Beneficial mutualistic fungus Suillus luteus provided excellent buffering insurance in Scots pine defense responses under pathogen challenge at transcriptome level

Abstract Background Mutualistic mycorrhiza fungi that live in symbiosis with plants facilitates nutrient and water acquisition, improving tree growth and performance. In this study, we evaluated the potential of mutualistic fungal inoculation to improve the growth and disease resistance of Scots pin...

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Main Authors: Zilan Wen, Minna J. Manninen, Fred O. Asiegbu
Format: Article
Language:English
Published: BMC 2025-01-01
Series:BMC Plant Biology
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Online Access:https://doi.org/10.1186/s12870-024-06026-z
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author Zilan Wen
Minna J. Manninen
Fred O. Asiegbu
author_facet Zilan Wen
Minna J. Manninen
Fred O. Asiegbu
author_sort Zilan Wen
collection DOAJ
description Abstract Background Mutualistic mycorrhiza fungi that live in symbiosis with plants facilitates nutrient and water acquisition, improving tree growth and performance. In this study, we evaluated the potential of mutualistic fungal inoculation to improve the growth and disease resistance of Scots pine (Pinus sylvestris L.) against the forest pathogen Heterobasidion annosum. Results In co-inoculation experiment, Scots pine seedlings were pre-inoculated with mutualistic beneficial fungus (Suillus luteus) prior to H. annosum infection. The result revealed that inoculation with beneficial fungus promoted plant root growth. Transcriptome analyses revealed that co-inoculated plants and plants inoculated with beneficial fungus shared some similarities in defense gene responses. However, pathogen infection alone had unique sets of genes encoding pathogenesis-related (PR) proteins, phenylpropanoid pathway/lignin biosynthesis, flavonoid biosynthesis, chalcone/stilbene biosynthesis, ethylene signaling pathway, JA signaling pathway, cell remodeling and growth, transporters, and fungal recognition. On the other hand, beneficial fungus inoculation repressed the expression of PR proteins, and other defense-related genes such as laccases, chalcone/stilbene synthases, terpene synthases, cytochrome P450s. The co-inoculated plants did not equally enhance the induction of PR genes, chalcone/stilbene biosynthesis, however genes related to cell wall growth, water and nutrient transporters, phenylpropanoid/lignin biosynthesis/flavonoid biosynthesis, and hormone signaling were induced. Conclusion S. luteus promoted mutualistic interaction by suppressing plant defense responses. Pre-inoculation of Scots pine seedlings with beneficial fungus S. luteus prior to pathogen challenge promoted primary root growth, as well as had a balancing buffering role in plant defense responses and cell growth at transcriptome level.
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spelling doaj-art-d4a685b468434e159f9308e4e6a476942025-01-05T12:12:58ZengBMCBMC Plant Biology1471-22292025-01-0125111610.1186/s12870-024-06026-zBeneficial mutualistic fungus Suillus luteus provided excellent buffering insurance in Scots pine defense responses under pathogen challenge at transcriptome levelZilan Wen0Minna J. Manninen1Fred O. Asiegbu2Forest Pathology Research Lab, Faculty of Agriculture and Forestry, Department of Forest Sciences, University of HelsinkiForest Pathology Research Lab, Faculty of Agriculture and Forestry, Department of Forest Sciences, University of HelsinkiForest Pathology Research Lab, Faculty of Agriculture and Forestry, Department of Forest Sciences, University of HelsinkiAbstract Background Mutualistic mycorrhiza fungi that live in symbiosis with plants facilitates nutrient and water acquisition, improving tree growth and performance. In this study, we evaluated the potential of mutualistic fungal inoculation to improve the growth and disease resistance of Scots pine (Pinus sylvestris L.) against the forest pathogen Heterobasidion annosum. Results In co-inoculation experiment, Scots pine seedlings were pre-inoculated with mutualistic beneficial fungus (Suillus luteus) prior to H. annosum infection. The result revealed that inoculation with beneficial fungus promoted plant root growth. Transcriptome analyses revealed that co-inoculated plants and plants inoculated with beneficial fungus shared some similarities in defense gene responses. However, pathogen infection alone had unique sets of genes encoding pathogenesis-related (PR) proteins, phenylpropanoid pathway/lignin biosynthesis, flavonoid biosynthesis, chalcone/stilbene biosynthesis, ethylene signaling pathway, JA signaling pathway, cell remodeling and growth, transporters, and fungal recognition. On the other hand, beneficial fungus inoculation repressed the expression of PR proteins, and other defense-related genes such as laccases, chalcone/stilbene synthases, terpene synthases, cytochrome P450s. The co-inoculated plants did not equally enhance the induction of PR genes, chalcone/stilbene biosynthesis, however genes related to cell wall growth, water and nutrient transporters, phenylpropanoid/lignin biosynthesis/flavonoid biosynthesis, and hormone signaling were induced. Conclusion S. luteus promoted mutualistic interaction by suppressing plant defense responses. Pre-inoculation of Scots pine seedlings with beneficial fungus S. luteus prior to pathogen challenge promoted primary root growth, as well as had a balancing buffering role in plant defense responses and cell growth at transcriptome level.https://doi.org/10.1186/s12870-024-06026-zBeneficial and mutualistic fungiCo-inoculationPlant defense responsePlant growthSuillusHeterobasidion
spellingShingle Zilan Wen
Minna J. Manninen
Fred O. Asiegbu
Beneficial mutualistic fungus Suillus luteus provided excellent buffering insurance in Scots pine defense responses under pathogen challenge at transcriptome level
BMC Plant Biology
Beneficial and mutualistic fungi
Co-inoculation
Plant defense response
Plant growth
Suillus
Heterobasidion
title Beneficial mutualistic fungus Suillus luteus provided excellent buffering insurance in Scots pine defense responses under pathogen challenge at transcriptome level
title_full Beneficial mutualistic fungus Suillus luteus provided excellent buffering insurance in Scots pine defense responses under pathogen challenge at transcriptome level
title_fullStr Beneficial mutualistic fungus Suillus luteus provided excellent buffering insurance in Scots pine defense responses under pathogen challenge at transcriptome level
title_full_unstemmed Beneficial mutualistic fungus Suillus luteus provided excellent buffering insurance in Scots pine defense responses under pathogen challenge at transcriptome level
title_short Beneficial mutualistic fungus Suillus luteus provided excellent buffering insurance in Scots pine defense responses under pathogen challenge at transcriptome level
title_sort beneficial mutualistic fungus suillus luteus provided excellent buffering insurance in scots pine defense responses under pathogen challenge at transcriptome level
topic Beneficial and mutualistic fungi
Co-inoculation
Plant defense response
Plant growth
Suillus
Heterobasidion
url https://doi.org/10.1186/s12870-024-06026-z
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AT minnajmanninen beneficialmutualisticfungussuillusluteusprovidedexcellentbufferinginsuranceinscotspinedefenseresponsesunderpathogenchallengeattranscriptomelevel
AT fredoasiegbu beneficialmutualisticfungussuillusluteusprovidedexcellentbufferinginsuranceinscotspinedefenseresponsesunderpathogenchallengeattranscriptomelevel