciable percentage of cells with DNA content above 32 AU. In the pricked seedlings, one day after treatment, in the proximal bud (P-T16) almost 100% of the cells exhibited DNA contents less than 32 AU, while, in the distal bud (D-T16) the decrease in the proportion of cells with a high nuclear content was less pronounced. All these features were more-or-less maintained over the next four days, with P-T20 not being very different from P-T16 nor D-T20 from D-T16. This means that (1) the signal sent from the pricked cotyledon caused virtually all the cells in (or close to) G2 to divide in the proximal bud, (2) the effect was much less in the distal bud (storage of a symmetry-breaking information?) and (3) the cell cycle then virtually ceased to evolve during at least the four subsequent days. (Figure modified from Desbiez et al.20).
Induction of Meristems in the Hypocotyl of Flax Seedlings
With flax seedlings, combining a manipulation stimulus (transferring the seedlings from one nutrient medium to another) with a transient (1 to 3 days) depletion of calcium in the nutrient medium was shown to result in the induction of numerous (up to several tens per plant) epidermal meristems in the seedling hypocotyls16,31 (Fig. 3). When nonstimulated seedlings were subjected to calcium depletion (curve D in Fig. 4), or when stimulated seedlings were not subjected to calcium depletion (not shown), very few meristems (usually not more than two) were produced. When calcium depletion was delayed relative to the manipulation stimulus, the production of meristems was correspondingly delayed (curves A–C in Fig. 4). This means that a meristem-production signal, induced by the manipulation stimulus, was stored within the seedlings, without apparent effect, until calcium depletion finally allowed this stored signal to be recalled and take effect (meristem formation). For storage periods of up to eight days, no loss of potency of the stored signal was observed. There was a quite consistent 2–3 day delay between initiating the calcium depletion treatment and meristem outgrowth.
Figure 4
(A–D) A typical example of the time course of the production of epidermal meristems in flax hypocotyls. The seedlings were given a manipulation stimulus (↓) on day 4 (curves A–C) and they were subjected to transient calcium depletion (−) beginning on days 4 (curves A and D), 8 (curve B) or 12 (curve C). In each case, 10 seedlings were sampled per day up to the 30th day and the curves represent the mean number of epidermal meristems produced per seedling. For the seedlings subjected to both the manipulation stimulus and the transient calcium depletion (curves A–C), it appears clearly (1) that the final number of meristems per seedling was always approximately the same (12–14 in this present case) but that delaying the calcium depletion treatment relative to the manipulation stimulus resulted in correspondingly delaying the production of meristems and (2) that the number of meristems produced in the nonstimulated controls (curve D) was always very low (″ 2 in this present case). (Figure modified from Verdus et al.16).
We did not find any treatment other than calcium depletion that had an effect on the recall of the stored meristem-production signal. Nevertheless, a variety of physical or other environmental stimuli were able to induce storage of a meristem-production signal. This includes drought, wind, cold shock (roots bathing for 1 min in a medium at 4°C) and electromagnetic radiation emitted at non-thermal levels either at 0.9 GHz by a GSM (Global System for Mobile communication) telephone or at 105 GHz by a Gunn oscillator.16,31–35 The total number of meristems produced was dependent on the type of stimulus applied. Moreover, combining several stimuli increased meristem production. This suggests that the storage of the meristem-production signal depends quantitatively on the nature and the intensity of the initial stimulation. A significant season-effect occurred (increased production of meristems in the period from April to June), which may be a suggestion that other, still unknown circuits of events interfere with the storage and recall functions in the elicitation of the final response (meristem production).
