Skip to main content
Log in

Transcriptome analysis and identification of the low potassium stress-responsive gene SiSnRK2.6 in foxtail millet (Setaria italica L.)

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

The transcriptome is beneficial for dissecting the mechanism of millet in response to low potassium stress and SiSnRK2.6 was identified as a potential target for improving low potassium stress tolerance.

Abstract

Foxtail millet (Setaria italica L.), which originated in China, has high nutrient utilization character. Nevertheless, the molecular mechanism of its tolerance to low potassium stress is largely unclear. In this research, the low potassium tolerant variety “Yugu28” was screened out by low potassium stress treatment, and the transcriptome of “Yugu28” under low potassium stress was comprehensively analyzed. A total of 4254 differentially expressed genes (DEGs) were identified, including 1618 up-regulated and 2636 down-regulated genes, respectively. In addition, there were 302 transcription factor (TF) genes in the DEGs and MYB TFs accounted for the highest proportion, which was 14.9%. After functional analysis of all DEGs, a total of 7 genes involved in potassium transport and potassium ion channels and 50 genes corresponding to hormones were screened. The expression levels of randomly selected 17 DEGs were verified by qRT-PCR and the results coincided well with the RNA-seq analysis, indicating the reliability of our transcriptome data. Moreover, one of the ABA signaling pathway genes, SiSnRK2.6, was identified and selected for further functional verification. Compared with the wild type, transgenic rice with ecotopic expression of SiSnRK2.6 showed remarkably increased root length and root number, indicating that overexpression of SiSnRK2.6 can enhance the resistance of transgenic plants to low potassium stress.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

All data supporting the conclusions of this article are provided within the article and its Supplementary Information. The transcriptome data used in the current study are available in the National Center for Biotechnology Information (NCBI) Sequence Read Archive (SRA) database (https://www.ncbi.nlm.nih.gov/sra) (accession number: PRJNA1052939).

References

  • Agarwal M, Hao Y, Kapoor A, Dong C, Fujii H, Zheng X, Zhu J (2006) A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J Biol Chem 281:37636–37645

    Article  CAS  PubMed  Google Scholar 

  • Ahmad I, Mian A, Maathuis F (2016) Overexpression of the rice AKT1 potassium channel affects potassium nutrition and rice drought tolerance. J Exp Bot 67:2689–2698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ashley M, Grant M, Grabov A (2006) Plant responses to potassium deficiencies: a role for potassium transport proteins. J Exp Bot 57:425–436

    Article  CAS  PubMed  Google Scholar 

  • Bañuelos M, Garciadeblas B, Cubero B, Rodrıguez-Navarro A (2002) Inventory and functional characterization of the HAK potassium transporters of rice. Plant Physiol 130:784–795

    Article  PubMed  PubMed Central  Google Scholar 

  • Boscari A, Clement M, Volkov V, Golldack D, Hybiak J, Miller A, Amtmann A, Fricke W (2009) Potassium channels in barley: cloning, functional characterization and expression analyses in relation to growth and development. Plant Cell Environ 32:1761–1777

    Article  CAS  PubMed  Google Scholar 

  • Buschmann P, Vaidyanathan R, Gassmann W, Schroeder J (2000) Enhancement of Na+ uptake currents, time-dependent inward-rectifying K+ channel currents, and K+ channel transcripts by K+ starvation in wheat root cells. Plant Physiol 122:1387–1397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cakmak I (2005) The role of potassium in alleviating detrimental effects of abiotic stresses in plants. J Plant Nutr Soil Sc 168:521–530

    Article  CAS  Google Scholar 

  • Cao X, Hu L, Chen X, Zhang R, Cheng D, Li H, Xu Z, Li L, Zhou Y, Liu A, Song J, Liu C, Liu J, Zhao Z, Chen M, Ma Y (2019) Genome-wide analysis and identification of the low potassium stress responsive gene SiMYB3 in foxtail millet (Setaria italica L.). BMC Genomics 20:136–149

