Combined transcriptome and metabolome analysis of Polygonatum cyrtonema Hua in response to Botrytis deweyae infection

The fungal pathogen Botrytis deweyae, first identified as the causative agent of gray mold disease in China, has become a critical biotic constraint limiting the sustainable production of Polygonatum cyrtonema Hua in major cultivation regions. To investigate the physiological reactions and transcrip...

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Main Authors: Fuqiang Yin, Wanli Ma, Zhien Xiao, Yuxin Liu, Tiantian Guo, Yue Yuan, Shaotian Zhang, Guoli Li, Ming Liu
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-07-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2025.1617308/full
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author Fuqiang Yin
Wanli Ma
Wanli Ma
Zhien Xiao
Yuxin Liu
Tiantian Guo
Yue Yuan
Shaotian Zhang
Guoli Li
Ming Liu
author_facet Fuqiang Yin
Wanli Ma
Wanli Ma
Zhien Xiao
Yuxin Liu
Tiantian Guo
Yue Yuan
Shaotian Zhang
Guoli Li
Ming Liu
author_sort Fuqiang Yin
collection DOAJ
description The fungal pathogen Botrytis deweyae, first identified as the causative agent of gray mold disease in China, has become a critical biotic constraint limiting the sustainable production of Polygonatum cyrtonema Hua in major cultivation regions. To investigate the physiological reactions and transcriptome gene changes of P. cyrtonema after B. deweyae infection, in this study, we investigated the defense enzyme activity, transcriptome differential genes (DEGs), and differential metabolites (DAMs) of P. cyrtonema. When B. deweyae invaded the leaves of P. cyrtonema, the activities of phenylalanine deaminase (PAL), catalase (CAT), and peroxidase (POD) increased. The most responsive Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways in the transcriptome were plant-pathogen interaction, plant hormone signal transduction, the mitogen-activated protein kinase (MAPK) signaling pathway, and phenylpropanoid biosynthesis (phenylpropanoid biosynthesis) metabolic pathways. Among the DEGs, AP2 ERF-ERFs, WRKYs, and C2H2 were highly predictive of transcription factors (TFs), with WRKYs being important TFs in the P. cyrtonema MAPK pathway. In the metabolome, coumaric acid, α-linolenic acid, and jasmonic acid (JA) are important metabolites that respond to B. deweyae infection. Correlation analysis between the transcriptome and metabolome revealed that phenylpropanoid metabolism and α-linolenic acid metabolism pathways are associated with the most significant response of P. cyrtonema to B. deweyae infection, with phenylpyruvate being an important metabolite in the phenylpropanoid metabolic pathway. Additionally, the observed upregulation of α-linolenic acid and JA synthesis suggests potential activation of JA-dependent induced systemic resistance (ISR) against B. deweyae, possibly mediated through downstream MYC transcription factors. These findings indicate that JA signaling contributes significantly to P. cyrtonema defense response against fungal infection. Our findings provide foundational insights that may support the development of disease-resistant cultivars or biostimulant strategies for P. cyrtonema and related medicinal plants.
