J Integr Plant Biol ›› 2024, Vol. 66 ›› Issue (11): 2490-2504.DOI: 10.1111/jipb.13764  cstr: 32098.14.jipb.13764

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  • 收稿日期:2024-01-25 接受日期:2024-07-29 出版日期:2024-11-01 发布日期:2024-11-25

Anchorene, a carotenoid-derived growth regulator, modulates auxin homeostasis by suppressing GH3-mediated auxin conjugation

Danping Ke1,2†, Yinpeng Xie3,4†, Haipeng Li1,2†, Liqun Hu1, Yi He1, Chao Guo1, Yahui Zhai1, Jinggong Guo1,2, Kun Li1,2, Zongyan Chu2, Junli Zhang1, Xuebin Zhang1, Salim Al‐Babili5,6, Kai Jiang7*, Yuchen Miao1,2* and Kun‐Peng Jia1,2*   

  1. 1. National Key Laboratory of Cotton Bio‐breeding and Integrated Utilization, State Key Laboratory of Crop Stress Adaptation and Improvement, Henan Joint International Laboratory for Crop Multi‐Omics Research, School of Life Sciences, Henan University, Kaifeng 450046, China
    2. Sanya Institute of Henan University, Sanya 572025, China
    3. State Key Laboratory for Crop Stress Resistance and High‐Eficiency Production/Shaanxi Key Laboratory of Apple, College of Horticulture, Northwest A&F University, Yangling 712100, China
    4. Institute of Plant and Food Science, Department of Biology, School of Life Sciences, Southern University of Science and Technology (SUSTech), Shenzhen 518055, China
    5. The BioActives Lab, Center for Desert Agriculture, King Abdullah University of Science and Technology, Thuwal 23955‐6900, Kingdom of Saudi Arabia
    6. Plant Science Program, Biological and Environmental Science and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST), Thuwal 23955‐6900, Kingdom of Saudi Arabia
    7. Laboratory of Cell Metabolism and Diseases, State Key Laboratory of Conservation and Utilization of Bio‐Resources in Yunnan, Center for Life Sciences, School of Life Sciences, Yunnan University, Kunming 650500, China
    †These authors contribute equally to this work.
    *Correspondences: Yuchen Miao (miaoych@henu.edu.cn); Kai Jiang (jiangk@ynu.edu.cn); Kun‐Peng Jia (kunpengjia_0515@126.com; Dr. Jia is fully responsible for the distribution of all materials associated with this article in the manuscript).
  • Received:2024-01-25 Accepted:2024-07-29 Online:2024-11-01 Published:2024-11-25
  • Supported by:
    This work was supported by the National Natural Science Foundation of China (32170271), by the Natural Science Foundation of Henan Province (222300420024) and the Project of Sanya Yazhou Bay Science and Technology City (SCKJ‐JYRC‐2022‐19).

Abstract: Anchorene, identified as an endogenous bioactive carotenoid-derived dialdehyde and diapocarotenoid, affects root development by modulating auxin homeostasis. However, the precise interaction between anchorene and auxin, as well as the mechanisms by which anchorene modulates auxin levels, remain largely elusive. In this study, we conducted a comparative analysis of anchorene's bioactivities alongside auxin and observed that anchorene induces multifaceted auxin-like effects. Through genetic and pharmacological examinations, we revealed that anchorene's auxin-like activities depend on the indole-3-pyruvate-dependent auxin biosynthesis pathway, as well as the auxin inactivation pathway mediated by Group II Gretchen Hagen 3 (GH3) proteins that mainly facilitate the conjugation of indole-3-acetic acid (IAA) to amino acids, leading to the formation of inactivated storage forms. Our measurements indicated that anchorene treatment elevates IAA levels while reducing the quantities of inactivated IAA–amino acid conjugates and oxIAA. RNA sequencing further revealed that anchorene triggers the expression of numerous auxin-responsive genes in a manner reliant on Group II GH3s. Additionally, our in vitro enzymatic assays and biolayer interferometry (BLI) assay demonstrated anchorene's robust suppression of GH3.17-mediated IAA conjugation with glutamate. Collectively, our findings highlight the significant role of carotenoid-derived metabolite anchorene in modulating auxin homeostasis, primarily through the repression of GH3-mediated IAA conjugation and inactivation pathways, offering novel insights into the regulatory mechanisms of plant bioactive apocarotenoids.

Key words: Anchorene, auxin conjugation, carotenoid‐derived bioactive apocarotenoid, Gretchen Hagen 3, root development

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