Integrative transcriptome and WGCNA analysis reveal key genes mainly in response to Alternaria alternata in Populus simonii × P. nigra

In order to explore the molecular mechanisms of Populus simonii × P. nigra response to stress and screen for genes conferring resistance to Alternaria alternata, we carried out measurements of physiological and biochemical indices and transcriptomic sequence analysis of leaves of Populus simonii × P...

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Main Authors: Siyuan Liu, Lijuan Dai, Guanzheng Qu, Xinming Lu, Hong Pan, Xiaoyu Fu, Airong Dong, Libin Yang
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-02-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2025.1540718/full
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author Siyuan Liu
Siyuan Liu
Siyuan Liu
Lijuan Dai
Guanzheng Qu
Xinming Lu
Hong Pan
Xiaoyu Fu
Airong Dong
Airong Dong
Libin Yang
author_facet Siyuan Liu
Siyuan Liu
Siyuan Liu
Lijuan Dai
Guanzheng Qu
Xinming Lu
Hong Pan
Xiaoyu Fu
Airong Dong
Airong Dong
Libin Yang
author_sort Siyuan Liu
collection DOAJ
description In order to explore the molecular mechanisms of Populus simonii × P. nigra response to stress and screen for genes conferring resistance to Alternaria alternata, we carried out measurements of physiological and biochemical indices and transcriptomic sequence analysis of leaves of Populus simonii × P. nigra inoculated with A. alternata. The results showed that the variation trends of multiple hormone contents and enzyme activities were broadly similar at different time points, with H2O2, SA, JA, PPO, SOD, PAL and POD showing a trend of increasing and then decrease after inoculation with the pathogen. The contents of H2O2 peaked on the second day and subsequently declined. The contents of SA and JA, as well as the enzymatic activities of SOD, PAL, and POD, reached their maxima on the third day before exhibiting a downward tendency. In contrast, the activity of PPO peaked on the fourth day. Whereas ABA content continued to increase until the fifth day and CAT content decreased and then increased. We subsequently identified 14,997 differentially expressed genes (DEGs) among the transcriptomic sequences(|log2FoldChange| > 1 and FDR value < 0.05), with genes encoding members of the ERF, MYB, bZIP, and WRKY transcription factor families being differentially expressed. Gene modules that were significantly associated with the ABA, PAL, JA, and SOD activity were identified using weighted gene co-expression network analysis (WGCNA). Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analysis showed that these genes were mainly related to biological stress, signal transduction, cell wall, and photosynthesis. Within these modules, we also identified hub genes in the regulatory network, including GLK1/2 transcriptional activators, 14-3-3 proteins, cytosine 5 methyltransferases, and a variety of proteins associated with photosynthesis and respiration. This study showed that these hub genes, which play a pivotal role in the co-expression network, which may indicate a potential role in defense process of Populus simonii × P. nigra against A. alternata. Additionally, we analyzed the gene expression regulation and defense mechanisms of Populus simonii × P. nigra adversity stress, providing new insights into how plants respond to biological stress.
