Intraspecific chemical cues drive informed germination bet-hedging in an invasive plant

doi:10.1093/jpe/rtag111

J Plant Ecol ›› Advance articles DOI:10.1093/jpe/rtag111

Intraspecific chemical cues drive informed germination bet-hedging in an invasive plant

Hongyang Chen^1,2,3†, Shiyu Diao^1,2,3†, Tiantian Qin^1,2,3, Kaiyun Fu⁴, Hanyue Wang^1,2,3*, Shengtianzi Dong^1,2,3*

1 The College of Life Sciences, Shihezi University, 832003, China;
2 The Key Laboratory of Oasis Town and Mountain-basin System Ecology, Xinjiang Production and Construction Corps, 832003, China;
3 Ministry of Education Key Laboratory of Xinjiang Phytomedicine Resource Utilization, 832003, China;
4 Institute of Plant Protection, Xinjiang Academy of Agricultural Sciences, 830091, China
^†These authors contributed equally: Hongyang Chen, Shiyu Diao
^*Authors for correspondence: Shengtianzi Dong, Hanyue Wang
Address: No. 221, North 4th Road, Xiangyang Subdistrict, Shihezi City, Xinjiang Uyghur Autonomous Region, China.
Telephone Number: +8613677563285
Email: dongsheng97@126.com

Received:2026-01-16 Revised:2026-04-23 Accepted:2026-05-21 Published:2026-05-30
Supported by:
This work was supported by the Major Science and Technology Public Relations Project Fund of the Science and Technology Department of Xinjiang Uygur Autonomous Region (grant number 2023A02006).

种内化学信号驱动入侵植物知情种子萌发两头下注策略

Abstract

Abstract: Optimizing germination timing in unpredictable environments is critical for invasive annual plant populations to balance range expansion against intraspecific competition. However, the chemical mechanisms by which soil seed banks perceive population density and regulate dormancy accordingly remain poorly understood. Using the globally invasive Ambrosia trifida L. as a model, this study integrates concentration-response bioassays with combined metabolomic and transcriptomic analyses to elucidate the intraspecific chemical signaling pathways regulating seed germination. We identified four key secondary metabolites forming a functionally differentiated regulatory network (P < 0.01). Vanillin exhibits a biphasic concentration-response, promoting germination at low concentrations while inhibiting it at high levels. Umbelliferone acts as a linear germination inhibitor, whereas Trifolin serves as a linear promoter. Notably, Angelicin is exclusively seed-derived and functions as a concentration-dependent promoter, representing a seed bank-specific density signal. Integrated multi-omics analysis reveals that Angelicin upregulates ribosome biogenesis and hormone signaling while concurrently enriching nucleotide and lipid metabolism. This robust gene-metabolite co-regulation signifies a coordinated molecular reprogramming that primes seeds for rapid establishment, extending the signal's function beyond simple dormancy release. These findings provide evidence for a chemically mediated density-dependent regulatory system that integrates legacy signals from senesced vegetation with real-time cues from the seed bank, which may allow populations to dynamically modulate germination fractions in response to intraspecific density. This study offers a new perspective on bet-hedging strategies in invasive species and identifies candidate targets for management interventions based on disrupting intraspecific chemical communication.

Key words: Ambrosia trifida, bet-hedging, intraspecific chemical communication, plant invasion, seed germination

摘要：
在资源分布不可预测的环境中，优化萌发时机对于入侵性一年生植物种群在扩张分布范围与缓解种内竞争之间取得平衡至关重要。然而，土壤种子库感知种群密度并据此调控休眠的化学机制仍不清楚。本研究以全球性入侵植物三裂叶豚草（Ambrosia trifida L.）为模式物种，将浓度–响应生物测定与代谢组学、转录组学联合分析相结合，以阐明调控种子萌发的种内化学信号通路。研究鉴定出四种构成功能分化调控网络的关键次生代谢物（P < 0.01）。香草醛（Vanillin）表现出双相浓度–响应特征，在低浓度下促进萌发，而在高浓度下抑制萌发；伞形酮（Umbelliferone）作为线性萌发抑制剂，三叶豆苷（Trifolin）则作为线性促进剂。值得注意的是，异补骨脂素（Angelicin）完全由种子产生，作为浓度依赖型促进剂发挥作用，代表一种种子库特异的密度信号。多组学整合分析揭示，异补骨脂素在上调核糖体生物合成与激素信号转导的同时，也协同富集核苷酸代谢与脂质代谢通路。这种稳健的基因–代谢物协同调控体现出一种有序的分子重编程过程，可为种子的快速建植作好准备，使该信号的功能超越了单纯的休眠解除。上述发现为一种化学信号介导的密度依赖调控系统提供了证据——该系统整合了来自衰败植株的“历史信号”与来自种子库的“实时信号”，或可使植物种群响应种内密度对萌发比例进行动态调节。本研究为理解入侵物种的两头下注策略提供了新视角，并为基于干扰种内化学通讯的管理措施提出了候选靶点。

关键词: 三裂叶豚草, 两头下注策略, 种内化学通讯, 植物入侵, 种子萌发

Hongyang Chen, Shiyu Diao, Tiantian Qin, Kaiyun Fu, Hanyue Wang, Shengtianzi Dong. Intraspecific chemical cues drive informed germination bet-hedging in an invasive plant[J]. J Plant Ecol, DOI: 10.1093/jpe/rtag111.

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