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Article

Heavy Fruit Load Inhibits the Development of Citrus Summer Shoots Primarily Through Competing for Carbohydrates

by
Yin Luo
,
Yu-Jia Li
,
Yong-Zhong Liu
*,
Yan-Mei Xiao
,
Hui-Fen Li
and
Shariq Mahmood Alam
National Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops, College of Horticulture & Forestry Sciences, Huazhong Agricultural University, Wuhan 430070, China
*
Author to whom correspondence should be addressed.
Horticulturae 2026, 12(1), 14; https://doi.org/10.3390/horticulturae12010014
Submission received: 30 October 2025 / Revised: 19 December 2025 / Accepted: 22 December 2025 / Published: 24 December 2025
(This article belongs to the Section Developmental Physiology, Biochemistry, and Molecular Biology)
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Abstract

The excessive and random production of summer shoots poses significant challenges to pest and disease management and the improvement of fruit quality in citrus orchards. Although heavy fruit load has been observed to reduce summer shoot numbers, the mechanism is not well understood. This study combined a field investigation with a de-fruiting experiment to demonstrate that significant negative correlation exists between fruit load and summer shoot numbers in citrus orchard. Metabolomic analysis further indicated that fruits at the cell expansion stage function as dominant carbohydrate sinks, attracting more soluble sugars. De-fruiting significantly elevated sugar content and upregulated the transcript levels of sink strength-related genes (Sucrose synthase, CsSUS4/5/6) by more than 3.0-fold in the axillary buds. Additionally, exogenous application of sugar-related DAMs (differentially accumulated metabolites), such as sucrose, significantly promoted axillary bud outgrowth. Taken together, our findings confirm that heavy fruit load suppresses shoot branching, primarily through competing for soluble sugars. This provides a physiological basis for managing summer shoots by regulating fruit load, offering a practical strategy to enhance citrus orchard management and the effectiveness of pest and disease control programs.

1. Introduction

Citrus is one of the most important fruit crops in the world with a nutritional contribution to human health. It is widely cultivated in the tropical and subtropical regions and can produce three to six flushes of new shoots per year under a normal environment [1]. Although this precocious budbreak accelerates canopy development and early fruiting, excessive and uncontrolled shoot branching often leads to excessively tall and dense trees, which makes disease and pest control very difficult, ultimately reducing yield and fruit quality [2,3,4]. Understanding the regulatory mechanisms that control axillary bud outgrowth is crucial, as shoot branching arises from the outgrowth of these buds. Gaining such insights will allow for the precise manipulation of shoot architecture, ultimately improving field management practices and enhancing fruit quality.
Shoot branching, defined as the formation of shoots from buds [5], is a primary determinant of plant architecture. The number, size, density, and spatial distribution of shoots collectively shape the plant structure [6], which continually influences field management practices, crop productivity, and production quality, especially in perennial fruit trees [3,4]. In citrus, shoot branching patterns are governed by the formation and subsequent outgrowth of axillary buds [7] as the species exhibits a pronounced self-pruning characteristic during shoot development [1]. Axillary buds originate from the axillary meristem and can remain dormant or active to form a branch [8]. Their fate is regulated by multiple factors, including environmental conditions such as soil moisture (rainfall and irrigation) and temperature, which directly influence the timing and extent of new shoot flushing [9]. These environmental factors, along with hormones and nutrients, play a critical role in axillary bud outgrowth [10,11]. In recent years, research on the underlying regulatory metabolites has increasingly focused on phytohormones and soluble carbohydrates [11,12,13,14].
The outgrowth of axillary buds is typically suppressed by the apical buds or shoot tips, a phenomenon known as apical dominance that is regulated by the interaction of multiple phytohormones [15,16]. Among these, auxin is considered the central regulator of axillary bud outgrowth [16,17]; cytokinin and strigolactone are two other key phytohormones that directly promote and inhibit axillary bud outgrowth, respectively [18,19]. Notably, apical-derived auxin prevents axillary bud outgrowth by suppressing cytokinin production and promoting strigolactone synthesis [19,20,21]. Additionally, abscisic acid (ABA) has been reported to inhibit axillary bud outgrowth primarily via interaction with auxin [22,23], while brassinosteroids (BRs) can release apical dominance by suppressing the transcription of BRANCHED1 (BRC1) [24]. Gibberellins (GAs), which are primarily involved in internode elongation, leaf development, and the suppression of reproductive development [25], can also repress axillary bud formation by modulating DELLA-SPL9 complex activity [26] or polar auxin transport [27].
Similarly to auxin, soluble sugars are the key nutrients and signaling molecules for axillary bud growth [28,29,30]. They are synthesized in source leaves and then transported to sink tissues, such as the developing axillary buds. In most species such as citrus, sucrose is the main form of transport in phloem [31]. The distribution of sucrose is governed by sink strength, the capacity of a sink organ to attract photo assimilates [32]; this strength is largely determined by the activity of sucrose synthase (SUS) and cell wall invertase (CwINV) [33]. Interestingly, sugar was even suggested as the initial stimulus for the release of apical dominance; when apical tips are removed, sucrose is rapidly redistributed to the axillary buds, promoting their growth [34]. Moreover, numerous reports have established a link between bud dormancy and a low intracellular sugar status in axillary buds [30]. Upon entering bud cells, sucrose is metabolized to provide carbon and energy for growth [28]. In addition to its metabolic role, sucrose can play role in signaling mechanism mainly through three pathways, namely trehalose 6-phosphate (Tre6P)-dependent pathway [35], hexokinase pathway [36], and the glycolysis dependent oxidative pentose phosphate pathway [29], to regulate axillary bud outgrowth.
As noted, apical dominance and bud dormancy are antagonistically regulated by auxin and sugars. This principle is applied in horticulture, where timely decapitation of apical buds reliably induces axillary bud outgrowth and promotes new shoot growth [1,16]. Li et al. [17] found that decapitation in citrus promotes axillary bud outgrowth by regulating both hormone and carbohydrate metabolism, along with associated signal transduction [17]. Conversely, it is commonly observed that a high fruit load can limit summer shoot development in citrus [37,38]. Nevertheless, the precise physiological mechanism by which a heavy fruit load inhibits axillary bud outgrowth during summer remains unclear. In this study, we performed a comparative analysis of sugar- and hormone-related metabolites in fruits and axillary buds by using GC-MS and LC-MS/MS, respectively. We further examined the impact of fruit removal (de-fruiting) on axillary bud outgrowth, sugar- and hormone-related metabolites, and transcript levels of sink strength-related genes. On the other hand, we also investigated the influence of exogenous treatment of differently accumulated metabolites (DAMs) on axillary bud growth. Our findings indicate that a heavy fruit load inhibits axillary bud growth primarily through carbohydrate competition, which provides the theoretical basis for the application of a ‘fruit load-mediated sprout suppression’ strategy in field management.

