Foxtail millet (Setaria italica (L.) P. Beauv) CIPKs are responsive to ABA and abiotic stresses

Autoři: Jinfeng Zhao aff001;  Aili Yu aff001;  Yanwei Du aff001;  Gaohong Wang aff001;  Yanfang Li aff001;  Genyou Zhao aff001;  Xiangdong Wang aff002;  Wenzhong Zhang aff001;  Kai Cheng aff001;  Xin Liu aff001;  Zhenhua Wang aff001;  Yuwen Wang aff001
Působiště autorů: Millet Research Institute, Shanxi Academy of Agricultural Sciences, Shanxi Key Laboratory of Genetic Resources and Breeding in Minor Crops, Changzhi, Shanxi, People's Republic of China aff001;  Tangshan Academy of Agricultural Sciences, Tangshan, Hebei, People's Republic of China aff002
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0225091


CBL-interacting protein kinases (CIPKs) have been shown to regulate a variety of environmental stress-related signalling pathways in plants. Foxtail millet (Setaria italica (L.) P. Beauv) is known worldwide as a relatively stress-tolerant C4 crop species. Although the foxtail millet genome sequence has been released, little is known about the functions of CIPKs in foxtail millet. Therefore, a systematic genome-wide analysis of CIPK genes in foxtail millet was performed. In total, 35 CIPK members were identified in foxtail millet and divided into four subgroups (I to IV) on the basis of their phylogenetic relationships. Phylogenetic and gene structure analyses clearly divided all SiCIPKs into intron-poor and intron-rich clades. Cis-element analysis subsequently indicated that these SiCIPKs may be involved in responses to abiotic stimuli, hormones, and light signalling during plant growth and development, and stress-induced expression profile analysis revealed that all the SiCIPKs are involved in various stress signalling pathways. These results suggest that the CIPK genes in foxtail millet exhibit the basic characteristics of CIPK family members and play important roles in response to abiotic stresses. The results of this study will contribute to future functional characterization of abiotic stress responses mediated by CIPKs in foxtail millet.

Klíčová slova:

Cereal crops – Flowering plants – Gene expression – Millet – Plant resistance to abiotic stress – Sequence motif analysis – Stress signaling cascade – Thermal stresses


1. Zhu JK. Salt and drought stress signal transduction in plants. Annual Review of Plant Biology. 2002; 53: 247–273. doi: 10.1146/annurev.arplant.53.091401.143329 12221975

2. Yu QY, An LJ, Li WL. The CBL-CIPK network mediates different signaling pathways in plants. Plant Cell Reports. 2014; 33(2): 203–214. doi: 10.1007/s00299-013-1507-1 24097244

3. Hu W, Xia ZQ, Yan Y, Ding ZH, Tie WW, Wang LZ, et al. Genome-wide gene phylogeny of CIPK family in cassava and expression analysis of partial drought-induced genes. Frontiers in Plant Science. 2015; 6: 914. doi: 10.3389/fpls.2015.00914 26579161

4. Shi J, Kim KN, Ritz O, Albrecht V, Gupta R, Harter K, et al. Novel protein pinases associated with calcineurin B-Like calcium sensors in Arabidopsis. Plant Cell. 1999; 11: 2393–2405. doi: 10.1105/tpc.11.12.2393 10590166

5. Albrecht V, Ritz O, Linder S, Harter K, Kudla J. The NAF domain defines a novel protein-protein interaction module conserved in Ca2+-regulated kinases. Embo Journal. 2001; 20: 1051–1063. doi: 10.1093/emboj/20.5.1051 11230129

6. Liu J, Ishitani M, Halfter U, Kim CS, Zhu JK. The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc Natl Acad Sci. 2000; 97: 3730–3734. doi: 10.1073/pnas.060034197 10725382

7. Halfter U, Ishitani M, Zhu JK. The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proc Natl Acad Sci. 2000; 97: 3735–3740. doi: 10.1073/pnas.040577697 10725350

8. Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK. Regulation of SOS1, A plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci. 2002; 99: 8436–8441. doi: 10.1073/pnas.122224699 12034882

