Lessons from a century of apical dominance research

Abstract

The process of apical dominance by which the apical bud/shoot tip of the plant inhibits the outgrowth of axillary buds located below has been studied for more than a century. Different approaches were used over time, with first the physiology era, the genetic era, and then the multidisciplinary era. During the physiology era, auxin was thought of as the master regulator of apical dominance acting indirectly to inhibit bud outgrowth via unknown secondary messenger(s). Potential candidates were cytokinin (CK) and abscisic acid (ABA). The genetic era with the screening of shoot branching mutants in different species revealed the existence of a novel carotenoid-derived branching inhibitor and led to the significant discovery of strigolactones (SLs) as a novel class of plant hormones. The re-discovery of the major role of sugars in apical dominance emerged from modern physiology experiments and involves ongoing work with genetic material affected in sugar signalling. As crops and natural selection rely on the emergent properties of networks such as this branching network, future work should explore the whole network, the details of which are critical but not individually sufficient to solve the 'wicked problems' of sustainable food supply and climate change.

Keywords: Apical dominance; auxin; axillary bud; cytokinins; genetics; physiology; shoot branching; strigolactones; sugars; tillering.

Fig. 1.

Branching-focused research output over the years. The Clarivate Analytics Web of Science was used to search outputs from 1 January 1965 to 20 October 2022 with ‘shoot branching’ OR ‘apical dominance’ OR ‘axillary bud’ OR ‘bud outgrowth’ OR ‘bud dormancy’ in Topic (which searches the title, abstract, author keywords, and keywords plus). Search results were refined for document types of article and early access, and Web of Science categories of Plant Sciences, Horticulture, Agronomy, Biochemistry and Molecular Biology, and Multidisciplinary Sciences, producing 2436 articles. Each publicly available article was screened manually and categorized. Papers were selected across eight branching hypothesis bins including abscisic acid (ABA), auxin, auxin transport, cytokinin (CK), gibberellin (GA), secondary messenger, strigolactone, and sugar/nutrients. Papers were excluded that either did not focus on the branching topic or were mostly descriptive rather than hypothesis testing, leading to 483 hypothesis-testing articles. Articles covering multiple bins were plotted with a contributed fraction to each associated bin.

Fig. 2.

Simplified model of the hormonal control of branching showing (A) the whole branching network and (B and C) stages involved in producing a branch once an axillary bud is formed using the example of branching after decapitation; (B) an inhibited bud, (C) initial bud release after decapitation, and (D) the sustained growth stage. Apically derived auxin (IAA) stimulates SL biosynthesis, reduces CK levels and represses export of IAA from the bud. SL up-regulates BRC1 expression. SL also represses IAA export from the bud by acting on PIN polarity at the plasma membrane. SL may also act by a BRC1-independent pathway(s). CK has the opposite role to SL, and there is some feedback between SL and CKs. BRC1 acts to inhibit bud release and may act partly through ABA, although the role of ABA is unclear. Sucrose inhibits SL and promotes CK and IAA. Enhanced IAA levels and transport from the bud promote sustained growth, at least partly through enhancing GA. Buds are inhibited (B) primarily due to high SL levels and a poor sugar supply. Decapitation (C) induces bud release by reducing stem IAA, and enhancing sucrose supply, reducing SL, and enhancing CK in the bud. Sustained growth (D) will follow even if stem IAA and sucrose are restored, provided that IAA-enhanced GA levels cause bud elongation and enhanced auxin transport continues from the bud. Hormone levels and signalling are not shown separately. Potential effects of SL that are independent of both BRC1 and IAA transport are not shown. The dashed lines for IAA in C and D are to represent nodes either close to, or at a distance from, the decapitation site; depending on their position, these nodes may, or may not, have depleted IAA content. Arrows indicate promotion and blunt ends indicate suppression.

Fig. 3.

Simplified SL biosynthesis pathways in different species. The core pathways leading to CL are shown in a green box. CL is the precursor of both canonical and non-canonical SL after its conversion to CLA by the CYP711A/MAX1 subfamily. Canonical SLs have the 4 rings labeled A–D as shown in 5DS.

Fig. 4.

Simplified scheme of the SL signaling pathway. SL is perceived by D14, an alpha–beta hydrolase which hydrolyses SL into the ABC-ring and D-ring. The D-ring covalently binds to D14, and a complex with the MAX2 F-box and the SMXL6/7/8 proteins is formed, leading to ubiquitination-dependent degradation of SMXL/6/7/8. These proteins act as repressors of the SL signalling pathway by recruiting TPL co-repressors to repress the transcription of BRC1. In the presence of SL, degradation of the SMXL6/7/8 proteins releases the transcriptional activity of BRC1.