In order to study independently the mechanisms for the storage and recall functions, flax seedlings were subjected to either only a physical stimulus (manipulation stimulus, cold shock or radiation from a GSM telephone) or only the calcium depletion treatment or else to both cold shock and a calcium depletion treatment, then they were fixed by dipping into liquid nitrogen and their composition in soluble proteins was examined by two-dimensional electrophoresis.32–33 The seedlings subjected to manipulation stimulus or cold shock treatment were fixed after increasing lengths of time (e.g., 0, 1, 5, 10, 30, 60 or 120 min) after being stimulated. The treatments by radiation from a GSM telephone and by calcium depletion lasted two and 12 hours, respectively, and then the seedlings were immediately fixed and analysed for protein composition. Comparing the experimental seedlings with controls subjected to neither the physical stimuli nor the calcium depletion treatment, two different types of changes were observed in the gels: (1) in some cases, spots were apparently slightly displaced relative to the neighbouring spots (pI shift), while (2) in other cases spots seemed to appear or disappear. Possible artefactual changes were eliminated by statistical analysis. The results are given in Table 1. Some changes in the protein spots appear only as a consequence of seedling stimulation and are often specific of each particular type of stimulation applied. This is the case with “Toucher 1” and “Toucher2” (specific of the manipulation stimulus), “CSE” and “CSF” (specific of cold shock) and “Nok” (specific of the irradiation with a GSM telephone). Such protein changes thus may be related to the storage of the information elicited by various types of stimuli. On the contrary, the changes of “Depl1” and“Depl2”, which occur only as a consequence of calcium depletion, may be related to the recall function. All the other modifications of protein spots (CSA” to “CSD” and “CSG”), which occur both after seedling stimulation and after calcium depletion, correspond to nonspecific responses probably not associated with the memorization process. It is still not clear why, among the protein spots (“CSA”, “CSC”, “CSD” and “CSG”) that are modified by either cold shock or calcium depletion, only the first two are modified when both cold shock and calcium depletion are applied.
Table 1
Early changes in flax proteins induced by different types of treatments
| Protein | Effect of | |||||
| Protein spot | Molecular weight (kDa) | Manipulation stimulus | Cold shock | Radiation of GSM telephone | Ca depletion | Cold shock plus Ca depletion |
| Toucher 1 | 57 | 0–10 min | ||||
| Toucher 2 | 51 | 5–10 min | ||||
| CSA | 66 | 30–120 min | ||||
| CSB | 53 | 30–120 min | ||||
| CSC | 44 | 30–120 min | ||||
| CSD | 46 | 1–60 min | ||||
| CSE | 39 | 1–120 min | ||||
| CSF | 30 | 30–120 min | ||||
| CSG | 30 | 1–60 min | ||||
| Nok | 30 | |||||
| Depl1 | 30 | |||||
| Depl2 | 21 | |||||
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The protein spots of interest have been given a reference symbol (1st column) and their molecular weight has been indicated (second column). After the various treatments applied to the seedlings, protein spots simply undergoing a pI shift are indicated in light grey while those appearing de novo are indicated in dark grey. With the short-lasting stimuli (manipulation stimulus, cold shock), it was possible to study transient protein changes (for instance, at the intersection of the 4th column and the 5th line, “30–120 min” means that the pI shift of the spot “CSA” began then ceased to be visible after 30 and 120 min, respectively). With the long-lasting treatments (irradiation with a GSM telephone, Ca depletion treatment), only permanent (or at least long-lasting) protein changes could be observed.
Taking advantage of the extreme sensitivity of the SIMS (Secondary Ion Mass Spectrometry) methodology (see e.g., Thellier et al.36 for a description of the principle and performances of the SIMS method), it was possible to measure 31P/12C ratios in the protein spots. In the case of the spot “Toucher 1”, it was observed that the 31P/12C ratio in this protein (1) was not significantly different from zero in the control seedlings, while (2) it increased up to approximately 4·10−4 and 6·10−4 in the 5th and 10th min after the manipulation stimulus and was back to zero after the 30th min. This time-course of the 31P/12C ratio was identical to that observed for the pI shift of this protein spot in the gel (Fig. 5). This suggests that the slight, transient displacements of protein spots that are observed in gels as a consequence of seedling stimulation may correspond to transient protein phosphorylation. Note that the molecular weight of a phosphate group is a little less than 0.1 kDa, whereas the limit for the detection of a modification of the molecular weight of a protein by electrophoresis is of the order of 0.5 kDa. Therefore, in the present case of the change in spot position, it was not possible to evaluate the change in the molecular weight nor to check if this change corresponded to the change in the phosphorylation status.
Figure 5
Time courses of the change in the position of the protein spot “Toucher1” in the gels and of the change in the 31P/12C ratio in this protein, after application of a manipulation stimulus to the seedlings under study. At the times (min) 0, 5, 10, 30, 60 and 120, the white arrows indicate the position of the “Toucher 1” spot in the gels. At the same time-values the curve represents the changes in the 31P/12C ratio in this particular protein spot. Although nonnegligible error bars exist, it is obvious that the change of the pI shift of this spot is strongly correlated with a change in the phosphorylation status of the corresponding protein.