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spelling doaj-art-6587b1a8f50a4ecabe0b1cf76e3474172025-08-20T02:46:20ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2025-07-011610.3389/fpls.2025.16173081617308Combined transcriptome and metabolome analysis of Polygonatum cyrtonema Hua in response to Botrytis deweyae infectionFuqiang Yin0Wanli Ma1Wanli Ma2Zhien Xiao3Yuxin Liu4Tiantian Guo5Yue Yuan6Shaotian Zhang7Guoli Li8Ming Liu9College of Biological and Food Engineering, Chongqing Three Gorges University, Chongqing, ChinaCollege of Biological and Food Engineering, Chongqing Three Gorges University, Chongqing, ChinaGuangdong Provincial Key Laboratory of Plant Molecular Breeding, South China Agricultural University, Guangzhou, ChinaCollege of Biological and Food Engineering, Chongqing Three Gorges University, Chongqing, ChinaCollege of Biological and Food Engineering, Chongqing Three Gorges University, Chongqing, ChinaCollege of Biological and Food Engineering, Chongqing Three Gorges University, Chongqing, ChinaCollege of Biological and Food Engineering, Chongqing Three Gorges University, Chongqing, ChinaCollege of Biological and Food Engineering, Chongqing Three Gorges University, Chongqing, ChinaDepartment of Basic Medical Sciences, Chongqing Three Gorges Medical College, Chongqing, ChinaCollege of Biological and Food Engineering, Chongqing Three Gorges University, Chongqing, ChinaThe fungal pathogen Botrytis deweyae, first identified as the causative agent of gray mold disease in China, has become a critical biotic constraint limiting the sustainable production of Polygonatum cyrtonema Hua in major cultivation regions. To investigate the physiological reactions and transcriptome gene changes of P. cyrtonema after B. deweyae infection, in this study, we investigated the defense enzyme activity, transcriptome differential genes (DEGs), and differential metabolites (DAMs) of P. cyrtonema. When B. deweyae invaded the leaves of P. cyrtonema, the activities of phenylalanine deaminase (PAL), catalase (CAT), and peroxidase (POD) increased. The most responsive Kyoto Encyclopedia of Genes and Genomes (KEGG) pathways in the transcriptome were plant-pathogen interaction, plant hormone signal transduction, the mitogen-activated protein kinase (MAPK) signaling pathway, and phenylpropanoid biosynthesis (phenylpropanoid biosynthesis) metabolic pathways. Among the DEGs, AP2 ERF-ERFs, WRKYs, and C2H2 were highly predictive of transcription factors (TFs), with WRKYs being important TFs in the P. cyrtonema MAPK pathway. In the metabolome, coumaric acid, α-linolenic acid, and jasmonic acid (JA) are important metabolites that respond to B. deweyae infection. Correlation analysis between the transcriptome and metabolome revealed that phenylpropanoid metabolism and α-linolenic acid metabolism pathways are associated with the most significant response of P. cyrtonema to B. deweyae infection, with phenylpyruvate being an important metabolite in the phenylpropanoid metabolic pathway. Additionally, the observed upregulation of α-linolenic acid and JA synthesis suggests potential activation of JA-dependent induced systemic resistance (ISR) against B. deweyae, possibly mediated through downstream MYC transcription factors. These findings indicate that JA signaling contributes significantly to P. cyrtonema defense response against fungal infection. Our findings provide foundational insights that may support the development of disease-resistant cultivars or biostimulant strategies for P. cyrtonema and related medicinal plants.https://www.frontiersin.org/articles/10.3389/fpls.2025.1617308/fullBotrytis deweyaemetabolometranscriptomedisease resistancePolygonatum cyrtonema Hua
spellingShingle Fuqiang Yin
Wanli Ma
Wanli Ma
Zhien Xiao
Yuxin Liu
Tiantian Guo
Yue Yuan
Shaotian Zhang
Guoli Li
Ming Liu
Combined transcriptome and metabolome analysis of Polygonatum cyrtonema Hua in response to Botrytis deweyae infection
Frontiers in Plant Science
Botrytis deweyae
metabolome
transcriptome
disease resistance
Polygonatum cyrtonema Hua
title Combined transcriptome and metabolome analysis of Polygonatum cyrtonema Hua in response to Botrytis deweyae infection
title_full Combined transcriptome and metabolome analysis of Polygonatum cyrtonema Hua in response to Botrytis deweyae infection
title_fullStr Combined transcriptome and metabolome analysis of Polygonatum cyrtonema Hua in response to Botrytis deweyae infection
title_full_unstemmed Combined transcriptome and metabolome analysis of Polygonatum cyrtonema Hua in response to Botrytis deweyae infection
title_short Combined transcriptome and metabolome analysis of Polygonatum cyrtonema Hua in response to Botrytis deweyae infection
title_sort combined transcriptome and metabolome analysis of polygonatum cyrtonema hua in response to botrytis deweyae infection
topic Botrytis deweyae
metabolome
transcriptome
disease resistance
Polygonatum cyrtonema Hua
url https://www.frontiersin.org/articles/10.3389/fpls.2025.1617308/full
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