Dodder Parasitism Leads to the Enrichment of Pathogen <i>Alternaria</i> and Flavonoid Metabolites in Soybean Root

Dodders (<i>Cuscuta chinensis</i>) are rootless and holoparasitic herbs that can infect a variety of host plants, including the vitally important economic and bioenergy crop soybean (<i>Glycine max</i>). Although dodder parasitism severely affects the physiology of host plant...

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Main Authors: Wen Luo, Yuanli Li, Ruiping Luo, Gehong Wei, Yongxin Liu, Weimin Chen
Format: Article
Language:English
Published: MDPI AG 2023-06-01
Series:Agronomy
Subjects:
Online Access:https://www.mdpi.com/2073-4395/13/6/1571
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author Wen Luo
Yuanli Li
Ruiping Luo
Gehong Wei
Yongxin Liu
Weimin Chen
author_facet Wen Luo
Yuanli Li
Ruiping Luo
Gehong Wei
Yongxin Liu
Weimin Chen
author_sort Wen Luo
collection DOAJ
description Dodders (<i>Cuscuta chinensis</i>) are rootless and holoparasitic herbs that can infect a variety of host plants, including the vitally important economic and bioenergy crop soybean (<i>Glycine max</i>). Although dodder parasitism severely affects the physiology of host plants, little is known about its effects on fungal communities and root secondary metabolites in hosts. In this study, variations in root-associated fungal communities and root metabolites of soybean under different parasitism conditions were investigated using ITS rRNA gene sequencing and UPLC–MS/MS metabolome detection technologies. The results showed that dodder parasitism significantly altered the composition and diversity of the fungal communities in the rhizosphere and endosphere of soybean. The relative abundance of the potential pathogenic fungus <i>Alternaria</i> significantly increased in the root endosphere of dodder-parasitized soybean. Furthermore, correlation analysis indicated that the fungal community in the root endosphere was susceptible to soil factors under dodder parasitism. Meanwhile, the content of soil total nitrogen was significantly and positively correlated with the relative abundance of <i>Alternaria</i> in the rhizosphere and endosphere of soybean. Metabolomic analysis indicated that dodder parasitism altered the accumulation of flavonoids in soybean roots, with significant upregulation of the contents of kaempferol and its downstream derivatives under different parasitism conditions. Taken together, this study highlighted the important role of dodder parasitism in shaping the fungal communities and secondary metabolites associated with soybean roots, providing new insights into the mechanisms of multiple interactions among dodder, soybean, microbial communities and the soil environment.
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spelling doaj.art-36117af2017f44a295699780457df2232023-11-18T08:55:04ZengMDPI AGAgronomy2073-43952023-06-01136157110.3390/agronomy13061571Dodder Parasitism Leads to the Enrichment of Pathogen <i>Alternaria</i> and Flavonoid Metabolites in Soybean RootWen Luo0Yuanli Li1Ruiping Luo2Gehong Wei3Yongxin Liu4Weimin Chen5State Key Laboratory of Crop Stress Biology in Arid Areas, Shaanxi Key Laboratory of Agricultural and Environmental Microbiology, College of Life Sciences, Northwest A&F University, Xianyang 712100, ChinaState Key Laboratory of Crop Stress Biology in Arid Areas, Shaanxi Key Laboratory of Agricultural and Environmental Microbiology, College of Life Sciences, Northwest A&F University, Xianyang 712100, ChinaCrop Research Institute of Ningxia Academy of Agriculture and Forestry Sciences, Yinchuan Comprehensive Experimental Station of National Soybean Industry Technology System, Yinchuan 750105, ChinaState Key Laboratory of Crop Stress Biology in Arid Areas, Shaanxi Key Laboratory of Agricultural and Environmental Microbiology, College of Life Sciences, Northwest A&F University, Xianyang 712100, ChinaShenzhen Branch, Guangdong Laboratory of Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture and Rural Affairs, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen 518120, ChinaState Key Laboratory of Crop Stress Biology in Arid Areas, Shaanxi Key Laboratory of Agricultural and Environmental Microbiology, College of Life Sciences, Northwest A&F University, Xianyang 712100, ChinaDodders (<i>Cuscuta chinensis</i>) are rootless and holoparasitic herbs that can infect a variety of host plants, including the vitally important economic and bioenergy crop soybean (<i>Glycine max</i>). Although dodder parasitism severely affects the physiology of host plants, little is known about its effects on fungal communities and root secondary metabolites in hosts. In this study, variations in root-associated fungal communities and root metabolites of soybean under different parasitism conditions were investigated using ITS rRNA gene sequencing and UPLC–MS/MS metabolome detection technologies. The results showed that dodder parasitism significantly altered the composition and diversity of the fungal communities in the rhizosphere and endosphere of soybean. The relative abundance of the potential pathogenic fungus <i>Alternaria</i> significantly increased in the root endosphere of dodder-parasitized soybean. Furthermore, correlation analysis indicated that the fungal community in the root endosphere was susceptible to soil factors under dodder parasitism. Meanwhile, the content of soil total nitrogen was significantly and positively correlated with the relative abundance of <i>Alternaria</i> in the rhizosphere and endosphere of soybean. Metabolomic analysis indicated that dodder parasitism altered the accumulation of flavonoids in soybean roots, with significant upregulation of the contents of kaempferol and its downstream derivatives under different parasitism conditions. Taken together, this study highlighted the important role of dodder parasitism in shaping the fungal communities and secondary metabolites associated with soybean roots, providing new insights into the mechanisms of multiple interactions among dodder, soybean, microbial communities and the soil environment.https://www.mdpi.com/2073-4395/13/6/1571<i>Cuscuta</i>flavonoid metabolitelegume plantparasitism statusrhizosphereroot-associated microbiome
spellingShingle Wen Luo
Yuanli Li
Ruiping Luo
Gehong Wei
Yongxin Liu
Weimin Chen
Dodder Parasitism Leads to the Enrichment of Pathogen <i>Alternaria</i> and Flavonoid Metabolites in Soybean Root
Agronomy
<i>Cuscuta</i>
flavonoid metabolite
legume plant
parasitism status
rhizosphere
root-associated microbiome
title Dodder Parasitism Leads to the Enrichment of Pathogen <i>Alternaria</i> and Flavonoid Metabolites in Soybean Root
title_full Dodder Parasitism Leads to the Enrichment of Pathogen <i>Alternaria</i> and Flavonoid Metabolites in Soybean Root
title_fullStr Dodder Parasitism Leads to the Enrichment of Pathogen <i>Alternaria</i> and Flavonoid Metabolites in Soybean Root
title_full_unstemmed Dodder Parasitism Leads to the Enrichment of Pathogen <i>Alternaria</i> and Flavonoid Metabolites in Soybean Root
title_short Dodder Parasitism Leads to the Enrichment of Pathogen <i>Alternaria</i> and Flavonoid Metabolites in Soybean Root
title_sort dodder parasitism leads to the enrichment of pathogen i alternaria i and flavonoid metabolites in soybean root
topic <i>Cuscuta</i>
flavonoid metabolite
legume plant
parasitism status
rhizosphere
root-associated microbiome
url https://www.mdpi.com/2073-4395/13/6/1571
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