A single-nucleus and spatial transcriptomic atlas of the shoot apex reveals insights into the vegetative-to-reproductive transition in loquat

doi:10.1016/j.jia.2025.12.031

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Chongbin Zhao^1*, Jiale Huang^1*, Yuanyuan Jiang^2*, Jie Jiang¹, Wenbing Su³, Shunquan Lin¹, Guibing Hu^1#, Xianghui Yang^1#, Ze Peng¹^#

¹State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources/Key Laboratory of Innovation and Utilization of Horticultural Crop Resources in South China (Ministry of Agriculture and Rural Affairs)/College of Horticulture, South China Agricultural University, Guangzhou 510642, China

²Guangdong Provincial Key Laboratory of Utilization and Conservation of Food and Medicinal Resources in Northern Region, Shaoguan University, Shaoguan 512005, China

³Fruit Research Institute, Fujian Academy of Agricultural Sciences, Fuzhou 350013, China

Highlights

l This study presents the first single-cell and spatial transcriptomic resource for loquat shoot apices during the vegetative-to-reproductive transition.

l Epidermal and shoot meristematic cells exhibited the most pronounced transcriptional changes, suggesting their crucial roles in floral initiation.

l A total of 43 candidate genes were identified as key regulators in the initiation of floral bud differentiation in loquat shoot apices, driven by a coordinated network of photoperiod- and circadian rhythm-related genes.

Abstract
References

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摘要

开花与坐果时间是决定果树经济价值的重要因素。然而，调控植物从营养生长向生殖生长转变的机制尚未在单细胞及空间层面得到深入阐明。本研究构建了枇杷（Eriobotrya japonica）茎尖的单核转录组（snRNA-seq）与空间转录组（stRNA-seq）整合图谱。通过snRNA-seq共获得42,546个高质量细胞核，可划分为22个细胞亚群，归属于七大细胞类型。拟时序分析重构了细胞发育轨迹，揭示其呈现出向外部和内部组织分化的分支模式，并识别出与细胞分化动态相关的关键基因。通过比较花芽分化前与启动阶段的转录组，共检测到3,329个差异表达基因，其中包括67个拟南芥成花基因的同源基因。其中，表皮层与茎尖分生组织细胞展现出最为显著的转录组重塑，凸显了这两类细胞在花芽分化启动过程中的核心地位。此外，研究还预测了43个关键候选基因（如EjCRY2与EjAGL79），它们均位于细胞发育轨迹的关键分支点，可能在细胞命运决定中发挥关键作用，并参与了以光周期和昼夜节律为主导的调控网络。空间转录组分析结果与单核转录组数据高度吻合，进一步验证了表皮及茎尖分生组织等关键区域的细胞类型鉴定。综上所述，本研究不仅为枇杷及其他果树的单细胞与空间转录组研究提供了宝贵的可用于细胞类型鉴定的标记基因与数据资源，其所鉴定的候选基因有助于未来深入解析枇杷花芽启动的分子机制，并为通过分子育种手段定向调控枇杷开花与结果时间提供了潜在靶点。

Abstract

Flowering time and subsequent fruiting significantly influence the economic value of fruit trees. However, the regulatory mechanisms underlying the vegetative-to-reproductive transition remain understudied, particularly at single-cell and spatial levels. Here, we present a single-nucleus (snRNA-seq) and spatial transcriptomic (stRNA-seq) atlas of shoot apices in loquat (Eriobotrya japonica), a perennial fruit crop with both nutritional and medicinal importance. From the snRNA-seq dataset, 42,546 nuclei were profiled and resolved into 22 clusters corresponding to seven major cell types. Pseudotime analysis reconstructed developmental trajectories, revealing bifurcated lineages toward external and internal tissues, and identified genes dynamically associated with cell differentiation. Comparative analysis between the pre-initiation and onset stages of floral bud initiation uncovered 3,329 differentially expressed genes, including 67 homologs of Arabidopsis flowering-related genes, with the most pronounced transcriptional changes observed in epidermal and shoot meristematic cells, underscoring their central roles in floral initiation. Moreover, 43 key candidate genes, such as EjCRY2 and EjAGL79, associated with pseudotime branch points critical for cell fate decisions were predicted to act within a regulatory network dominated by photoperiod- and circadian rhythm-related pathways. Finally, integration with stRNA-seq demonstrated well concordance with snRNA-seq results and supported cell-type annotations particularly for epidermal and shoot meristematic cells. Collectively, the marker genes and associated datasets generated here provide a valuable resource for advancing single-cell and spatial transcriptomic research in loquat and potentially other fruit tree species. In addition, the identified candidate genes represent promising targets for in-depth functional studies and for breeding strategies aimed at manipulating flowering and fruiting time in loquat.

Keywords: flowering loquat shoot apical meristem snRNA-seq spatial transcriptomics

Online: 18 December 2025

Fund:

This research was funded by the National Natural Science Foundation of China (32202429), Natural Science Foundation of Guangdong Province (2024A1515013141, 2022A1515012273), Guangzhou Science and Technology Project (2025A04J5441), Fujian Academy of Agricultural Sciences (GJYS202404, DWHZ2024-11), the Open Fund of the Guangdong Provincial Key Laboratory of Utilization and Conservation of Food and Medicinal Resources in Northern Region (Grant number FMR2022009Z).

About author: Chongbin Zhao, E-mail: zhaocb@stu.scau.edu.cn; Jiale Huang, E-mail: 709582263@stu.scau.edu.cn; Yuanyuan Jiang, E-mail: yyjiang613@163.com; #Correspondence Ze Peng, E-mail: zepeng@scau.edu.cn; Xianghui Yang, E-mail: gzyxh@scau.edu.cn; Guibing Hu, E-mail: guibing@scau.edu.cn *These authors contributed equally to this study.

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Chongbin Zhao, Jiale Huang, Yuanyuan Jiang, Jie Jiang, Wenbing Su, Shunquan Lin, Guibing Hu, Xianghui Yang, Ze Peng. 2025. A single-nucleus and spatial transcriptomic atlas of the shoot apex reveals insights into the vegetative-to-reproductive transition in loquat. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.12.031

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