Integrated Transcriptomic and Metabolomic Analyses Reveal the Importance of the Terpenoid, Fatty Acid, and Flavonoid Pathways in Rice Cell Death and Defense

Lesion mimic mutants provide unique tools to investigate plant–pathogen interactions, often exhibiting hypersensitive responses in the absence of biotic or abiotic stresses. The overexpression of the S-domain receptor-like kinase gene, <i>SPL11</i> cell-<i>d</i>eath <i>...

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Main Authors: Pengfei Bai, Yanfang Liu, Laisa Gomes-Dias, Rachel Combs-Giroir, Shaoxing Dai, Naeyeoung Choi, Yun Lin, Matthew Bernier, Emmanuel Hatzakis, Guo-Liang Wang, Joshua J. Blakeslee
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Language:English
Published: MDPI AG 2025-02-01
Series:Plants
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Online Access:https://www.mdpi.com/2223-7747/14/5/665
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author Pengfei Bai
Yanfang Liu
Laisa Gomes-Dias
Rachel Combs-Giroir
Shaoxing Dai
Naeyeoung Choi
Yun Lin
Matthew Bernier
Emmanuel Hatzakis
Guo-Liang Wang
Joshua J. Blakeslee
author_facet Pengfei Bai
Yanfang Liu
Laisa Gomes-Dias
Rachel Combs-Giroir
Shaoxing Dai
Naeyeoung Choi
Yun Lin
Matthew Bernier
Emmanuel Hatzakis
Guo-Liang Wang
Joshua J. Blakeslee
author_sort Pengfei Bai
collection DOAJ
description Lesion mimic mutants provide unique tools to investigate plant–pathogen interactions, often exhibiting hypersensitive responses in the absence of biotic or abiotic stresses. The overexpression of the S-domain receptor-like kinase gene, <i>SPL11</i> cell-<i>d</i>eath <i>s</i>uppressor <i>2</i> (<i>SDS2</i>), in rice leads to constitutive programmed cell death and enhanced resistance to fungal and bacterial pathogens. However, the mechanisms underlying this broad-spectrum resistance remain unclear. This study integrates transcriptomic and metabolomic analyses of the <i>SDS2-ACT</i> mutant to uncover gene expression and metabolic shifts associated with disease resistance. To identify <i>SDS2-</i>specific physiological changes related to pathogen resistance, leaf tissues from the <i>SDS2-ACT</i> mutant and the Kitkaake WT line were subjected to both transcriptomic and non-targeted metabolic profiling. Transcriptomic analyses identified 1497 differentially expressed genes (DEGs), including up-regulated genes involved in terpenoid and flavonoid biosynthesis, phytohormone signaling, and defense-related pathways (including pathogenesis-related [PR] genes). Metabolomic profiling revealed significant alterations in the accumulation of several compound classes, including putative: terpenoids, phenylpropanoids, phytohormones, fatty acids, and sugars. These changes are likely correlated with the observed cell death and resistance phenotypes in the SDS2-ACT mutant. This study provides an overall landscape of the transcriptomic and metabolomic alterations in a lesion mimic mutant, identifying candidate defense-related genes and metabolites for functional analysis in rice.
