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

Bai, Pengfei; Liu, Yanfang; Gomes-Dias, Laisa; Combs-Giroir, Rachel; Dai, Shaoxing; Choi, Naeyeoung; Lin, Yun; Bernier, Matthew; Hatzakis, Emmanuel; Wang, Guo-Liang; Blakeslee, Joshua J.

doi:10.3390/plants14050665

Open AccessArticle

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

by

Pengfei Bai

^1,†

,

Yanfang Liu

^1,2,†,

Laisa Gomes-Dias

^3,4,5,†

,

Rachel Combs-Giroir

^3,6,

Shaoxing Dai

⁷

,

Naeyeoung Choi

¹,

Yun Lin

^3,4,

Matthew Bernier

⁸,

Emmanuel Hatzakis

⁹,

Guo-Liang Wang

^1,*

and

Joshua J. Blakeslee

^3,4,7,*

¹

Department of Plant Pathology, The Ohio State University, Columbus, OH 43210, USA

²

Quality Standard and Testing Technology Research Institute, Yunnan Academy of Agricultural Sciences, Kunming 650200, China

³

Department of Horticulture and Crop Science, The Ohio State University, Columbus, OH 43210, USA

⁴

Laboratory for the Analysis of Metabolites from Plants (LAMP), The Ohio State University, Columbus, OH 43210, USA

⁵

Food Science and Technology Program, Federal University of Tocantins, Palmas 77001, TO, Brazil

⁶

Center for Applied Plant Sciences, The Ohio State University, Columbus, OH 43210, USA

⁷

Institute of Primate Translational Medicine, Kunming University of Science and Technology, Kunming 650500, China

⁸

Campus Chemical Instrumentation Center (CCIC), The Ohio State University, Columbus, OH 43210, USA

⁹

Department of Food Science and Technology, The Ohio State University, Columbus, OH 43210, USA

^*

Authors to whom correspondence should be addressed.

^†

These authors contributed equally to this work.

Plants 2025, 14(5), 665; https://doi.org/10.3390/plants14050665

Submission received: 30 January 2025 / Revised: 6 February 2025 / Accepted: 18 February 2025 / Published: 21 February 2025

(This article belongs to the Special Issue Plant Resistance against Bacterial and Fungal Pathogens: Mechanisms and Applications)

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Abstract

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, SPL11 cell-death suppressor 2 (SDS2), 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 SDS2-ACT mutant to uncover gene expression and metabolic shifts associated with disease resistance. To identify SDS2-specific physiological changes related to pathogen resistance, leaf tissues from the SDS2-ACT 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.

Keywords: rice blast; cell death; metabolomics; transcriptomics; terpenoid; gibberellins

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MDPI and ACS Style

Bai, P.; Liu, Y.; Gomes-Dias, L.; Combs-Giroir, R.; Dai, S.; Choi, N.; Lin, Y.; Bernier, M.; Hatzakis, E.; Wang, G.-L.; et al. Integrated Transcriptomic and Metabolomic Analyses Reveal the Importance of the Terpenoid, Fatty Acid, and Flavonoid Pathways in Rice Cell Death and Defense. Plants 2025, 14, 665. https://doi.org/10.3390/plants14050665

AMA Style

Bai P, Liu Y, Gomes-Dias L, Combs-Giroir R, Dai S, Choi N, Lin Y, Bernier M, Hatzakis E, Wang G-L, et al. Integrated Transcriptomic and Metabolomic Analyses Reveal the Importance of the Terpenoid, Fatty Acid, and Flavonoid Pathways in Rice Cell Death and Defense. Plants. 2025; 14(5):665. https://doi.org/10.3390/plants14050665

Chicago/Turabian Style

Bai, Pengfei, Yanfang Liu, Laisa Gomes-Dias, Rachel Combs-Giroir, Shaoxing Dai, Naeyeoung Choi, Yun Lin, Matthew Bernier, Emmanuel Hatzakis, Guo-Liang Wang, and et al. 2025. "Integrated Transcriptomic and Metabolomic Analyses Reveal the Importance of the Terpenoid, Fatty Acid, and Flavonoid Pathways in Rice Cell Death and Defense" Plants 14, no. 5: 665. https://doi.org/10.3390/plants14050665

APA Style

Bai, P., Liu, Y., Gomes-Dias, L., Combs-Giroir, R., Dai, S., Choi, N., Lin, Y., Bernier, M., Hatzakis, E., Wang, G.-L., & Blakeslee, J. J. (2025). Integrated Transcriptomic and Metabolomic Analyses Reveal the Importance of the Terpenoid, Fatty Acid, and Flavonoid Pathways in Rice Cell Death and Defense. Plants, 14(5), 665. https://doi.org/10.3390/plants14050665

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

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