2. Materials and Methods

2.1. Plant Materials and Growth Conditions

The orchard of seven-year-old ‘Newhall’ navel orange trees (Citrus sinensis. Osbeck cv. ‘Newhall’) grafted on trifoliate orange (Poncirus trifoliata. Raf.) was used for the field investigation and other experiments, which is located at Huazhong Agricultural University, Wuhan, P.R. China (E 114°21′2″, N 30°28′35″). Six trees with similar vigor and fruit load were selected. On 24 June 2022 (after fruit set), three trees (n = 3) were completely de-fruited, and the remaining three trees were kept as the non-de-fruited control group. New shoots per branch were counted ten days after treatment. Furthermore, ten primary axillary buds (positioned 1st from the apex) were randomly labeled and their lengths were measured from 0 to 9 days after de-fruiting (DAdFs). In addition, at least another ten axillary buds were collected at 0, 3, 6, and 9 DAdFs, respectively, for microscopic observation.
For metabolite analysis, three trees of comparable vigor and fruit load were selected during the fruit cell expansion stage (17 July 2022). From the fruit-bearing shoots of each tree, at least 100 axillary buds located at the 1st to 3rd positions beneath a fruit and four randomly selected fruits were collected. A parallel de-fruiting experiment was conducted using three additional trees with similar characteristics. On each tree, fruits were removed from half of the fruit-bearing shoots, while the remaining half served as non-de-fruited controls. After 3 days of de-fruiting treatment, at least 100 axillary buds were collected per tree from equivalent nodal positions on both control (fruit-bearing) and de-fruited branches. These samples were used for subsequent metabolite profiling and qRT-PCR analysis. All samples were immediately flash-frozen in liquid nitrogen and stored at −80 °C for further analysis.
Lemon (Citrus limon Burm. f. cv. Eureka) seedlings were grown in tissue culture tubes under long-day conditions (16 h light/8 h dark at 25 °C). From 80-day-old seedlings, single-node stem segments approximately 1.5 cm in length, each containing one axillary bud, were excised. Following leaf removal, these explants were used for subsequent metabolite treatments.

