Defective cytokinin signaling reprograms lipid and flavonoid gene-to-metabolite networks to mitigate high salinity in Arabidopsis

Cytokinin (CK) in plants regulates both developmental processes and adaptation to environmental stresses. and type-B triple mutants are almost completely defective in CK signaling, and the mutant was reported to be salt tolerant. Here, we demonstrate that the mutant is also more tolerant to salt str...

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Published in:Proceedings of the National Academy of Sciences - PNAS 2021-11, Vol.118 (48)
Main Authors: Abdelrahman, Mostafa, Nishiyama, Rie, Tran, Cuong Duy, Kusano, Miyako, Nakabayashi, Ryo, Okazaki, Yozo, Matsuda, Fumio, Chávez Montes, Ricardo A, Mostofa, Mohammad Golam, Li, Weiqiang, Watanabe, Yasuko, Fukushima, Atsushi, Tanaka, Maho, Seki, Motoaki, Saito, Kazuki, Herrera-Estrella, Luis, Tran, Lam-Son Phan
Format: Article
Language:English
Subjects:
Adaptation, Physiological - genetics
Amino acids
Anthocyanins
Arabidopsis
Arabidopsis - metabolism
Arabidopsis Proteins - metabolism
Biological Sciences
Chain branching
Cytokinins
Cytokinins - metabolism
Cytokinins - physiology
Environmental stress
Flavonoids
Flavonoids - genetics
Flavonoids - metabolism
Food security
Gene Expression - genetics
Gene Expression Profiling - methods
Gene Expression Regulation - drug effects
Gene Expression Regulation - genetics
Gene Expression Regulation, Plant - genetics
Gene Regulatory Networks - genetics
Histidine
Lipid metabolism
Lipid Metabolism - genetics
Lipid Metabolism - physiology
Lipids
Lipids - physiology
Metabolic pathways
Metabolites
Metabolomics - methods
Mutants
Prestressing
Salinity
Salinity effects
Salinity tolerance
Salt
Salt Stress - genetics
Salt Stress - physiology
Salt tolerance
Salt Tolerance - genetics
Signal Transduction - physiology
Signaling
Sterols
Stress, Physiological - genetics
Sugar
Transcription
Transcriptomes
Trehalose
Triglycerides
γ-Aminobutyric acid
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Summary:Cytokinin (CK) in plants regulates both developmental processes and adaptation to environmental stresses. and type-B triple mutants are almost completely defective in CK signaling, and the mutant was reported to be salt tolerant. Here, we demonstrate that the mutant is also more tolerant to salt stress than wild-type (WT) plants. A comprehensive metabolite profiling coupled with transcriptome analysis of the and mutants was conducted to elucidate the salt tolerance mechanisms mediated by CK signaling. Numerous primary (e.g., sugars, amino acids, and lipids) and secondary (e.g., flavonoids and sterols) metabolites accumulated in these mutants under nonsaline and saline conditions, suggesting that both prestress and poststress accumulations of stress-related metabolites contribute to improved salt tolerance in CK-signaling mutants. Specifically, the levels of sugars (e.g., trehalose and galactinol), amino acids (e.g., branched-chain amino acids and γ-aminobutyric acid), anthocyanins, sterols, and unsaturated triacylglycerols were higher in the mutant plants than in WT plants. Notably, the reprograming of flavonoid and lipid pools was highly coordinated and concomitant with the changes in transcriptional levels, indicating that these metabolic pathways are transcriptionally regulated by CK signaling. The discovery of the regulatory role of CK signaling on membrane lipid reprogramming provides a greater understanding of CK-mediated salt tolerance in plants. This knowledge will contribute to the development of salt-tolerant crops with the ability to withstand salinity as a key driver to ensure global food security in the era of climate crisis.
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.2105021118