The Sucrose Regulation of Plant Shoot Branching

Abstract

The branching characteristics of plants represent crucial agronomic traits that significantly influence both yield and economic value. The formation of branches involves several stages, including the initiation of axillary meristems and the activation and continued growth of lateral buds. These processes are collaboratively regulated by genetic factors, hormones, nutritional availability, and environmental conditions. Recently, sucrose has emerged as a significant factor impacting plant branching characteristics. Sucrose not only serves as a carbon source, providing essential nutrition and energy for branching growth, but also integrates multiple regulatory factors to jointly influence branching development. This review summarizes the structural enzyme genes involved in the sucrose synthesis pathway and the key co-factors in signal transduction pathways, the interactions between sucrose and plant hormones and transcription factors, and the regulatory role of sucrose metabolites in plant branching. Furthermore, it highlights critical issues that require further investigation regarding the role of sucrose in regulating branching.

1. Introduction

Shoot branching initiates in axillary buds, which develop into vegetative stems, inflorescences, and flowers. This phenomenon, known as bud outgrowth, plays a pivotal role in the survival strategies of plants, allowing them to effectively navigate the challenges posed by shading, optimize photosynthesis, and adapt to conditions of limited nutrient availability [1]. The development of lateral branches is a significant factor that shapes the overall architecture of a plant, influencing its growth patterns and resource allocation. In monocot crops, the lateral branches that emerge from the base of the stem are referred to as tillers. The number of tillers produced is recognized as a critical agronomic trait that directly impacts the plant’s yield potential. Effective tillering is fundamental to the production of successful panicles, which are essential for securing high crop yields that are vital for agricultural productivity [2]. In contrast, in horticultural crops like tomatoes, an overabundance of shoot branching can complicate the allocation of carbohydrates within the plant. This imbalance can disrupt the delicate equilibrium between vegetative growth and reproductive development, potentially hindering the overall health and productivity of the crop [3]. Branching significantly influences the visual appeal of ornamental plants [4]. The formation of lateral branches generally occurs in two stages: 1. Initiation of lateral buds: A group of cells in the axil of the leaf primordium receives a specific initiation signal, prompting the cells to divide and form axillary meristems. With ongoing division, protrusions gradually develop into the lateral bud primordium. 2. Growth and development of lateral buds: Following the formation of the lateral bud primordium, it continues to elongate and grow, ultimately forming lateral buds, which further develop into lateral branches [5,6].Two theories explain the origin of lateral buds: one posits that the axillary meristem is directly derived from the apical meristem, while the other suggests that differentiated cells dedifferentiate and regain meristematic capabilities [7,8,9]. When lateral buds are formed under unfavorable external conditions, some may cease differentiation and growth, entering a dormant state. However, when conditions become favorable, these buds can exit dormancy and resume growth and development into lateral branches [6]. After the formation of axillary buds, a significant developmental choice presents itself: to either proceed with growth and evolve into branches or to stay dormant in the axils. This process is influenced by an interplay of genetic elements, plant hormones, environmental factors, and the availability of nutrients [10].

