Apical dominance

Current Biology

Magazine researchers have recognized that simply visiting sites for measurements is enough to alter experimental results. And some of the early discoveries about plant touch sensitivity were found serendipitously by accidentally activating the touchresponse pathway during seemingly innocuous experimental procedures. Within a few minutes, simple perturbations or harvesting of plant tissue are enough to activate robust touch-sensitive gene regulatory changes. Without knowledge of the exquisite sensitivities of plants, researchers can unintentionally affect their experimental results. It’s good to be aware that your plants are much more perceptive than they might appear! Where can I find out more? Braam, J. (2005). In touch: Plant responses to mechanical stimuli. New Phytol. 165, 373–389. Braam, J., and Davis, R.W. (1990). Rain-, wind-, and touch-induced expression of calmodulin and calmodulin-related genes in Arabidopsis. Cell 60, 357–364. Chehab, E.W., Yao, C., Henderson, Z., Kim, S., and Braam, J. (2012). Arabidopsis touch-induced morphogenesis is jasmonate mediated and protects against pests. Curr. Biol. 22,701–706. Haswell, E.S., and Verslues, P.E. (2015). The ongoing search for the molecular basis of plant mechanosensing. J. Gen. Physiol. 145, 398–394. Iida, H. (2014). Mugifumi, a beneficial farm work of adding mechanical stress by treading to wheat and barley seedlings. Front. Plant Sci. 5, 453. Jaffe, M.J. (1973). Thigmomorphogenesis: the response of plant growth and development to mechanical stimulation. Planta 114, 143–157. Lange, M.J.P., and Lange, T. (2015). Touchinduced changes in Arabidopsis morphology dependent on gibberellin breakdown. Nat. Plants 1, 14025. Monshausen, G.B., and Haswell, E.S. (2013). A force of nature: molecular mechanisms of mechanoperception in plants. J. Exp. Bot. 64, 4663–4680. Moulia, B., Coutand, C., and Julien, J.-L. (2015). Mechanosensitive control of plant growth: bearing the load, sensing, transducing, and responding. Front. Plant Sci. 6, 52. Moulia, B. (2013). Plant biomechanics and mechanobiology are convergent paths to flourishing interdisciplinary research. J. Exp. Bot. 64, 4617–4633. Peyronnet, R., Tran, D., Girault, T., and Frachisse, J-M. (2014). Mechanosensitive channels: feeling tension in a world under pressure. Front. Plant Sci. 5, 558. Shih, H.-W., Miller, N.D., Dai, C,.Spalding, E.P., and Monshausen, G.B. (2014). The receptor-like kinase FERONIA is required for mechanical signal transduction in Arabidopsis seedlings. Curr. Biol. 24, 1887–1892. Toyota, M., and Gilroy, S. (2013). Gravitropism and mechanical signaling in plants. Am. J. Bot. 100, 111–125.

Department of BioSciences, Rice University, Houston, TX 77005, USA *E-mail: [email protected]

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Quick guide

Sucrose flow Auxin flow Decapitation site New branch

Apical dominance Francois F. Barbier, Elizabeth A. Dun, and Christine A. Beveridge* What is apical dominance? It’s the phenomenon in plants where a main shoot dominates and inhibits the outgrowth of other shoots. In plants with strong apical dominance, main shoot tip damage or shoot tip loss, caused by pruning or herbivory, leads to the outgrowth of compact embryonic shoots (axillary buds) into branches. This decapitation process can cause a relatively unbranched plant to become bushy, drastically changing its morphology (Figure 1). Whereas apical dominance describes the control by the shoot tip over axillary buds, the term shoot branching can be used more widely to describe plant branching, regardless of the cause or form of control. What are the main ideas about how apical dominance is achieved? Growing shoot tips produce an inhibitory hormone, auxin, which moves downwards within the stem and inhibits the outgrowth of axillary buds located along the stem below. Auxin cannot enter the buds and therefore acts via secondary mechanisms. Auxin regulates two classes of upwardly-mobile hormones, strigolactones and cytokinins, which inhibit and promote bud outgrowth, respectively. Strigolactone and cytokinin signalling is at least partly integrated by BRANCHED1/TEOSINTE BRANCHED1 (BRC1/TB1), a budlocalised transcription factor that inhibits bud outgrowth. Auxin flowing in the main stem may also inhibit bud growth by suppressing auxin flow from the bud; this auxin flow requires a specialised polar auxin transport pathway. In addition to these hormonal mechanisms, the strong demand for sugars by the growing shoot tip(s) is thought to contribute to the suppression of bud growth. Sugars themselves may act as a hormone-like signal, triggering the earliest stage of bud growth. When the shoot tip is removed (Figure 1), auxin levels progressively decrease down the stem; however, this occurs too slowly to account for the early bud growth that is

