JXB Advance Access originally published online on April 29, 2007
Journal of Experimental Botany 2007 58(8):2069-2078; doi:10.1093/jxb/erm063
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© 2007 The Author(s).
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/2.0/uk/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.This paper is available online free of all access charges (see http://jxb.oxfordjournals.org/open_access.html for further details)
RESEARCH PAPER |
Cumulative activation of axillary buds by nodal roots in Trifolium repens L.
AgResearch Grasslands, Private Bag 11008, Palmerston North, New Zealand
* To whom correspondence should be addressed. E-mail: mike.hay{at}agresearch.co.nz
Received 29 November 2006; Revised 19 February 2007 Accepted 5 March 2007
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Abstract |
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In Trifolium repens the rate of outgrowth of an axillary bud was closely correlated with its duration of exposure to a nearby nodal root. The dose-dependent nature of this relationship, over 0–22 d, is consistent with the concept that axillary buds are cumulatively activated by a root signal (RS) such that the longer they receive the signal the higher is their level of activation and hence their rate of outgrowth. Furthermore, the activation level attained by a bud was subsequently retained following the excision of the nodal root providing the source of its activation: its rate of growth 3–6 weeks after root excision still reflected the initial level of activation of the bud. Thus, once activated, a bud required relatively little RS to maintain its rate of outgrowth, implying that activation involves the establishment of an autonomous control mechanism within the bud itself. This provides an explanation of how a strongly activated apical bud can continue growth at relatively low RS levels when it is distanced from its nearest root system, while at the same time the prevailing low RS environment leads to weak activation of the axillary buds emerging from it.
Key words: Axillary bud outgrowth, branch development, bud activation, bud emergence, cumulative activation, nodal roots, root signals, stem elongation, Trifolium repens
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Introduction |
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In many angiosperm species, including Trifolium repens (Erith, 1924), axillary buds initiated during the early growth of a seedling grow out to form branches soon after emerging from their parent apical bud (PAB) as they themselves develop into actively growing apical buds. These can remain in an activated state over long periods in coexistence with later-formed relatively inactive buds that fail to grow out into branches (Harper, 1977; Bell, 1984; Cain, 1994).
Until now, most studies of axillary bud development have been undertaken using orthotropic plants and the pre-eminent mechanism regulating axillary bud activity is widely considered to involve their suppression by apical tissues (apical dominance) (Tamas, 1995). Strong evidence suggests that bud suppression is linked to the polar basipetal transport of auxin (indole acetic acid), with recent studies indicating that its effect is indirect (McSteen and Leyser, 2005; Tanaka et al., 2006). Evidence from mutational, grafting, and physiological studies using the model systems of Arabidopsis thaliana, Pisum sativum, and Petunia hybrida indicates, in addition, that signals from the roots are also involved in the regulation of axillary bud outgrowth. These appear to be of two types; namely, positively acting signal(s) (inclusive of cytokinins) and a novel long-range, acropetally transported, inhibitory signal that requires interaction with auxin to facilitate the repression of axillary bud outgrowth (Foo et al., 2005; McSteen and Leyser, 2005; Snowden et al., 2005; Dun et al., 2006). It can thus be conceived that the stimulation of an axillary bud is dependent upon its receipt of a net positive signal. Such a signal is the resultant of a positive influence from the root combined with a negative influence derived from auxin from the apical bud interacting with both the root-supplied inhibitory signal and with cytokinin biosynthesis.
The influence of roots on shoot branching is easier to investigate in plagiotropic clonal plants than in conventional orthotropic model systems because the presence or absence of nodal roots can be readily manipulated in the former. In this respect, Trifolium repens is a useful experimental plant (Thomas et al., 2003b). When a shoot-tip cutting is grown with a root system only at its base, the rate of development of successively produced axillary buds along the horizontal main stem declines from node to node in the absence of nodal root formation (Thomas et al., 2002). Outgrowth of a root at a newly emerged node in a region of weak axillary bud activity leads to a renewed burst of branch outgrowth at, and distal to, that node, repeating the branching pattern observed at the basal end of the shoot. This suggests that the outgrowth of axillary buds that would otherwise remain relatively inactive is stimulated by the presence of root-derived signal(s) (RS) the strength of which decreases from node to node as they become increasingly distanced from a root (Thomas et al., 2003a). This reduction in activation of successively produced axillary buds at the time of their emergence from their PAB occurs despite the latter remaining fully activated.
