Eucommia ulmoides male flower as a remarkable edible floral resource exerts lifespan/healthspan-promoting effects on Caenorhabditis elegans

Qi Chen; Xuan Yang; Esra Capanoglu; Amel Thanina Amrouche; Lipeng Wu; Jingyang Luo; Yuhang Zhu; Yixuan Wang; Xiongtao Jiang; Dayong Zhang; Baiyi Lu

doi:10.1039/d2fo03006c

Eucommia ulmoides male flower as a remarkable edible floral resource exerts lifespan/healthspan-promoting effects on Caenorhabditis elegans

Qi Chen, Xuan Yang, Esra Capanoglu, Amel Thanina Amrouche, Lipeng Wu, Jingyang Luo, Yuhang Zhu, Yixuan Wang, Xiongtao Jiang, Dayong Zhang, Baiyi Lu^*

^*Corresponding author for this work

Department of Food Engineering

Research output: Contribution to journal › Article › peer-review

9 Citations (Scopus)

Abstract

Natural products, especially phytochemicals, can effectively improve the health of various model organisms and ultimately prolong their lifespan. As an emerging resource of plant-based food, edible flowers have potential anti-aging effects. Here, we showed that twelve out of 30 drug-food homologous flowers’ extracts significantly extended the lifespan of C. elegans, and the Eucommia ulmoides male flower was screened out by comparing centrally. The lifespan of C. elegans increased by 18.61% under the treatment of 100 μg mL⁻¹ floral extract (EUFE). Interestingly, this effect was attenuated when EUFE was administered late or at higher concentrations. Significantly, EUFE improved health indicators that decline with aging including pharyngeal pumping, mobility, muscle morphology, and lipofuscin accumulation. EUFE also enhanced the resistance of C. elegans to oxidative/heat stress. The longevity-extending effect of EUFE was dependent on transcription factor DAF-16 and mitochondrial function. Moreover, EUFE triggered the nuclear translocation of DAF-16 and promoted downstream LGG-1 and SOD3 protein expression. In body-wall muscles, EUFE stimulated mitochondrial fission and mitophagy to mitigate age-related mitochondrial impairments. The transcriptional checkpoints of daf-16, drp-1, eat-3, lgg-1, and dct-1 further showed that EUFE regulated DAF-16 signaling and mitochondrial homeostasis. Finally, the interpretation of the EUFE components by correlation analysis, UHPLC-QE-MS, and verification experiments showed that aucubin, geniposide, and asperuloside are the main active compounds. We revealed the excellent lifespan/healthspan-promoting efficacy of EUFE and highlighted that edible flowers are worthy of further investigation as anti-aging dietary resources. Meanwhile, related mechanisms enriched the hypothesis that mitochondria might be involved in the healthspan modulation of longevity pathways.

Original language	English
Pages (from-to)	457-470
Number of pages	14
Journal	Food and Function
Volume	14
Issue number	1
DOIs	https://doi.org/10.1039/d2fo03006c
Publication status	Published - 7 Dec 2022

Bibliographical note

Publisher Copyright:
© 2023 The Royal Society of Chemistry.

Funding

The authors greatly thank Prof. Tavernarakis at the University of Crete for providing the nematode strains. We are also grateful to SunyBiotech (Fujian, China) and Angela Pasparaki (the technician in Prof. Tavernarakis's Lab) for their timely communication and assistance in nematode mailing, culture, etc. We also thank the Caenorhabditis Genetics Center (University of Minnesota, USA). This work was supported by the Zhejiang Provincial Basic Public Welfare Research [LGN20C200010], the Fundamental Research Funds for the Provincial Universities, Zhejiang Institute of Economics and Trade [19SBYB07], the Zhejiang Provincial Major R & D Program [2019C02070].