9. Wang RK, Li LL, Cao ZH, Zhao Q, Li M, Zhang LY, et al. Molecular cloning and functional characterization of a novel apple MdCIPK6L gene reveals its involvement in multiple abiotic stress tolerance in transgenic plants. Plant Molecular Biology. 2012; 79: 123–135. doi: 10.1007/s11103-012-9899-9 22382993

10. Hu DG, Li M, Luo H, Dong QL, Yao YX, You CX, et al. Molecular cloning and functional characterization of MdSOS2 reveals its involvement in salt tolerance in apple callus and Arabidopsis. Plant Cell Rep. 2012; 31: 713–722. doi: 10.1007/s00299-011-1189-5 22108717

11. Zhao JF, Sun ZF, Zheng J, Guo XY, Dong ZG, Huai JL, et al. Cloning and characterization of a novel CBL-interacting protein kinase from maize. Plant Molecular Biology. 2009; 69: 661–674. doi: 10.1007/s11103-008-9445-y 19105030

12. Zhang YM, Linghu JJ, Wang D, Liu X, Yu AL, Li FT, et al. Foxtail Millet CBL4 (SiCBL4) interacts with SiCIPK24, modulates plant salt stress tolerance. Plant Mol Biol Rep. 2017; 35: 634–646.

13. Xu J, Li HD, Chen LQ, Wang Y, Liu LL, H L, et al. A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell. 2006; 125(7): 1347–1360. doi: 10.1016/j.cell.2006.06.011 16814720

14. Huang C, Ding S, Zhang H, Du H, An L. CIPK7 is involved in cold response by interacting with CBL1 in Arabidopsis thaliana. Plant Science. 2011; 181: 57–64. doi: 10.1016/j.plantsci.2011.03.011 21600398

15. Yang WQ, Kong ZS, Omo-Ikerodah E, Xu WY, Li Qun, Xue YB. Calcineurin B-like interacting protein kinase OsCIPK23 functions in pollination and drought stress responses in rice (Oryza sativa L.). Journal of Genetics & Genomics. 2008; 35: 531–543.

16. He L, Yang X, Wang L, Zhu L, Zhou T, Deng J, et al. Molecular cloning and functional characterization of a novel cotton CBL-interacting protein kinase gene (GhCIPK6) reveals its involvement in multiple abiotic stress tolerance in transgenic plants. Biochemical & Biophysical Research Communications. 2013; 435: 209–215. doi: 10.1016/j.bbrc.2013.04.080 23660187

17. Luan S, Lan WZ, Lee SC, Salt DE, Williams L. Potassium nutrition, sodium toxicity, and calcium signalling: connections through the CBL-CIPK network. Current Opinion in Plant Biology. 2009; 12: 339–346. doi: 10.1016/j.pbi.2009.05.003 19501014

18. Weinl S, Kudla J. The CBL-CIPK Ca2+-decoding signalling network: function and perspectives. New Phytologist. 2009; 184: 517–528. 19860013

19. Gao P, Zhao PM, Wang J, Wang HY, Du XM, Wang GL, et al. Co-expression and preferential interaction between two calcineurin B-like proteins and a CBL-interacting protein kinase from cotton. Plant Physiol Biochem. 2008; 46(10): 935–940. doi: 10.1016/j.plaphy.2008.05.001 18573665

20. Tripathi V, Parasuraman B, Laxmi A, Chattopadhyay D. CIPK6, a CBL-interacting protein kinase is required for development and salt tolerance in plants. Plant Journal. 2010; 58(5): 778–790. doi: 10.1111/j.1365-313X.2009.03812.x 19187042

21. Hu HC, Wang YY, Tsay YF. AtCIPK8, a CBL-interacting protein kinase, regulates the low-affinity phase of the primary nitrate response. Plant Journal. 2009; 57: 264–278. doi: 10.1111/j.1365-313X.2008.03685.x 18798873

22. D' Angelo C, Weinl S, Batistic O, Pandey GK, Cheong YH, Schültke S, et al. Alternative complex formation of the Ca-regulated protein kinase CIPK1 controls abscisic acid-dependent and independent stress responses in Arabidopsis. Plant Journal. 2006; 48: 857–872. doi: 10.1111/j.1365-313X.2006.02921.x 17092313

