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Arabidopsis transcriptomic analysis reveals cesium inhibition of root growth involves abscisic acid signaling

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Abstract

Main conclusion

This is the first report on the involvement of abscisic acid signaling in regulating post-germination growth under Cs stress, not related to potassium deficiency.

Abstract

Cesium (Cs) is known to exert toxicity in plants by competition and interference with the transport of potassium (K). However, the precise mechanism of how Cs mediates its damaging effect is still unclear. This fact is mainly attributed to the large effects of lower K uptake in the presence of Cs that shadow other crucial effects by Cs that were not related to K. RNA-seq was conducted on Arabidopsis roots grown to identify putative genes that are functionally involved to investigate the difference between Cs stress and low K stress. Our transcriptome data demonstrated Cs-regulated genes only partially overlap to low K-regulated genes. In addition, the divergent expression trend of High-affinity K+ Transporter (HAK5) from D4 to D7 growth stage suggested participation of other molecular events besides low K uptake under Cs stress. Potassium deficiency triggers expression level change of the extracellular matrix, transfer/carrier, cell adhesion, calcium-binding, and DNA metabolism genes. Under Cs stress, genes encoding translational proteins, chromatin regulatory proteins, membrane trafficking proteins and defense immunity proteins were found to be primarily regulated. Pathway enrichment and protein network analyses of transcriptome data exhibit that Cs availability are associated with alteration of abscisic acid (ABA) signaling, photosynthesis activities and nitrogen metabolism. The phenotype response of ABA signaling mutants supported the observation and revealed Cs inhibition of root growth involved in ABA signaling pathway. The rather contrary response of loss-of-function mutant of Late Embryogenesis Abundant 7 (LEA7) and Translocator Protein (TSPO) further suggested low K stress and Cs stress may activate different salt tolerance responses. Further investigation on the crosstalk between K transport, signaling, and salt stress-responsive signal transduction will provide a deeper understanding of the mechanisms and molecular regulation underlying Cs toxicity.

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Data availability

The RNA-seq data were submitted to NCBI Gene Expression Omnibus (GEO): GSE214426.

Abbreviations

ABI5:

ABA insensitive 5

ABR:

ABA-response protein

AHG1:

ABA-hypersensitive germination 1

CsCl:

Cesium chloride

DEGs:

Differentially expressed genes

HAI3:

Highly ABA-induced PP2C gene 3

HAK5:

High-affinity K + transporter 5

LEA7:

Late embryogenesis abundant 7

TSPO:

Translocator protein

References

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Funding

This work was supported by the RIKEN CSRS research fund.

Author information

Authors and Affiliations

Authors

Contributions

OWD and YM performed transcriptome data analyses. OWD conducted validation experiments and drafted the manuscript. TM conducted genotyping test of mutants. MM participated in the coordination of the study. RS conceived, revised, and edited the manuscript. All authors have read and approved the final manuscript for submission.

Corresponding author

Correspondence to Ryoung Shin.

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Conflict of interest

All authors declare that we have no significant competing financial or professional interests that might have affected the work and presentation described in this manuscript.

Additional information

Communicated by Dorothea Bartels.

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Supplementary Information

Below is the link to the electronic supplementary material.

425_2023_4304_MOESM1_ESM.xlsx

Supplementary file1 Suppl. Data S1 List of differentially expressed genes with a false discovery rate of P < 0.05 and showing more than a 2-fold change in expression. (XLSX 263 kb)

Supplementary file2 Suppl. Fig. S1 An overview of root sample preparation for RNA sequencing. (JPG 686 kb)

425_2023_4304_MOESM3_ESM.jpg

Supplementary file3 Suppl. Fig. S2 Gene Ontology (GO) annotation of the genes with a significant fold change and false discovery cut-off. The charts represent the association of the low K-induced and Cs-induced genes in the molecular function (a), biological processes (b), and cellular components (c). Percentage represents the proportion of each GO term. (JPG 1237 kb)

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Supplementary file4 Suppl. Fig. S3 Protein–protein interaction string network of low-K-induced DEGs related to nitrogen metabolism, photosynthesis, glucosinolate biosynthesis, flavonoid biosynthesis, pentose and glucuronate interconversions and plant hormone signal transduction. (JPG 1644 kb)

425_2023_4304_MOESM5_ESM.jpg

Supplementary file5 Suppl. Fig. S4 A representative of 8-day-old seedlings (WT and mutants) grown under low K and Cs conditions. (JPG 3119 kb)

Supplementary file6 (DOCX 13 kb)

Supplementary file7 (DOCX 15 kb)

Supplementary file8 (DOCX 14 kb)

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Ong, WD., Makita, Y., Miyazaki, T. et al. Arabidopsis transcriptomic analysis reveals cesium inhibition of root growth involves abscisic acid signaling. Planta 259, 36 (2024). https://doi.org/10.1007/s00425-023-04304-y

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  • DOI: https://doi.org/10.1007/s00425-023-04304-y

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