Funders	Funder number
Angela Pasparaki
Fundamental Research Funds for the Provincial Universities
Zhejiang Institute of Economics and Trade	19SBYB07
Zhejiang Provincial Major R & D Program	2019C02070
University of Minnesota
Basic Public Welfare Research Program of Zhejiang Province	LGN20C200010

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title = "Eucommia ulmoides male flower as a remarkable edible floral resource exerts lifespan/healthspan-promoting effects on Caenorhabditis elegans",

abstract = "Natural products, especially phytochemicals, can effectively improve the health of various model organisms and ultimately prolong their lifespan. As an emerging resource of plant-based food, edible flowers have potential anti-aging effects. Here, we showed that twelve out of 30 drug-food homologous flowers{\textquoteright} extracts significantly extended the lifespan of C. elegans, and the Eucommia ulmoides male flower was screened out by comparing centrally. The lifespan of C. elegans increased by 18.61% under the treatment of 100 μg mL−1 floral extract (EUFE). Interestingly, this effect was attenuated when EUFE was administered late or at higher concentrations. Significantly, EUFE improved health indicators that decline with aging including pharyngeal pumping, mobility, muscle morphology, and lipofuscin accumulation. EUFE also enhanced the resistance of C. elegans to oxidative/heat stress. The longevity-extending effect of EUFE was dependent on transcription factor DAF-16 and mitochondrial function. Moreover, EUFE triggered the nuclear translocation of DAF-16 and promoted downstream LGG-1 and SOD3 protein expression. In body-wall muscles, EUFE stimulated mitochondrial fission and mitophagy to mitigate age-related mitochondrial impairments. The transcriptional checkpoints of daf-16, drp-1, eat-3, lgg-1, and dct-1 further showed that EUFE regulated DAF-16 signaling and mitochondrial homeostasis. Finally, the interpretation of the EUFE components by correlation analysis, UHPLC-QE-MS, and verification experiments showed that aucubin, geniposide, and asperuloside are the main active compounds. We revealed the excellent lifespan/healthspan-promoting efficacy of EUFE and highlighted that edible flowers are worthy of further investigation as anti-aging dietary resources. Meanwhile, related mechanisms enriched the hypothesis that mitochondria might be involved in the healthspan modulation of longevity pathways.",

author = "Qi Chen and Xuan Yang and Esra Capanoglu and Amrouche, {Amel Thanina} and Lipeng Wu and Jingyang Luo and Yuhang Zhu and Yixuan Wang and Xiongtao Jiang and Dayong Zhang and Baiyi Lu",

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doi = "10.1039/d2fo03006c",

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AU - Chen, Qi

AU - Yang, Xuan

AU - Capanoglu, Esra

AU - Amrouche, Amel Thanina

AU - Wu, Lipeng

AU - Luo, Jingyang

AU - Zhu, Yuhang

AU - Wang, Yixuan

AU - Jiang, Xiongtao

AU - Zhang, Dayong

AU - Lu, Baiyi

PY - 2022/12/7

Y1 - 2022/12/7

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AB - Natural products, especially phytochemicals, can effectively improve the health of various model organisms and ultimately prolong their lifespan. As an emerging resource of plant-based food, edible flowers have potential anti-aging effects. Here, we showed that twelve out of 30 drug-food homologous flowers’ extracts significantly extended the lifespan of C. elegans, and the Eucommia ulmoides male flower was screened out by comparing centrally. The lifespan of C. elegans increased by 18.61% under the treatment of 100 μg mL−1 floral extract (EUFE). Interestingly, this effect was attenuated when EUFE was administered late or at higher concentrations. Significantly, EUFE improved health indicators that decline with aging including pharyngeal pumping, mobility, muscle morphology, and lipofuscin accumulation. EUFE also enhanced the resistance of C. elegans to oxidative/heat stress. The longevity-extending effect of EUFE was dependent on transcription factor DAF-16 and mitochondrial function. Moreover, EUFE triggered the nuclear translocation of DAF-16 and promoted downstream LGG-1 and SOD3 protein expression. In body-wall muscles, EUFE stimulated mitochondrial fission and mitophagy to mitigate age-related mitochondrial impairments. The transcriptional checkpoints of daf-16, drp-1, eat-3, lgg-1, and dct-1 further showed that EUFE regulated DAF-16 signaling and mitochondrial homeostasis. Finally, the interpretation of the EUFE components by correlation analysis, UHPLC-QE-MS, and verification experiments showed that aucubin, geniposide, and asperuloside are the main active compounds. We revealed the excellent lifespan/healthspan-promoting efficacy of EUFE and highlighted that edible flowers are worthy of further investigation as anti-aging dietary resources. Meanwhile, related mechanisms enriched the hypothesis that mitochondria might be involved in the healthspan modulation of longevity pathways.

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SN - 2042-6496

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ER -

Eucommia ulmoides male flower as a remarkable edible floral resource exerts lifespan/healthspan-promoting effects on Caenorhabditis elegans

Abstract

Bibliographical note

Funding

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