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spelling doaj-art-e58341e0582548ecb4917bd5a358b0ca2025-08-20T02:06:13ZengMDPI AGPlants2223-77472025-02-0114566510.3390/plants14050665Integrated Transcriptomic and Metabolomic Analyses Reveal the Importance of the Terpenoid, Fatty Acid, and Flavonoid Pathways in Rice Cell Death and DefensePengfei Bai0Yanfang Liu1Laisa Gomes-Dias2Rachel Combs-Giroir3Shaoxing Dai4Naeyeoung Choi5Yun Lin6Matthew Bernier7Emmanuel Hatzakis8Guo-Liang Wang9Joshua J. Blakeslee10Department of Plant Pathology, The Ohio State University, Columbus, OH 43210, USADepartment of Plant Pathology, The Ohio State University, Columbus, OH 43210, USADepartment of Horticulture and Crop Science, The Ohio State University, Columbus, OH 43210, USADepartment of Horticulture and Crop Science, The Ohio State University, Columbus, OH 43210, USAInstitute of Primate Translational Medicine, Kunming University of Science and Technology, Kunming 650500, ChinaDepartment of Plant Pathology, The Ohio State University, Columbus, OH 43210, USADepartment of Horticulture and Crop Science, The Ohio State University, Columbus, OH 43210, USACampus Chemical Instrumentation Center (CCIC), The Ohio State University, Columbus, OH 43210, USADepartment of Food Science and Technology, The Ohio State University, Columbus, OH 43210, USADepartment of Plant Pathology, The Ohio State University, Columbus, OH 43210, USADepartment of Horticulture and Crop Science, The Ohio State University, Columbus, OH 43210, USALesion mimic mutants provide unique tools to investigate plant–pathogen interactions, often exhibiting hypersensitive responses in the absence of biotic or abiotic stresses. The overexpression of the S-domain receptor-like kinase gene, <i>SPL11</i> cell-<i>d</i>eath <i>s</i>uppressor <i>2</i> (<i>SDS2</i>), in rice leads to constitutive programmed cell death and enhanced resistance to fungal and bacterial pathogens. However, the mechanisms underlying this broad-spectrum resistance remain unclear. This study integrates transcriptomic and metabolomic analyses of the <i>SDS2-ACT</i> mutant to uncover gene expression and metabolic shifts associated with disease resistance. To identify <i>SDS2-</i>specific physiological changes related to pathogen resistance, leaf tissues from the <i>SDS2-ACT</i> mutant and the Kitkaake WT line were subjected to both transcriptomic and non-targeted metabolic profiling. Transcriptomic analyses identified 1497 differentially expressed genes (DEGs), including up-regulated genes involved in terpenoid and flavonoid biosynthesis, phytohormone signaling, and defense-related pathways (including pathogenesis-related [PR] genes). Metabolomic profiling revealed significant alterations in the accumulation of several compound classes, including putative: terpenoids, phenylpropanoids, phytohormones, fatty acids, and sugars. These changes are likely correlated with the observed cell death and resistance phenotypes in the SDS2-ACT mutant. This study provides an overall landscape of the transcriptomic and metabolomic alterations in a lesion mimic mutant, identifying candidate defense-related genes and metabolites for functional analysis in rice.https://www.mdpi.com/2223-7747/14/5/665rice blastcell deathmetabolomicstranscriptomicsterpenoidgibberellins
spellingShingle Pengfei Bai
Yanfang Liu
Laisa Gomes-Dias
Rachel Combs-Giroir
Shaoxing Dai
Naeyeoung Choi
Yun Lin
Matthew Bernier
Emmanuel Hatzakis
Guo-Liang Wang
Joshua J. Blakeslee
Integrated Transcriptomic and Metabolomic Analyses Reveal the Importance of the Terpenoid, Fatty Acid, and Flavonoid Pathways in Rice Cell Death and Defense
Plants
rice blast
cell death
metabolomics
transcriptomics
terpenoid
gibberellins
title Integrated Transcriptomic and Metabolomic Analyses Reveal the Importance of the Terpenoid, Fatty Acid, and Flavonoid Pathways in Rice Cell Death and Defense
title_full Integrated Transcriptomic and Metabolomic Analyses Reveal the Importance of the Terpenoid, Fatty Acid, and Flavonoid Pathways in Rice Cell Death and Defense
title_fullStr Integrated Transcriptomic and Metabolomic Analyses Reveal the Importance of the Terpenoid, Fatty Acid, and Flavonoid Pathways in Rice Cell Death and Defense
title_full_unstemmed Integrated Transcriptomic and Metabolomic Analyses Reveal the Importance of the Terpenoid, Fatty Acid, and Flavonoid Pathways in Rice Cell Death and Defense
title_short Integrated Transcriptomic and Metabolomic Analyses Reveal the Importance of the Terpenoid, Fatty Acid, and Flavonoid Pathways in Rice Cell Death and Defense
title_sort integrated transcriptomic and metabolomic analyses reveal the importance of the terpenoid fatty acid and flavonoid pathways in rice cell death and defense
topic rice blast
cell death
metabolomics
transcriptomics
terpenoid
gibberellins
url https://www.mdpi.com/2223-7747/14/5/665
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