Genome-Wide Identification and Expression Analysis of WNK Kinase Gene Family in Acorus
Abstract
:1. Introduction
2. Results
2.1. Identification and Physicochemical Properties of the Acorus WNKs
2.2. Phylogenetic Analysis
2.3. Protein Conservative Domain and Gene Structure Analysis
2.4. Collinearity and Location Analysis on Chromosomes
2.5. Cis-Elements Analysis
2.6. Expression Pattern of WNKs
2.7. qRT-PCR Analysis
3. Discussion
4. Materials and Methods
4.1. Data Sources
4.2. Identification and Physicochemical Properties of the WNK Gene Family
4.3. Phylogenetic Analysis of WNKs
4.4. Gene Structure and Conserved Motif Analysis
4.5. Chromosomal Localization and Synteny Analysis
4.6. Cis-Acting Regulatory Elements Analysis
4.7. Expression Pattern
4.8. Treatment of Plant Materials
4.9. qRT-PCR Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Manning, G.; Whyte, D.B.; Martinez, R.; Hunter, T.; Sudarsanam, S. The protein kinase complements of the human genome. Science 2002, 298, 1912–1934. [Google Scholar] [CrossRef] [PubMed]
- Hanks, S.K.; Hunter, T. Protein kinases 6. The eukaryotic protein kinase superfamily: Kinase (catalytic) domain structure and classification. FASEB J. 1995, 9, 576–596. [Google Scholar] [CrossRef] [PubMed]
- Edwin, G.K. 1 The enzymology of control by phosphorylation. Enzymology 1986, 17, 3–20. [Google Scholar]
- Kumar, K.; Raina, S.K.; Sultan, S.M. Arabidopsis MAPK signaling pathways and their cross talks in abiotic stress response. J. Plant Biochem. Biotechnol. 2020, 29, 700–714. [Google Scholar] [CrossRef]
- Nakamichi, N.; Murakami-Kojima, M.; Sato, E.; Kishi, Y.; Yamashino, T.; Mizuno, T. Compilation and characterization of a novel WNK family of protein kinases in Arabiodpsis thaliana with reference to circadian rhythms. Biosci. Biotechnol. Biochem. 2002, 66, 2429–2436. [Google Scholar] [CrossRef] [PubMed]
- Xu, B.; English, J.M.; Wilsbacher, J.L.; Stippec, S.; Goldsmith, E.J.; Cobb, M.H. WNK1, a novel mammalian serine/threonine protein kinase lacking the catalytic lysine in subdomain II. J. Biol. Chem. 2000, 275, 16795–16801. [Google Scholar] [CrossRef] [PubMed]
- Veríssimo, F.; Jordan, P. WNK kinases, a novel protein kinase subfamily in multi-cellular organisms. Oncogene 2001, 20, 5562–5569. [Google Scholar] [CrossRef] [PubMed]
- Kahle, K.T.; Rinehart, J.; Ring, A.; Gimenez, I.; Gamba, G.; Hebert, S.C.; Lifton, R.P. WNK protein kinases modulate cellular Cl- flux by altering the phosphorylation state of the Na-K-Cl and K-Cl cotransporters. Physiology 2006, 21, 326–335. [Google Scholar] [CrossRef]
- Uchida, S.; Sohara, E.; Rai, T.; Sasaki, S. Regulation of with-no-lysine kinase signaling by Kelch-like proteins. Biol. Cell 2014, 106, 45–56. [Google Scholar] [CrossRef]
- Huang, C.-L.; Cha, S.K.; Wang, H.-R.; Xie, J.; Cobb, M.H. WNKs: Protein kinases with a unique kinase domain. Exp. Mol. Med. 2007, 39, 565–573. [Google Scholar] [CrossRef]
- Wang, Y.; Liu, K.; Liao, H.; Zhuang, C.; Ma, H.; Yan, X. The plant WNK gene family and regulation of flowering time in Arabidopsis. Plant Biol. 2008, 10, 548–562. [Google Scholar] [CrossRef] [PubMed]
- Murakami-Kojima, M.; Nakamichi, N.; Yamashino, T.; Mizuno, T. The APRR3 component of the clock-associated APRR1/TOC1 quintet is phosphorylated by a novel protein kinase belonging to the WNK family, the gene for which is also transcribed rhythmically in Arabidopsis thaliana. Plant Cell Physiol. 2002, 43, 675–683. [Google Scholar] [CrossRef] [PubMed]
- Hong-Hermesdorf, A.; Brüx, A.; Grüber, A.; Grüber, G.; Schumacher, K. A WNK kinase binds and phosphorylates V-ATPase subunit C. FEBS Lett. 2006, 580, 932–939. [Google Scholar] [CrossRef] [PubMed]