23. Kolukisaoglu U, Weinl S, Blazevic D, Batistic O, Kudla J. Calcium sensors and their interacting protein kinases: Genomics of the Arabidopsis and rice CBL-CIPK signalling networks. Plant Physiol. 2004; 134: 43–58. doi: 10.1104/pp.103.033068 14730064

24. Poonam K, Sibaji S, Indu T, Akhilesh KY, Amita P, Sanjay K, et al. Comprehensive structural, interaction and expression analysis of CBL and CIPK complement during abiotic stresses and development in rice. Cell Calcium. 2014; 56(2): 81–95. doi: 10.1016/j.ceca.2014.05.003 24970010

25. Sun T, Wang Y, Wang M, Li T, Zhou Y, Wang X, et al. Identification and comprehensive analyses of the CBL and CIPK gene families in wheat (Triticum aestivum L.). Bmc Plant Biology. 2015; 15: 269. doi: 10.1186/s12870-015-0657-4 26537110

26. Li LB, Zhang YR, Liu KC, Ni ZF, Fang ZJ, Sun QX, et al. Identification and bioinformatics analysis of SnRK2 and CIPK family genes in Sorghum. Agricultural Sciences in China. 2010; 9: 19–30.

27. Mo CY, Wan SM, Xia YQ, Ren N, Zhou Y, Jiang XY. Expression Patterns and Identified Protein-Protein Interactions Suggest That Cassava CBL-CIPK Signal Networks Function in Responses to Abiotic Stresses. Frontiers in Plant Science. 2018; 9: 269. doi: 10.3389/fpls.2018.00269 29552024

28. Cui XY, Du YT, Fu JD, Yu TF, Wang CT, Chen M, et al. Wheat CBL-interacting protein kinase 23 positively regulates drought stress and ABA responses. BMC Plant Biol. 2018; 18: 93. doi: 10.1186/s12870-018-1306-5 29801463

29. Abdula SE, Lee HJ, Ryu H, Kang KK, Nou I, Sorrells ME, et al. Overexpression of BrCIPK1 Gene Enhances Abiotic Stress Tolerance by Increasing Proline Biosynthesis in Rice. Plant Mol Biol Rep. 2016; 34(2): 501–511.

30. Tai FJ, Yuan ZH, Li SP, Wang Q, Liu FY, Wang W. ZmCIPK8, a CBL-interacting protein kinase, regulates maize response to drought stress.Plant Cell Tiss Organ Cult. 2016; 124(3): 459–469.

31. Pan WH, Shen JQ, Zheng ZZ, Yan X, Shou JX, Wang WX, et al. Overexpression of the Tibetan Plateau annual wild barley (Hordeum spontaneum) HsCIPKs enhances rice tolerance to heavy metal toxicities and other abiotic stresses. Rice. 2018; 11: 51. doi: 10.1186/s12284-018-0242-1 30209684

32. Yan Y, He XY, Hu W, Liu GY, Wang P, He CZ, et al. Functional analysis of MeCIPK23 and MeCBL1/9 in cassava defense response against Xanthomonas axonopodis pv. Manihotis. Plant Cell Rep. 2018; 37(6): 887–900. doi: 10.1007/s00299-018-2276-7 29523964

33. Sheng LX, Meng XY, Wang M, Zang S, Feng LG. Improvement in Submergence Tolerance of Cherry Through Regulation of Carbohydrate Metabolism and Plant Growth by PsERF and PsCIPK. Appl Biochem Biotechnol. 2018; 184(1): 63–79. doi: 10.1007/s12010-017-2530-4 28608173

34. Guo YL, Huang Y, Gao J, Pu YY, Wang N, Shen WY, et al. CIPK9 is involved in seed oil regulation in Brassica napus L. and Arabidopsis thaliana (L.) Heynh. Biotechnol Biofuels. 2018; 11: 124. doi: 10.1186/s13068-018-1122-z 29743952

35. Zhang G, Liu X, Quan Z, Cheng S, Xu X, Pan S, et al. Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential. Nature Biotechnology. 2012; 30(6): 549–554. doi: 10.1038/nbt.2195 22580950

36. Muthamilarasan M, Prasad M. Advances in Setaria genomics for genetic improvement of cereals and bioenergy grasses. Theoretical & Applied Genetics. 2015; 128: 1–14. doi: 10.1007/s00122-014-2399-3 25239219

37. Muthamilarasan M, Theriappan P, Prasad M. Recent advances in crop genomics for ensuring food security. Current Science. 2013; 104: 155–158.