These observations have led to the hypotheses (i) that the activation level of an axillary bud is dependent upon the duration and intensity of the root signal it receives following emergence from its parent apical bud and (ii) that the level of activation reached by an axillary bud is maintained thereafter in the face of declining root signal strength.
These two hypotheses were tested in three experiments by determining axillary bud activation levels induced in response to variation in the levels of net root signal they received. Exposure to root signals was varied by excising nodal roots after allowing different periods for their outgrowth.
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Materials and methods |
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Plant material
All experiments were carried out using a glasshouse-grown stock clone of a single genotype of Trifolium repens L. selected from a Spanish ecotype collection (AgResearch Accession number C1067) that remains fully vegetative at temperatures above 12 °C irrespective of photoperiod (Thomas, 1982) and shows a pattern of branching in response to nodal root treatments that is typical for the species (Thomas et al., 2002).
Culture of experimental plants
Plants were grown from shoot-tip cuttings planted in 1.3 l polyethylene planter bags filled with a commercially obtained 60:40 peat moss:coarse sand mix supplemented with Osmocote fertilizer (Thomas et al., 2002). After about three weeks, basal branches were trimmed off each plant to leave a single main stem axis growing away from the planter bag containing its basal root system. All branches subsequently forming on the main stem were retained. Outgrowth of nodal roots from this developing shoot system was prevented by growing it over a surface of dry plastic mesh.
Treatments were imposed when the axillary bud at the node of the tenth phytomer from the base of the main stem was newly emerged from its parent apical bud (Fig. 1), at which time its subtending leaf was half expanded (0.7 on Carlson's leaf development scale (Carlson, 1966)). In the appropriate treatments, outgrowth of a single nodal root from phytomer 10 (P 10) was then stimulated by firmly pressing the node to a mound of moist potting mix contained in a 200 ml pot. Outgrowth of roots was prevented at all phytomers subsequently emerging distal to P 10 (Fig. 1). Nodal roots were then either retained or excised at various times following the start of their stimulated outgrowth. Control plants remained unrooted at P 10. The responses of the axillary buds at, and distal to, P 10 were then assessed at intervals throughout their post-emergence development.
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Experiments were all conducted under natural photoperiods in a heated glasshouse with average maximum day/minimum night temperatures of 25/12 °C.
Experiment 1
On 23 April 2002, 36 plants were allocated to six treatment groups (A–F), each treatment having six replicates, as shown below.
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Experiment 2
On 2 May 2002, 24 plants were allocated to four treatment groups (A–D), each of which had six replicates, as shown below.
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Experiment 3
On 9 June 2004, 42 plants were allocated to seven treatment groups (A–G), with six replicates. At this time, outgrowth of nodal roots was stimulated at P 10 in six of these treatments, the seventh remaining unrooted at P 10 as an untreated control. In the six treated groups, nodal roots were excised 3, 4, 5, 6, 7, or 8 d after the start of stimulation and their lengths measured at those times. Axillary bud/branch growth at the experimental phytomer, P 10, was measured on all plants at the start of the experimental treatments on 9 June and 8, 16, 24, and 45 d thereafter.
Analysis and presentation of data
Phytomers on the main stem were numbered acropetally with the first branched phytomer distal to the youngest basal nodal root designated phytomer 1 and successively formed phytomers termed phytomers 2, 3 etc (Fig. 1). Branches were similarly identified by the position of their phytomer of origin on the main stem.
Means and standard errors were calculated independently (Genstat, 2001) for number of emerged leaves on, and stem length of, the axillary tissues originating at each phytomer position on the main stem.
Analysis of the effects of disbudding and days of nodal root growth on the relative rate of leaf emergence from buds at phytomer positions P 10–14 in Experiments 1 and 2 was performed using the APREPMEASURES procedure in Genstat that adjusts for repeated observations on the same plants and utilizes the Greenhouse–Geisser epsilon statistic to adjust degrees of freedom of the ANOVA to ensure tests are appropriately conservative (Greenhouse and Geisser, 1959).