- Xie, M.; Wu, D.; Duan, G.; Wang, L.; He, R.; Li, X.; Tang, D.; Zhao, X.; Liu, X. AtWNK9 is regulated by ABA and dehydration and is involved in drought tolerance in Arabidopsis. Plant Physiol. Biochem. 2014, 77, 73–83. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Suo, H.; Zheng, Y.; Liu, K.; Zhuang, C.; Kahle, K.T.; Ma, H.; Yan, X. The soybean root-specific protein kinase GmWNK1 regulates stress-responsive ABA signaling on the root system architecture. Plant J. 2010, 64, 230–242. [Google Scholar] [CrossRef]
- Su, B.; Zhang, J.; Wang, J.; Liu, B.; Kong, F.; Sun, Z. Genome-wide identification and expression analysis of WNK kinase gene family in soybean. Res. Sq. 2023, 1. [Google Scholar] [CrossRef]
- Manuka, R.; Saddhe, A.A.; Kumar, K. Genome-wide identification and expression analysis of WNK kinase gene family in rice. Comput. Biol. Chem. 2015, 59, 56–66. [Google Scholar] [CrossRef]
- Kumar, K.; Rao, K.P.; Biswas, D.K.; Sinha, A.K. Rice WNK1 is regulated by abiotic stress and involved in internal circadian rhythm. Plant Signal. Behav. 2011, 6, 316–320. [Google Scholar] [CrossRef]
- Givnish, T.J.; Zuluaga, A.; Spalink, D.; Gomez, M.S.; Lam, V.K.Y.; Saarela, J.M.; Sass, C.; Iles, M.S.G.; de Sousa, D.J.L.; Leebens-Mack, J.; et al. Monocot plastid phylogenomics, timeline, net rates of species diversification, the power of multi-gene analyses, and a functional model for the origin of monocots. Am. J. Bot. 2018, 105, 1888–1910. [Google Scholar] [CrossRef]
- Ma, L.; Liu, K.-W.; Hsiao, Y.Y.; Qi, Y.-Y.; Fu, T.; Tang, G.-D.; Zhang, D.; Sun, W.-H.; Liu, D.-K.; Li, Y.; et al. Diploid and tetraploid genomes of Acorus and the evolution of monocots. Nat. Commun. 2023, 14, 3661. [Google Scholar] [CrossRef]
- Chen, C.; Chen, H.; Zhang, Y.; Thomas, H.R.; Frank, M.H.; He, Y.; Xia, R. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Mol. Plant 2020, 13, 1194–1202. [Google Scholar] [CrossRef] [PubMed]
- Tang, B.-L. (WNK)ing at death: With-no-lysine (Wnk) kinases in neuropathies and neuronal survival. Brain Res. Bull. 2016, 125, 92–98. [Google Scholar] [CrossRef] [PubMed]
- Schmutz, J.; Cannon, S.B.; Schlueter, J.; Ma, J.; Mitros, T.; Nelson, W.; Hyten, D.L.; Song, Q.; Thelen, J.J.; Cheng, J.; et al. Genome sequence of the palaeopolyploid soybean. Nature 2010, 463, 178–183. [Google Scholar] [CrossRef] [PubMed]
- Gill, N.; Findley, S.; Walling, J.G.; Hans, C.; Ma, J.; Doyle, J.; Stacey, G.; Jackson, S.A. Molecular and chromosomal evidence for allopolyploidy in soybean. Plant Physiol. 2009, 151, 1167–1174. [Google Scholar] [CrossRef] [PubMed]
- Richardson, C.; Alessi, D.R. The regulation of salt transport and blood pressure by the WNK-SPAK/OSR1 signaling pathway. J. Cell Sci. 2008, 121, 3293–3304. [Google Scholar] [CrossRef] [PubMed]
- Villa, F.; Goebel, J.; Rafiqi, F.H.; Deak, M.; Thastrup, J.; Alessi, D.R.; van Aalten, D.M. Structural insights into the recognition of substrates and activators by the OSR1 kinase. EMBO Rep. 2007, 8, 839–845. [Google Scholar] [CrossRef] [PubMed]
- Gamba, G. Role of WNK kinases in regulating tubular salt and potassium transport and in the development of hypertension. Am. J. Physiol. Renal Physiol. 2005, 288, 245–252. [Google Scholar] [CrossRef] [PubMed]
- Nishimura, N.; Sarkeshik, A.; Nito, K.; Park, S.Y.; Wang, A.; Carvalho, P.C.; Lee, S.; Caddell, D.F.; Cutler, S.R.; Chory, J. PYR/PYL/RCAR family members are major in-vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis. Plant J. 2010, 61, 290–299. [Google Scholar] [CrossRef]
- Sah, S.-K.; Reddy, K.R.; Li, J. Abscisic acid and abiotic stress tolerance in crop plants. Front. Plant Sci. 2016, 7, 571. [Google Scholar] [CrossRef]
- Verma, V.; Ravindran, P.; Kumar, P.P. Plant hormone-mediated regulation of stress responses. BMC Plant Biol. 2016, 16, 1–10. [Google Scholar] [CrossRef]