Current Biology 27, R853–R909, September 11, 2017 © 2017 Elsevier Ltd

INTACT

DECAPITATED

Figure 1. Model of systemic regulation of apical dominance by auxin and sucrose. The growing shoot tip of the intact plant (left) inhibits axillary bud outgrowth through maintaining a strong sink strength for sugars (blue dashed arrows) and by producing auxin (red dashed arrow). After decapitation (right), sucrose distribution is rapidly modified and auxin in the stem is progressively depleted. This process triggers bud release and growth into branches (white arrows). The plants pictured are 23-day-old garden pea (Pisum sativum cv Torsdag) plants grown under 18 hour photoperiod. Decapitated plants had the shoot tip removed above the highest expanded leaf 11 days prior to the photograph being taken. We would like to thank Thien Long Tran for providing the plants that appear in this figure.

observed. In contrast, after the loss of the growing shoot tip, sugars are rapidly redistributed. Why is shoot branching important? Plant survival and reproduction depend on the maintenance of plant growth and development. In plants with strong apical dominance, the growth of dormant axillary buds into branches after shoot tip loss is an absolute requirement for completion of the plant life cycle, because a shoot tip is needed to give rise to flowers and seeds. In contrast, plants with weak or no apical dominance are bushy and may respond much less to loss of a shoot tip. The modulation of shoot branching is also required in intact plants. Through the fine-tuning of shoot branching, canopy structure can be optimised to environmental conditions: maximising the ability to obtain nutrient

Current Biology

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resources, improving light interception, and enabling shade avoidance and seasonal growth.

Plant cell walls

Why is this important for crops? Modulating shoot architecture in many agricultural, forestry and horticultural crops, as well as in ornamental industries, is still heavily reliant on the age old process of pruning. Crop yields are generally tightly correlated with plant architecture and therefore with shoot branching. In some cases, increased branching positively correlates with yield (increased number of seeds and fruits) and in some cases it negatively correlates with it (decreased size of fruits, increased lodging or shoot bending). Moreover, plant architecture is an important trait in the resistance against pests and diseases though its effect on the canopy structure and airflow. Changes in shoot architecture have led to massive yield increases in major crops such as maize and rice, and in horticultural species such as apples. The most famous example is the domestication of maize, with increased TB1 gene expression leading to non-branched plants with bigger kernels and resistance to lodging. Any future important questions? The recent discovery of the involvement of sugars in apical dominance is driving a reassessment of the current models of shoot branching. In species bearing buds with established vascular connections and with photosynthetic potential, the role of sugars is unlikely to be simply limited to that of an energy and carbohydrate source, thus emphasising potential signalling roles for sugars. And the mechanism of action of plant hormones in controlling bud growth at the cellular level is still poorly understood. Where can I find out more? Barbier, F.F., Lunn, J.E., and Beveridge, C.A. (2015). Ready, steady, go! A sugar hit starts the race to shoot branching. Curr. Opin. Plant Biol. 25, 39–45. Mason, M.G., Ross, J.J., Babst, B.A., Wienclaw, B.N., and Beveridge, C.A. (2014). Sugar demand, not auxin, is the initial regulator of apical dominance. Proc. Natl. Acad. Sci. USA 111, 6092–6097. Mathan, J., Bhattacharya, J., and Ranjan, A. (2016). Enhancing crop yield by optimizing plant developmental features. Development. 143, 3283–3294. Rameau, C., Bertheloot, J., Leduc, N., Andrieu, B., Foucher, F., and Sakr, S. (2015). Multiple pathways regulate shoot branching. Front. Plant Sci. 5, 741.