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Results |
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Axillary bud outgrowth in response to growth of a nodal root at phytomer 10
Axillary branch development was markedly stimulated at the rooted node, and at other nodes distal to it. This is apparent by comparing treatments A and E in Experiment 1 (Fig. 2) in which the height of the solid black bars shows the numbers of emerged leaves on, and lengths of, branches at all emerged phytomers on the main stem 22 d after stimulation of nodal root outgrowth began at phytomer 10 (P 10). In the nodally-rooted treatment (A), bud outgrowth at P 10 was faster than at P 9, immediately proximal to it, and than at P 10 in the unrooted control (E). No bud outgrowth had been stimulated distal to P 12 by that time. The acropetal effect of the nodal root became even more noticeable over the next three-week period, as indicated by comparing the final heights of the bars in treatments A and E. A sectorial response to the nodal root (sensu Marshall and Price, 1997) was particularly apparent by this time, bud activation at phytomers on the same side of the main stem as the nodal root (namely P 10 and P 12) being much greater than on the opposite side (P 11).
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Closely similar responses were observed in Experiment 2 (Fig. 3) over the 53 d period during which axillary bud growth was measured in response to a nodal root at P 10. Comparison of treatments A (nodal root at P 10 for 41 d) and D (no nodal root at P 10) shows the rate of leaf emergence on branches developed from axillary buds at P 10–14 was increased 3–5-fold by the presence of a nodal root at P 10 (Fig. 3a). Stem elongation of branches was even more strongly stimulated: none occurred in the absence of a nodal root in treatment D (Fig. 3b). Again, a sectorial response to a nodal root was marked, elongation of branch stems at P 11 and P 13 in treatment A being less than in those either side of them.
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Effect of nodal root excision on the continued outgrowth of axillary buds at, and distal to, phytomer 10
Outgrowth of distal axillary buds was still continuing to respond to the previous presence of a nodal root at P 10 at the time of final measurements, even though the excision of that root had occurred 22 d before in Experiment 1 (Fig. 2) and 37 d and 45 d before in treatments B and C, respectively, of Experiment 2 (Fig. 3). The rates of branch outgrowth from the bud at P 10 were highest in both experiments, though, when the nodal roots were retained, this effect being greater with regard to elongation of a branch than for its rate of leaf emergence. For example, excision of nodal roots after 22 d from plants in Experiment 1 treatment C had no effect on leaf emergence rate of the branch at P 10 compared with that on the continuously rooted controls in treatment A, but reduced the branch elongation rate to 57% of the continuously rooted plants (Table 1). Similar comparative reductions followed nodal root excision after 16 d or 8 d in Experiment 2. Comparison of branch outgrowth rates at P 10, 11, and 12 following nodal root excision shows that faster growing branches were less adversely affected by nodal root excision than were the slower growing ones (Table 1). The latter were of three types: those associated with nodal roots that grew for only short periods before excision, those situated at nodes further from the rooted node, and those on the opposite side of the main stem from the rooted node (P 10), i.e. those at P 11.
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Effect of short duration of exposure to nodal roots on axillary bud outgrowth
In Experiment 3, exposure to a nodal root for 3d or 4d was found to induce a small, albeit statistically non-significant, bud response and 5 d and longer had a marked stimulatory effect. Comparison of Fig. 4a and b shows that, as the duration of exposure to a nodal root before its excision increased from 0 d to 8 d, the rate of leaf emergence from the axillary bud at P 10 increased linearly, whereas its stem elongation rate showed an approximately exponential response. Following exposure to a nodal root for only 3 or 4 d, stem elongation was very slow and the buds never grew out into elongating branches. Buds receiving 5 d and longer of exposure to a nodal root developed into elongating branches, the length of which increased as the duration of exposure increased. The rates of leaf emergence and stem elongation on the axillary buds at P 10, and branches derived from them, still reflected the duration of their previous exposure to the influence of a nodal root, even during the period from 24–45 d after the start of treatment (Fig. 4a, b).