The nutrient transfer theory of apical dominance, proposed by Wardlaw and Mortimer [11], suggested that the growth of buds is hindered by competition for resources. Recent studies have refined this concept, concentrating on sugar nutrients in particular, and proposing that the demand for sugar at the tip of the bud is what primarily upholds apical dominance, thereby limiting sugar availability to the axillary buds [12,13]. Axillary buds are viewed as sink organs with reduced photosynthetic capacity. In order to promote their growth, these buds engage in competition for sugar to meet their metabolic needs [14]. Plants convert atmospheric CO₂ into carbon skeletons through the process of photosynthesis, ultimately producing carbohydrates such as sucrose and starch, which serve as energy sources for both the plants themselves and other organisms. However, the starch synthesized in photosynthetic tissues is inherently unstable and is rapidly transformed into monosaccharides or disaccharides for immediate use or transport by plants. This type of starch is often referred to as transitional starch, as it plays a crucial role in sucrose synthesis and in supporting plant growth, development, and metabolism [15,16]. Triose phosphate serves as a precursor for the synthesis of starch or sucrose. It facilitates the transport of certain triose phosphates into the cytoplasm via phosphate transporters, where they are subsequently converted into sucrose through the action of various enzymes [17]. The enzymes that play a role in this conversion include cytoplasmic aldolase (ALD), fructose-1,6-bisphosphatase (FBP), phosphohexose isomerase (PHI), glucose-6-phosphate isomerase (PGI), UDP-glucose pyrophosphorylase (UDPG), sucrose phosphate synthase (SPS), and sucrose phosphate phosphatase (SPP) [18]. After its synthesis, sucrose is distributed to different organs according to their priority needs for carbohydrates. After sucrose is synthesized in the source tissue, it is loaded into the sieve element/companion cell complex of the phloem via the apoplast or symplast pathway. The sucrose is then transported from the “source” to the “sink” driven by the turgor pressure gradient. Upon reaching the sink organ, sucrose is degraded into hexose or hexose derivatives through the action of sucrose invertase and sucrose synthase, subsequently participating in metabolic and biosynthetic processes [19]. Additionally, sucrose, hexose, and trehalose can function as signaling molecules to regulate gene expression and influence plant development. Sugar serves as an early signal that initiates the activation of axillary buds [20]. After the pea apical bud has been removed, sucrose begins to accumulate in the axillary buds before auxin levels rise, thus promoting the swift development of lateral buds [12]. Changes in the levels of trehalose 6-phosphate, which function both as a signaling molecule and a regulator of sucrose concentrations, are linked to the growth variations in lateral buds following the removal of the apical bud. This indicates that trehalose 6-phosphate is involved in the sucrose-mediated process that releases bud dormancy [21]. In addition, the onset of bud growth in different species is significantly tied to the activity of genes that regulate sugar transport, metabolism, and signaling pathways [22,23,24]. These findings support the theory that the growing shoot tip inhibits bud outgrowth by acting as a strong sink for sugars, thus depriving the axillary buds [25,26]. Yoon et al. reviewed the preferential metabolic and developmental responses to sucrose and summarized sucrose-dependent signaling pathways in plants. However, their review on the regulation of branching by sucrose was not sufficiently comprehensive [27]. This review intends to clarify the way sucrose affects branching in plants, aiming to establish a theoretical basis for a more comprehensive insight into the metabolic regulation of sucrose during plant growth and development, along with the genetic improvement of the optimal plant type.

2. Effects of Sucrose Anabolism and Transport-Related Genes on Plant Branching

The functional loss of genes associated with sucrose synthesis and transport, along with their encoded proteins, results in the impairment of sucrose production and transport. This disruption ultimately affects the delivery of sucrose to the “sink” tissues, thereby influencing the branching development of plants [28,29,30,31,32,33,34,35,36]. Additionally, the level of trehalose 6-phosphate (Tre6P) in plants is strongly positively correlated with sugar levels and is referred to as the sugar fuel gauge. Tre6P regulates sugar levels by facilitating source–sink transport and other feedback mechanisms, thereby aiding plants in optimizing their branching structure through signal transduction [21,37,38].

FBP serves as a critical rate-limiting enzyme in sucrose synthesis, and its associated gene is closely linked to the branching patterns of plants. In the case of rice (Oryza sativa), the cytoplasmic gene known as FBP1 is designated as monoculm 2 (MOC2). The mutation involving the deletion of the gene Os01g64660, which encodes this enzyme, results in a notable decrease in the number of tillers observed in the rice mutant moc2 compared to the wild type [16]. Additionally, the homologous gene MOC3 (Os04g56780)/TAB1/OsWUS is crucial for the development of axillary buds [28]. A genome-wide association study (GWAS) conducted on the rice diversity population II (S-RDP-II) pinpointed MOC2 as a significant gene affecting tiller diversity [29]. In the shoots of gs1; 2 mutants, the lack of OscFBP2 led to a reduction in sucrose levels and suppressed the tillering process during the early developmental phases of rice. However, NH4⁺ administration was capable of recovering the expression levels of OsCFBP2 [30]. In transgenic tobacco plants expressing cyanobacterial fructose-1,6-bisphosphatase, an increase in the concentration of sedoheptulose-1,7-bisphosphatase within the cytosol led to enhanced production of lateral shoots and leaves when grown under elevated CO₂ conditions [39,40]. Similarly, transgenic Arabidopsis plants that overexpressed cyanobacterial fructose-1,6-bisphosphatase-II (AcF) in the cytosol exhibited a marked increase in lateral shoot numbers at higher CO₂ levels. Moreover, AcF plants showed elevated sucrose and hexose levels in comparison to their wild-type counterparts. The expression levels of the genes MAX1, MAX4, YUCCA8, YUCCA9, and BRC1, which are involved in the biosynthesis and response to auxin or strigolactone (SL), were found to be reduced in AcF plants relative to wild types [41]. Therefore, it can be inferred that the enhancement of branching by sucrose synthesis-related enzymes is attributed to their provision of adequate carbon resources, the modulation of hormone metabolism-related gene expression, and the potential involvement of carbon and nitrogen metabolism in a synergistic manner.