    Article  PubMed  PubMed Central  Google Scholar 

  • Chérel I, Lefoulon C, Boeglin M, Sentenac H (2014) Molecular mechanisms involved in plant adaptation to low K+ availability. J Exp Bot 65:833–848

    Article  PubMed  Google Scholar 

  • Cutler S, Rodriguez P, Finkelstein R, Abrams S (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679

    Article  CAS  PubMed  Google Scholar 

  • Ding Z, Li S, An X, Liu X, Qin H, Wang D (2009) Transgenic expression of MYB15 confers enhanced sensitivity to abscisic acid and improved drought tolerance in Arabidopsis thaliana. J Genet Genomics 36:17–29

    Article  CAS  PubMed  Google Scholar 

  • Du Q, Zhao X, Xia L, Jiang C, Wang X, Han Y, Wang J, Yu H (2019) Effects of potassium deficiency on photosynthesis, chloroplast ultrastructure, ROS, and antioxidant activities in maize (Zea mays L.). J Integr Agr 18:395–406

    Article  CAS  Google Scholar 

  • Fernando R, Nettleton D, Southey B, Dekkers J, Rothschild M, Soller M (2004) Controlling the proportion of false positives in multiple dependent tests. Genetics 166:611–619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fuchs I, Stolzle S, Ivashikina N, Hedrich R (2005) Rice K+ uptake channel OsAKT1 is sensitive to salt stress. Planta 221:212–221

    Article  CAS  PubMed  Google Scholar 

  • Garciadeblas B, Benito B, Rodríguez-Navarro A (2002) Molecular cloning and functional expression in bacteria of the potassium transporters CnHAK1 and CnHAK2 of the seagrass Cymodocea nodosa. Plant Mol Biol 50:623–633

    Article  CAS  PubMed  Google Scholar 

  • Gierth M, Mäser P, Schroeder J, (2005) The potassium transporter AtHAK5 functions in K+ deprivation-induced high-affinity K+ uptake and AKT1 K+ channel contribution to K+ uptake kinetics in Arabidopsis roots. Plant Physiol 137:1105–1114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han M, Wu W, Wu W, Wang Y (2016) Potassium transporter KUP7 is involved in K+ acquisition and translocation in Arabidopsis root under K+-limited conditions. Mol Plant 9:437–446

    Article  CAS  PubMed  Google Scholar 

  • Hirsch R, Lewis B, Spalding E, Sussman M (1998) A role for the AKT1 potassium channel in plant nutrition. Science 280:918–921

    Article  CAS  PubMed  ADS  Google Scholar 

  • Huang W, Jiang W, Yao Y, Song X, Liu Y, Chen S, Zhao D, Wu G, Yuan H, Ren C, Sun Z, Wu J, Kang Q (2021) Transcriptome profiling of flax (Linum usttatissimum L.) response to low potassium stress. Acta Agron Sin 47:1070–1081

    Google Scholar 

  • Kim D, Langmead B, Salzberg S (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Long Y, Qi G, Li J, Xu Z, Wu W, Wang Y (2014) The Os-AKT1 channel is critical for K+ uptake in rice roots and is modulated by the rice CBL1-CIPK23 complex. Plant Cell 26:3387–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li W, Xu G, Abdel A, Yu L (2018) Plant HAK/KUP/KT K+ transporters: function and regulation. Cell Develop Biolo 74:133–141

    CAS  Google Scholar 

  • Li Y, Feng Z, Wei H, Cheng S, Hao P, Yu S, Wang H (2021) Silencing of GhKEA4 and GhKEA12 revealed their potential functions under salt and potassium stresses in upland cotton. Front Plant Sci 12:789775–789795

    Article  PubMed  PubMed Central  Google Scholar 

  • Liao Y, Smyth G, Shi W (2014) featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30:923–930