2.2. Microscopic Observation of Axillary Bud Morphology and Length Calculation

A fully automated fluorescence microscope Leica M205 FA (Leica Microsystems, Wetzlar, Germany) was employed to investigate the morphology of axillary buds collected from de-fruiting branches at 0, 3, 6, and 9 DAdFs. For anatomical examinations, axillary buds were bisected at the center with a scalpel and the cross sections were observed. High-resolution images of axillary buds with clearly defined shoot apical meristem (SAM) structures were acquired for further analysis. Axillary bud length was defined as the vertical distance from the SAM to the line connecting the bases of the two bracts.

2.3. Sugar Content Measurement

Sugar contents in the axillary buds and fruit pulps were analyzed by Gas Chromatography-Mass spectrometry (GC-MS) using an Agilent 8890-5977B system (MetWare, Wuhan, China). Briefly, 20 mg of powdered samples was extracted with 500 μL of extraction solution [methanol—isopropanol—ddH2O (3:3:2, V/V/V)]. After centrifugation, 12.5 μL of the supernatant was mixed with 20 μL of internal standard (250 μg/mL) and evaporated under nitrogen. The sample was then freeze-dried to obtain the residue. The residue was reconstituted in 100 μL of methoxyamine hydrochloride in pyridine (15 mg/mL). Then, 100 μL of BSTFA was added, and the mixture was incubated at 37 °C for 30 min for derivatization. The mixture was analyzed by GC-MS using an Agilent 8890 gas chromatograph coupled with a 5977B mass spectrometer and a DB-5MS column (30 m × 0.25 mm × 0.25 μm). Samples (1 μL) were injected in split mode (5:1) with helium carrier gas at 1 mL/min. Oven temperature program: 160 °C for 1 min, ramp to 200 °C at 6 °C/min, ramp to 270 °C at 10 °C/min, ramp to 300 °C at 5 °C/min, ramp to 320 °C at 20 °C/min (hold for 5.5 min). Samples were analyzed in SIM mode (ion source 230 °C, transfer line 280 °C).

2.4. Hormone Content Measurement

Hormone contents in the axillary buds and fruit pulps were analyzed by Liquid chromatography (coupled with Tandem Mass Spectrometry) through the AB Sciex QTRAP 6500 LC-MS/MS platform in Wuhan Metware Biotechnology Co., Ltd. (Wuhan, China). Briefly, 50 mg of the powdered sample was dissolved in 1 mL of a methanol/ddH2O/formic acid mixture (15:4:1, V/V/V). Ten microliters of internal standard solution with a concentration of 100 ng/mL was added. After centrifugation, the supernatant was transferred, evaporated to dryness, reconstituted in 100 μL of 80% methanol, and filtered through a 0.22 μm membrane for LC-MS/MS (UPLC, ExionLC™ system (Sciex, Framingham, MA, USA)). The UPLC and ESI-MS/MS analytical conditions were performed according to a previously described method [39] with small modifications. The ESI-MS/MS analyses were conducted on a QTRAP® 6500+ LC-MS/MS system from Sciex (Framingham, MA, USA) equipped with an ESI Turbo Ion-Spray interface and controlled by Analyst 1.6.3 software. The ESI source operation parameters were modified: ion source, ESI+/−; source temperature (550 °C), ion spray voltage (+5500 V/−4500 V); curtain gas (CUR, 35 psi). Phytohormones were analyzed using scheduled multiple reaction monitoring (MRM) with optimized declustering potentials (DPs) and collision energies (CEs) for each transition. MultiQuant 3.0.3 software (Sciex) was used to quantify all metabolites.

2.5. The Application of Metabolites

Single-node stem segments were cultured vertically cultured in sugar-free Murashige and Tucker (MT) medium and supplemented with test metabolites including sucrose, glucose, fructose, xylose, inositol, or IAA. Their final concentrations were 10.4 mg/g, 0.22 mg/g, 0.12 mg/g, 0.01 mg/g, 0.63 mg/g, and 25 ng/g, respectively. Each metabolite treatment included three biological replicates (n = 3), with each replicate consisting of 10 stems.

2.6. RNA Extraction and Gene Expression Analysis

Total RNA was extracted using a modified Trizol method described previously [40]. RNA quality was estimated by NanoDropTM 2000 (Thermo Fisher Scientific, Waltham, MA, USA). The cDNA was synthesized using the Transccript One-step gDNA Removal and cDNA Synthesis SuperMix Kit (TransGen Biotech, Beijing, China; Code# AT311-03). Gene expression was measured by RT-qPCR with three biological replicates using the QuantStudio 6 Flex system (Thermo Fisher Scientific, Waltham, MA, USA), and the data were analyzed using the 2−ΔΔCt method [41]. The gene-specific primers were designed using the NCBI Primer-BLAST tool (https://blast.ncbi.nlm.nih.gov/Blast.cgi, accessed on 29 October 2025) based on the representative CDS sequence from CPBD (Citrus Pan-genome to Breeding Database, http://citrus.hzau.edu.cn/) and are listed in Table S3.

