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First published online June 17, 2005; 10.1104/pp.104.058743 Plant Physiology 138:1665-1672 (2005) © 2005 American Society of Plant Biologists Auxin Dynamics after Decapitation Are Not Correlated with the Initial Growth of Axillary Buds1Australian Research Council Centre of Excellence for Integrative Legume Research, and School of Integrative Biology, The University of Queensland, St. Lucia, Queensland, 4072, Australia (S.E.M., M.C.H.C., S.K., C.A.B.); and School of Plant Science, University of Tasmania, Hobart, Tasmania, 7001, Australia (J.J.R.)
One of the first and most enduring roles identified for the plant hormone auxin is the mediation of apical dominance. Many reports have claimed that reduced stem indole-3-acetic acid (IAA) levels and/or reduced basipetal IAA transport directly or indirectly initiate bud growth in decapitated plants. We have tested whether auxin inhibits the initial stage of bud release, or subsequent stages, in garden pea (Pisum sativum) by providing a rigorous examination of the dynamics of auxin level, auxin transport, and axillary bud growth. We demonstrate that after decapitation, initial bud growth occurs prior to changes in IAA level or transport in surrounding stem tissue and is not prevented by an acropetal supply of exogenous auxin. We also show that auxin transport inhibitors cause a similar auxin depletion as decapitation, but do not stimulate bud growth within our experimental time-frame. These results indicate that decapitation may trigger initial bud growth via an auxin-independent mechanism. We propose that auxin operates after this initial stage, mediating apical dominance via autoregulation of buds that are already in transition toward sustained growth.
Decapitated garden pea (Pisum sativum) seedlings, bearing axillary buds in leaf axils separated by long internodes, were one of the first systems used to study apical dominance in plants (Snow, 1931  ). In pea, several axillary buds respond to decapitation by enlarging, but only a few of these reach sustained growth; dormancy remains imposed or is reimposed in the remainder (Stafstrom and Sussex, 1988). This autoregulation of shoot branching is achieved by long-distance signaling (for review, see Napoli et al., 1999). The transition of axillary buds from dormancy to sustained growth in vegetative shoots involves several developmental stages typified by expression of particular molecular markers (Stafstrom and Sussex, 1988; Napoli et al., 1999; Shimizu-Sato and Mori, 2001). The action of long-distance signals at any one or more of these stages could mediate apical dominance.
It is well known that the application of auxin to the stump of decapitated plants inhibits axillary bud outgrowth, although less is known about the stage at which auxin acts. A frequently overlooked feature of this inhibition is that it is rarely complete with axillary buds usually growing a small but measurable amount prior to or during inhibition. The results of experiments with auxin transport inhibitors also appear to be consistent with a key role for auxin in apical dominance. These compounds are reported to promote lateral outgrowth (naphthylphtalamic acid [NPA], Tamas, 1987
Genetic evidence for roles of long-distance signals in the control of bud outgrowth has been obtained by studies with mutants at nonallelic RAMOSUS (RMS) loci in pea (Beveridge, 2000
Hypotheses on the role of auxin in apical dominance state that auxin acts indirectly but is the critical regulator transported from the shoot tip (for review, see Cline, 1991
Despite the progress summarized above, many questions remain unanswered. At present, there are few published data on the relative timing of auxin depletion and bud outgrowth after decapitation. Hall and Hillman (1975)
Studies with RMS genes (Foo et al., 2005
Timing of Bud Outgrowth Using time-lapse photography under a dissecting microscope, we observed that decapitation of garden pea plants with seven leaves expanded caused bud growth at nodes 7, 6, and 2 within 4 to 6 h after shoot tip removal (Fig. 1; nodes are counted acropetally, with node 1 being the first node above the cotyledons). Buds at nodes 1 and 7 were separated by up to 20 cm. Buds of decapitated plants continued to grow at a fairly constant rate throughout the 24-h recording period. Buds of intact plants did not grow out during this time (Fig. 1). Removal of young source leaves from the shoot tip did not result in outgrowth of buds at node 2 (debladed, Fig. 1C).
