Integrated transcriptome and metabolome analyses reveals the mechanisms of function loss of Lr29 leaf rust resistance gene at high temperatures in wheat

Leaf rust (LR) is one of the most common diseases of wheat. The resistance gene Lr29 provides wide resistance to LR, but loses its function under high temperatures. Despite the importance of this gene, the mechanism of resistance is unclear. In this study we investigated the resistance mechanism of...

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Main Authors: Liwen Wang, Yang Yu, Hang Li, Mingzhu Lu, Shubo Cao, Ziqi Li, Haoyuan Song, Laszlo Purnhauser, Jinlong Li, Jiajie Wu
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.2025.1537921/full
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author Liwen Wang
Yang Yu
Hang Li
Mingzhu Lu
Shubo Cao
Ziqi Li
Haoyuan Song
Laszlo Purnhauser
Jinlong Li
Jiajie Wu
author_facet Liwen Wang
Yang Yu
Hang Li
Mingzhu Lu
Shubo Cao
Ziqi Li
Haoyuan Song
Laszlo Purnhauser
Jinlong Li
Jiajie Wu
author_sort Liwen Wang
collection DOAJ
description Leaf rust (LR) is one of the most common diseases of wheat. The resistance gene Lr29 provides wide resistance to LR, but loses its function under high temperatures. Despite the importance of this gene, the mechanism of resistance is unclear. In this study we investigated the resistance mechanism of the Lr29 gene to LR at the seedling stage, as well as the reasons behind the loss of gene function at high temperatures by using integrated transcriptome and metabolome analyses. Results suggests that the pathways of reactive oxygen species (ROS), which could be due to expression of genes including LOX (lipoxygenase), APX (ascorbate peroxidase) and GST (glutathione S-transferase), play a key role in the resistance of Lr29 to LR, furthermore flavonoids, such as epicatechin, cosmosiin, apiin, vitexin and rutin, were identified as the key metabolites linked to Lr29 resistance. We also found that, at high temperatures, Lr29 downregulated the genes and metabolites associated with glycolysis and the tricarboxylic acid (TCA) cycle, while genes and metabolites related to the shikimic acid pathway were upregulated. This study might provide a valuable theoretical foundation for the cloning of the Lr29 gene, the analysis of its disease resistance mechanism, and the understanding of how temperature affects gene function.
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spelling doaj-art-37130add8ac84e9fa694bcffaff45eca2025-08-20T02:03:36ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2025-02-011610.3389/fpls.2025.15379211537921Integrated transcriptome and metabolome analyses reveals the mechanisms of function loss of Lr29 leaf rust resistance gene at high temperatures in wheatLiwen Wang0Yang Yu1Hang Li2Mingzhu Lu3Shubo Cao4Ziqi Li5Haoyuan Song6Laszlo Purnhauser7Jinlong Li8Jiajie Wu9State Key Laboratory of Wheat Improvement, College of Agronomy, Shandong Agricultural University, Tai’an, ChinaState Key Laboratory of Wheat Improvement, College of Agronomy, Shandong Agricultural University, Tai’an, ChinaState Key Laboratory of Wheat Improvement, College of Agronomy, Shandong Agricultural University, Tai’an, ChinaState Key Laboratory of Wheat Improvement, College of Agronomy, Shandong Agricultural University, Tai’an, ChinaState Key Laboratory of Wheat Improvement, College of Agronomy, Shandong Agricultural University, Tai’an, ChinaState Key Laboratory of Wheat Improvement, College of Agronomy, Shandong Agricultural University, Tai’an, ChinaState Key Laboratory of Wheat Improvement, College of Agronomy, Shandong Agricultural University, Tai’an, ChinaLaboratory of Plant Pathology, Cereal Research Non-Profit Co. Ltd., Szeged, HungaryState Key Laboratory of Wheat Improvement, College of Agronomy, Shandong Agricultural University, Tai’an, ChinaState Key Laboratory of Wheat Improvement, College of Agronomy, Shandong Agricultural University, Tai’an, ChinaLeaf rust (LR) is one of the most common diseases of wheat. The resistance gene Lr29 provides wide resistance to LR, but loses its function under high temperatures. Despite the importance of this gene, the mechanism of resistance is unclear. In this study we investigated the resistance mechanism of the Lr29 gene to LR at the seedling stage, as well as the reasons behind the loss of gene function at high temperatures by using integrated transcriptome and metabolome analyses. Results suggests that the pathways of reactive oxygen species (ROS), which could be due to expression of genes including LOX (lipoxygenase), APX (ascorbate peroxidase) and GST (glutathione S-transferase), play a key role in the resistance of Lr29 to LR, furthermore flavonoids, such as epicatechin, cosmosiin, apiin, vitexin and rutin, were identified as the key metabolites linked to Lr29 resistance. We also found that, at high temperatures, Lr29 downregulated the genes and metabolites associated with glycolysis and the tricarboxylic acid (TCA) cycle, while genes and metabolites related to the shikimic acid pathway were upregulated. This study might provide a valuable theoretical foundation for the cloning of the Lr29 gene, the analysis of its disease resistance mechanism, and the understanding of how temperature affects gene function.https://www.frontiersin.org/articles/10.3389/fpls.2025.1537921/fulldifferentially expressed genesLr29 genemetabolomePuccinia triticinatemperaturestranscriptome
spellingShingle Liwen Wang
Yang Yu
Hang Li
Mingzhu Lu
Shubo Cao
Ziqi Li
Haoyuan Song
Laszlo Purnhauser
Jinlong Li
Jiajie Wu
Integrated transcriptome and metabolome analyses reveals the mechanisms of function loss of Lr29 leaf rust resistance gene at high temperatures in wheat
Frontiers in Plant Science
differentially expressed genes
Lr29 gene
metabolome
Puccinia triticina
temperatures
transcriptome
title Integrated transcriptome and metabolome analyses reveals the mechanisms of function loss of Lr29 leaf rust resistance gene at high temperatures in wheat
title_full Integrated transcriptome and metabolome analyses reveals the mechanisms of function loss of Lr29 leaf rust resistance gene at high temperatures in wheat
title_fullStr Integrated transcriptome and metabolome analyses reveals the mechanisms of function loss of Lr29 leaf rust resistance gene at high temperatures in wheat
title_full_unstemmed Integrated transcriptome and metabolome analyses reveals the mechanisms of function loss of Lr29 leaf rust resistance gene at high temperatures in wheat
title_short Integrated transcriptome and metabolome analyses reveals the mechanisms of function loss of Lr29 leaf rust resistance gene at high temperatures in wheat
title_sort integrated transcriptome and metabolome analyses reveals the mechanisms of function loss of lr29 leaf rust resistance gene at high temperatures in wheat
topic differentially expressed genes
Lr29 gene
metabolome
Puccinia triticina
temperatures
transcriptome
url https://www.frontiersin.org/articles/10.3389/fpls.2025.1537921/full
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