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Growth rate of the apical bud on the main stem
During the final (sixth) week after the start of experimental treatments in Experiment 1, the rate of leaf emergence from the apical bud on the main stem was increased from 1.43±0.07 per week in control plants lacking P 10 nodal roots in treatment E to 1.96±0.08 per week in plants with a P 10 root (treatment A). The effect was closely similar in Experiment 2.
Disbudding treatments in Experiment 1 also increased the rate of leaf emergence from main stem apical buds from 1.68±0.09 per week in intact control plants in treatment C to 1.89±0.12 in disbudded plants in D and, in plants lacking nodal roots throughout, from 1.43±0.07 in control plants of treatment E to 2.07±0.09 in disbudded plants in F. In plants retaining their P 10 nodal roots in treatments A and B, disbudding in B failed to raise the rate of leaf emergence above the high rate obtained in response to nodal rooting alone in A, the respective rates in A and B being 1.96±0.08 and 1.96±0.04.
Growth rates of branch apical buds relative to those of their parent apical buds on the main stem
The extent to which axillary buds were converted into fully functional branch apical buds was determined by comparing their leaf emergence rates with those of their parent main stem apical buds during the final week of Experiments 1 and 2 (Table 2). This comparison shows that, even at this time, 3 and 4 weeks after nodal root excision in Experiment 1 treatment C and Experiment 2 treatment B, respectively, the leaf emergence rates of the branches at P 10 were very similar to those of their PABs.
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Position-related differences in response of axillary buds to the influence of a nodal root at P 10
The only axillary buds that showed a continued response to the presence of a nodal root after its excision were those that had already emerged from the apical bud at that time. No effect of previous exposure to the influence of a nodal root was detected in axillary buds still contained within their PAB at the time of root excision in any of the three experiments.
In Experiment 2 (Fig. 3), the youngest emerged axillary bud at the time of nodal root excision after 8 d was that at P 12. At this time the bud at P 10 in treatments A, B, and C, each of which had by then been exposed to the influence of a nodal root for 8 d, had only just begun to show a measurable response to the nodal root (Fig. 3a, solid black segment of vertical bars). This bud remained more highly activated following nodal root excision after 8 d (treatment C) than that on the unrooted control plants (treatment D) whereas buds at, and distal to, P 11 showed no response to the 8 d exposure. After 16 d of exposure to the nodal root, the youngest emerged axillary bud in treatment B, positioned at P 14, was sufficiently activated that its rate of leaf emergence remained greater following nodal root excision than that in the control treatment (D). Axillary buds at phytomers distal to P 14 showed no measurable growth after root excision.
The presence of a nodal root at P 10, although strongly stimulating axillary buds distal to it, had no stimulatory effect on proximal buds. This was particularly apparent in Experiment 1 with respect to branch elongation (Fig. 2b). In treatment C, elongation of branches at, and distal to, the nodal root at P 10 continued after its excision, whereas those at P 8 and P 9 immediately proximal to it remained extremely short. This difference in response occurred despite the fact that, during the 3 weeks after nodal root excision, all branches were dependent solely on the same basal root system.
Growth rates of nodal root systems
In Experiment 3, outgrowth of a root at P 10 on the main stem was rapid following stimulation by contact with a moist substratum (Fig. 5a), young roots reaching a mean length of 7 mm after 3 d and 10 mm after 4 d, a time sufficient to induce continued bud outgrowth following root excision (Fig. 4). For the first 5 d after stimulation of their outgrowth, nodal roots grew by elongation of their primary axis only, lateral roots not beginning to emerge at their bases until after about 6–7 d. Root elongation was approximately linear over a period of 8 d in Experiment 3 (Fig. 5a). In Experiments 1 and 2, where nodal roots were retained for longer periods, the increase in root dry weight was exponential (Fig. 5b).
