Integration of transcriptomics, metabolomics, and hormone analysis revealed the formation of lesion spots inhibited by GA and CTK was related to cell death and disease resistance in bread wheat (Triticum aestivum L.)

Cong Li; Lei Yan; Qian Liu; Rong Tian; Surong Wang; Muhammad Faisal Umer; Muhammad Junaid Jalil; Md Nahibuzzaman Lohani; Yanlin Liu; Huaping Tang; Qiang Xu; Qiantao Jiang; Guoyue Chen; Pengfei Qi; Yunfeng Jiang; Lulu Gou; Qifu Yao; Youliang Zheng; Yuming Wei; Jian Ma

doi:10.1186/s12870-024-05212-3

BMC Plant Biology (Jun 2024)

Integration of transcriptomics, metabolomics, and hormone analysis revealed the formation of lesion spots inhibited by GA and CTK was related to cell death and disease resistance in bread wheat (Triticum aestivum L.)

Cong Li,
Lei Yan,
Qian Liu,
Rong Tian,
Surong Wang,
Muhammad Faisal Umer,
Muhammad Junaid Jalil,
Md Nahibuzzaman Lohani,
Yanlin Liu,
Huaping Tang,
Qiang Xu,
Qiantao Jiang,
Guoyue Chen,
Pengfei Qi,
Yunfeng Jiang,
Lulu Gou,
Qifu Yao,
Youliang Zheng,
Yuming Wei,
Jian Ma

Affiliations

Cong Li: State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University
Lei Yan: State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University
Qian Liu: State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University
Rong Tian: State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University
Surong Wang: State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University
Muhammad Faisal Umer: State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University
Muhammad Junaid Jalil: State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University
Md Nahibuzzaman Lohani: State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University
Yanlin Liu: State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University
Huaping Tang: State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University
Qiang Xu: State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University
Qiantao Jiang: State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University
Guoyue Chen: State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University
Pengfei Qi: State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University
Yunfeng Jiang: State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University
Lulu Gou: State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University
Qifu Yao: College of Agroforestry Engineering and Planning, Guizhou Key Laboratory of Biodiversity Conservation and Utilization in the Fanjing Mountain Region, Tongren University
Youliang Zheng: State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University
Yuming Wei: State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University
Jian Ma: State Key Laboratory of Crop Gene Exploration and Utilization in Southwest China, Sichuan Agricultural University

DOI: https://doi.org/10.1186/s12870-024-05212-3
Journal volume & issue: Vol. 24, no. 1
pp. 1 – 14

Abstract

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Abstract Background Wheat is one of the important grain crops in the world. The formation of lesion spots related to cell death is involved in disease resistance, whereas the regulatory pathway of lesion spot production and resistance mechanism to pathogens in wheat is largely unknown. Results In this study, a pair of NILs (NIL-Lm5 W and NIL-Lm5 M) was constructed from the BC1F4 population by the wheat lesion mimic mutant MC21 and its wild genotype Chuannong 16. The formation of lesion spots in NIL-Lm5 M significantly increased its resistance to stripe rust, and NIL-Lm5 M showed superiour agronomic traits than NIL-Lm5 W under stripe rust infection.Whereafter, the NILs were subjected to transcriptomic (stage N: no spots; stage S, only a few spots; and stage M, numerous spots), metabolomic (stage N and S), and hormone analysis (stage S), with samples taken from normal plants in the field. Transcriptomic analysis showed that the differentially expressed genes were enriched in plant-pathogen interaction, and defense-related genes were significantly upregulated following the formation of lesion spots. Metabolomic analysis showed that the differentially accumulated metabolites were enriched in energy metabolism, including amino acid metabolism, carbohydrate metabolism, and lipid metabolism. Correlation network diagrams of transcriptomic and metabolomic showed that they were both enriched in energy metabolism. Additionally, the contents of gibberellin A7, cis-Zeatin, and abscisic acid were decreased in leaves upon lesion spot formation, whereas the lesion spots in NIL-Lm5 M leaves were restrained by spaying GA and cytokinin (CTK, trans-zeatin) in the field. Conclusion The formation of lesion spots can result in cell death and enhance strip rust resistance by protein degradation pathway and defense-related genes overexpression in wheat. Besides, the formation of lesion spots was significantly affected by GA and CTK. Altogether, these results may contribute to the understanding of lesion spot formation in wheat and laid a foundation for regulating the resistance mechanism to stripe rust.

Published in BMC Plant Biology

ISSN: 1471-2229 (Online)
Publisher: BMC
Country of publisher: United Kingdom
LCC subjects: Science: Botany
Website: http://bmcplantbiol.biomedcentral.com

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