As buds at node 2 grew out rapidly after decapitation, we investigated the effect of IAA on bud outgrowth at this node in more detail, taking advantage of the distance between this node and the apical bud. Buds at node 2 of decapitated plants treated with 3 mg g–1 IAA in lanolin to the decapitated stump started to grow out at a similar time to decapitated control plants (Fig. 1C). During the 24-h experimental treatment, the bud outgrowth kinetics of decapitated plants treated with IAA were similar to those of decapitated plants that were not treated with IAA (Fig. 1C). Since previous, longer-term studies indicated that IAA inhibits decapitation-induced bud outgrowth, we extended the experimental period to 37 h. Figure 2 shows that during the first 20 h of this longer-term experiment, we observed a significant increase in the length of buds at node 2 of decapitated plants with or without auxin compared with intact controls. However, approximately 24 h after decapitation and IAA application, bud growth in the auxin-treated decapitated plants was suppressed and 37 h after the start of the experiment, buds of plants treated with IAA were much shorter than those of decapitated plants that were not treated with IAA (Fig. 2).
To observe the effect of decreased export of endogenous auxin from the shoot tip on axillary bud outgrowth in intact plants, we treated the oldest unexpanded internode (above node 7) with NPA and measured bud outgrowth at nodes 7 and 2 (Figs. 1, A and C, and 2). Interestingly, NPA did not induce bud outgrowth at these nodes over the 24-h experimental period shown in Figure 1. A longer-term NPA treatment of 37 h (Fig. 2) or 3 d (data not shown) also did not induce the outgrowth of buds at node 2.
We set out to determine the endogenous levels of three auxins, IAA, indole-3-butyric acid (IBA), and 4-chloro-indole-3-acetic acid (4Cl-IAA) in plants similar to those used for the bud outgrowth analysis. In plants of this developmental stage (7 leaves expanded), IAA was clearly the most abundant auxin with IBA and 4Cl-IAA levels being lower than the limit of detection. No dilution of the internal standard was observed using 4 ng/sample of both IBA and 4Cl-IAA standards and we calculated that if these auxins are present at all at this developmental stage in pea, their levels must be approximately 200 times lower than those of IAA (data not shown). IAA levels were quantified from stem segments of intact and decapitated plants at 4 and 6 h after decapitation (Fig. 3). At 4 h, IAA levels were obtained from 9 adjacent 1-cm stem sections from below the apical bud (Fig. 3B). IAA levels in decapitated plants were reduced compared with intact plants at all stem sections for a length of 4 or 5 cm down the stem, with the greatest decreases at upper nodes. The location of the depletion in auxin level was consistent with an IAA transport rate of just over 1 cm h–1. Similar results in terms of auxin transport rates were obtained 8 h after the start of treatment (data not shown). In the apical regions of the plant (node 7), a 6-h decapitation treatment induced a reduction in IAA concentration (Fig. 3C) that correlated with the onset of bud outgrowth (Fig. 1A). However, this correlation did not exist in the lower nodes of the plant. Note that 4 h after decapitation, no change in endogenous IAA level was detected at node 6 (i.e. approximately 7 cm from the apex; Fig. 3B), even though buds at this node started growing within 4 to 6 h of decapitation (Fig. 1B). Furthermore, bud growth was observed at node 2 within 6 h after decapitation (Figs. 1C and 2), whereas no change in endogenous IAA level was observed in adjacent tissues at this time point (Fig. 3D).
At 6 h after treatment, exogenous IAA supplied to the decapitated stump caused a substantial increase in the IAA level measured at node 7 (Fig. 3C). NPA and decapitation caused similar and substantial decreases in endogenous IAA in stem tissues adjacent to node 7 (Fig. 3C). At this node, a decrease was also apparent 3 d after NPA treatment (data not shown) and in plants treated with the auxin transport inhibitor TIBA (data not shown). In contrast, decapitation, NPA, TIBA (data not shown), or the combined decapitation and IAA treatment did not have an effect on IAA levels at node 2 within 6 h of the treatment (Fig. 3D).
It is possible that a small change in auxin level in particular stem tissues may go undetected in our analysis of 1-cm stem sections. For this reason, we monitored the flow of physiological quantities of radiolabeled [3H]IAA in the polar auxin transport stream following supply to the shoot tip. Transport of [3H]IAA in intact and decapitated plants comparable to those used for bud outgrowth measurements was observed as a basipetal wave of radioactivity (Fig. 4). All plants were supplied with [3H]IAA and then either left intact (Fig. 4, A–E) or decapitated after 1 h (Fig. 4F). Intact plants were harvested at 0.5, 1.1, 2, 3, and 5.2 h, whereas the decapitated plants were harvested at 5.6 h after 3H-IAA treatment. The auxin transport profiles in intact and decapitated plants were consistent with the profile of endogenous auxin depletion observed in decapitated plants; the rate of transport seemed fairly consistent over the time course of the experiment, moving at about 1.0 to 1.2 cm h–1. The transport of auxin already in the polar auxin transport stream did not appear to be reduced by decapitation within 4 h (Fig. 4E) or 6 h (data not shown) after decapitation. A similar polar IAA transport rate is observed in pea at other developmental stages (data not shown) and in other species (Goldsmith, 1977
Using this method, we also assessed the degree to which NPA blocks auxin transport from the shoot tip. Plants pretreated with NPA for 2 h were supplied with [3H]IAA to the shoot tip and the transport of this label was observed after a further 4 h. Extremely low quantities of [3H]IAA were exported from the shoot tip of NPA-treated plants compared with control plants (Fig. 5). Similar results were obtained for plants pretreated with TIBA (data not shown).