    Article  CAS  PubMed  Google Scholar 

  • Livak K, Schmittgen T (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lopez-Bucio J, Cruz-Ramirez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Cur Opin Plant Biolo 6:280–287

    Article  CAS  Google Scholar 

  • Ma Q, Dai X, Xu Y, Guo J, Liu Y, Chen N, Xiao J, Zhang D, Xu Z, Zhang X, Chong K (2009) Enhanced tolerance to chilling stress in OsMYB3R-2 transgenic rice is mediated by alteration in cell cycle and ectopic expression of stress genes. Plant Physiol 150:244–256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maathuis F, Sanders D (1997) Regulation of K+ absorption in plant root cells by external K+: interplay of different plasma membrane K+ transporters. J Exp Bot 48:451–458

    Article  CAS  PubMed  Google Scholar 

  • Mortazavi A, Williams B, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628

    Article  CAS  PubMed  Google Scholar 

  • Mustilli A, Merlot S, Vavasseur A, Fenzi F, Giraudat J (2002) Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14:3089–3099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nadeem F, Ahmad Z, Wang R, Han J, Shen Q, Chang F, Diao X, Zhang F, Li×, (2018) Foxtail millet [Setaria italica (L.) Beauv.] grown under low nitrogen shows a smaller root system, enhanced biomass accumulation, and nitrate transporter expression. Front Plant Sci 9:205–217

    Article  PubMed  PubMed Central  Google Scholar 

  • Okada T, Nakayama H, Shinmyo A, Yoshida K (2008) Expression of OsHAK genes encoding potassium ion transporters in rice. Plant Biotechnol 25:241–245

    Article  CAS  Google Scholar 

  • Pasquali G, Biricolti S, Locatelli F, Baldoni E, Mattana M (2008) Osmyb4 expression improves adaptive responses to drought and cold stress in transgenic apples. Plant Cell Rep 27:1677–1686

    Article  CAS  PubMed  Google Scholar 

  • Philippar K, Fuchs I, Luthen H, Hoth S, Bauer C, Haga K, Thiel G, Ljung K, Sandberg G, Bottger M, Becker D, Hedrich R (1999) Auxin-induced K+ channel expression represents an essential step in coleoptile growth and gravitropism. Proc Natl Acad Sci U S A 96:12186–12191

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Robinson M, McCarthy D, Smyth G (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140

    Article  CAS  PubMed  Google Scholar 

  • Römheld V, Kirkby E (2010) Research on potassium in agriculture: needs and prospects. Plant Soil 335:155–180

    Article  Google Scholar 

  • Santa-Maria G, Rubio F, Dubcovsky J, Rodriguez-Navarro A (1997) The HAK1 gene of barley is a member of a large gene family and encodes a high-affinity potassium transporter. Plant Cell 9:2281–2289

    CAS  PubMed  PubMed Central  Google Scholar 

  • Senn ME, Rubio F, Bañuelos M, Rodrıguez-Navarro A (2001) Comparative functional features of plant potassium HvHAK1 and HvHAK2 transporters. J Biol Chem 276:44563–44569

    Article  CAS  PubMed  Google Scholar 

  • Shaibur M, Shamim A, Kawai S (2008) Growth response of hydroponic rice seedlings at elevated concentrations of potassium chloride. J Agric Rural Dev 6:43–53

    Google Scholar 

  • Singh K, Foley R, Onate-Sanchez L (2002) Transcription factors in plant defense and stress responses. Cur Opin Plant Biolo 5:430–436

    Article  CAS  Google Scholar 

  • Spalding E, Hirsch R, Lewis D, Qi Z, Sussman M, Lewis B (1999) Potassium uptake supporting plant growth in the absence of AKT1 channel activity. J Gen Physiol 113:909–918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waadt R, Seller C, Hsu P, Takahashi Y, Munemasa S, Schroeder J (2022) Plant hormone regulation of abiotic stress responses. Nat Rev Mol Cell Biol 23:680–694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Wu W (2013) Potassium transport and signaling in higher plants. Annu Rev Plant Biol 64:41–426

