April 23, 2014

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

PNAS April 7, 2014

(click here to download the original article) 

Michael G. Masona, John J. Rossb, Benjamin A. Babstc, Brittany N. Wienclawc, and Christine A. Beveridgea,*

aSchool of Biological Sciences, The University of Queensland, St. Lucia, QLD 4072, Australia; bSchool of Plant Science, University of Tasmania, Sandy Bay, TAS
7005, Australia
cBiosciences Department, Brookhaven National Laboratory, Upton, NY 11973-5000
* To whom correspondence should be addressed (c.beveridge@uq.edu.au)

            The role of auxin in maintaining apical dominance in plants has been a mainstay of plant physiology for 80 years. Auxin synthesized in the apical meristem moves downward, inhibiting lateral bud growth to promote upward growth at the apex (Taiz and Zeiger, 1991), a good strategy for capturing light in a competitive environment. If the meristem is removed, auxin supply is cut off and bud dormancy is broken. Undergraduate students still conduct the classic experiment in General Botany involving auxin application to cut bean stalks to restore apical dominance, confirming in theory and practice the power of indole acetic acid to maintain bud dormancy. When I conducted this same experiment as a student at Humboldt State in the 90s, we replicated its effect with naphthalene acetic acid. Due to a common structural motif of both molecules, either could simulate the effect of an intact meristem, more proof than an undergraduate ordinarily required to accept the theory put forth in textbooks. It is therefore no less than astonishing to see this theory overturned. This has been brought about by recent evidence that casts serious doubt on auxin as the primary motivator of bud release (Cline, 1996; Beveridge et al., 2000; Cline et al., 2001; Morris et al., 2005). This shift in thinking has culminated in a report last week by the group of Christine Beveridge at the University of Queensland, Australia, published in the Proceedings of the National Academy of Sciences (Mason et al., 2014).
The authors used digital time-lapse photography to observe lateral bud growth following selective removal of the apical meristem or leaves lower down the stem. In this way, they show that the emerging leaves at the apex constitute a sucrose sink whose demand for sugar helps keep lateral buds in a dormant state. The constant supply of auxin from the apex is evidently only a part of dormancy, and it can be broken while auxin remains if sucrose is suddenly made available, for example by the removal of the sugar sink at the apex. To demonstrate this, the authors removed the apex of pea plants and measured the rate at which the lateral buds grew. When plants were decapitated, the kinetics of lateral bud growth easily outpaced the downward rate of auxin depletion once its source at the apex was removed. Bud release preceded the disappearance of the hormone once thought to be the key to repressing lateral bud growth. Instead, dormancy was being broken by something else. That something else was sucrose, which could be supplied exogenously with the same effect, i.e. bud release, even while the apical meristem was still intact. Using 11C labeled sucrose, the rate of downward sugar travel to dormant buds was shown to coincide with their release much more closely than the depletion of auxin. This effect could be blocked by girdling the stem above the youngest nodes, effectively blocking sugar transport. By selectively removing certain leaves at various distances from the apex, the authors narrowed down both the source and the sink of the sugars which effected the transition to lateral bud growth. The mature leaves closest to dormant buds provide the sucrose which triggers lateral growth, a signal that is substantially more available in the absence of the emerging leaves at the apex. These developing leaves have not yet become photosynthetically self-sufficient and ordinarily monopolize these sugars during the early stages of their development at the expense of buds lower on the stem. Bud dormancy is partly maintained by the BRANCHED1 (BRC1) protein which inhibits cell cycle and meristem activity (Gonzáez-Grandío et al., 2013). The levels of transcripts encoding this protein are controlled by cytokinin and strigolactone in pea, and the authors show that both decapitation (remove of sucrose sink) and sucrose application suppress BRC1 transcript accumulation.
These findings mark a significant change in our view of one of the most basic processes in plant development, and it has come about recently through a series of papers which have re-examined long held assumptions about the role of auxin. Additional work in this area will continue to elaborate the role of auxin in maintaining bud dormancy in conjunction with other hormones such as strigolactone and cytokinin, but it is clear that sucrose availability is necessary and sufficient to break dormancy. New avenues for research have been opened by this work regarding the interaction of gene expression, hormonal action, and metabolite supply in activating lateral branch growth. Future work in this area has great potential to affect how we conduct many basic aspects of agriculture and how we view the role of metabolites in controlling central processes in plant biology.

Beveridge CA, Symons GM, Turnbull CGN (2000) Auxin inhibition of decapitation-induced branching is dependent on graft-transmissible signals regulated by genes Rms1 and Rms2. Plant Physiol 123: 689-698
Cline MG (1996) Exogenous auxin effects on lateral bud outgrowth in decapitated shoots. Ann Botany 78: 255-266
Cline MG, Chatfield SP, Leyser O (2001) NAA restores apical dominance in the axr3-1 mutant of Arabidopsis thaliana. Ann Botany 87: 61-65
Gonzáez-Grandío E, Poza-Carrión C, Sorzano COS, Cubas P (2013) BRANCHED1 promotes axillary bud dormancy in response to shade in Arabidopsis. Plant Cell 25: 834-850
Mason MG, Ross JJ, Babst BA, Wienclaw BN, Beveridge CA (2014) Sugar demand, not auxin, is the initial regulator of apical dominance. Proc Natl Acad Sci
Morris SE, Cox MCH, Ross JJ, Krisantini S, Beveridge CA (2005) Auxin dynamics after decapitation are not correlated with the initial growth of axillary buds. Plant Physiol 138: 1665-1672
Taiz L, Zeiger E (1991) Plant Physiology. Benjamin Cummings Publishing Co., Redwood City, California

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