Using various databases, the N-terminal sequence of the protein “CSE” was found to match (80% identity) that of the saccharopine dehydrogenase (an enzyme involved in lysine metabolism) of a yeast species. The lack of a database with the N-terminal sequences of flax proteins makes it difficult to try to identify the other proteins that we have found to be involved in the storage of the meristem-production signal in flax seedlings.
Complementary Experiments with Arabidopsis
In stark contrast to the flax proteome, the Arabidopsis proteome has been the subject of many studies. Therefore, although no example of storage and recall of signals have been identified in this plant species so far, it appeared interesting to subject Arabidopsis seedlings to signals which are known to be stored in flax seedlings (e.g., cold shock or GSM-telephone radiation) and to check whether the application of these signals can also modify the Arabidopsis proteome. A single experiment has been carried out so far,32 in a manner similar to that with the flax seedlings. The results are given in Table 2. Six protein spots (P1 to P6) were found to be associated with the storage function. With four of them (P1, P2, P3 and P6), identical modifications were caused by cold shock and by GSM-telephone radiation, while, with the two others, the modifications (appearance of spot P4 and disappearance of spot P5) were specific of the GSM telephone radiation. Using N-terminal sequencing, the proteins P3, P4 and P5 were identified as being a carbonic anhydrase of the α-type, a cleaved pherophorine and a spermidine synthase.
Table 2
Early changes in Arabidopsis proteins as induced by cold shock or radiation from a GSM telephone
| Effect of | |||
| Protein Spot | Tentative Identification | Cold Shock | GSM telephone Radiation |
| P1 | - | pI shift | pI shift |
| P2 | - | Spot disappears | Spot disappears |
| P3 | Carbonic anhydrase (α) | pI shift | pI shift |
| P4 | Cleaved pherophorin | No effect | Spot appears |
| P5 | Spermidine synthase | No effect | Spot disappears |
| P6 | unknown | pI shift | pI shift |
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The cold shock was applied during 1 min and the seedlings were fixed 9 min later; the GSM telephone radiation was applied during 2 hours and the seedlings were fixed immediately after this treatment. Protein identification was carried out by N-terminal sequencing. The quantities of proteins P1 and P2 were insufficient for carrying out N-terminal sequencing. The N-terminal sequence of protein P6 did not correspond to any sequence found in the databases.
Conclusion
Although we are still far from a complete understanding of the mechanisms involved in the memory processes occurring in plants, the use of two-dimensional electrophoresis has shown that typical protein modifications occur after application of treatments that store or recall environmental signals. Since the protein modifications observed in the gels were sometimes immediate (e.g., already present 1 min after seedling stimulation), sometimes delayed (e.g., appearing after 30 min) and sometimes transient (e.g., existing between 1 and 60 min after the stimulation), this suggests that the storage function does not correspond to a unique event but to a more or less complicated circuit of events. Moreover, the transience seems to be very similar to wound-induced changes in protein synthesis and transcript accumulation.29–30,37 It is also noteworthy that a carefully calibrated, low-amplitude, short-duration 900 MHz electromagnetic field has evoked the accumulation of a specific mRNA similar to that evoked by injurious stimuli in the tomato plant.38
Figure 3
Experimenting with flax seedlings. (Top) Time course of the experiments. Flax seeds were germinated during three days in the dark then under light. The seedlings were stimulated (manipulation stress, drought, wind, cold shock or radiation from a GSM telephone or from a 105 GHz Gunn oscillator) for instance on the 4th day then they were subjected to transient calcium depletion (beginning for instance at the moment when the stimulus was applied). Seedlings were sampled during the following 20 days or so, for counting the epidermal meristems appearing in the hypocotyls. (Bottom) Scheme of the flax seedlings and enlargement of a zone of the hypocotyl showing the view of an epidermal meristem.
Abbreviations
| AU | arbitrary units |
| GHz | gigahertz |
| GSM | global system for mobile communication |
| SIMS | secondary ion mass spectrometry |
Footnotes
Previously published online as a Plant Signaling & Behavior E-publication: http://www.landesbioscience.com/journals/psb/abstract.php?id=2164
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