Loss of flavonoids homeostasis leads to pistillody in sua-CMS of Nicotiana tabacum

Abstract The homeotic transformation of stamens into pistil-like structures (pistillody) causes cytoplasmic male sterility (CMS). This phenomenon is widely present in plants, and might be induced by intracellular communication (mitochondrial retrograde signaling), but its systemic regulating mechani...

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Main Authors: Jie Xu, Zhuo Wei, Jugou Liao, Keliang Tao, Junpeng Zhang, Yu Jiang, Yongzhi Niu, Yunye Zheng, Limeng Zhang, Xuemei Wei
Format: Article
Language:English
Published: BMC 2025-01-01
Series:BMC Plant Biology
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Online Access:https://doi.org/10.1186/s12870-025-06122-8
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author Jie Xu
Zhuo Wei
Jugou Liao
Keliang Tao
Junpeng Zhang
Yu Jiang
Yongzhi Niu
Yunye Zheng
Limeng Zhang
Xuemei Wei
author_facet Jie Xu
Zhuo Wei
Jugou Liao
Keliang Tao
Junpeng Zhang
Yu Jiang
Yongzhi Niu
Yunye Zheng
Limeng Zhang
Xuemei Wei
author_sort Jie Xu
collection DOAJ
description Abstract The homeotic transformation of stamens into pistil-like structures (pistillody) causes cytoplasmic male sterility (CMS). This phenomenon is widely present in plants, and might be induced by intracellular communication (mitochondrial retrograde signaling), but its systemic regulating mechanism is still unclear. In this study, morphological observation showed that the stamens transformed into pistil-like structures, leading to flat and dehiscent pistils, and fruit set decrease in sua-CMS (MS K326, somatic fusion between Nicotiana. tabacum L. K326 and Nicotiana suaveolens). Transcriptome data analysis presented that the expression levels of B-class MADS genes, including pMADS1, GLO1, GLO2, pMADS2.1, pMADS2.2, significantly reduced in the pistil-like structure of sua-CMS. DEGs were enriched in flavonoid and phenylpropanoid biosynthesis pathways. Transcriptome and metabolomics analysis revealed that the expression levels of CHI/CHS (key enzymes regulating flavonoid synthesis), and the contents of flavonoids reduced significantly in the pistil-like structures of sua-CMS. Chemical fluorescence staining assay showed that reactive oxygen species (ROS) levels were higher in the pistil-like structure of sua-CMS. Application of external flavonoids (hesperetin) reduced the frequency of pistillody and ROS levels. These results suggested that the metabolism of flavonoids played important roles in regulating pistillody through ROS in sua-CMS. Our study provides new insights into the regulatory mechanism of pistillody in plants.
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series BMC Plant Biology
spelling doaj-art-bd0b402df6414edbb5b89b518c79cbea2025-01-26T12:23:24ZengBMCBMC Plant Biology1471-22292025-01-0125111310.1186/s12870-025-06122-8Loss of flavonoids homeostasis leads to pistillody in sua-CMS of Nicotiana tabacumJie Xu0Zhuo Wei1Jugou Liao2Keliang Tao3Junpeng Zhang4Yu Jiang5Yongzhi Niu6Yunye Zheng7Limeng Zhang8Xuemei Wei9Yuxi Zhongyan Tobacco Seed CO., LtdSchool of Ecology and Environmental Sciences, Biocontrol Engineering Research Center of Crop Diseases & Pests, Ministry of Education Key Laboratory for Transboundary Ecosecurity of Southwest China, Yunnan UniversitySchool of Ecology and Environmental Sciences, Biocontrol Engineering Research Center of Crop Diseases & Pests, Ministry of Education Key Laboratory for Transboundary Ecosecurity of Southwest China, Yunnan UniversitySchool of Ecology and Environmental Sciences, Biocontrol Engineering Research Center of Crop Diseases & Pests, Ministry of Education Key Laboratory for Transboundary Ecosecurity of Southwest China, Yunnan UniversitySchool of Engineering, Dali UniversitySchool of Engineering, Dali UniversityYuxi Zhongyan Tobacco Seed CO., LtdYuxi Zhongyan Tobacco Seed CO., LtdYuxi Zhongyan Tobacco Seed CO., LtdSchool of Engineering, Dali UniversityAbstract The homeotic transformation of stamens into pistil-like structures (pistillody) causes cytoplasmic male sterility (CMS). This phenomenon is widely present in plants, and might be induced by intracellular communication (mitochondrial retrograde signaling), but its systemic regulating mechanism is still unclear. In this study, morphological observation showed that the stamens transformed into pistil-like structures, leading to flat and dehiscent pistils, and fruit set decrease in sua-CMS (MS K326, somatic fusion between Nicotiana. tabacum L. K326 and Nicotiana suaveolens). Transcriptome data analysis presented that the expression levels of B-class MADS genes, including pMADS1, GLO1, GLO2, pMADS2.1, pMADS2.2, significantly reduced in the pistil-like structure of sua-CMS. DEGs were enriched in flavonoid and phenylpropanoid biosynthesis pathways. Transcriptome and metabolomics analysis revealed that the expression levels of CHI/CHS (key enzymes regulating flavonoid synthesis), and the contents of flavonoids reduced significantly in the pistil-like structures of sua-CMS. Chemical fluorescence staining assay showed that reactive oxygen species (ROS) levels were higher in the pistil-like structure of sua-CMS. Application of external flavonoids (hesperetin) reduced the frequency of pistillody and ROS levels. These results suggested that the metabolism of flavonoids played important roles in regulating pistillody through ROS in sua-CMS. Our study provides new insights into the regulatory mechanism of pistillody in plants.https://doi.org/10.1186/s12870-025-06122-8Nicotiana tabacumPistillodyB-class MADSFlavonoidsROS
spellingShingle Jie Xu
Zhuo Wei
Jugou Liao
Keliang Tao
Junpeng Zhang
Yu Jiang
Yongzhi Niu
Yunye Zheng
Limeng Zhang
Xuemei Wei
Loss of flavonoids homeostasis leads to pistillody in sua-CMS of Nicotiana tabacum
BMC Plant Biology
Nicotiana tabacum
Pistillody
B-class MADS
Flavonoids
ROS
title Loss of flavonoids homeostasis leads to pistillody in sua-CMS of Nicotiana tabacum
title_full Loss of flavonoids homeostasis leads to pistillody in sua-CMS of Nicotiana tabacum
title_fullStr Loss of flavonoids homeostasis leads to pistillody in sua-CMS of Nicotiana tabacum
title_full_unstemmed Loss of flavonoids homeostasis leads to pistillody in sua-CMS of Nicotiana tabacum
title_short Loss of flavonoids homeostasis leads to pistillody in sua-CMS of Nicotiana tabacum
title_sort loss of flavonoids homeostasis leads to pistillody in sua cms of nicotiana tabacum
topic Nicotiana tabacum
Pistillody
B-class MADS
Flavonoids
ROS
url https://doi.org/10.1186/s12870-025-06122-8
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