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Effect of disbudding proximal branches on outgrowth of distal axillary buds
In treatments B, D, and F of Experiment 1 (Fig. 2) the net positive stimulus to the distal axillary buds emerging from the main stem PABs was increased, in comparison with A, C, and E, respectively, by disbudding the branches proximal to them. Comparison of treatments E and F confirms the positive effect of disbudding on axillary bud outgrowth in the absence of nodal roots at P 10. Disbudding at the time of excising the nodal root at P 10 (treatment D) had approximately the same stimulatory effect on axillary bud outgrowth over the following 3 weeks, as did retention of the nodal root in the absence of disbudding (treatment A). Both in plants where the P 10 nodal root was retained (treatments A and B) and in those from which this root was excised after 22 d (treatments C and D), disbudding enhanced axillary bud outgrowth. This was particularly apparent at the younger, more distal, phytomers that emerged from the apical bud of the main stem after disbudding took place. For instance, in treatment C, without disbudding, no outgrowth of buds was detected at newly emerging phytomers distal to P 14 following nodal root excision, whereas outgrowth of newly emerging buds at P 15 to P 17 was clearly apparent in disbudded plants (treatment D).
Comparison of the results from treatments A and B shows there was a slightly additive effect of combining disbudding with the continuing presence of a nodal root, branch growth over the final 3-week period being greater in response to the combined treatments (B) than to either one alone (A or F).
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Discussion |
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The results from the present set of experiments support the retention of the two hypotheses proposed in the Introduction, namely (i) that the activation of an axillary bud is dependent upon the duration and intensity of root signal it receives following its emergence from its parent apical bud and (ii) that the level of activation reached by an axillary bud is maintained thereafter in the face of declining root signal intensity.
The results of all three experiments supported the first hypothesis. Activation of the axillary bud at P 10, together with those at more distal phytomers, was increased by the presence of a nodal root at that phytomer (Figs 2, 3, 4
) and, in Experiments 2 and 3, the level of activation attained was directly related to the duration of root presence, and the ability of buds to respond to a nodal root was confined to those that had already emerged from their PAB at the time of nodal root excision. Besides the influence of a nodal root at P 10, the intensity of the signal from the basal root system was also important. In Experiment 1, for example, disbudding of proximal branches had a strong stimulatory effect over and above that of nodal roots alone (Fig. 2), both on newly emerging buds and on those previously emerged from their PABs, possibly by allowing greater transport of RS acropetally in the shoot (Thomas et al., 2003b).
The second hypothesis was supported by the observation that, following nodal root excision in Experiments 2 and 3, the level of bud activation attained by that time was maintained for a period of at least 5 weeks after removal of the root's influence, during which time the signal received from the basal root system was seen to be inadequate to stimulate activation of equivalent buds in control plants lacking a nodal root throughout.
Activation of axillary buds
Outgrowth of axillary buds in T. repens depends upon a signal received from roots that is transported acropetally in the vascular system of the shoot (Thomas et al., 2002, 2003a, b). An alternative possibility, that the positive influence of a nodal root is brought about by that root's removal of a basipetally transported inhibitory influence from the apical bud, is unlikely. Were this so, the nodal root at P 10 would have been expected to enhance the rate of outgrowth of the slowly growing axillary buds proximal to it at P 8 and P 9 by removing the inhibitory influence, but this was not the case. The concept of the acropetal transport of RS is further substantiated by the lack of outgrowth of axillary buds in response to decapitation when they are well distanced from a nodal root in contrast to the strong outgrowth of such buds that occurs when the availability of net positive signal is increased by the removal of branches basal to them (Thomas et al., 2003a). The strong positive response to increasing duration of root presence from 0 d to 22 d in the present study is interpreted as indicating that the nodal root at P 10 continuously exports a positive signal, the influence of which remains fairly constant as root size increases. However, over time, as the plant grows and the number of organs distal to the root increases, the root signal intensity in the vicinity of axillary buds as they emerge from their PAB appears to be incrementally diluted, as evidenced by the successive reductions in their activation as their phytomeric distance from the nodal root increases (Thomas et al., 2002; this study Fig. 2; Table 2). Thus each individual axillary bud within a plant acquires its own activation level depending upon the duration and the intensity of RS to which it is exposed upon its emergence from its PAB. A bud's activation level then determines its subsequent rate of growth. This highlights the important implication that axillary bud outgrowth involves two steps: firstly, the establishment of a level of activation of its stem apical meristem (SAM) and, secondly, the subsequent autonomously regulated maintenance of a steady rate of SAM functioning and growth of organs derived from it.
