Transcriptomic characterization of Trichoderma harzianum T34 primed tomato plants: assessment of biocontrol agent induced host specific gene expression and plant growth promotion

Abstract In this study, we investigated the intricate interplay between Trichoderma and the tomato genome, focusing on the transcriptional and metabolic changes triggered during the late colonization event. Microarray probe set (GSE76332) was utilized to analyze the gene expression profiles changes...

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Main Authors: Mohd Aamir, V. Shanmugam, Manish Kumar Dubey, Fohad Mabood Husain, Mohd Adil, Waquar Akhter Ansari, Ashutosh Rai, Pankaj Sah
Format: Article
Language:English
Published: BMC 2023-11-01
Series:BMC Plant Biology
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Online Access:https://doi.org/10.1186/s12870-023-04502-6
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author Mohd Aamir
V. Shanmugam
Manish Kumar Dubey
Fohad Mabood Husain
Mohd Adil
Waquar Akhter Ansari
Ashutosh Rai
Pankaj Sah
author_facet Mohd Aamir
V. Shanmugam
Manish Kumar Dubey
Fohad Mabood Husain
Mohd Adil
Waquar Akhter Ansari
Ashutosh Rai
Pankaj Sah
author_sort Mohd Aamir
collection DOAJ
description Abstract In this study, we investigated the intricate interplay between Trichoderma and the tomato genome, focusing on the transcriptional and metabolic changes triggered during the late colonization event. Microarray probe set (GSE76332) was utilized to analyze the gene expression profiles changes of the un-inoculated control (tomato) and Trichoderma-tomato interactions for identification of the differentially expressed significant genes. Based on principal component analysis and R-based correlation, we observed a positive correlation between the two cross-comaparable groups, corroborating the existence of transcriptional responses in the host triggered by Trichoderma priming. The statistically significant genes based on different p-value cut-off scores [(p adj-values or q-value); p adj-value < 0.05], [(p cal-values); p cal-value < 0.05; p cal < 0.01; p cal < 0.001)] were cross compared. Through cross-comparison, we identified 156 common genes that were consistently significant across all probability thresholds, and showing a strong positive corelation between p-value and q-value in the selected probe sets. We reported TD2, CPT1, pectin synthase, EXT-3 (extensin-3), Lox C, and pyruvate kinase (PK), which exhibited upregulated expression, and Glb1 and nitrate reductase (nii), which demonstrated downregulated expression during Trichoderma-tomato interaction. In addition, microbial priming with Trichoderma resulted into differential expression of transcription factors related to systemic defense and flowering including MYB13, MYB78, ERF2, ERF3, ERF5, ERF-1B, NAC, MADS box, ZF3, ZAT10, A20/AN1, polyol sugar transporter like zinc finger proteins, and a novel plant defensin protein. The potential bottleneck and hub genes involved in this dynamic response were also identified. The protein–protein interaction (PPI) network analysis based on 25 topmost DEGS (p cal-value < 0.05) and the Weighted Correlation Gene Network Analysis (WGCNA) of the 1786 significant DEGs (p cal-value < 0.05) we reported the hits associated with carbohydrate metabolism, secondary metabolite biosynthesis, and the nitrogen metabolism. We conclude that the Trichoderma-induced microbial priming re-programmed the host genome for transcriptional response during the late colonization event and were characterized by metabolic shifting and biochemical changes specific to plant growth and development. The work also highlights the relevance of statistical parameters in understanding the gene regulatory dynamics and complex regulatory networks based on differential expression, co-expression, and protein interaction networks orchestrating the host responses to beneficial microbial interactions.
