Plant, Cell and Environment (2009) 32, 694–703 doi: 10.1111/j.1365-3040.2009.01930.x The control of shoot branching: an example of plant information processing OTTOLINE LEYSER Department of Biology, Area 11, University of York, York YO10 5YW, UK ABSTRACT the apical–basal axis defined by the establishment of the shoot apical meristem at one end, and the root apical mer- Throughout their life cycle, plants adjust their body plan istem at the other. Post-embryonically, the meristems give to suit the environmental conditions in which they are rise to the entire shoot and root systems, respectively. Fur- growing. A good example of this is in the regulation of thermore, the tissues they establish can produce secondary shoot branching. Axillary meristems laid down in each leaf meristems, which if activated can produce entirely new formed from the primary shoot apical meristem can remain axes of growth with the same developmental potential as dormant, or activate to produce a branch. The decision the primary root or shoot from which they were derived. whether to activate an axillary meristem involves the assess- Thus, the body plan of a plant is determined continuously ment of a wide range of external environmental, internal throughout its life cycle, allowing it to be exquisitely envi- physiological and developmental factors. Much of this infor- ronmentally responsive. Plants can alter their body plan to mation is conveyed to the axillary meristem via a network suit their environment, and thus the environmentally regu- of interacting hormonal signals that can integrate inputs lated development of new growth axes is functionally from diverse sources, combining multiple local signals to equivalent to environmentally regulated animal behav- generate a rich source of systemically transmitted informa- iours. This review considers the mechanisms regulating tion. Local interpretation of the information provides shoot branching behaviours. The control of root branching another layer of control, ensuring that appropriate deci- is discussed elsewhere in this issue. sions are made. Rapid progress in molecular biology is uncovering the component parts of this signalling network, and combining this with physiological studies and math- HORMONAL CONTROL OF ematical modelling will allow the operation of the system to SHOOT BRANCHING be better understood. As described above, central to the regulation of animal behaviour is the nervous system. Sensory organs gather Key-words: auxin; auxin transport; axillary bud; cytokinin; information about the internal and external environment dormancy; strigolactone; TCP. and relay this information to the brain, where it is inte- BEHAVIOUR AND BODY PLAN grated, resulting in decisions about appropriate actions, which are transmitted back out into the body to direct the Multi-cellular organisms generally start life as a single toti- chosen response. Plants do not have a brain and they do not potent cell. Subsequently, the cell divides, and the daughters have a nervous system. Instead, information from the envi- specialize to assume particular functions. This is develop- ronment is integrated and processed in a distributed way ment. In most of higher animals, development proceeds in a throughout the plant body using a range of long-distance constant environment directed entirely by the animal’s signals, prominent among which are the phytohormones. genetic programme. The mechanisms of development are With respect to shoot branching, phytohormones play a complex and dependent on stochastic events and feedback central role in regulating the activity of secondary shoot regulation, so despite a high degree of homeostasis and meristems. The accumulation of data over many decades is redundancy in the system, the results for genetically identi- now allowing a more holistic understanding of the network cal animals are not always the same. None the less, the basic of interacting hormones that controls branching. Although body plan of the resulting embryo is essentially invariant. there are still substantial gaps in our knowledge, a frame- Post-embryonically, released into an inconstant environ- work for understanding environmentally responsive branch ment, animals cope by altering their behaviour. Thus, the regulation is now emerging. most environmentally responsive part of an animal’s anatomy is the wiring in the brain. In contrast, higher plants end embryogenesis in a very BACKGROUND rudimentary state.The basic body axes are established, with Shoot branches are derived from secondary shoot apical Correspondence: O. Leyser. Fax: +01904-328682; e-mail: hmol1@ meristems laid down in the axil of each leaf produced by the york.ac.uk primary shoot apical meristem. Branch number variation © 2009 The Author 694 Journal compilation © 2009 Blackwell Publishing Ltd Control of shoot branching 695 between species and cultivars can be due in part to the protonated form in the low pH of the apoplast, allowing it establishment of these meristems, but most of the environ- to cross the plasma membrane