SRK2C, a SNF1-related Protein Kinase 2, Improves Drought Tolerance by Controlling Stress-responsive Gene Expression in Arabidopsis Thaliana

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2004 Nov 25

PMID 15561775

Citations 123

Authors

Taishi Umezawa

Riichiro Yoshida

Kyonoshin Maruyama

Kazuko Yamaguchi-Shinozaki

Kazuo Shinozaki

Affiliations

Soon will be listed here.

Abstract

Protein phosphorylation/dephosphorylation are major signaling events induced by osmotic stress in higher plants. Here, we showed that a SNF1-related protein kinase 2 (SnRK2), SRK2C, is an osmotic-stress-activated protein kinase in Arabidopsis thaliana that can significantly impact drought tolerance of Arabidopsis plants. Knockout mutants of SRK2C exhibited drought hypersensitivity in their roots, suggesting that SRK2C is a positive regulator of drought tolerance in Arabidopsis roots. Additionally, transgenic plants with CaMV35S promoter::SRK2C-GFP displayed higher overall drought tolerance than control plants. Whereas stomatal regulation in 35S::SRK2C-GFP plants was not altered, microarray analysis revealed that their drought tolerance coincided with up-regulation of many stress-responsive genes, for example, RD29A, COR15A, and DREB1A/CBF3. From these results, we concluded that SRK2C is capable of mediating signals initiated during drought stress, resulting in appropriate gene expression. Our present study reveals new insights around signal output from osmotic-stress-activated SnRK2 protein kinase as well as supporting feasibility of manipulating SnRK2 toward improving plant osmotic-stress tolerance.

Citing Articles

Comparative physiological and transcriptomic analyses reveal genotype specific response to drought stress in Siberian wildrye (Elymus sibiricus).

An Y, Wang Q, Cui Y, Liu X, Wang P, Zhou Y Sci Rep. 2024; 14(1):21060.

PMID: 39256456 PMC: 11387644. DOI: 10.1038/s41598-024-71847-9.

Interaction of Soybean ( (L.) ) Class II ACBPs with MPK2 and SAPK2 Kinases: New Insights into the Regulatory Mechanisms of Plant ACBPs.

Moradi A, Lung S, Chye M Plants (Basel). 2024; 13(8).

PMID: 38674555 PMC: 11055065. DOI: 10.3390/plants13081146.

Grape SnRK2.7 Positively Regulates Drought Tolerance in Transgenic .

Lan G, Ma W, Nai G, Liang G, Lu S, Ma Z Int J Mol Sci. 2024; 25(8).

PMID: 38674058 PMC: 11049990. DOI: 10.3390/ijms25084473.

Characterization of sucrose nonfermenting-1-related protein kinase 2 (SnRK2) gene family in Haynaldia villosa demonstrated SnRK2.9-V enhances drought and salt stress tolerance of common wheat.

Liu J, Wei L, Wu Y, Wang Z, Wang H, Xiao J BMC Genomics. 2024; 25(1):209.

PMID: 38408894 PMC: 10895793. DOI: 10.1186/s12864-024-10114-7.

Heterogeneous Expression of Subclass II of SNF1-Related Kinase 2 Improves Drought Tolerance via Stomatal Regulation in Poplar.

Horvat B, Shikakura Y, Ohtani M, Demura T, Kikuchi A, Watanabe K Life (Basel). 2024; 14(1).

PMID: 38276290 PMC: 10817443. DOI: 10.3390/life14010161.

References

Ichimura K, Mizoguchi T, Yoshida R, Yuasa T, Shinozaki K . Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant J. 2000; 24(5):655-65. DOI: 10.1046/j.1365-313x.2000.00913.x. View

Knight H, Zarka D, Okamoto H, Thomashow M, Knight M . Abscisic acid induces CBF gene transcription and subsequent induction of cold-regulated genes via the CRT promoter element. Plant Physiol. 2004; 135(3):1710-7. PMC: 519084. DOI: 10.1104/pp.104.043562. View

Gilmour S, Zarka D, Stockinger E, Salazar M, Houghton J, Thomashow M . Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. Plant J. 1999; 16(4):433-42. DOI: 10.1046/j.1365-313x.1998.00310.x. View

Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K . Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol. 1999; 17(3):287-91. DOI: 10.1038/7036. View