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spelling doaj.art-6beaa3cd5cdd4f09920a39fc639ec6502023-11-12T12:11:55ZengBMCBMC Plant Biology1471-22292023-11-0123113810.1186/s12870-023-04502-6Transcriptomic characterization of Trichoderma harzianum T34 primed tomato plants: assessment of biocontrol agent induced host specific gene expression and plant growth promotionMohd Aamir0V. Shanmugam1Manish Kumar Dubey2Fohad Mabood Husain3Mohd Adil4Waquar Akhter Ansari5Ashutosh Rai6Pankaj Sah7Division of Plant Pathology, ICAR-Indian Agricultural Research InstituteDivision of Plant Pathology, ICAR-Indian Agricultural Research InstituteDepartment of Biotechnology, University Centre for Research & Development (UCRD), Chandigarh UniversityDepartment of Food Science and Nutrition, College of Food and Agriculture Sciences, King Saud UniversityPlant, Food and Environmental Sciences, Dalhousie UniversityDepartment of Botany, Centre for Advanced Study, Institute of Science, Banaras Hindu UniversityDepartment of Basic and Social Sciences, College of Horticulture, Banda University of Agriculture and Technology, Uttar PradeshApplied Sciences Department, College of Applied Sciences and Pharmacy, University of Technology and Applied Sciences-MuscatAbstract In this study, we investigated the intricate interplay between Trichoderma and the tomato genome, focusing on the transcriptional and metabolic changes triggered during the late colonization event. Microarray probe set (GSE76332) was utilized to analyze the gene expression profiles changes of the un-inoculated control (tomato) and Trichoderma-tomato interactions for identification of the differentially expressed significant genes. Based on principal component analysis and R-based correlation, we observed a positive correlation between the two cross-comaparable groups, corroborating the existence of transcriptional responses in the host triggered by Trichoderma priming. The statistically significant genes based on different p-value cut-off scores [(p adj-values or q-value); p adj-value < 0.05], [(p cal-values); p cal-value < 0.05; p cal < 0.01; p cal < 0.001)] were cross compared. Through cross-comparison, we identified 156 common genes that were consistently significant across all probability thresholds, and showing a strong positive corelation between p-value and q-value in the selected probe sets. We reported TD2, CPT1, pectin synthase, EXT-3 (extensin-3), Lox C, and pyruvate kinase (PK), which exhibited upregulated expression, and Glb1 and nitrate reductase (nii), which demonstrated downregulated expression during Trichoderma-tomato interaction. In addition, microbial priming with Trichoderma resulted into differential expression of transcription factors related to systemic defense and flowering including MYB13, MYB78, ERF2, ERF3, ERF5, ERF-1B, NAC, MADS box, ZF3, ZAT10, A20/AN1, polyol sugar transporter like zinc finger proteins, and a novel plant defensin protein. The potential bottleneck and hub genes involved in this dynamic response were also identified. The protein–protein interaction (PPI) network analysis based on 25 topmost DEGS (p cal-value < 0.05) and the Weighted Correlation Gene Network Analysis (WGCNA) of the 1786 significant DEGs (p cal-value < 0.05) we reported the hits associated with carbohydrate metabolism, secondary metabolite biosynthesis, and the nitrogen metabolism. We conclude that the Trichoderma-induced microbial priming re-programmed the host genome for transcriptional response during the late colonization event and were characterized by metabolic shifting and biochemical changes specific to plant growth and development. The work also highlights the relevance of statistical parameters in understanding the gene regulatory dynamics and complex regulatory networks based on differential expression, co-expression, and protein interaction networks orchestrating the host responses to beneficial microbial interactions.https://doi.org/10.1186/s12870-023-04502-6TrichodermaMicroarrayTranscriptional reprogrammingFDR correctionWCGNA analysisDNA motif
spellingShingle Mohd Aamir
V. Shanmugam
Manish Kumar Dubey
Fohad Mabood Husain
Mohd Adil
Waquar Akhter Ansari
Ashutosh Rai
Pankaj Sah
Transcriptomic characterization of Trichoderma harzianum T34 primed tomato plants: assessment of biocontrol agent induced host specific gene expression and plant growth promotion
BMC Plant Biology
Trichoderma
Microarray
Transcriptional reprogramming
FDR correction
WCGNA analysis
DNA motif
title Transcriptomic characterization of Trichoderma harzianum T34 primed tomato plants: assessment of biocontrol agent induced host specific gene expression and plant growth promotion
title_full Transcriptomic characterization of Trichoderma harzianum T34 primed tomato plants: assessment of biocontrol agent induced host specific gene expression and plant growth promotion
title_fullStr Transcriptomic characterization of Trichoderma harzianum T34 primed tomato plants: assessment of biocontrol agent induced host specific gene expression and plant growth promotion
title_full_unstemmed Transcriptomic characterization of Trichoderma harzianum T34 primed tomato plants: assessment of biocontrol agent induced host specific gene expression and plant growth promotion
title_short Transcriptomic characterization of Trichoderma harzianum T34 primed tomato plants: assessment of biocontrol agent induced host specific gene expression and plant growth promotion
title_sort transcriptomic characterization of trichoderma harzianum t34 primed tomato plants assessment of biocontrol agent induced host specific gene expression and plant growth promotion
topic Trichoderma
Microarray
Transcriptional reprogramming
FDR correction
WCGNA analysis
DNA motif
url https://doi.org/10.1186/s12870-023-04502-6
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