Mechanism of Action of <i>Fusarium oxysporum</i> CCS043 Utilizing Allelochemicals for Rhizosphere Colonization and Enhanced Infection Activity in <i>Rehmannia glutinosa</i>

<i>Rehmannia glutinosa</i> is an important medicinal herb; but its long-term cultivation often leads to continuous cropping problems. The underlying cause can be attributed to the accumulation of and alterations in root exudates; which interact with soil-borne pathogens; particularly <...

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Main Authors: Feiyue Yuan, Fuxiang Qiu, Jiawei Xie, Yongxi Fan, Bao Zhang, Tingting Zhang, Zhongyi Zhang, Li Gu, Mingjie Li
Format: Article
Language:English
Published: MDPI AG 2024-12-01
Series:Plants
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Online Access:https://www.mdpi.com/2223-7747/14/1/38
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author Feiyue Yuan
Fuxiang Qiu
Jiawei Xie
Yongxi Fan
Bao Zhang
Tingting Zhang
Zhongyi Zhang
Li Gu
Mingjie Li
author_facet Feiyue Yuan
Fuxiang Qiu
Jiawei Xie
Yongxi Fan
Bao Zhang
Tingting Zhang
Zhongyi Zhang
Li Gu
Mingjie Li
author_sort Feiyue Yuan
collection DOAJ
description <i>Rehmannia glutinosa</i> is an important medicinal herb; but its long-term cultivation often leads to continuous cropping problems. The underlying cause can be attributed to the accumulation of and alterations in root exudates; which interact with soil-borne pathogens; particularly <i>Fusarium oxysporum</i>; triggering disease outbreaks that severely affect its yield and quality. It is therefore crucial to elucidate the mechanisms by which root exudates induce <i>F. oxysporum</i> CCS043 outbreaks. In this study; the genome of <i>F. oxysporum</i> CCS043 from <i>R. glutinosa’s</i> rhizosphere microbiota was sequenced and assembled de novo; resulting in a 47.67 Mb genome comprising 16,423 protein-coding genes. Evolutionary analysis suggests that different <i>F. oxysporum</i> strains may adapt to the host rhizosphere microecosystem by acquiring varying numbers of specific genes while maintaining a constant number of core genes.The allelopathic effects of ferulic acid; verbascoside; and catalpol on <i>F. oxysporum</i> CCS043 were examined at the physiological and transcriptomic levels. The application of ferulic acid was observed to primarily facilitate the proliferation and growth of <i>F. oxysporum</i> CCS043; whereas verbascoside notably enhanced the biosynthesis of infection-related enzymes such as pectinase and cellulase. Catalpol demonstrated a moderate level of allelopathic effects in comparison to the other two. Furthermore; 10 effectors were identified by combining the genomic data. Meanwhile; it was found that among the effector-protein-coding genes; ChiC; VRDA; csn; and chitinase exhibited upregulated expression across all treatments. The expression patterns of these key genes were validated using qRT-PCR. Transient overexpression of the two effector-encoding genes in detached <i>R. glutinosa</i> leaves provided further confirmation that ChiC (GME8876_g) and csn (GME9251_g) are key effector proteins responsible for the induction of hypersensitive reactions in <i>R. glutinosa</i> leaf cells. This study provides a preliminary indication that the use of allelochemicals by <i>F. oxysporum</i> CCS043 can promote its own growth and proliferation and enhance infection activity. This finding offers a solid theoretical basis and data support for elucidating the fundamental causes of fungal disease outbreaks in continuous cropping of <i>R. glutinosa</i> and for formulating effective mitigation strategies.
