Sucrose metabolism and hormone interaction determine the fate of different florets within central spikelet of wheat

doi:10.1016/j.jia.2025.05.018

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Wan Sun^1,², Jie Ren¹, Xuechen Xiao¹, Wanqing Zhang¹, Haoran Li¹, Zhimin Wang¹, Zhigan Zhao¹, Zhencai Sun¹, Xubo Zhang³^#, Yinghua Zhang^1,⁴^#

¹ College of Agronomy and Biotechnology, China Agricultural University, Beijing 100193, China

² Department of Agricultural and Forest Sciences and Engineering, University of Lleida–AGROTECNIO-CERCA Center, Lleida 25198, Spain

³ Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China

⁴ Engineering Technology Research Center for Agriculture in Low Plain Areas, Hebei 061800, China

Highlights

Proximal floret (F1) developed earlier than distal floret (F5) within a spikelet.

IAA-starch synergy in F1 establishes a competitive metabolic sink, whereas ABA-T6P interplay in F5 enforces developmental arrest.

Tissue-specific regulation in fertile florets: lemmas supplied carbon by photosynthesis, anthers decomposed sucrose to synthesize starch, ovaries activated lipid biosynthesis for embryogenesis.

Abstract
References

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摘要

在小麦中部小穗中，靠近穗轴的小花原基通常发育为可育小花，而远离穗轴的小花原基通常会败育，但其内在的调控机制尚不明确。为阐明这一机制，本研究通过两年田间试验，从表型、生理、细胞和转录组学水平上解析了可育小花（F1）与败育小花（F5）的发育差异。研究结果表明：相比F5小花，F1小花发育较快，这与小花和花药细胞形态的时序性差异相吻合。这种差异与两类小花的代谢策略分化密切相关—F1通过提高光合效率、降低热耗散优先进行淀粉生物合成，而F5在资源限制下将碳流转向海藻糖代谢途径。同时，本研究通过转录分析共鉴定出17,711个差异基因，主要富集于碳水化合物代谢通路：F1中淀粉合成关键基因（WAXY, SS, GBE1）显著上调，而F5中海藻糖代谢基因（TPS.5, TPS.6, TPP.7）占主导，揭示了"生长-存活"代谢权衡机制。激素分析显示，F1通过上调编码TDC和YUCCA相关基因进而提升生长素（IAA）水平，F5则通过NCED介导脱落酸（ABA）积累。此外，研究还进一步揭示了可育小花的组织特异性调控机制：稃片通过富集光合基因实现局部碳源供给，花药依赖蔗糖裂解基因维持花粉发育，子房则激活脂质合成基因启动胚胎发生。综上所述，该研究提出中部小穗不同小花的发育调控模型：近轴小花通过IAA-淀粉协同作用建立竞争优势性代谢库，而远端小花通过ABA-T6P互作触发发育停滞，从而实现资源优化配置并促进其生殖成功，该调控框架为通过碳分配与激素信号改良小花育性提供了新视角。

Abstract

In the central spikelet, floret primordia proximal to rachis typically develop into fertile florets, while those distal ones tend to abort. However, the mechanism driving these divergent outcomes remain unclear. To elucidate this mechanism, a two-year field experiment was conducted, analyzing the differences between fertile (floret 1) and abortive florets (floret 5) at phenotypic, physiological, cellular, and transcriptional levels. Our results showed that floret 1 (F1) developed earlier than floret 5 (F5), evidenced as distinct floret and anther cell morphology. This developmental difference was associated with distinct metabolic strategies: F1 prioritizes starch biosynthesis by enhancing photosynthetic efficiency and reducing thermal dissipation, while F5 diverts carbon to trehalose metabolism under resource constraints. Transcriptomic profiling revealed 17,711 differentially expressed genes, predominantly enriched in carbohydrate metabolism. Key starch-related genes (WAXY, SS, GBE1) were upregulated in F1, while trehalose synthesis genes (TPS.5, TPS.6, TPP.7) dominated in F5, reflecting a metabolic trade-off between growth and survival. Hormonal profiling revealed elevated indole-3-acetic acid (IAA) levels in F1, driven by upregulated genes encoding enzymes of TDC and YUCCA, whereas abscisic acid (ABA) level increased in F5, mediated by NCED. Specially, tissue-specific regulation in fertile floret was clarified: lemma tissues enriched in photosynthesis genes supplied localized carbon, anthers relied on sucrose cleavage genes to sustain pollen development, and ovary activated lipid biosynthesis genes for embryogenesis. Collectively, we propose a model where IAA-starch synergy in proximal florets establishes a competitive metabolic sink, whereas ABA-T6P interplay in distal florets enforces developmental arrest, thereby optimizing resource allocation and reproductive success. The proposed regulatory framework provides novel views for improving floret fertility through carbohydrate partitioning and hormone signal.

Keywords: fertile floret abortive floret sucrose metabolism hormone

Online: 16 May 2025

Fund:

This research was supported by the Scientific and Technological Innovation Team Project of Seed Industry for Saline-alkali Tolerant Crop in Hebei Province, China (23327501D), the National Natural Science Foundation of China (32472227), the earmarked fund for China Agriculture Research System (CARS-3) and China Scholarship Council (CSC 202306350120).

About author: #Correspondence Xubo Zhang, E-mail: zhangxb@igsnrr.ac.cn; Yinghua Zhang, E-mail: zhangyh1216@126.com

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Wan Sun, Jie Ren, Xuechen Xiao, Wanqing Zhang, Haoran Li, Zhimin Wang, Zhigan Zhao, Zhencai Sun, Xubo Zhang, Yinghua Zhang. 2025. Sucrose metabolism and hormone interaction determine the fate of different florets within central spikelet of wheat. Journal of Integrative Agriculture, Doi:10.1016/j.jia.2025.05.018

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