2.7. Statistical Analysis

Statistical analysis was performed using IBM SPSS Statistics (v27.0). Differences were considered statistically significant at p < 0.05, as determined by using Student’s t-test or Duncan’s multiple range test.

3. Results

3.1. Fruit Load Affects the Number of Summer Shoots

In the field, it was found that the ‘Newhall’ navel orange has three peaks of new shoot growth after flowering and during fruit development and ripening; these peaks occurred at 69–76 DAFs (days after flowering), 104–111 DAFs, and 125–133 DAFs, respectively (Figure 1A). Moreover, the branches with heavy fruit load (BHFLs, branch with over 80 fruits) had less than 8 new shoots while branches without fruit load (BLFL, branches without fruit) generated about 25 new shoots in the summer (Figure 1B). Specifically, in any given branch of similar diameter, the number of summer shoots decreased as the fruit number increased (Figure 1C). In addition, there was a significant negative correlation between the yield and the number of summer shoots; when the yield surpassed 3.3 kg per 125 dm3 of canopy, the number of summer shoots dropped to zero (Figure 1D).

3.2. Effects of De-Fruiting on the Development of Axillary Buds

To characterize the effect of fruit on axillary bud outgrowth, we removed fruits and found that over 75% of de-fruiting branches generated new shoots while the sprouting percentage was zero in the control branches at 10 DAdFs (Figure 2A). At 0 DAdFs, the bud was in dormancy and its SAM was enclosed by leaf primordia and tightly wrapped bracts (Figure 2B,C); at 3 and 6 DAdFs, the bracts were loosened but the SAM did not show obvious elongation (Figure 2D,E); at 9 DAdFs, the axillary bud broke through the bracts and grew rapidly to form a new shoot (Figure 2H,I). Moreover, we also found that the length of axillary buds elongated slowly and showed no significant difference before 7 DAdFs, although a slow increase was observed after 4 DAdFs. After 7 DAdFs, the buds grew rapidly and became new shoots (Figure 2J).

3.3. Comparison of Sugar- and Hormone-Related Metabolites Between Fruits and Axillary Buds on Fruit-Bearing Shoots

During the fruit cell expansion stage or summer shoot development stage, metabolites related to soluble sugars and phytohormones were analyzed in fruits and axillary buds of fruit-bearing shoots. A total of 32 sugar- and 88 hormone-related metabolites were detected (Tables S1 and S2). Among them, the contents of 23 sugar-related metabolites and 47 hormone-related metabolites were significantly different between the fruits and axillary buds (Figure 3). The DAMs of soluble sugars included 17 monosaccharides, 5 disaccharides, and 1 trisaccharide (Figure 3A). As for phytohormones, the DAMs contained 16 auxin-related metabolites (Figure 3B), 14 cytokinin-related metabolites (Figure 3C), 7 jasmonates (Figure 3D), and 10 other hormones (Figure 3E). Specifically, the contents of sucrose and most monosaccharides were significantly higher in the fruits than those in the axillary buds except for a few soluble sugars such as raffinose, lactose, and fucose, of which the contents were significantly lower in the fruits than in the axillary buds (Figure 3A); on the other hand, the contents of most auxin-related and cytokinin-related metabolites were markedly lower in the fruits than those in the axillary buds; in addition, the contents of GA3, ABA-GE, and ABA were significantly higher in the fruits than those in the axillary buds (Figure 3B–E).

3.4. Influence of De-Fruiting on Sugar and Hormone Levels in Axillary Buds

When removing the fruits, we found that the contents of some soluble sugars and phytohormones were significantly influenced in the axillary buds at 3 DAdFs (Figure 4). In detail, de-fruiting significantly increased the contents of inositol, glucose, maltose, galacturonic acid (gal-A), xylose, and glucuronic-A, while the contents of raffinose and fucose were significantly decreased (Figure 4A). Moreover, the contents of most detected hormones were significantly increased by de-fruiting at 3 DAdFs except for salicylic acid (SA) and aminocyclopropane carboxylic acid (ACC) (Figure 4B–D); the contents of maltose (Figure 4A), trans-Zeatin riboside (tZR), and GA3 (Figure 4C, D) were undetectable in the dormant axillary buds but were markedly increased by de-fruiting at 3 DAdFs.

