Integrated Transcriptome and Metabolome Analysis Reveals the Molecular Mechanism of Rust Resistance in Resistant (Youkang) and Susceptive (Tengjiao) <i>Zanthoxylum armatum</i> Cultivars

Chinese pepper rust is a live parasitic fungal disease caused by <i>Coleosporium zanthoxyli</i>, which seriously affects the cultivation and industrial development of <i>Z. armatum</i>. Cultivating and planting resistant cultivars is considered the most economical and environ...

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Main Authors: Shan Han, Xiu Xu, Huan Yuan, Shujiang Li, Tiantian Lin, Yinggao Liu, Shuying Li, Tianhui Zhu
Format: Article
Language:English
Published: MDPI AG 2023-09-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/24/19/14761
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author Shan Han
Xiu Xu
Huan Yuan
Shujiang Li
Tiantian Lin
Yinggao Liu
Shuying Li
Tianhui Zhu
author_facet Shan Han
Xiu Xu
Huan Yuan
Shujiang Li
Tiantian Lin
Yinggao Liu
Shuying Li
Tianhui Zhu
author_sort Shan Han
collection DOAJ
description Chinese pepper rust is a live parasitic fungal disease caused by <i>Coleosporium zanthoxyli</i>, which seriously affects the cultivation and industrial development of <i>Z. armatum</i>. Cultivating and planting resistant cultivars is considered the most economical and environmentally friendly strategy to control this disease. Therefore, the mining of excellent genes for rust resistance and the analysis of the mechanism of rust resistance are the key strategies to achieve the targeted breeding of rust resistance. However, there is no relevant report on pepper rust resistance at present. The aim of the present study was to further explore the resistance mechanism of pepper by screening the rust-resistant germplasm resources in the early stage. Combined with the analysis of plant pathology, transcriptomics, and metabolomics, we found that compared with susceptible cultivar TJ, resistant cultivar YK had 2752 differentially expressed genes (DEGs, 1253 up-, and 1499 downregulated) and 321 differentially accumulated metabolites (DAMs, 133 up- and 188 down-accumulated) after pathogen infection. And the genes and metabolites related to phenylpropanoid metabolism were highly enriched in resistant varieties, which indicated that phenylpropanoid metabolism might mediate the resistance of <i>Z. armatum</i>. This finding was further confirmed by a real-time quantitative polymerase chain reaction analysis, which revealed that the expression levels of core genes involved in phenylpropane metabolism in disease-resistant varieties were high. In addition, the difference in flavonoid and MeJA contents in the leaves between resistant and susceptible varieties further supported the conclusion that the flavonoid pathway and methyl jasmonate may be involved in the formation of Chinese pepper resistance. Our research results not only help to better understand the resistance mechanism of <i>Z. armatum</i> rust but also contribute to the breeding and utilization of resistant varieties.
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spelling doaj.art-0da285c7c0e34a7bab63c8ae2dfcb5162023-11-30T20:46:59ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-09-0124191476110.3390/ijms241914761Integrated Transcriptome and Metabolome Analysis Reveals the Molecular Mechanism of Rust Resistance in Resistant (Youkang) and Susceptive (Tengjiao) <i>Zanthoxylum armatum</i> CultivarsShan Han0Xiu Xu1Huan Yuan2Shujiang Li3Tiantian Lin4Yinggao Liu5Shuying Li6Tianhui Zhu7College of Forestry, Sichuan Agricultural University, Chengdu 611130, ChinaCollege of Forestry, Sichuan Agricultural University, Chengdu 611130, ChinaCollege of Forestry, Sichuan Agricultural University, Chengdu 611130, ChinaCollege of Forestry, Sichuan Agricultural University, Chengdu 611130, ChinaCollege of Forestry, Sichuan Agricultural University, Chengdu 611130, ChinaCollege of Forestry, Sichuan Agricultural University, Chengdu 611130, ChinaCollege of Forestry, Sichuan Agricultural University, Chengdu 611130, ChinaCollege of Forestry, Sichuan