Sucrose transporters (SUTs) and sugars that will eventually be exported transporters (SWEET) play essential roles in the movement of sucrose to different plant organs. The functional loss of these proteins disrupts sucrose transport mechanisms, subsequently inhibiting the growth and development of plant branching. The homologous genes associated with SUTs, specifically OsSUT1, LoSUT2, and LoSUT4, as well as the SWEET homologous gene, CmSweet17, exhibit high expression levels during the germination of axillary buds. This indicates their critical involvement in the early stages of plant growth. Moreover, the expression of RhSUC2 in roses and CmSweet17 in chrysanthemums is notably activated when subjected to external sucrose inputs. This response underscores the adaptive mechanisms these plants have developed in relation to sucrose availability [31,32,33]. In rice, the disruption of OsSUT2 and OsSUT4 negatively affects tillering [34,35], while the enhanced expression of OsSUT1 leads to an increase in both the number of tillers and sucrose levels [36].

Tre6P acts as a precursor in the synthesis of trehalose and plays a vital role as a signaling molecule in the regulation of sucrose [42]. The level of Tre6P serves as an indicator of sucrose efficiency in plants, and variations in its ratio to sucrose can significantly impact plant metabolism and growth [37,38]. After the removal of the tops of pea plants, an increase in sucrose concentration at the shoot’s base is observed, which in turn triggers higher levels of Tre6P and promotes the growth of axillary buds [21]. The localized reduction in Tre6P levels in the axillary buds of Arabidopsis supports its role in the regulation of axillary bud development. Lines with reduced Tre6P concentrations in their buds exhibited a noteworthy delay in the release of these buds. It is probable that increased Tre6P in the vascular system facilitates branching by improving the distribution of sucrose toward the buds and through the activation of the transcription factor FLOWERING LOCUS T [38]. Recent findings indicate that the synthesis of Tre6P is stimulated in SL mutants, accompanied by transcriptional alterations in the regulatory components of Tre6P signaling. An increase in Tre6P in the vasculature led to a promotion of branching in brc1 mutants, although it did not enhance branching in SL mutants. In contrast, a reduction in Tre6P levels in max2 plants resulted in inhibited and significantly postponed branching. Given that SL signaling can elevate Tre6P levels, yet excess Tre6P does not further influence SL deficiency, this implies that the Tre6P pathway is among the targets utilized by SLs to regulate shoot branching [43]. Additionally, the significant energy regulator SnRK1a phosphorylates OsNAC23, which directly suppresses the expression of TPP1, causing an increase in Tre6P levels. This relationship creates a functional loop involving OsNAC23, Tre6P, and SnRK1a that manages sugar homeostasis and synchronizes plant growth. In conditions of carbon deprivation, SnRK1a becomes activated, leading to the suppression of tillering. On the other hand, when there is an excess of carbon, SnRK1a is repressed, promoting an increase in tillering [35]. While Tre6P may enhance branching by modulating the expression of flowering genes, documented interactions between flowering-related genes and branching have been restricted to a limited number of plant species, and their exact regulatory pathways still require validation [44]. The way in which Tre6P triggers the signaling pathways that activate lateral buds is also not fully understood.

3. Sucrose Participates in the Regulation of Plant Branching by Hormones

Sucrose can induce branching by influencing plant hormones, specifically indole-3-acetic acid (IAA), cytokinin (CK), and SL [45,46,47]. It regulates branching by inhibiting the expression of genes responsible for IAA synthesis, while simultaneously upregulating genes that encode auxin transporters and auxin inhibitory genes to counteract the effects of IAA [48,49]. Additionally, sucrose promotes CK synthesis and inhibits SL synthesis. Furthermore, sucrose can also regulate branching independently of the IAA pathway by promoting CK synthesis or by inhibiting SL synthesis and the plant’s ability to perceive SL signals [50,51].