3.5. Influence of De-Fruiting on Sink Strength-Related Genes in the Axillary Buds

Sucrose partition into sink organs is mainly decided by the sink strength, which is related to the enzyme activities of cell wall invertase and sucrose synthesis [33]. Here, the transcripts of genes encoding them were analyzed. The transcript levels of CsCwINV4 (Figure 5A) and CsSUS1/2/4/5/6 (Figure 5B) in the axillary buds were significantly enhanced by de-fruiting. Specifically, transcript levels of CsSUS4/5/6 in the de-fruiting axillary buds were increased over 3-fold compared with those in the control axillary buds (Figure 5).

3.6. Influence of Applying Sugar-Related DAMs and IAA on Axillary Bud Outgrowth

As found in Figure 3A, the contents of about 15 sugar-related metabolites were significantly higher in fruits than in axillary buds. Here, we supplemented some DAMs-related sugars such as sucrose, glucose, fructose, xylose, and inositol into the MT medium, respectively. At 10 days after supplementation, the axillary buds of the lemon stem were significantly elongated by sucrose treatment. At 20 days after supplementation, all treatments significantly promoted axillary bud outgrowth; in particular, the sucrose-containing medium significantly increased the length of young shoots derived from axillary buds by approximately four-fold compared to the control (Figure 6A,C). In addition, we also supplemented IAA into the MT medium with a final concentration of 25 ng/g and observed no significant difference in the young shoots as compared to the control at 10 or 20 days after supplementation (Figure 6B,D).

4. Discussion

Fruit setting and subsequent fruit cell expansion are crucial processes for orchard yield and plant reproduction; these processes are regulated by numerous nutrients and different phytohormones [42]. Moreover, they also influence other developmental processes such as root development [43], flowering, and shoot development [44]. In citrus production, managing the development of new shoots is critical not only for optimizing fruit yield but also for effective pest and disease control. Excessive vegetative growth can create favorable environments for pests and diseases, such as the psyllid Diaphorina citri Kuwayama (Hemiptera: Sternorrhyncha: Liviidae) and Huanglongbing (HLB) [45], which can significantly reduce fruit quality and yield. A heavy fruit load, which depends on the cultivation of fruiting shoots [46] and fruit retention [47], can weaken reproductive growth in the following season [48,49], as well as significantly reduce vegetative growth in the current season in citrus mandarin trees [37]. Here, we found that an increase in fruit numbers significantly reduced the number of ‘Newhall’ summer shoots (Figure 1) while de-fruiting promoted bud outgrowth and significantly increased the number of shoots (Figure 2). These results further demonstrated that heavy fruit load can inhibit the outgrowth of axillary buds, significantly reducing vegetative growth in the current season of citrus trees.
The regulation of shoot branching or axillary bud outgrowth involves cross-talk between various plant hormones and soluble sugars [11,12,49]. There is a long-standing debate over the relative importance of plant hormones and carbohydrates as key factors controlling the outgrowth of axillary buds. A decade ago, much emphasis was given to auxin, which was considered the central phytohormone to regulate the dormancy of axillary buds with auxin’s basipetal transportation (from the apex towards the base) or second messenger theory [15,16,19,20,21]. Later, sugar was considered as the initial regulator of apical dominance; when the shoot tips were removed, sugars were rapidly redistributed to and accumulated in axillary buds, which significantly correlated with bud release in Pisum sativum [34]. Several reports have found that dormant buds have lower sugar levels [17,29,30,34]. However, it is usually found that decapitation only promotes the outgrowth of the top one to three axillary buds in fruit crop shoots, suggesting sugar redistribution is not sufficient to promote the outgrowth of more buds in fruit crops. Li et al. [17] found that decapitation promotes citrus axillary bud outgrowth through comprehensively regulating plant hormone and carbohydrate metabolism. Given that a higher auxin concentration inhibits bud growth [50] while soluble sugars are required for bud release [30,51,52], the effect of decapitation on bud outgrowth may be due to the transient decrease in auxin and fast available sugars in the axillary buds. Similarly to apical buds or shoot tips, fruits have the role in inhibiting the axillary bud outgrowth beneath them (Figure 2A). Collectively, this inhibition of axillary bud outgrowth likely contributes to the significant reduction in summer shoot numbers observed at the whole-tree level under heavy fruit load during the cell expansion stage (Figure 1B) [37,38]. However, at the cell expansion stage, the fruits produce a lot of gibberellic acid 3 (GA3) (Figure 3E) for fruit growth [1]. In contrast, the apical bud primarily produces auxin, which is then transported basipetally [53,54]. This suggests that the underlying mechanism for fruits inhibiting axillary bud outgrowth is different from the apical dominance mechanism.
According to the source–sink model, developing roots, leaves, flowers, and fruits belong to sink organs while the mature leaves belong to the source organ which photosynthesizes and supplies carbohydrates to such sink organs; moreover, these organs usually exchange signals and compete for metabolites [55,56], eventually abiding by a ‘feedback-balance’ mechanism or compromising mutually for their own growth and development [44]. As reported before, the apical bud inhibiting the outgrowth of axillary buds, which is a key mechanism controlling plant branching, is mainly attributed to the competition for sucrose and indole-3-acetic acid (IAA) transportation from the apex towards the plant base [12,16,17]. Goetz et al. [49] suggested that the inhibition of inflorescence shoot growth due to heavy fruit load involves auxin and sugar signaling during the end of the flowering transition. Moreover, Shalom et al. [48] found that heavy fruit load weakened the reproductive growth of the next season by changing the homeostasis of abscisic acid (ABA) and IAA in citrus buds [48]. Interestingly, it has been suggested that the strong and significant reduction in root development during loquat (Eriobotrya japonica Lindl.) fruit development is due to the increased competition for carbohydrates by fruits and the alteration in the hormonal balance of ABA and IAA [57]. Here, we found that fruits accumulated higher levels of most sugars and lower levels of most hormone-related metabolites compared to the dormant axillary buds (Figure 3), highlighting that the majority of the carbohydrates produced by the leaves were transported towards the fruits and lesser carbohydrates were moved towards the buds; this might have kept the buds dormant. However, both the contents of inositol, glucose, and maltose (Figure 4) and the transcript levels of sink strength-related genes (e.g., CsSUS4/5/6) (Figure 5) in axillary buds were significantly increased after de-fruiting. Because sucrose distribution into sink organs is mainly decided by the sink strength [33], the transcript induction of these sink strength-related genes after de-fruiting further indicated that more sucrose was allocated into axillary buds for their outgrowth. Moreover, exogenous application of some sugar-related DAMs such as sucrose, glucose, fructose, xylose, and inositol can significantly enhance axillary bud outgrowth (Figure 6). It is well known that the most active period of fruit development (cell expansion stage) has a strong sink strength for carbohydrate [58]. The present results suggest that the developing fruits attract much soluble sugars from the source leaves and limit carbohydrate allocation to axillary buds, which then inhibits axillary bud outgrowth and keeps the buds at the dormant stage, significantly reducing summer shoot emergence. Since the contents of most hormone-related metabolites in the fruits were significantly lower than those in the dormant axillary buds (Figure 3), it is unlikely that fruits inhibit bud outgrowth by producing or competing for these hormones. Therefore, the increase in auxin- and cytokinin-related metabolites in axillary buds after de-fruiting (Figure 4) is possibly due to the local biosynthesis for bud outgrowth, rather than a result of redistribution from fruits. This further supports that it is the carbohydrate rather than plant hormones that plays a key role in fruits inhibiting axillary bud outgrowth in the current season.