School of Biological Sciences, The University of Queensland, St. Lucia, QLD 4072, Australia. *E-mail: [email protected]

Herman Höfte* and Aline Voxeur Plants are able to generate large leaf surfaces that act as two-dimensional solar panels with a minimum investment in building material, thanks to a hydrostatic skeleton. This requires high intracellular pressures (up to 1 MPa), which depend on the presence of strong cell walls. The walls of growing cells (also called primary walls), are remarkably able to reconcile extreme tensile strength (up to 100 MPa) with the extensibility necessary for growth. All walled organisms are confronted with this dilemma — the need to balance strength and extensibility — and bacteria, fungi and plants have evolved independent solutions to cope. In this Primer, we discuss how plant cells have solved this problem, allowing them to support often very large increases in volume and to develop a broad variety of shapes (Figure 1A,B,D). This shape variation reflects the targeted deposition of wall material combined with local variations in cell-wall extensibility, processes that remain incompletely understood. Once the cell has reached its final size, it can lay down secondary wall layers, the composition and architecture of which are optimized to exert specific functions in different cell types (Figure 1E–G). Such functions include: providing mechanical support, for instance, for fibre cells in tree trunks or grass internodes; impermeabilising and strengthening vascular tissue to resist the negative pressure of the transpiration stream; increasing the surface area of the plasma membrane to facilitate solute exchange between cells (Figure 1C); or allowing important elastic deformation, for instance, to support the opening and closing of stomates. Specialized secondary walls, such as those constituting seed mucilage, are stored in a dehydrated form in seedcoat epidermis cells and show rapid swelling upon hydration of the seed. Other walls, in particular in reserve tissues, can accommodate large amounts of storage polysaccharides, which can be easily

mobilized as a carbon source. Here we will discuss some general principles underlying wall architecture and wall growth that have emerged from recent studies, as well as future questions for investigation (Box 1). Wall strength and toughness conferred by co-evolved polymers Plant cell walls consist primarily of carbohydrates and phenolic compounds (Figure 2), with only minor amounts of structural proteins (up to 10%), a composition optimal for photosynthetic organisms, which have access to abundant C-sources, but with often limited access to nitrogen and sulphur present in proteins. Plant organs, like other biological materials, have hierarchical architectures at multiple length scales (from nanometer up to meter scales) yielding mechanical properties that far exceed those of the simple combination of individual components. At the scale of the cell wall, the recipe for the exceptional strength and toughness appears to reside in the combination of a network of rigid, and mostly oriented, cellulose microfibrils with an energydissipative hydrogel consisting of matrix polysaccharides. (In material science ‘strong’ is defined as resistant to deformation; ‘tough’ as resistant to failure or crack propagation). Critical factors for the synergistic mechanical effects of the two components are the strong interfacial bonding between matrix and microfibrils and the presence of sacrificial reversible bonds within the hydrogel. Without delving Box 1. Some outstanding questions in cell-wall biology. • What is the mechanism underlying the stress-induced orientation of cortical microtubules? • How is matrix secretion coordinated with cellulose deposition? • What controls the formation of the biomechanical hotspots and what prevents the interaction between cellulose and xyloglucan in vivo? • How do matrix-polymer modifications influence cell-wall rheology and cell expansion? • How does the cell detect stress and strain, and to what extent is this perception involved in growth control? • How is the insertion of new wall material coupled to wall relaxation?

Current Biology 27, R853–R909, September 11, 2017 © 2017 Published by Elsevier Ltd. R865