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spelling doaj-art-0d1e16f83bb048f5b0d1ab10b4428ac02025-01-10T13:19:33ZengMDPI AGPlants2223-77472024-12-011413810.3390/plants14010038Mechanism of Action of <i>Fusarium oxysporum</i> CCS043 Utilizing Allelochemicals for Rhizosphere Colonization and Enhanced Infection Activity in <i>Rehmannia glutinosa</i>Feiyue Yuan0Fuxiang Qiu1Jiawei Xie2Yongxi Fan3Bao Zhang4Tingting Zhang5Zhongyi Zhang6Li Gu7Mingjie Li8College of Bee Science and Biomedicine, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Bee Science and Biomedicine, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaKey Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of JunCao Science and Ecology, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Bioengineering, Henan University of Technology, Zhengzhou 450001, ChinaCollege of Bee Science and Biomedicine, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Bee Science and Biomedicine, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Bee Science and Biomedicine, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Bee Science and Biomedicine, Fujian Agriculture and Forestry University, Fuzhou 350002, China<i>Rehmannia glutinosa</i> is an important medicinal herb; but its long-term cultivation often leads to continuous cropping problems. The underlying cause can be attributed to the accumulation of and alterations in root exudates; which interact with soil-borne pathogens; particularly <i>Fusarium oxysporum</i>; triggering disease outbreaks that severely affect its yield and quality. It is therefore crucial to elucidate the mechanisms by which root exudates induce <i>F. oxysporum</i> CCS043 outbreaks. In this study; the genome of <i>F. oxysporum</i> CCS043 from <i>R. glutinosa’s</i> rhizosphere microbiota was sequenced and assembled de novo; resulting in a 47.67 Mb genome comprising 16,423 protein-coding genes. Evolutionary analysis suggests that different <i>F. oxysporum</i> strains may adapt to the host rhizosphere microecosystem by acquiring varying numbers of specific genes while maintaining a constant number of core genes.The allelopathic effects of ferulic acid; verbascoside; and catalpol on <i>F. oxysporum</i> CCS043 were examined at the physiological and transcriptomic levels. The application of ferulic acid was observed to primarily facilitate the proliferation and growth of <i>F. oxysporum</i> CCS043; whereas verbascoside notably enhanced the biosynthesis of infection-related enzymes such as pectinase and cellulase. Catalpol demonstrated a moderate level of allelopathic effects in comparison to the other two. Furthermore; 10 effectors were identified by combining the genomic data. Meanwhile; it was found that among the effector-protein-coding genes; ChiC; VRDA; csn; and chitinase exhibited upregulated expression across all treatments. The expression patterns of these key genes were validated using qRT-PCR. Transient overexpression of the two effector-encoding genes in detached <i>R. glutinosa</i> leaves provided further confirmation that ChiC (GME8876_g) and csn (GME9251_g) are key effector proteins responsible for the induction of hypersensitive reactions in <i>R. glutinosa</i> leaf cells. This study provides a preliminary indication that the use of allelochemicals by <i>F. oxysporum</i> CCS043 can promote its own growth and proliferation and enhance infection activity. This finding offers a solid theoretical basis and data support for elucidating the fundamental causes of fungal disease outbreaks in continuous cropping of <i>R. glutinosa</i> and for formulating effective mitigation strategies.https://www.mdpi.com/2223-7747/14/1/38<i>Rehmannia glutinosa</i><i>F. oxysporum</i> CCS043allelopathyroot exudateseffector protein
spellingShingle Feiyue Yuan
Fuxiang Qiu
Jiawei Xie
Yongxi Fan
Bao Zhang
Tingting Zhang
Zhongyi Zhang
Li Gu
Mingjie Li
Mechanism of Action of <i>Fusarium oxysporum</i> CCS043 Utilizing Allelochemicals for Rhizosphere Colonization and Enhanced Infection Activity in <i>Rehmannia glutinosa</i>
Plants
<i>Rehmannia glutinosa</i>
<i>F. oxysporum</i> CCS043
allelopathy
root exudates
effector protein
title Mechanism of Action of <i>Fusarium oxysporum</i> CCS043 Utilizing Allelochemicals for Rhizosphere Colonization and Enhanced Infection Activity in <i>Rehmannia glutinosa</i>
title_full Mechanism of Action of <i>Fusarium oxysporum</i> CCS043 Utilizing Allelochemicals for Rhizosphere Colonization and Enhanced Infection Activity in <i>Rehmannia glutinosa</i>
title_fullStr Mechanism of Action of <i>Fusarium oxysporum</i> CCS043 Utilizing Allelochemicals for Rhizosphere Colonization and Enhanced Infection Activity in <i>Rehmannia glutinosa</i>
title_full_unstemmed Mechanism of Action of <i>Fusarium oxysporum</i> CCS043 Utilizing Allelochemicals for Rhizosphere Colonization and Enhanced Infection Activity in <i>Rehmannia glutinosa</i>
title_short Mechanism of Action of <i>Fusarium oxysporum</i> CCS043 Utilizing Allelochemicals for Rhizosphere Colonization and Enhanced Infection Activity in <i>Rehmannia glutinosa</i>
title_sort mechanism of action of i fusarium oxysporum i ccs043 utilizing allelochemicals for rhizosphere colonization and enhanced infection activity in i rehmannia glutinosa i
topic <i>Rehmannia glutinosa</i>
<i>F. oxysporum</i> CCS043
allelopathy
root exudates
effector protein
url https://www.mdpi.com/2223-7747/14/1/38
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