Agricultural University, Chengdu 611130, ChinaChinese pepper rust is a live parasitic fungal disease caused by <i>Coleosporium zanthoxyli</i>, which seriously affects the cultivation and industrial development of <i>Z. armatum</i>. Cultivating and planting resistant cultivars is considered the most economical and environmentally friendly strategy to control this disease. Therefore, the mining of excellent genes for rust resistance and the analysis of the mechanism of rust resistance are the key strategies to achieve the targeted breeding of rust resistance. However, there is no relevant report on pepper rust resistance at present. The aim of the present study was to further explore the resistance mechanism of pepper by screening the rust-resistant germplasm resources in the early stage. Combined with the analysis of plant pathology, transcriptomics, and metabolomics, we found that compared with susceptible cultivar TJ, resistant cultivar YK had 2752 differentially expressed genes (DEGs, 1253 up-, and 1499 downregulated) and 321 differentially accumulated metabolites (DAMs, 133 up- and 188 down-accumulated) after pathogen infection. And the genes and metabolites related to phenylpropanoid metabolism were highly enriched in resistant varieties, which indicated that phenylpropanoid metabolism might mediate the resistance of <i>Z. armatum</i>. This finding was further confirmed by a real-time quantitative polymerase chain reaction analysis, which revealed that the expression levels of core genes involved in phenylpropane metabolism in disease-resistant varieties were high. In addition, the difference in flavonoid and MeJA contents in the leaves between resistant and susceptible varieties further supported the conclusion that the flavonoid pathway and methyl jasmonate may be involved in the formation of Chinese pepper resistance. Our research results not only help to better understand the resistance mechanism of <i>Z. armatum</i> rust but also contribute to the breeding and utilization of resistant varieties.https://www.mdpi.com/1422-0067/24/19/14761<i>Zanthoxylum armatum</i><i>Coleosporium zanthoxyli</i>transcriptomemetabolomedisease resistancephenylpropanoid metabolism
spellingShingle Shan Han
Xiu Xu
Huan Yuan
Shujiang Li
Tiantian Lin
Yinggao Liu
Shuying Li
Tianhui Zhu
Integrated Transcriptome and Metabolome Analysis Reveals the Molecular Mechanism of Rust Resistance in Resistant (Youkang) and Susceptive (Tengjiao) <i>Zanthoxylum armatum</i> Cultivars
International Journal of Molecular Sciences
<i>Zanthoxylum armatum</i>
<i>Coleosporium zanthoxyli</i>
transcriptome
metabolome
disease resistance
phenylpropanoid metabolism
title Integrated Transcriptome and Metabolome Analysis Reveals the Molecular Mechanism of Rust Resistance in Resistant (Youkang) and Susceptive (Tengjiao) <i>Zanthoxylum armatum</i> Cultivars
title_full Integrated Transcriptome and Metabolome Analysis Reveals the Molecular Mechanism of Rust Resistance in Resistant (Youkang) and Susceptive (Tengjiao) <i>Zanthoxylum armatum</i> Cultivars
title_fullStr Integrated Transcriptome and Metabolome Analysis Reveals the Molecular Mechanism of Rust Resistance in Resistant (Youkang) and Susceptive (Tengjiao) <i>Zanthoxylum armatum</i> Cultivars
title_full_unstemmed Integrated Transcriptome and Metabolome Analysis Reveals the Molecular Mechanism of Rust Resistance in Resistant (Youkang) and Susceptive (Tengjiao) <i>Zanthoxylum armatum</i> Cultivars
title_short Integrated Transcriptome and Metabolome Analysis Reveals the Molecular Mechanism of Rust Resistance in Resistant (Youkang) and Susceptive (Tengjiao) <i>Zanthoxylum armatum</i> Cultivars
title_sort integrated transcriptome and metabolome analysis reveals the molecular mechanism of rust resistance in resistant youkang and susceptive tengjiao i zanthoxylum armatum i cultivars
topic <i>Zanthoxylum armatum</i>
<i>Coleosporium zanthoxyli</i>
transcriptome
metabolome
disease resistance
phenylpropanoid metabolism
url https://www.mdpi.com/1422-0067/24/19/14761
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