Sugar demand, not auxin, is the initial regulator of apical dominance

Abstract

For almost a century the plant hormone auxin has been central to theories on apical dominance, whereby the growing shoot tip suppresses the growth of the axillary buds below. According to the classic model, the auxin indole-3-acetic acid is produced in the shoot tip and transported down the stem, where it inhibits bud growth. We report here that the initiation of bud growth after shoot tip loss cannot be dependent on apical auxin supply because we observe bud release up to 24 h before changes in auxin content in the adjacent stem. After the loss of the shoot tip, sugars are rapidly redistributed over large distances and accumulate in axillary buds within a timeframe that correlates with bud release. Moreover, artificially increasing sucrose levels in plants represses the expression of BRANCHED1 (BRC1), the key transcriptional regulator responsible for maintaining bud dormancy, and results in rapid bud release. An enhancement in sugar supply is both necessary and sufficient for suppressed buds to be released from apical dominance. Our data support a theory of apical dominance whereby the shoot tip's strong demand for sugars inhibits axillary bud outgrowth by limiting the amount of sugar translocated to those buds.

Keywords: decapitation; girdling; long-distance signaling; shoot branching; sink demand.

Fig. 1.

Mature leaves are the source of the rapid decapitation-induced signal. (A) Positions of leaves (numbered), girdle (5) (triangle), and sites of decapitation (B–E, upper arrow, and E, lower arrow) used in this study. (B) Decapitation as well as removal of expanding leaves (node –11) within the shoot tip, but not the mature (node –5) leaves, induced rapid bud release at node 2; n = 4. The dotted line with an asterisk indicates the time at which the growth kinetics between buds of intact and decapitated plants became significantly different according to nonoverlapping 95% confidence intervals between the two treatments after an ANOVA analysis of data from three separate experiments, n = 11–12. (C) Stem girdling below node 4 prevented rapid bud release. n = 4. (D) Defoliating plants from nodes 3 to 8 prevented the decapitation-induced rapid bud release. n = 3 or 4. (E) Decapitation of the plants low on the stem delayed bud release. n = 4. All data are mean ± SEM.

Fig. 2.

Loss of apical dominance causes rapid carbon redistribution and sucrose accumulation in axillary buds. (A) Speed of ¹¹C-photoassimilate flow through the phloem is rapid but unchanged after decapitation. n = 3. (B) Decapitation rapidly increased the amount of ¹¹C radioactivity that accumulated at node 2 after ¹¹CO₂ feeding to the uppermost fully expanded leaf. n = 3. Data represent the increase in radioactivity observed in decapitated plants over intact controls ± SEM. Dotted line indicates the time at which the difference became statistically significant based on a one-sample, two-tailed t test. (C) Sucrose, but not glucose, accumulated in node 2 buds after decapitation. Twenty to twenty-four buds per replicate, n = 6. An ANOVA with a Dunnett’s multiple comparison of means test was performed comparing all samples with intact controls. (D) Decapitation after ¹⁴C-sucrose feeding to node 4 petioles enhanced ¹⁴C uptake in node 2 buds. Six buds per replicate, n = 4. Statistical significance from intact controls was determined using a two-tailed t test. All data are mean ± SEM. *Statistical difference from controls (P ≤ 0.05).

Fig. 3.

Sucrose addition rapidly initiates bud release and suppresses the branching repressor, BRC1. (A) Sucrose feeding via the nodes 3 and 5 petioles rapidly initiated bud release of intact plants. (B) Sucrose feeding via the node 3 petiole rescued the delayed bud release of plants decapitated low on the stem; n = 4. (C) BRC1 expression in node 2 buds was inhibited within 2 h by both decapitation and sucrose supply to intact plants (P ≤ 0.05). Twenty buds were collected per replicate, n = 3. *Statistical difference from controls (P ≤ 0.05) based on a two-tailed t test. All data are mean ± SEM.

Fig. 4.

Apical dominance is controlled by sugar and hormone responses. Apical dominance is maintained in intact plants predominately by limiting the axillary bud’s access to sugars. After the loss of the shoot tip, sugars rapidly accumulate in axillary buds and, as the sugar content of the buds surpasses a threshold, the buds are released. In contrast, the loss of the apical supply of auxin results in a depletion of auxin in the stem. However, auxin depletion will differ spatially and temporally along the stem because auxin depletion is relatively slow and therefore the growing buds in the upper shoot will be affected before those lower on the stem. In this model, auxin is predominately involved in prioritizing the later stages of branch growth, whereas sugars are predominately responsible for the initial bud release. Line diagrams reveal mechanisms at each bud; the width of solid lines indicates abundance, with dashed lines indicating low levels.