5. Conclusions

In citrus production, devastating threats such as citrus canker, Huanglongbing (HLB), and citrus psyllid are closely linked to the emergence of new shoots, which provide abundant resources for these pests and pathogens. Moreover, the concurrent occurrence of multiple issues further reduces the efficiency of pesticide applications. We confirmed that improving fruit load inhibited axillary bud outgrowth or shoot branching, as fruits were primarily competing for soluble sugars with axillary buds rather than producing and exporting hormones to influence their outgrowth. This mechanism provides a physiological basis for utilizing fruit load as a natural means to regulate vegetative growth, thereby helping to alleviate key pest and disease pressures and ultimately contributing to improved fruit productivity and optimized orchard management.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/horticulturae12010014/s1, Table S1: Basic characteristics and concentrations of sugar-related metabolites (µg/g DW); Table S2: Basic characteristics and concentrations of identified hormone-related metabolites (ng/g FW); Table S3: Primers used in quantitative RT-PCR analysis.

Author Contributions

Y.L.: Visualization, investigation, data analysis, review, and editing. Y.-J.L., Y.-M.X. and H.-F.L.: Investigation. S.M.A.: Review and editing. Y.-Z.L.: Visualization, review, and editing. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the National Natural Science Foundation of China (Grant No. 32172509) and the earmarked fund for CARS-26.

Data Availability Statement

The original contributions presented in this study are included in the article/Supplementary Materials. Further inquiries can be directed to the corresponding author.

Conflicts of Interest

There is no conflict of interest.