The branching of plants is affected by the specific type and concentration of hormones, with sucrose contributing to the induction of branching by enhancing, counteracting, and inhibiting different plant hormones. Specifically, IAA and SL serve to inhibit the growth of lateral buds, while CK encourages it. In the phase of axillary bud growth, a negative relationship can be observed between the concentration of sucrose and the level of auxin, suggesting an antagonistic interaction between the two [45]. In Lilium lancifolium, the interaction between the LlbHLH35 and LlSusy1 components regulates sucrose metabolism influenced by auxin during the initiation of bulbils. A reduced level of auxin within leaf axils, as a result of NPA treatment or the silencing of LlYUC6 and LlTAR1, boosts sucrose metabolism by activating the expression of LlSusy1 and LlCWIN2, thus aiding in the initiation of bulbils [46]. Sucrose and CK exhibit a synergistic effect on promoting plant branching. In decapitated and defoliated nodes of Rosa hybrid, sucrose promotes bud outgrowth only in the presence of light, which is necessary for CK synthesis [47].

Previous research has shown that vacuolar invertases (VInv) and CKs play vital roles in the outgrowth of buds induced by sucrose. VInv acts as an enzyme that hydrolyzes sucrose into fructose and glucose. Experimental feeding in potato (Solanum tuberosum) has revealed that sugars promote both the branching and elongation of stems, with sucrose having a more pronounced effect compared to glucose and fructose. In the experiments, radioactively labeled sugars were observed moving through the stem and subsequently into the lateral buds [48]. Analyses through chromatography and mass spectrometry demonstrated that sucrose stimulates the synthesis and accumulation of CKs within the stem nodes, supporting the idea that CKs may mediate the bud outgrowth induced by sucrose [25,49]. Moreover, sucrose and CKs both enhance the activity of VInv, indicating that the mechanism of sucrose-induced bud outgrowth via VInv is, in part, reliant on CKs. These observations imply that the shoot branching driven by sucrose arises from the combined effects of sucrose and CKs. Consistent with this notion, it has been found that sucrose represses bud reactions to SL, mostly independent of CK concentrations [31]. Importantly, research has indicated that the availability of sugars diminishes the inhibitory influence of SL on bud outgrowth. This phenomenon is not limited to roses and has been observed in a variety of flowering species, including both dicots and monocots, as well as annual and perennial plants [45,50,51]. The D53 protein, known as an SL repressor (DWARF53), functions as a negative regulator in the SL pathway. In contrast, the F-box protein D3 (DWARF3), which is related to MAX2, plays a crucial role in the SL signaling process in Arabidopsis. Furthermore, D14, categorized as an α/β-fold hydrolase (DWARF14), acts as a receptor for SL signaling. When SL is present on its own, a complex forms involving D14, D3, and D53, resulting in the swift degradation of both D14 and D53, thereby inhibiting tillering. On the other hand, enhancing D14 expression can lead to increased levels of D53 protein and stimulate tillering induced by sucrose. The presence of sucrose significantly elevates the levels of D53. However, this enhancement can be effectively counteracted by the overexpression of D3/MAX2. Moreover, when D3 is overexpressed, the negative influence that sucrose exerts on the SL-induced inhibition of tillering in rice becomes ineffective. Collectively, these findings indicate that sucrose influences the D3/MAX2 pathway, ultimately relieving the repressive impact of SL on shoot branching and tillering [51]. To summarize, the regulation of branching by sucrose occurs mainly through the pathways involving IAA, CK, and SL. Specifically, within the IAA pathway, sucrose inhibits the expression of genes associated with IAA synthesis while simultaneously enhancing the expression of genes encoding auxin transporters and auxin inhibitory proteins. This dual mechanism not only regulates IAA levels but also modifies its impact on plant growth and development [45,46]. Additionally, sucrose is known to stimulate the synthesis of CK, while simultaneously inhibiting the production of SL. The regulation of branching by sucrose can occur through the promotion of CK synthesis, independent of the IAA pathway. Furthermore, by inhibiting SL synthesis, sucrose reduces the plant’s sensitivity to SL signals, further enhancing its ability to regulate branching effectively. Moreover, is there a separate regulatory pathway for sucrose and auxin that functions without the involvement of CK and SL to influence branching? Overall, this intricate interaction highlights the significant role of sucrose in plant developmental processes.