and enter cells passively. In mental responsiveness and hence, phenotypic plasticity in the cytoplasm, the pH is higher and the auxin ionizes, trap- shoot branching derives from the regulation of the activity ping it in the cell unless exported actively, for example, by of the axillary meristems after they have formed. Axillary members of the PIN-FORMED (PIN) family of auxin meristems frequently initiate a few unexpanded leaves and efflux carrier proteins, which in the stem are basally local- then arrest their growth, forming a small axillary bud. The ized. Consistent with these observations, radiolabelled bud may subsequently reactivate to produce a branch, auxin applied to the stump of the decapitated primary shoot which makes leaves, which themselves bear tertiary shoot can inhibit the activity of axillary buds below it without the apical meristems in their axils, and thus genetically identical accumulation of radiolabel in the bud (Prasad et al. 1993; plants can occupy a huge area of phenotype space ranging Booker, Chatfield & Leyser 2003). from a single unbranched shoot, to a dense bush with high- order branching. THE SECOND MESSENGER HYPOTHESIS The regulation of axillary bud activation can be influ- enced by a panoply of environmental factors. Probably the At least two distinct mechanisms have been proposed to most famous of these is damage to the primary shoot apex. account for the indirect inhibitory effect of auxin. The first It was the investigation of the response of dormant axillary involves auxin in the primary stem regulating the production buds to the removal of the primary shoot apex above them of a second mobile signal that can move upward into the bud that first suggested a role for mobile hormonal signals in to regulate its activity.There is good evidence that cytokinin the control of shoot branching. In a classic series of experi- plays such a role in mediating the inhibition of bud growth by ments, Thimann and Skoog demonstrated that the removal auxin. Cytokinin is a potent and direct activator of bud of the primary apex results in the activation of dormant outgrowth (Sachs & Thimann 1967), and auxin has been axillary buds in the subtending leaf axils, a phenomenon shown to down-regulate cytokinin synthesis both locally at dubbed apical dominance (Thimann & Skoog 1933). They the node in the main stem (Tanaka et al. 2006) as well as in showed that bud activation could be prevented by applica- the roots (Bangerth 1994). For example, in pea, decapitation tion of the hormone auxin (at the time referred to as ‘the results in an increase in cytokinin export from roots and in growth substance’) to the decapitated stump. As it was increased transcription of cytokinin biosynthetic genes in known that the primary shoot apex is a good source of the stem. Both these responses are prevented by the appli- auxin and that this auxin is transported basipetally down cation of auxin to the decapitated stump.In the absence of an the stem, these results led to the hypothesis that apical apical auxin supply, both these responses would increase dominance is mediated by auxin. cytokinin availability to buds and promote their activation. The ability of auxin to modulate cytokinin synthesis in Arabidopsis is dependent on the AXR1 gene (Nordström THE ROLES OF AUXIN IN BUD INHIBITION et al. 2004), part of the canonical auxin signalling pathway Even now, after 75 years, the mechanism – or more likely in which the TRANSPORT INHIBITOR RESPONSE mechanisms of action – of auxin in the inhibition of bud 1/AUXIN SIGNALING BOX PROTEIN (TIR1/AFB) activation are matters of some debate. The most straight- family binds auxin and transduces the auxin signal to forward explanation, that auxin from the primary apex is changes in gene expression by targeting members of transported into the buds and directly inhibits their activity, the INDOLE-3-ACETIC ACID INDUCIBLE (Aux/IAA) is not consistent with the evidence and was discounted transcriptional repressor protein family for degradation very early in investigations of the phenomenon (e.g. Snow (Leyser 2006). Consistent with a role for this pathway in bud 1937). An important nail in the coffin of this idea came regulation, AXR1 is necessary for the full inhibition of Ara- from the two-branched pea or bean systems developed by bidopsis buds by apical auxin (Chatfield et al. 2000). Tissue- Snow (Snow 1931). To make a two-branched pea/bean, the specific expression of AXR1 in an axr1 mutant background primary shoot is removed just above the cotyledonary node, demonstrated that AXR1 acts in the xylem parenchyma to resulting in the activation of buds in the cotyledon axils. mediate this effect, which is the main site of polar auxin These grow out to form two branches, which may continue transport down the shoot (Booker et al. 2003). to grow evenly, but frequently, one will come to dominate the other, with the subordinate shoot stopping growth alto- THE CANALIZATION HYPOTHESIS gether. Removal of the dominant shoot results in the reac- tivation of the subordinate shoot.