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Figure 1. Effect of fruit load on the number of summer shoots. (A) The percentage of new shoot emergence after flowering in ‘Newhall’ navel orange. Data are presented as mean ± SD (n = 9 trees). Different lowercase letters indicate statistically significant differences using the Duncan test (p < 0.05). (B) The number of fruits and summer shoots on the branches. BHFL: Branch with heavy fruit load. BLFL: Branch with less fruit load. (C) The number of fruits and summer shoots per branch with varying diameters. Data are presented as mean ± SD (n = 5 branches). Asterisk (*) indicates a significant difference with each other, while (ns) represents non-significance among treatments determined by the t-test (* p < 0.05 and ** p < 0.01). (D) Correlation analysis of yield and number of new summer shoots.
Figure 1. Effect of fruit load on the number of summer shoots. (A) The percentage of new shoot emergence after flowering in ‘Newhall’ navel orange. Data are presented as mean ± SD (n = 9 trees). Different lowercase letters indicate statistically significant differences using the Duncan test (p < 0.05). (B) The number of fruits and summer shoots on the branches. BHFL: Branch with heavy fruit load. BLFL: Branch with less fruit load. (C) The number of fruits and summer shoots per branch with varying diameters. Data are presented as mean ± SD (n = 5 branches). Asterisk (*) indicates a significant difference with each other, while (ns) represents non-significance among treatments determined by the t-test (* p < 0.05 and ** p < 0.01). (D) Correlation analysis of yield and number of new summer shoots.
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Figure 2. De-fruiting induced the outgrowth of axillary buds. (A) Sprouting percentage of fruit-bearing (CK) and de-fruited (DF) branches 10 days after de-fruiting treatment. Data are presented as mean ± SD (n = 3 trees). Asterisks (**) indicate a significant difference with the control determined by the t-test (p < 0.01). (B–I) The morphological changes in axillary buds after de-fruiting. The red arrowheads indicate the dissected axillary buds. The white arrowheads indicate the position of the shoot apical meristem (SAM) in the dissected axillary buds. (J) The length of axillary buds at different times after de-fruiting. Data are presented as mean ± SD (n = 10 buds). Different lowercase letters indicate statistically significant differences using the Duncan test (p < 0.05).
Figure 2. De-fruiting induced the outgrowth of axillary buds. (A) Sprouting percentage of fruit-bearing (CK) and de-fruited (DF) branches 10 days after de-fruiting treatment. Data are presented as mean ± SD (n = 3 trees). Asterisks (**) indicate a significant difference with the control determined by the t-test (p < 0.01). (B–I) The morphological changes in axillary buds after de-fruiting. The red arrowheads indicate the dissected axillary buds. The white arrowheads indicate the position of the shoot apical meristem (SAM) in the dissected axillary buds. (J) The length of axillary buds at different times after de-fruiting. Data are presented as mean ± SD (n = 10 buds). Different lowercase letters indicate statistically significant differences using the Duncan test (p < 0.05).
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Figure 3. Differently accumulated metabolites (DAMs) between fruits and axillary buds. Contents of metabolites related to soluble sugars (A), auxin (B), jasmonic acid (C), cytokinin (D), and other phytohormones (E). ETH: ethylene; GA: gibberellin; SA: salicylic acid; SL: strigolactone; ABA: abscisic acid. Data are presented as mean ± SD (n = 3). Asterisk (*) indicates a significant difference with the control determined by the t-test (p < 0.05). The abbreviations and full names of metabolites are listed in Supplementary Tables S1 and S2.
Figure 3. Differently accumulated metabolites (DAMs) between fruits and axillary buds. Contents of metabolites related to soluble sugars (A), auxin (B), jasmonic acid (C), cytokinin (D), and other phytohormones (E). ETH: ethylene; GA: gibberellin; SA: salicylic acid; SL: strigolactone; ABA: abscisic acid. Data are presented as mean ± SD (n = 3). Asterisk (*) indicates a significant difference with the control determined by the t-test (p < 0.05). The abbreviations and full names of metabolites are listed in Supplementary Tables S1 and S2.
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Figure 4. DAMs between the axillary buds of fruit-bearing (CK) and de-fruiting (DF) branches at 3 DAdFs. Contents of metabolites related to soluble sugar (A), auxin (B), cytokinin (C), and other phytohormones (D). JA: jasmonic acid; SA: salicylic acid; SL: strigolactone; GA: gibberellin; ETH: ethylene. Data are presented as mean ± SD (n = 3). Asterisk (*) indicates a significant difference with the control determined by the t-test (p < 0.05). The abbreviations and full names of metabolites are listed in Supplementary Tables S1 and S2.
Figure 4. DAMs between the axillary buds of fruit-bearing (CK) and de-fruiting (DF) branches at 3 DAdFs. Contents of metabolites related to soluble sugar (A), auxin (B), cytokinin (C), and other phytohormones (D). JA: jasmonic acid; SA: salicylic acid; SL: strigolactone; GA: gibberellin; ETH: ethylene. Data are presented as mean ± SD (n = 3). Asterisk (*) indicates a significant difference with the control determined by the t-test (p < 0.05). The abbreviations and full names of metabolites are listed in Supplementary Tables S1 and S2.
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Figure 5. Comparison of CsCwINVs (A) and CsSUSs (B) transcript levels between axillary buds on fruit-bearing (CK) and de-fruiting (DF) branches at 3 DAdFs. CsACTIN (Cs1g05000.1) was used as an internal control. Data are presented as mean ± SD (n = 3). Asterisk (*) indicates a significant difference while (ns) represents non-significance as compared to the control, determined by the t-test (p < 0.05).
Figure 5. Comparison of CsCwINVs (A) and CsSUSs (B) transcript levels between axillary buds on fruit-bearing (CK) and de-fruiting (DF) branches at 3 DAdFs. CsACTIN (Cs1g05000.1) was used as an internal control. Data are presented as mean ± SD (n = 3). Asterisk (*) indicates a significant difference while (ns) represents non-significance as compared to the control, determined by the t-test (p < 0.05).
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Figure 6. The response of axillary buds in lemon single-node stems to sugar-related metabolites or indole acetic acid (IAA). (A) Representative image of lemon single-node stems cultured on medium supplemented with sugar-related metabolites at 20 days after treatment. (B) Representative image of lemon single-node stems cultured on medium supplemented with IAA at 20 days after treatment. (C) The young shoot length derived from the outgrowth of axillary buds in lemon single-node stems cultured in medium supplemented with sugar-related metabolites. (D) The young shoot length derived from the outgrowth of axillary buds in lemon single-node stems cultured in medium supplemented with IAA. Data are presented as mean ± SD (n = 10). Asterisk (*) indicates a significant difference while (ns) represents non-significance as compared to the control determined by the t-test (* p < 0.05 and ** p < 0.01).
Figure 6. The response of axillary buds in lemon single-node stems to sugar-related metabolites or indole acetic acid (IAA). (A) Representative image of lemon single-node stems cultured on medium supplemented with sugar-related metabolites at 20 days after treatment. (B) Representative image of lemon single-node stems cultured on medium supplemented with IAA at 20 days after treatment. (C) The young shoot length derived from the outgrowth of axillary buds in lemon single-node stems cultured in medium supplemented with sugar-related metabolites. (D) The young shoot length derived from the outgrowth of axillary buds in lemon single-node stems cultured in medium supplemented with IAA. Data are presented as mean ± SD (n = 10). Asterisk (*) indicates a significant difference while (ns) represents non-significance as compared to the control determined by the t-test (* p < 0.05 and ** p < 0.01).
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MDPI and ACS Style