Mitsuhara I, Ugaki M, Hirochika H, Ohshima M, Murakami T, Gotoh Y . Efficient promoter cassettes for enhanced expression of foreign genes in dicotyledonous and monocotyledonous plants. Plant Cell Physiol. 1996; 37(1):49-59. DOI: 10.1093/oxfordjournals.pcp.a028913. View

Albrecht V, Weinl S, Blazevic D, DAngelo C, Batistic O, Kolukisaoglu U . The calcium sensor CBL1 integrates plant responses to abiotic stresses. Plant J. 2003; 36(4):457-70. DOI: 10.1046/j.1365-313x.2003.01892.x. View

Hoyos M, Zhang S . Calcium-independent activation of salicylic acid-induced protein kinase and a 40-kilodalton protein kinase by hyperosmotic stress. Plant Physiol. 2000; 122(4):1355-63. PMC: 58971. DOI: 10.1104/pp.122.4.1355. View

Hawes M, Gunawardena U, Miyasaka S, Zhao X . The role of root border cells in plant defense. Trends Plant Sci. 2000; 5(3):128-33. DOI: 10.1016/s1360-1385(00)01556-9. View

Hughes T, Mao M, Jones A, Burchard J, Marton M, Shannon K . Expression profiling using microarrays fabricated by an ink-jet oligonucleotide synthesizer. Nat Biotechnol. 2001; 19(4):342-7. DOI: 10.1038/86730. View

10.

Sakuma Y, Liu Q, Dubouzet J, Abe H, Shinozaki K, Yamaguchi-Shinozaki K . DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Biophys Res Commun. 2002; 290(3):998-1009. DOI: 10.1006/bbrc.2001.6299. View

11.

Thomashow M . PLANT COLD ACCLIMATION: Freezing Tolerance Genes and Regulatory Mechanisms. Annu Rev Plant Physiol Plant Mol Biol. 2004; 50:571-599. DOI: 10.1146/annurev.arplant.50.1.571. View

12.

Li J, Assmann S . An Abscisic Acid-Activated and Calcium-Independent Protein Kinase from Guard Cells of Fava Bean. Plant Cell. 1996; 8(12):2359-2368. PMC: 161358. DOI: 10.1105/tpc.8.12.2359. View

13.

Hohmann S . Osmotic stress signaling and osmoadaptation in yeasts. Microbiol Mol Biol Rev. 2002; 66(2):300-72. PMC: 120784. DOI: 10.1128/MMBR.66.2.300-372.2002. View

14.

Zhang S, Klessig D . Salicylic acid activates a 48-kD MAP kinase in tobacco. Plant Cell. 1997; 9(5):809-24. PMC: 156958. DOI: 10.1105/tpc.9.5.809. View

15.

Maruyama K, Sakuma Y, Kasuga M, Ito Y, Seki M, Goda H . Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. Plant J. 2004; 38(6):982-93. DOI: 10.1111/j.1365-313X.2004.02100.x. View

16.

Wen J, Oono K, Imai R . Two novel mitogen-activated protein signaling components, OsMEK1 and OsMAP1, are involved in a moderate low-temperature signaling pathway in rice. Plant Physiol. 2002; 129(4):1880-91. PMC: 166777. DOI: 10.1104/pp.006072. View

17.

Cheong Y, Kim K, Pandey G, Gupta R, Grant J, Luan S . CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis. Plant Cell. 2003; 15(8):1833-45. PMC: 167173. DOI: 10.1105/tpc.012393. View

18.

Conley T, Sharp R, Walker J . Water Deficit Rapidly Stimulates the Activity of a Protein Kinase in the Elongation Zone of the Maize Primary Root. Plant Physiol. 1997; 113(1):219-226. PMC: 158133. DOI: 10.1104/pp.113.1.219. View

19.

Yoshida R, Hobo T, Ichimura K, Mizoguchi T, Takahashi F, Aronso J . ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. Plant Cell Physiol. 2003; 43(12):1473-83. DOI: 10.1093/pcp/pcf188. View

20.

Monks D, Aghoram K, Courtney P, Dewald D, Dewey R . Hyperosmotic stress induces the rapid phosphorylation of a soybean phosphatidylinositol transfer protein homolog through activation of the protein kinases SPK1 and SPK2. Plant Cell. 2001; 13(5):1205-19. PMC: 135558. DOI: 10.1105/tpc.13.5.1205. View