Clearly the RS requirements of the two steps of axillary bud outgrowth differ. In the first, a high level of bud activation is dependent upon a high level of RS in its vicinity as it emerges from its PAB. Once its activation level is raised, however, the second step, the autonomously regulated continuation of its outgrowth involving both leaf primordium initiation and internode elongation, can proceed at a much lower level of RS. Thus a strongly activated PAB, such as the apical bud on the main stem, can continue its growth at a relatively low level of RS availability while the axillary buds newly emerging from it into an environment of low RS availability are only weakly activated. A consequence of this is that buds along the same stem, dependent upon the same basal root system, can have different activation levels and therefore grow at different rates independently of each other, as seen along the stems of treatment E in Fig. 2. The growth rate of activated buds is not totally independent of RS availability, however. Although relative differences in bud activation are maintained, a gradual decrease in the growth rates of all buds occurs as RS availability declines, concomitant with continued shoot growth distal to nodal roots (Thomas et al., 2002).
Rates of axillary bud outgrowth in themselves give no true indication of the level of activation relative to the maximum attainable under a given environment. Within an intact plant, the rate of growth of the apical bud of the primary stem declines as its phytomeric distance from the nearest root increases (Thomas et al., 2002), and is also positively influenced by the presence of a nodal root close to it (Experiments 1 and 2). Therefore, the degree of activation achieved by an axillary bud must be considered relative to that of its PAB as a measure of the maximum rate attainable in that region of the stem. Reference to Table 2 shows, for instance, that axillary bud activation at the rooted node (P 10), assessed by rate of leaf emergence, reaches the same level as that of the PAB after exposure to the influence of the nodal root for 22 d and 16 d in Experiments 1 and 2, respectively, but only 66% of that of the PAB after exposure for 8 d in Experiment 2. Thus with the leaf appearance rates pertaining in these experiments it appears that the presence of a nodal root for a period of three to four phyllochrons is required for full activation of its associated axillary bud.
From a more general stand-point, the cumulative response of buds to pulses of nodal root influence seems closely analogous to the flowering response of buds to low temperature vernalization in which the level of response attained is likewise not only influenced both by duration and strength of the stimulus received (namely exposure to low temperature), but is also subsequently maintained, in the absence of the inducing signal, under non-extreme cultural conditions (Sheldon et al., 2000; Gendall et al., 2001; Sung and Amasino, 2006).
How widespread the cumulative and sustained response of axillary buds to RS, as detailed for T. repens, is amongst other plant species remains to be tested, but our experiments with other nodally-rooting, plagiotropic, clonal plants (Thomas and Hay, 2004) indicate that this is possibly generally the case in this particular group. In other plant model systems, such as Pisum for instance, axillary bud development has been described as divisible into three stages: ‘dormancy’, a transition stage, and sustained growth (Stafstrom and Sussex, 1992; Dun et al., 2006). These stages are not quite so apparent in T. repens. In this species, axillary buds are actively developing at the time of their emergence from their PAB with a vigour determined by that of their PAB (Thomas et al., 2003a), so the concept of an initial ‘dormant’ stage does not seem applicable. The rate of future growth of a bud is then determined by the activation of its SAM during a phase, of 3–4 phyllochrons immediately post-emergence, which can be considered equivalent to the transition stage in Pisum. In Pisum, axillary bud activation is reversible during this stage, however, whereas in T. repens the activation level reached was maintained in Experiment 2 for at least 45 d. Axillary bud outgrowth in T. repens seems to have no stage that is directly equivalent to the ‘checkpoint’ determining the switch from bud dormancy to the transition stage that has been described for Arabidopsis (Ward and Leyser, 2004).
The role of RS in axillary bud activation in T. repens, raises questions as to the nature of the translocated root signal(s) (RS) and the physiological processes by which an axillary bud's activation level is translated so as to determine its rates of leaf emergence and stem elongation.
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Acknowledgements |
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We thank Jocelyn Tilbrook and Rachel Sheridan for technical assistance and Fred Potter for statistical advice. This work was funded by the MeriNet programme, New Zealand Foundation for Research, Science and Technology, contracts C10X0203 and C10X0404.
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