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

  1. Christine A. Beveridgea,1
  1. aSchool of Biological Sciences, The University of Queensland, St. Lucia, QLD 4072, Australia;
  2. bSchool of Plant Science, University of Tasmania, Sandy Bay, TAS 7005, Australia; and
  3. cBiosciences Department, Brookhaven National Laboratory, Upton, NY 11973-5000
  1. Edited by Deborah P. Delmer, University of California, Davis, CA, and approved March 14, 2014 (received for review November 25, 2013)

Significance

It is commonly accepted that the plant hormone auxin mediates apical dominance. However, we have discovered that apical dominance strongly correlates with sugar availability and not apically supplied auxin. We have revealed that apical dominance is predominantly controlled by the shoot tip’s intense demand for sugars, which limits sugar availability to the axillary buds. These findings overturn a long-standing hypothesis on apical dominance and encourage us to reevaluate the relationship between hormones and sugars in this and other aspects of plant development.

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.

Footnotes

  • 1To whom correspondence should be addressed. E-mail: c.beveridge{at}uq.edu.au.
  • Author contributions: M.G.M., J.J.R., B.A.B., and C.A.B. designed research; M.G.M., J.J.R., B.A.B., and B.N.W. performed research; M.G.M. and B.A.B. contributed new reagents/analytic tools; M.G.M., J.J.R., B.A.B., and C.A.B. analyzed data; and M.G.M., J.J.R., B.A.B., and C.A.B. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1322045111/-/DCSupplemental.

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