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Spatiotemporal sucrose accumulation drives tissue-specific anthocyanin biosynthesis under low phosphorus in maize

Zu-Dong Xiao1, Wang Tang1, Zhen-Yuan Chen1, Yi-Hsuan Lin1, Xiao-Gui Liang1,2, Xin Wang1, Shou-Bing Huang1, Sebastian Munz3, Simone Graeff-Hönninger3, Si Shen1#, Shun-Li Zhou1#

1 State Key Laboratory of Maize Bio-breeding, College of Agronomy & Biotechnology, China Agricultural University, Beijing 100193, China

2 Key Laboratory of Crop Physiology, Ecology and Genetic Breeding, Ministry of Education/Jiangxi Province, Jiangxi Agricultural University, Nanchang 330045, Jiangxi, China

3 Department of Agronomy, Institute of Crop Science, University of Hohenheim, Stuttgart 70599, Germany

 Highlights 

Ÿ Sucrose is indispensable for low phosphorus-induced anthocyanin biosynthesis in maize.

Ÿ Sucrose accumulation and phosphate jointly shape tissue-specific distribution of anthocyanin under low phosphorus.

Ÿ PHOSPHATE STARVATION RESPONSE1 (PHR1) links sugar and low phosphorus signaling in anthocyanin biosynthesis.

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摘要  

低磷胁迫会诱导植物组织特异性合成花青素和积累糖,但糖和无机磷水平在调控花青素合成中的关系仍不清楚。本研究调查了低磷下玉米幼苗中糖积累与花青素合成的时空模式,并设计试验改变植株糖含量,探究了糖积累对低磷诱导花青素合成的意义。结果表明,低磷胁迫下花青素合成和蔗糖积累在时间和空间上高度耦合,其中叶鞘中无机磷含量最低而蔗糖和花青素水平最高;通过冷环割人为提高内源蔗糖含量可促进花青素合成,而通过叶片遮光降低蔗糖含量则抑制花青素合成;相关性分析显示蔗糖与花青素含量呈显著正相关关系。叶片和叶鞘在不同糖溶液中的离体培养试验进一步表明,蔗糖积累对低磷诱导的花青素合成必不可少。因此,低磷下花青素合成的时空模式由无机磷水平和蔗糖积累共同决定,且可通过改变无机磷和蔗糖的分布模式来调控花青素分布。对低磷处理叶鞘(有和无蔗糖积累)的转录组分析表明,PHR1可能介导了糖信号与低磷信号在调控花青素合成中的互作。本研究揭示了低磷条件下花青素组织特异性合成的调控机制,并为通过调控花青素提高磷利用效率提供了潜在的目标。



Abstract  

Low phosphorus (LP) stress induces tissue-specific anthocyanin biosynthesis and sugar accumulation in plants. However, the relationship between sugar levels and phosphate (Pi) availability in regulating anthocyanin remains unclear. This study investigated the spatiotemporal patterns of sugar accumulation and anthocyanin biosynthesis in maize seedlings, and conducted experiments modifying sugar status to examine the significance of sugar accumulation for LP-induced anthocyanin biosynthesis. The results demonstrated that, under LP conditions, anthocyanin biosynthesis and sucrose accumulation were spatially and temporally coupled, with leaf sheaths exhibiting the lowest Pi content and highest sucrose and anthocyanin levels. Artificially increasing endogenous sucrose through cold-girdling promoted anthocyanin biosynthesis, whereas reducing sucrose via leaf-shading inhibited it. Analysis revealed a significant positive correlation between sucrose and anthocyanin levels. In vitro incubation of leaves and sheaths with different sugars further confirmed that sucrose accumulation was indispensable for LP-induced anthocyanin biosynthesis. Therefore, the temporal and spatial patterns of anthocyanin biosynthesis under LP are determined by both tissue Pi levels and sucrose accumulation, and anthocyanin distribution can be modulated by altering Pi and sucrose patterns. Transcriptome analysis of LP-treated leaf sheaths, with or without sucrose accumulation, suggested that PHR1 may mediate the interaction between sugar and LP signaling pathways in regulating anthocyanin biosynthesis. These insights elucidate the mechanisms governing tissue-specific anthocyanin biosynthesis under LP conditions, while providing potential targets for improving phosphorus use efficiency via anthocyanin regulation.

Keywords:  low phosphorus       anthocyanin biosynthesis        spatiotemporal distribution        sucrose accumulation        maize seedlings  
Online: 21 October 2025  
Fund: 

This work was funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) – 328017493/GRK 2366 (Sino-German International Research Training Group AMAIZE-P), the Earmarked Fund for China Agriculture Research System (CARS; CARS-02-16), the 2115 Talent Development Program of China Agricultural University, the Talent Project of China Agricultural University for CARS, and the Key Unit Project of Academician Cooperation of Hebei Province.

About author:  #Correspondence Si Shen, E-mail, shensi@cau.edu.cn; Shun-Li Zhou, E-mail, zhoushl@cau.edu.cn

Cite this article: 

Zu-Dong Xiao, Wang Tang, Zhen-Yuan Chen, Yi-Hsuan Lin, Xiao-Gui Liang, Xin Wang, Shou-Bing Huang, Sebastian Munz, Simone Graeff-Hönninger, Si Shen, Shun-Li Zhou. 2025. Spatiotemporal sucrose accumulation drives tissue-specific anthocyanin biosynthesis under low phosphorus in maize. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.10.007

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