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.

The activation of Arabidopsis axillary buds involves a switch from slow to rapid committed outgrowth regulated by auxin and strigolactone

“…The two phases of outgrowth in Arabidopsis buds shown here differ from, and are compatible with, the growth phases proposed previously. Pea and rose buds are proposed to undergo ‘bud release’ immediately post‐decapitation, mediated by sucrose in an auxin‐independent manner, before entering an auxin‐sensitive ‘sustained growth’ phase coinciding with the initial phases of auxin export out of the bud (reviewed in Barbier et al ., 2019; Beveridge et al ., 2023). With our measurement method, we lacked the resolution to investigate bud release, as it involves minute changes in bud length.…”

“…Previous efforts to characterise different stages of bud regulation have led to a two‐phase model of bud outgrowth based primarily on data from pea and rose (reviewed in Beveridge et al ., 2023). The first stage of ‘bud release’ occurs immediately post‐decapitation, regulated in an auxin‐independent manner, followed by a second phase of ‘sustained growth’, during which auxin transport out of the bud would be established (Barbier et al ., 2015; Chabikwa et al ., 2019; Bertheloot et al ., 2020; Cao et al ., 2023).…”

“…We hypothesise that the lag phase corresponds to the time during which buds establish canalised auxin transport from the bud into the main stem, after which buds switch to a rapid growth phase, the rate of which is influenced by strigolactone, the presence of another bud, and possibly some aspects of the auxin transport network. These two phases are genetically and physiologically separable, but share regulatory inputs, and we hypothesise that they differ from (but are compatible with) the phases of outgrowth identified previously (Brewer et al ., 2009; Beveridge et al ., 2023). This work is consistent with existing models of bud activation based on a hysteretic switch in auxin transport (Prusinkiewicz et al ., 2009).…”

How do brassinosteroids fit in bud outgrowth models?

“…Many of these signals act via interactions with TEOSINTE BRANCHED1 ( TB1 ), a transcription factor gene that inhibits bud outgrowth in monocotyledons [known as BRANCHED1 ( BRC1 ) in dicotyledons]. An overview of the key interactors is shown in Box 1 , but more details can be found in recent reviews ( Beveridge et al , 2023 ; Dun et al , 2023 ; Kelly et al , 2023 ). Strigolactones (SLs) are a key inhibitor of branching, whereby promoting the expression of TB1 then can repress axillary bud outgrowth ( Dun et al , 2012 ).…”

“…To achieve optimal height and tiller number, it will be essential to have a full understanding of how hormonal, resource, and environmental signals act on stature and bud outgrowth. Although models for bud outgrowth regulation have been proposed ( Beveridge et al , 2023 ), they still lack some important information, such as why increased tillering occurs in GA-deficient plants.…”