Luo, Y.; Li, Y.-J.; Liu, Y.-Z.; Xiao, Y.-M.; Li, H.-F.; Alam, S.M. Heavy Fruit Load Inhibits the Development of Citrus Summer Shoots Primarily Through Competing for Carbohydrates. Horticulturae 2026, 12, 14. https://doi.org/10.3390/horticulturae12010014

AMA Style

Luo Y, Li Y-J, Liu Y-Z, Xiao Y-M, Li H-F, Alam SM. Heavy Fruit Load Inhibits the Development of Citrus Summer Shoots Primarily Through Competing for Carbohydrates. Horticulturae. 2026; 12(1):14. https://doi.org/10.3390/horticulturae12010014

Chicago/Turabian Style

Luo, Yin, Yu-Jia Li, Yong-Zhong Liu, Yan-Mei Xiao, Hui-Fen Li, and Shariq Mahmood Alam. 2026. "Heavy Fruit Load Inhibits the Development of Citrus Summer Shoots Primarily Through Competing for Carbohydrates" Horticulturae 12, no. 1: 14. https://doi.org/10.3390/horticulturae12010014

APA Style

Luo, Y., Li, Y.-J., Liu, Y.-Z., Xiao, Y.-M., Li, H.-F., & Alam, S. M. (2026). Heavy Fruit Load Inhibits the Development of Citrus Summer Shoots Primarily Through Competing for Carbohydrates. Horticulturae, 12(1), 14. https://doi.org/10.3390/horticulturae12010014

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