Although IBA is not an abundant endogenous auxin in pea plants with seven leaves expanded, we nevertheless used [3H]IBA to measure the rate of IBA transport in the polar transport stream. Labeled IBA had a transport rate that was similar to that of labeled IAA (Fig. 6). However, a substantially reduced proportion of [3H]IBA was exported from the shoot tip compared with [3H]IAA (data not shown).
Our results provide convincing evidence that the initial stage of axillary bud outgrowth after decapitation of pea is not triggered by a reduction in auxin level in the stem near the outgrowing bud. Decapitation induced bud growth at all nodes measured within 4 to 6 h after removal of the apical bud (Figs. 1 and 2). However, at this stage, IAA was deficient only in the stem segments near the top of the decapitated plant (Fig. 3). In more basal segments, the auxin content was similar to that of intact plants, but bud outgrowth still occurred. Although the absolute increase in bud length as a result of decapitation was modest (0.42 mm and 0.24 mm, respectively, for node 2 and node 7 over 24 h; in Fig. 1), it represented a percentage increase of 19% for node 2 and 43% for node 7 compared with the initial length of the buds at the start of the treatment (data not shown). Additionally, the fact that growth of buds at node 2 was sustained over a longer time scale (Fig. 2) indicates that decapitation induced structural growth. It is unlikely that bud outgrowth at lower nodes is caused by depletion of endogenous auxins other than IAA, since we did not detect significant amounts of either IBA or 4Cl-IAA in plants of the developmental stage used in this study. Additionally, we have shown that the transport rate of IBA is not faster than that of IAA (Fig. 6). Our results are consistent with a study in Arabidopsis, which also showed similar transport rates for IBA and IAA (Rashotte et al., 2003 ).
We have shown that a bud can commence growth even when auxin levels in the surrounding stem tissue are unchanged. Importantly, the converse is also true; a bud can remain dormant even when auxin levels are reduced in its vicinity. We observed the latter by using the auxin transport inhibitor, NPA, which did not stimulate bud outgrowth when applied in a lanolin ring to the stem (Figs. 1 and 2), but did reduce auxin content (Fig. 3) and auxin transport (Fig. 5). This finding appears to contradict earlier studies where auxin transport inhibitors did induce bud outgrowth in intact plants (Panigrahi and Audus, 1966 The auxin transport experiment(s) also served a second purpose. Measuring endogenous auxin levels in stem segments could not by itself preclude the possibility that decapitation caused a localized drop in auxin in a small portion of the stem near the axillary bud, which then led to initial bud outgrowth. Analyses of whole stem segments may have masked such a drop. The rate of auxin transport calculated in this study indicated that decapitation could not have reduced the auxin content in any portion of the stem near the more basal axillary buds, which nevertheless began to enlarge.