4. Sucrose Regulates Branching Development via Transcription Factors

Sucrose can influence the expression of various transcription factor families, thereby regulating plant branching both directly and indirectly [52,53,54,55]. Among these, the TCP family transcription factor TEOSINTE BRAIN CHED1 (TB1)/BRANCHED1 (BRC1) is recognized as the most significant regulator of branching [56,57]. Studies across multiple species have confirmed that sucrose downregulates the expression of TB1/BRC1 [54,55,58,59]. Furthermore, new transcription factors involved in sucrose-regulated branching are continually being identified, and ongoing research is exploring related transcription factors, their potential target genes, and associated functions.

During the development of axillary buds in both monocotyledons and dicotyledons, the TB1 homologous genes BRC1/BRANCHED2 (BRC2) integrate various factors, including genes, hormones, nutrients, and light, to play a pivotal regulatory role [60,61,62]. In Pisum sativum, elevated sucrose levels have been shown to repress the expression of BRC1, which consequently leads to a rapid release of shoots [12]. Similarly, sucrose can inhibit BRC1 expression, thereby promoting the elongation of wheat axillary buds [53]. Research on the lateral branches of Sorghum bicolor, Triticum aestivum, and Rosa rugosa has also demonstrated that sucrose supply is closely linked to reduced BRC1 expression and enhanced axillary bud growth [25,53,54]. Furthermore, the overexpression of fructose-1,6-bisphosphatase in cells can increase sucrose levels in Arabidopsis, decrease BRC1 expression, and facilitate lateral branch growth [41]. In tomatoes, auxin, CK, SL, and sugars converge on a common BR-BZR1-BRC1 cascade that regulates bud outgrowth [55]. Additionally, sucrose is associated with the accumulation of the light-responsive transcription factor HY5 (HYPOCOTYL5) in leaves. Increased levels of HY5 can activate the transcription of BR biosynthesis genes in vivo, inhibit BRC1 in lateral buds, and consequently promote the growth of tomato lateral branches [58].

Sugars alleviate the suppressive effects of SL on bud development and tillering, or shoot branching, via a molecular factor typically linked to the regulation of the circadian clock. CIRCADIAN CLOCK ASSOCIATED1 (OsCCA1), a transcription factor, plays a role in modulating the circadian rhythm in rice. When OsCCA1 is overexpressed, tillering is reduced; conversely, a decrease in its expression promotes enhanced tillering. OsCCA1 facilitates the transcription of the SL receptor D14, which subsequently hinders tillering. In contrast, the introduction of exogenous sucrose reduces the expression of OsCCA1 in the buds of tillers, thus encouraging their growth. This indicates that the circadian clock merges sugar signals with the SL pathway to support normal plant development aligned with circadian rhythms, where OsCCA1 is crucial to this mechanism [59]. Furthermore, the significance of the circadian clock in regulating lateral bud growth warrants further investigation.

The DNA-binding one-finger transcription factor (Dof) is a member of the single zinc finger protein superfamily. OSDOF11 acts as a regulator of sucrose transport. Mutants of Osdof11 in rice and plants subjected to Osdof11-RNAi showcase a phenotype marked by fewer tillers and exhibit a slower rate of sucrose transport. OSDOF11 binds directly to the promoter regions of sugar transporter genes OsSUT1, OsSWEET11, and OsSWEET14, coordinating their expression. Hence, OSDOF11 modulates sugar transport through the regulation of the expression of OsSUT1, OsSWEET11, and OsSWEET14 genes [63]. Despite the identification of numerous transcription factors associated with sucrose’s role in branching, their precise functional mechanisms remain to be confirmed, and the downstream target genes are not yet clearly defined, posing a considerable obstacle for ongoing research (Table 1).