    Article  Google Scholar 

  • Wang E, Hu L, Xue F, Li W, Xu Z, Li L, Zhou Y, Ma Y, Diao X, Jia G, Chen M, Min D (2015) Overexpression of millet transcription factor gene SiNAC45 to response of low potassium stress and ABA treatment in transgenic Arabidopsis. Acta Agron Sin 41:1445–1453

    Article  CAS  Google Scholar 

  • Wang X, Chen L, Liu W, Shen L, Wang F, Zhou Y, Zhang Z, Wu W, Wang Y (2016) AtKC1 and CIPK23 synergistically modulate AKT1-mediated low-potassium stress responses in Arabidopsis. Plant Physiol 170:2264–2277

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Li J, Li F, Pan Y, Cai D, Mao D, Chen L, Luan S (2021) Rice potassium transporter OsHAK8 mediates K+ uptake and translocation in response to low K+ stress. Front Plant Sci 12:730002–730014

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu J, Li H, Chen L, Wang Y, Liu L, He L, Wu W (2006) A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125:1347–1360

    Article  CAS  PubMed  Google Scholar 

  • Yang Y, Liu J, Wang W, Li LA, Ye Z, Yang Y (2003) Genotypic differences and some associated plant traits in potassium internal use efficiency of lowland rice (Oryza sativa L.). Nutr Cycl Agroecosys 67:273–282

    Article  CAS  Google Scholar 

  • Yi F, Huo M, Li J, Yu J (2022) Time-series transcriptomics reveals a drought-responsive temporal network and crosstalk between drought stress and the circadian clock in foxtail millet. Plant J 110:1213–1228

    Article  CAS  PubMed  Google Scholar 

  • Yoshida R, Hobo T, Ichimura K, Mizoguchi T, Takahashi F, Aronso J, Ecker J, Shinozaki K (2002) ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. Plant Cell Physiol 43:1473–1483

    Article  CAS  PubMed  Google Scholar 

  • Young E, Dombek K, Tachibana C, Ideker T (2003) Multiple pathways are co-regulated by the protein kinase Snf1 and the transcription factors Adr1 and Cat8. J Biol Chem 278:26146–26158

    Article  CAS  PubMed  Google Scholar 

  • Zhao S, Zhang M, Ma T, Wang Y (2016) Phosphorylation of ARF2 relieves its repression of transcription of the K+ transporter gene HAK5 in response to low potassium stress. Plant Cell 28:3005–3019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zimmermann S, Talke I, Ehrhardt T, Nast G, Muller-Rober B (1998) Characterization of SKT1, an inwardly rectifying potassium channel from potato, by heterologous expression in insect cells. Plant Physiol 116:879–890

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Najeeb Ullah Khan from China Agriculture University for improving the article’s English.

Funding

This research was supported by the PhD Research Startup Foundation of Henan University of Science and Technology (13480103), the Funding of Joint Research on Agricultural Variety Improvement of Henan Province (No.2022010401), and the Funding of Central Guides Local Science and Technology Development of Henan Province (Z20221341070).

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception and design. XM and JL designed the research. Material preparation, data collection and analysis were performed by XM, SD and NQ. ZH and BG provided technical assistance to XM. The first draft of the manuscript was written by XM, NUK conceived and supervised the writing and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Junxia Li.

Ethics declarations

Conflict of interest

The authors have no relevant financial or non-financial interests to disclose.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Ethical approval

Not applicable.

Additional information

Communicated by Hai-Chun Jing.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ma, X., Khan, N.U., Dai, S. et al. Transcriptome analysis and identification of the low potassium stress-responsive gene SiSnRK2.6 in foxtail millet (Setaria italica L.). Theor Appl Genet 137, 22 (2024). https://doi.org/10.1007/s00122-023-04532-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00122-023-04532-6

Navigation