As expected, decapitation did rapidly reduce auxin levels in the stem near the excision site (Fig. 3). To test whether this depletion altered the level of a second messenger that in turn rapidly moved to stimulate axillary bud outgrowth, auxin was applied to the cut stump immediately after decapitation. This application failed to significantly inhibit the initial stages of bud growth at node 2 (Fig. 1C). Therefore, it appears that the decapitation-induced signal initiating axillary bud growth is synthesized independently of auxin. Indeed, there is no evidence from our study that auxin is associated with the control of initial bud growth after decapitation. Our findings are consistent with those of Hall and Hillman (1975)
There is little doubt, however, that application of auxin to decapitated plants inhibits axillary bud outgrowth in the longer term. This was first demonstrated decades ago, and in Figure 2, we have shown that the same applies to the cultivar used in this study (see also Beveridge et al., 2000
In pea, there is therefore evidence for two mechanisms by which decapitation can stimulate axillary bud outgrowth. The first involves a rapidly transmitted signal that acts independently of auxin. In the second mechanism, which first comes into play around 24 h after decapitation, a lack of auxin allows long-term, sustained bud outgrowth. This latter mechanism may well involve an auxin-regulated second messenger, and the novel signal regulated by RMS1 is a candidate for that role. The possibility of two mechanisms is consistent with evidence that outgrowing buds can be restored to a dormant state by exogenous auxin (Stafstrom, 1995
The nature of these decapitation-induced long-distance signals that trigger initial bud outgrowth remains elusive. Biophysical consequences of decapitation, such as changes in water potential and electrical signaling (McIntyre, 1987 ; Stahlberg and Cosgrove, 1992; Wildon et al., 1992), are worthy of investigation, as these signals are rapidly transmitted and could be perceived directly or indirectly in, or near to, the axillary buds. We have shown that deblading, which could change water status, does not result in outgrowth of buds at node 2 (Fig. 1C). Secondly, as cytokinins are transported in the xylem sap and the supply of solutes delivered in the xylem sap to axillary buds increases rapidly after decapitation, cytokinins or other xylem mobile molecules may play a role in the initial stage of bud release (Mader et al., 2003). Another possibility is that decapitation removes a sink for photosynthates and nutrients and that the increased availability of these substances initiates axillary bud outgrowth. This is the nutrient diversion hypothesis proposed many decades ago (Loeb, 1918).
Our findings provide an explanation for the lack of bud outgrowth that can occur in intact plants with depleted auxin levels. For example, a 19-fold reduction of endogenous IAA levels in juvenile 35S-iaaL tobacco plants was not accompanied by enhanced axillary bud release, whereas decapitation does induce bud outgrowth at this developmental stage (Romano et al., 1991 Our comparison of the onset of bud outgrowth with the timing of changes in auxin level in the stem have led us to a somewhat surprising outcome. The results demonstrate that the dynamics of auxin depletion after decapitation are not correlated with initial axillary bud growth in pea. We have shown that instead, auxin acts as an autoregulation signal at a relatively advanced stage of bud growth, presumably via the RMS mediated signal(s) and that additional signals are required at earlier stages of bud growth. We should now turn our attention to analysis of the different stages of bud development, and to the significant role auxin plays in the autoregulation of bud outgrowth, rather than in the initiation of that process.
Plant Material and Growth Conditions
Experiments were conducted with garden pea (Pisum sativum) cv Torsdag plants grown under glasshouse conditions (Morris et al., 2001
Decapitation involved excision of the shoot tip immediately below the oldest unexpanded leaf, with seven expanded leaves remaining. Deblading involved removing the leaflets of the two youngest expanding leaves with the petioles remaining on the plant. Plants were treated with NPA by applying a ring of NPA in lanolin around the stem immediately below the oldest unexpanded leaf. NPA was dissolved in 100% ethanol and subsequently mixed through the lanolin to give a final NPA concentration of 10 mg g–1 (final ethanol concentration 10%). Treatment with 10 mg g–1 TIBA (data not shown) was conducted in a similar way. IAA treatment involved the addition of lanolin containing 3 mg g–1 IAA (final ethanol concentration 10%) to the decapitated stump.
Bud lengths were measured using a dissecting microscope connected to a time-lapse video recorder (Fig. 1) as described by Turnbull et al. (1997)
IAA, IBA, and 4Cl-IAA were extracted from frozen homogenized stem tissue in methanol:water (1:1) overnight at 4°C, purified using C18 Sep-Pak cartridges (Waters, Rydalmere, Australia), and analyzed using gas chromatography-mass spectrometry (Morris et al., 2001
[3H]IAA and [3H]IBA transport was analyzed as in Beveridge et al. (2000)
We thank Dr. Noel Davies for assistance with gas chromatography-mass spectrometry (IAA) analysis and Emily Yorsten, Jennifer Williams, Chuong Ngo, Eloise Foo, Jenny Gough, Benjamin Morris, and Sophie Noonan for technical assistance. Received December 23, 2004; returned for revision March 16, 2005; accepted March 19, 2005.
1 This work was supported by an Australian Postgraduate Award (scholarship to S.M.), by the Netherlands Organization for Scientific Research (scholarship to M.C.), and by the Australian Agency for International Development (scholarship to S.K.).  Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.058743. * Corresponding author; e-mail c.beveridge{at}botany.uq.edu.au; fax 61–7–3365–1699.
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