5. Regulation of Plant Branching by Sucrose Metabolites

Sucrose undergoes hydrolysis to produce fructose and glucose through the action of sucrose invertases (INVs). Providing exogenous sucrose, glucose, or fructose solutions to isolated potato tubers can induce branching. The silencing of the gene encoding VInv led to elevated sucrose concentrations and increased branching of tubers [64]. Sucrose, glucose, and fructose could all trigger bud outgrowth and antagonize the effect of auxin and SL on this process. Notably, glucose and fructose are more effective than sucrose in promoting bud outgrowth. These findings indicate that metabolic and/or signaling pathways downstream of glucose and fructose could be involved in this regulation [45]. Hexokinase 1 (HXK1) plays a vital role in glucose signaling; significantly, the overexpression of AtHXK1 in Arabidopsis enhances rosette branching [65], whereas the gin mutant of Arabidopsis, which lacks AtHXK1, displays reduced branching capabilities. Additionally, the levels of cytokinin (CK) and the expression of IPT3 in the gin mutant are markedly diminished, while the expression of CKX1 and MAX2 is heightened [66,67]. Furthermore, glucose and mannose were found to rapidly trigger shoot growth in rose and pea shoots, whereas 3-O-methylglucose (3-OMG) could not, and HXK-dependent signaling independent of downstream glucose metabolism was found to trigger shoot growth [66]. These results indicate that glucose acts as a beneficial signaling molecule promoting branching, chiefly by suppressing the expression of SL and boosting CK levels. Additionally, it is essential to investigate how non-metabolized sucrose analogs may stimulate branching. Do these analogs interact with the same downstream regulators as sucrose, or do they affect different branching regulators?

6. Conclusions

The process of bud branching is a sophisticated developmental program influenced by complex interactions among various genes, plant hormones, and environmental factors. A thorough understanding of the mechanisms governing bud branching and tillering is vital for the improvement of crop breeding and productivity. In this review, we discussed the progress of the complex regulatory mechanisms through which sucrose affects bud branching. Sucrose can serve not only as nutrients but also as signal substances to regulate the branching development of plants. Sucrose can interact with genes or transcription factors by promoting, antagonizing, and suppressing plant hormones, thereby integrating various factors to establish a regulatory network (Figure 1). The interplay between these biological processes may offer significant insights into the comprehensive understanding of shoot developmental regulation in plants.

Author Contributions

S.X., L.W., Y.C., and X.S. conceived of and designed the research. S.X. wrote the paper. L.W. and Y.W. revised the manuscript. All authors commented on the manuscript. All authors have read and agreed to the published version of the manuscript.

Data Availability Statement

No new data were created or analyzed in this study.

Conflicts of Interest

The authors declare no conflicts of interest.

Footnotes

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Figure and Table

Figure 1. The major regulatory network of plant branching through sucrose. The arrows indicate positive regulation; a line plus a dash indicates negative regulation. Genes are highlighted in red.

Table 1

Transcription factors that regulate the plant branching response by sucrose.

Species	TranscriptionFactors	Fingings	References
Solanum lycopersicum	SlBRC1/SlHY5/SlBZR1	The external application of sucrose can enhance the accumulation of SlBZR1 and SlHY5 in lateral buds, decrease the expression of SlBRC1, and thereby promote the growth of lateral buds.	[53,58,59]
Oryza sativa	OsTB1/OSDOF11/OsCCA1	OsTB1 expression was decreased in the tiller and bud base by sucrose treatment.The sucrose transport capability of osdof11 was inhibited, resulting in reduced tillering.When OsCCA1 is overexpressed, tillering is reduced; conversely, a decrease in its expression promotes enhanced tillering.	[56,63,64]
Triticum aestivum	TaTB1	The expression level of TB1 in axillary buds decreased after low sucrose treatment.	[54]
Pisum sativum	PsBRC1	The expression of the PsBRC1 gene in axillary buds of plants treated with sucrose significantly decreased within 2 h, which promoted the growth of axillary buds.	[12]
Arabidopsis	AtBRC1	Alterations in sugar partitioning affect hormone metabolism and responses, reducing AtBRC1 expression and thereby enhancing shoot branching.	[41]
Sorghum bicolor	SbBRC1	The expression level of SbBRC1 in axillary buds decreased after low sucrose treatment.	[55]
Rosa rugosa	RrBRC1	Sucrose treatment downregulates RrBRC1 expression and promotes axillary bud growth.	[25]

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