Artemisia argyi allelopathy: a generalist compromises hormone balance, element absorption, and photosynthesis of receptor plants

Abstract Background Allelopathy is expressed through the release of plant chemicals and is considered a natural alternative for sustainable weed management. Artemisia argyi (A. argyi) is widely distributed throughout Asia, and often dominates fields due to its strong allelopathy. However, the mechan...

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Main Authors: Jinxin Li, Tingting Zhao, Le Chen, Hong Chen, Dandan Luo, Changjie Chen, Yuhuan Miao, Dahui Liu
Format: Article
Language:English
Published: BMC 2022-07-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-022-03757-9
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author Jinxin Li
Tingting Zhao
Le Chen
Hong Chen
Dandan Luo
Changjie Chen
Yuhuan Miao
Dahui Liu
author_facet Jinxin Li
Tingting Zhao
Le Chen
Hong Chen
Dandan Luo
Changjie Chen
Yuhuan Miao
Dahui Liu
author_sort Jinxin Li
collection DOAJ
description Abstract Background Allelopathy is expressed through the release of plant chemicals and is considered a natural alternative for sustainable weed management. Artemisia argyi (A. argyi) is widely distributed throughout Asia, and often dominates fields due to its strong allelopathy. However, the mechanism of A. argyi allelopathy is largely unknown and need to be elucidated at the physiological and molecular levels. Results In this study, we used electron microscopy, ionomics analysis, phytohormone profiling, and transcriptome analysis to investigate the physiological and molecular mechanisms of A. argyi allelopathy using the model plant rice (Oryza sativa) as receptor plants. A. argyi water extract (AAWE)-treated rice plants grow poorly and display root morphological anomalies and leaf yellowing. We found that AAWE significantly inhibits rice growth by destroying the root and leaf system in multiple ways, including the integrity of ultrastructure, reactive oxygen species (ROS) homeostasis, and the accumulation of soluble sugar and chlorophyll synthesis. Further detection of the hormone contents suggests that AAWE leads to indole-3-acetic acid (IAA) accumulation in roots. Moreover, ionomics analysis shows that AAWE inhibits the absorption and transportation of photosynthesis-essential mineral elements, especially Mg, Fe, and Mn. In addition, the results of transcriptome analysis revealed that AAWE affects a series of crucial primary metabolic processes comprising photosynthesis in rice plants. Conclusions This study indicates that A. argyi realizes its strongly allelopathy through comprehensive effects on recipient plants including large-scale IAA synthesis and accumulation, ROS explosion, damaging the membrane system and organelles, and obstructing ion absorption and transport, photosynthesis and other pivotal primary metabolic processes of plants. Therefore, AAWE could potentially be developed as an environmentally friendly botanical herbicide due to its strong allelopathic effects.
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spelling doaj.art-058771f7dca44f479a0712bb42bcd6f22022-12-22T03:40:55ZengBMCBMC Plant Biology1471-22292022-07-0122111710.1186/s12870-022-03757-9Artemisia argyi allelopathy: a generalist compromises hormone balance, element absorption, and photosynthesis of receptor plantsJinxin Li0Tingting Zhao1Le Chen2Hong Chen3Dandan Luo4Changjie Chen5Yuhuan Miao6Dahui Liu7Key Laboratory of Traditional Chinese Medicine Resources and Chemistry of Hubei Province, Hubei University of Chinese MedicineKey Laboratory of Traditional Chinese Medicine Resources and Chemistry of Hubei Province, Hubei University of Chinese MedicineKey Laboratory of Traditional Chinese Medicine Resources and Chemistry of Hubei Province, Hubei University of Chinese MedicineKey Laboratory of Traditional Chinese Medicine Resources and Chemistry of Hubei Province, Hubei University of Chinese MedicineKey Laboratory of Traditional Chinese Medicine Resources and Chemistry of Hubei Province, Hubei University of Chinese MedicineKey Laboratory of Traditional Chinese Medicine Resources and Chemistry of Hubei Province, Hubei University of Chinese MedicineKey Laboratory of Traditional Chinese Medicine Resources and Chemistry of Hubei Province, Hubei University of Chinese MedicineKey Laboratory of Traditional Chinese Medicine Resources and Chemistry of Hubei Province, Hubei University of Chinese MedicineAbstract Background Allelopathy is expressed through the release of plant chemicals and is considered a natural alternative for sustainable weed management. Artemisia argyi (A. argyi) is widely distributed throughout Asia, and often dominates fields due to its strong allelopathy. However, the mechanism of A. argyi allelopathy is largely unknown and need to be elucidated at the physiological and molecular levels. Results In this study, we used electron microscopy, ionomics analysis, phytohormone profiling, and transcriptome analysis to investigate the physiological and molecular mechanisms of A. argyi allelopathy using the model plant rice (Oryza sativa) as receptor plants. A. argyi water extract (AAWE)-treated rice plants grow poorly and display root morphological anomalies and leaf yellowing. We found that AAWE significantly inhibits rice growth by destroying the root and leaf system in multiple ways, including the integrity of ultrastructure, reactive oxygen species (ROS) homeostasis, and the accumulation of soluble sugar and chlorophyll synthesis. Further detection of the hormone contents suggests that AAWE leads to indole-3-acetic acid (IAA) accumulation in roots. Moreover, ionomics analysis shows that AAWE inhibits the absorption and transportation of photosynthesis-essential mineral elements, especially Mg, Fe, and Mn. In addition, the results of transcriptome analysis revealed that AAWE affects a series of crucial primary metabolic processes comprising photosynthesis in rice plants. Conclusions This study indicates that A. argyi realizes its strongly allelopathy through comprehensive effects on recipient plants including large-scale IAA synthesis and accumulation, ROS explosion, damaging the membrane system and organelles, and obstructing ion absorption and transport, photosynthesis and other pivotal primary metabolic processes of plants. Therefore, AAWE could potentially be developed as an environmentally friendly botanical herbicide due to its strong allelopathic effects.https://doi.org/10.1186/s12870-022-03757-9AllelopathyArtemisia argyiBotanical herbicidePhotosynthesisPhytohormoneSubmicroscopic structure
spellingShingle Jinxin Li
Tingting Zhao
Le Chen
Hong Chen
Dandan Luo
Changjie Chen
Yuhuan Miao
Dahui Liu
Artemisia argyi allelopathy: a generalist compromises hormone balance, element absorption, and photosynthesis of receptor plants
BMC Plant Biology
Allelopathy
Artemisia argyi
Botanical herbicide
Photosynthesis
Phytohormone
Submicroscopic structure
title Artemisia argyi allelopathy: a generalist compromises hormone balance, element absorption, and photosynthesis of receptor plants
title_full Artemisia argyi allelopathy: a generalist compromises hormone balance, element absorption, and photosynthesis of receptor plants
title_fullStr Artemisia argyi allelopathy: a generalist compromises hormone balance, element absorption, and photosynthesis of receptor plants
title_full_unstemmed Artemisia argyi allelopathy: a generalist compromises hormone balance, element absorption, and photosynthesis of receptor plants
title_short Artemisia argyi allelopathy: a generalist compromises hormone balance, element absorption, and photosynthesis of receptor plants
title_sort artemisia argyi allelopathy a generalist compromises hormone balance element absorption and photosynthesis of receptor plants
topic Allelopathy
Artemisia argyi
Botanical herbicide
Photosynthesis
Phytohormone
Submicroscopic structure
url https://doi.org/10.1186/s12870-022-03757-9
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