38. Bennetzen JL, Schmutz J, Wang H, Percifield R, Hawkins J, Pontaroli AC, et al. Reference genome sequence of the model plant Setaria. Nature Biotechnology. 2012; 30(6): 555–561. doi: 10.1038/nbt.2196 22580951

39. Tang J, Lin J, Li H, Li X, Yang Q, Cheng ZM, et al. Characterization of CIPK family in Asian Pear (Pyrus bretschneideri Rehd) and co-expression analysis related to salt and osmotic stress responses. Frontiers in Plant Science. 2016; 7: 15026. doi: 10.3389/fpls.2016.01361 27656193

40. Bailey TL, Williams N, Misleh C, Li WW. MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res. 2006; 34(suppl-2): W369–73. doi: 10.1093/nar/gkl198 16845028

41. Hu B, Jin JP, Guo AY, Zhang H, Luo JH, Gao G. GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics. 2015; 31(8): 1296–1297. doi: 10.1093/bioinformatics/btu817 25504850

42. Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, et al. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research. 2002; 30(1): 325–327. doi: 10.1093/nar/30.1.325 11752327

43. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, et al. Clustal W and Clustal X version 2.0. Bioinformatics. 2007; 23: 2947–2948. doi: 10.1093/bioinformatics/btm404 17846036

44. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: molecular evolutionary genetics analysis version6.0. Mol Biol Evol. 2013; 30: 2725–2729. doi: 10.1093/molbev/mst197 24132122

45. Xu Y, Hui L, Li X, Jing L, Wang Z, Yang Q, et al. Systematic selection and validation of appropriate reference genes for gene expression studies by quantitative real-time PCR in pear. Acta Physiologiae Plantarum. 2015; 37: 1–16.

46. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt. Methods. 2001; 25(4): 402–408. doi: 10.1006/meth.2001.1262 11846609

47. Sun T, Wang Y, Wang M, Li T, Zhou Y, Wang X, et al. Identification and comprehensive analyses of the CBL and CIPK gene families in wheat (Triticum aestivum L.). Bmc Plant Biology. 2015; 15: 269. doi: 10.1186/s12870-015-0657-4 26537110

48. Xi Y, Liu J, Dong C, Cheng Z. The CBL and CIPK gene family in grapevine (Vitis vinifera): genome-wide analysis and expression profiles in response to various abiotic stresses. Frontiers in Plant Science. 2017; 8: 978. doi: 10.3389/fpls.2017.00978 28649259

49. Adams KL, Wendel JF. Polyploidy and genome evolution in plants. Current Opinion in Plant Biology. 2005; 8: 135–141. doi: 10.1016/j.pbi.2005.01.001 15752992

50. Kleist TJ, Spencley AL, Luan S. Comparative phylogenomics of the CBL-CIPK calcium-decoding network in the moss Physcomitrella, Arabidopsis, and other green lineages. Frontiers in Plant Science. 2014; 5: 187. doi: 10.3389/fpls.2014.00187 24860579

51. Bowe LM, Coat G, Depamphilis CW. Phylogeny of seed plants based on all three genomic compartments: extant gymnosperms are monophyletic and Gnetales' closest relatives are conifers. Proc Natl Acad Sci. 2000; 97: 4092–4097. doi: 10.1073/pnas.97.8.4092 10760278

52. Xiang Y, Huang Y, Xiong L. Characterization of stress-responsive CIPK genes in rice for stress tolerance improvement. Plant Physiology. 2007;144:1416–1428. doi: 10.1104/pp.107.101295 17535819

53. Chaves-Sanjuan A, Sanchez-Barrena MJ, Gonzalez-Rubio JM, Moreno M, Ragel P, Jimenez M, et al. Structural basis of the regulatory mechanism of the plant CIPK family of protein kinases controlling ion homeostasis and abiotic stress. Proc Natl Acad Sci. 2014; 111: 4532–4541. doi: 10.1073/pnas.1407610111 25288725