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spelling doaj-art-e885de4d818e4252bc85ccf0a9dc89c22025-08-20T02:12:58ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2025-02-011610.3389/fpls.2025.15407181540718Integrative transcriptome and WGCNA analysis reveal key genes mainly in response to Alternaria alternata in Populus simonii × P. nigraSiyuan Liu0Siyuan Liu1Siyuan Liu2Lijuan Dai3Guanzheng Qu4Xinming Lu5Hong Pan6Xiaoyu Fu7Airong Dong8Airong Dong9Libin Yang10Key Laboratory of Biodiversity, Institute of Natural Resources and Ecology, Heilongjiang Academy of Sciences, Harbin, ChinaState Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, ChinaCollege of Forestry, Northeast Forestry University, Harbin, ChinaState Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, ChinaState Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, ChinaKey Laboratory of Biodiversity, Institute of Natural Resources and Ecology, Heilongjiang Academy of Sciences, Harbin, ChinaKey Laboratory of Biodiversity, Institute of Natural Resources and Ecology, Heilongjiang Academy of Sciences, Harbin, ChinaKey Laboratory of Biodiversity, Institute of Natural Resources and Ecology, Heilongjiang Academy of Sciences, Harbin, ChinaState Key Laboratory of Tree Genetics and Breeding, Northeast Forestry University, Harbin, ChinaCollege of Forestry, Northeast Forestry University, Harbin, ChinaKey Laboratory of Biodiversity, Institute of Natural Resources and Ecology, Heilongjiang Academy of Sciences, Harbin, ChinaIn order to explore the molecular mechanisms of Populus simonii × P. nigra response to stress and screen for genes conferring resistance to Alternaria alternata, we carried out measurements of physiological and biochemical indices and transcriptomic sequence analysis of leaves of Populus simonii × P. nigra inoculated with A. alternata. The results showed that the variation trends of multiple hormone contents and enzyme activities were broadly similar at different time points, with H2O2, SA, JA, PPO, SOD, PAL and POD showing a trend of increasing and then decrease after inoculation with the pathogen. The contents of H2O2 peaked on the second day and subsequently declined. The contents of SA and JA, as well as the enzymatic activities of SOD, PAL, and POD, reached their maxima on the third day before exhibiting a downward tendency. In contrast, the activity of PPO peaked on the fourth day. Whereas ABA content continued to increase until the fifth day and CAT content decreased and then increased. We subsequently identified 14,997 differentially expressed genes (DEGs) among the transcriptomic sequences(|log2FoldChange| > 1 and FDR value < 0.05), with genes encoding members of the ERF, MYB, bZIP, and WRKY transcription factor families being differentially expressed. Gene modules that were significantly associated with the ABA, PAL, JA, and SOD activity were identified using weighted gene co-expression network analysis (WGCNA). Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analysis showed that these genes were mainly related to biological stress, signal transduction, cell wall, and photosynthesis. Within these modules, we also identified hub genes in the regulatory network, including GLK1/2 transcriptional activators, 14-3-3 proteins, cytosine 5 methyltransferases, and a variety of proteins associated with photosynthesis and respiration. This study showed that these hub genes, which play a pivotal role in the co-expression network, which may indicate a potential role in defense process of Populus simonii × P. nigra against A. alternata. Additionally, we analyzed the gene expression regulation and defense mechanisms of Populus simonii × P. nigra adversity stress, providing new insights into how plants respond to biological stress.https://www.frontiersin.org/articles/10.3389/fpls.2025.1540718/fulltranscriptomic sequencingPopulus simonii × Populus nigraWGCNAkey genesAlternaria alternata
spellingShingle Siyuan Liu
Siyuan Liu
Siyuan Liu
Lijuan Dai
Guanzheng Qu
Xinming Lu
Hong Pan
Xiaoyu Fu
Airong Dong
Airong Dong
Libin Yang
Integrative transcriptome and WGCNA analysis reveal key genes mainly in response to Alternaria alternata in Populus simonii × P. nigra
Frontiers in Plant Science
transcriptomic sequencing
Populus simonii × Populus nigra
WGCNA
key genes
Alternaria alternata
title Integrative transcriptome and WGCNA analysis reveal key genes mainly in response to Alternaria alternata in Populus simonii × P. nigra
title_full Integrative transcriptome and WGCNA analysis reveal key genes mainly in response to Alternaria alternata in Populus simonii × P. nigra
title_fullStr Integrative transcriptome and WGCNA analysis reveal key genes mainly in response to Alternaria alternata in Populus simonii × P. nigra
title_full_unstemmed Integrative transcriptome and WGCNA analysis reveal key genes mainly in response to Alternaria alternata in Populus simonii × P. nigra
title_short Integrative transcriptome and WGCNA analysis reveal key genes mainly in response to Alternaria alternata in Populus simonii × P. nigra
title_sort integrative transcriptome and wgcna analysis reveal key genes mainly in response to alternaria alternata in populus simonii p nigra
topic transcriptomic sequencing
Populus simonii × Populus nigra
WGCNA
key genes
Alternaria alternata
url https://www.frontiersin.org/articles/10.3389/fpls.2025.1540718/full
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