Branching out: new insights into sucrose-induced branching

Shoot branching initiates in axillary buds that develop into vegetative stems, inflorescences, and flowers. Branching, also known as bud outgrowth, is an important strategy for plants to avoid shade, maximize photosynthesis, and deal with limited nutrient availability (Evers et al., 2011). Branching is essential for shoot regeneration when the primary shoot is compromised and loses apical dominance. Bud outgrowth is controlled by plant hormones, including auxin, strigolactones, and cytokinins (CKs); nutrients (sugars, nitrogen, phosphates) and external cues (Domagalska and Leyser, 2011).

In plants, sugar is synthesized during photosynthesis in the chloroplasts of leaves (source organs) and either immediately hydrolyzed by cytosolic and/or cell wall invertases or stored in the vacuoles and then hydrolyzed by vacuolar invertases (VInv) at a later time. After sugars are synthesized, they are transported to the sink organs, which have little to no photosynthetic activity and import sugars from the sources to meet their demands and support growth (Mason et al., 2014).

The sugar source–sink relationships can significantly influence crop productivity. In tomato (Solanum lycopersicum), side-shoots are often manually removed to provide a higher amount of nutrients to fewer larger fruits (Heuvelink and Buiskool, 1995). In cereals, a small number of tillers prevents the plant from using all available nutrients and allows space for weeds to grow; whereas too many tillers cause lodging and smaller kernels (Evers et al., 2011). Axillary buds are strong sugar sinks, and, among sugars, sucrose promotes bud outgrowth the most (Mason et al., 2014; Salam et al., 2017); however, its mechanism of action is not well understood.

Previous work showed that VInv and CKs are important players in sucrose-induced bud outgrowth. VInv is an enzyme that hydrolyzes sucrose into fructose and glucose. Silencing of the VInv-encoding genes in potato (S. tuberosum) keeps sucrose availability high and leads to increased branching of the tuber (Salam et al., 2017). CKs are crucial plant hormones for cell division, growth, and differentiation, and are involved in many developmental processes, such as apical dominance, axillary bud growth, and leaf senescence. Sachs and Thimann (1967) showed that application of exogenous CKs in dormant buds promotes bud outgrowth. Almost five decades later, Barbier et al. (2015) found that sucrose promotes CK synthesis, which suggests that CKs may mediate sucrose-induced bud outgrowth.

In this issue of Plant Physiology, Salam et al. (2021) investigated how sucrose regulates bud initiation and elongation. To isolate these processes from photosynthetically-produced sucrose, the authors used etiolated potato sprouts, which grow in the darkness but do not perform photosynthesis so sucrose levels can be easily manipulated.

The authors used feeding experiments and showed that sugars promote stem branching and elongation, with sucrose having a stronger effect than glucose and fructose. Radioactively-labeled sugars translocated through the stem and moved into the lateral buds. Chromatography and mass spectrometry experiments showed that sucrose induces CK synthesis and accumulation in the stem nodes, consistent with the idea that sucrose-induced bud outgrowth may be mediated by CKs (Barbier et al., 2015; Kiba et al., 2019). These results indicate that sucrose-driven shoot branching is a cumulative effect of sucrose and CKs.

Subsequent studies of stems fed with combinations of sucrose, synthetic CKs, and CK inhibitors showed that sucrose promotes VInv activity before lateral bud elongation, which may suggest a role for VInv in sucrose-induced bud outgrowth. VInv activity was highest with sucrose and CK treatments and the lowest with CK inhibitor treatment. Applying synthetic CK promoted VInv activity and bud outgrowth without adding sucrose, while a combination of CK inhibitors and sucrose decreased VInv activity. This indicates that both sucrose and CKs induce branching through Vinv activity.

CRISPR/Cas9 vinv knock-out lines with minimal VInv-activity levels showed a slower increase in number of branches and bud length in response to feeding with synthetic CK, suggesting that CKs act partly through VInv in promoting bud burst and elongation. In short, both sucrose and CKs increase VInv activity, and sucrose-induced bud outgrowth via VInv partially depends on CKs.

In summary, this article shows that sucrose, rather than its components glucose and fructose, induces strong bud outgrowth and promotes the accumulation of CKs. Both sucrose and CKs promote VInv activity, which itself contributes to bud outgrowth (Figure 1). The authors shed light on shoot branching, which has a major impact on plant architecture and is very important in agriculture. Considering that shoot branching reflects the strength of the sugar sink, the abovementioned findings could help to manipulate the source–sink balance to adapt crops to specific environments and improve crop yields.

Figure 1.

Possible role of sucrose (SUC) in bud initiation and elongation. HEX (hexoses: glucose and fructose). Arrows show potential interactions.

Conflict of interest statement. The authors declare no conflict of interest.