54. Mahajan S, Tuteja N. Cold, salinity and drought stresses: An overview. Archives of Biochemistry and Biophysics. 2005; 444(2): 139–158. doi: 10.1016/ 16309626

55. Thomashow MF. Plant cold acclimation: Freezing tolerance genes and regulatory mechanisms. Annurevplant Physiolplant Molbiol. 1999; 50: 571–599. doi: 10.1146/annurev.arplant.50.1.571 15012220

56. Shinozaki K, Yamaguchi-Shinozaki K. Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr opin plant Biol. 2000; 3: 217–223. 10837265

57. Chen XF, Gu ZM, Xin D, Hao L, Liu CJ, Huang J, et al. Identification and characterization of putative CIPK genes in maize. Journal of Genetics and Genomics. 2011; 38: 77–87. doi: 10.1016/j.jcg.2011.01.005 21356527

58. Yu Y, Xia X, Yin W, Zhang H. Comparative genomic analysis of CIPK gene family in Arabidopsis and Populus. Plant Growth Regulation. 2007; 52: 101–110.

59. Tang RJ, Zhao FG, Garcia VJ, Kleist TJ, Yang L, Zhang HX et al. Tonoplast CBL-CIPK calcium signaling network regulates magnesium homeostasis in Arabidopsis. Proc Natl Acad. Sci. 2015;112:3134–3139. doi: 10.1073/pnas.1420944112 25646412

60. Zhu K, Chen F, Liu J, Chen X, Hewezi T, Cheng ZM. Evolution of an intron-poor cluster of the CIPK gene family and expression in response to drought stress in soybean. Scientific Reports. 2016; 6: 28225. doi: 10.1038/srep28225 27311690

61. Zhang H, Yang B, Liu WZ, Li H, Wang L, Wang B, et al. Identification and characterization of CBL and CIPK gene families in canola (Brassica napus L.). BMC Plant Biology. 2014; 14(1): 8–8. doi: 10.1186/1471-2229-14-8 24397480

62. Pandey GK, Kanwar P, Singh A, Steinhorst L, Pandey A, Yadav AK, et al. Calcineurin B-Like protein-interacting protein kinase CIPK21 regulates osmotic and salt stress responses in Arabidopsis. Plant Physiology. 2015; 169(1): 780–792. doi: 10.1104/pp.15.00623 26198257

63. Narusaka Y, Nakashima K, Shinwari ZK, Sakuma Y, Furihata T, Abe H, et al. Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J. 2003; 34: 137–148. doi: 10.1046/j.1365-313x.2003.01708.x 12694590

64. Nakashima K, Yamaguchi-shinozaki K. ABA signaling in stress-response and seed development. Plant Cell Reports. 2013; 32: 959–970. doi: 10.1007/s00299-013-1418-1 23535869

65. Verma V, Ravindran P, Kumar PP. Plant hormone-mediated regulation of stress responses. BMC Plant Biology. 2016; 16: 86. doi: 10.1186/s12870-016-0771-y 27079791

66. Zhang J, Jia W, Yang J, Ismail A M. Role of ABA in integrating plant responses to drought and salt stresses. Field Crops Res. 2006; 97: 111–119.

67. Bari R, Jones JD. Role of plant hormones in plant defence responses. Plant Molecular Biology. 2009; 69: 473–488. doi: 10.1007/s11103-008-9435-0 19083153

68. Jia XP, Bai JY, Fan BY, Zhang GN, Shi GA, Hou DY, et al. Cloning and sequence analysis of a putative CCT-motif gene in ten foxtail millet cultivars. The Journal of Animal & Plant Sciences. 2016; 26: 1526–1532.

69. Bray EA. Plant responses to water deficit. Trends Plant Sci. 1997; 2: 48–54.

70. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ. Plant cellular and molecular responses to high salinity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 2000; 51: 463–499. doi: 10.1146/annurev.arplant.51.1.463 15012199

71. Bajaj S, Targolli J, Liu LF, Ho THD, Wu R. Transgenic approaches to increase dehydration-stress tolerance in plants. Mol. Breed. 1999; 5: 493–503.

72. Holmberg N, Bu¨low L. Improving stress tolerance in plants by gene transfer. Trends Plant Sci. 1998; 3: 61–66.

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