- Wang, J.; Song, L.; Gong, X.; Xu, J.; Li, M. Functions of jasmonic acid in plant regulation and response to abiotic stress. Int. J. Mol. Sci. 2020, 21, 1446. [Google Scholar] [CrossRef] [PubMed]
- Feng, R.; Ren, M.; Lu, L.; Peng, M.; Guan, X.; Zhou, D.; Zhang, M.; Qi, D.; Li, K.; Tang, W.; et al. Involvement of abscisic acid-responsive element binding factors in cassava (Manihot esculenta) dehydration stress response. Sci. Rep. 2019, 9, 12661. [Google Scholar] [CrossRef] [PubMed]
- Gómez-Porras, J.L.; Riaño-Pachón, D.M.; Dreyer, I.; Mayer, J.E.; Mueller-Roeber, B. Genome-wide analysis of ABA-responsive elements ABRE and CE3 reveals divergent patterns in Arabidopsis and rice. BMC Genom. 2007, 8, 260. [Google Scholar] [CrossRef] [PubMed]
- Xu, B.-e.; Min, X.; Stippec, S.; Lee, B.H.; Goldsmith, E.J.; Cobb, M.H. Regulation of WNK1 by an autoinhibitory domain and autophosphorylation. J. Biol. Chem. 2002, 277, 48456–48462. [Google Scholar] [CrossRef] [PubMed]
- Kumar, K.; Kumar, M.; Kim, S.R.; Ryu, H.; Cho, Y.G. Insights into genomics of salt stress response in rice. Rice 2013, 6, 27. [Google Scholar] [CrossRef] [PubMed]
- Sun, Z.; Feng, Z.; Ding, Y.; Qi, Y.; Jiang, S.; Li, Z.; Wang, Y.; Qi, J.; Song, C.; Yang, S.; et al. RAF22, ABI1 and OST1 form a dynamic interactive network that optimizes plant growth and responses to drought stress in Arabidopsis. Mol. Plant 2022, 15, 1192–1210. [Google Scholar] [CrossRef]
- Duvaud, S.; Gabella, C.; Lisacek, F.; Stockinger, H.; Ioannidis, V.; Durinx, C. Expasy, the Swiss Bioinformatics Resource Portal, as designed by its users. Nucleic Acids Res. 2021, 49, 216–227. [Google Scholar] [CrossRef]
- Chou, K.C.; Shen, H.B. Cell-PLoc 2.0: An improved package of web-servers for predicting subcellular localization of proteins in various organisms. Nat. Protoc. 2010, 3, 153–162. [Google Scholar] [CrossRef]
- Kumar, S.; Stecher, G.; Tamura, K. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 2016, 33, 1870–1874. [Google Scholar] [CrossRef]
- Letunic, I.; Bork, P. Interactive Tree Of Life (iTOL) v5: An online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 2021, 49, 293–296. [Google Scholar] [CrossRef]
- Bailey, T.L.; Boden, M.; Buske, F.A.; Frith, M.; Grant, C.E.; Clementi, L.; Ren, J.; Li, W.W.; Noble, W.S. MEME suite: Tools for motif discovery and searching. Nucleic Acids Res. 2009, 37, 202–208. [Google Scholar] [CrossRef] [PubMed]
- Lescot, M.; Déhais, P.; Thijs, G.; Marchal, K.; Moreau, Y.; Van de Peer, Y.; Rouzé, P.; Rombauts, S. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 2022, 30, 325–327. [Google Scholar] [CrossRef] [PubMed]
- Li, B.; Dewey, C.N. RSEM: Accurate transcript quantification from RNA-seq data with or without a reference genome. BMC Bioinform. 2011, 12, 323. [Google Scholar] [CrossRef] [PubMed]
- Zhang, S.; Zhao, L.; Shan, C.; Shi, Y.; Ma, K.; Wu, J. Exploring the biosynthetic pathway of lignin in Acorus tatarinowii Schott using de novo leaf and rhizome transcriptome analysis. Biosci. Rep. 2021, 41, BSR20210006. [Google Scholar] [CrossRef]
- Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 2001, 25, 402–408. [Google Scholar] [CrossRef]
Name | Gene ID | AA 1 (aa) | Mw 2 (kDa) | pI 3 | II 4 | AI 5 | Gravy 6 | CDS 7 (bp) | Chromosome Location 8 |
Subcellular
Localization 9 |
---|---|---|---|---|---|---|---|---|---|---|
AcWNK1 | KAK1320341.1 | 618 | 70.12 | 5.75 | 44.91 | 68.61 | −0.72 | 1857 | Chr03: 12409169–12414188 | Nucleus |
AcWNK2 | KAK1319451.1 | 489 | 55.11 | 4.87 | 38.00 | 92.90 | −0.24 | 1470 | Chr04: 22866587–22873092 | Nucleus, Cytoplasmic |
AcWNK3 | KAK1318008.1 | 227 | 25.58 | 4.96 | 37.08 | 76.83 | −0.37 | 684 | Chr05: 10903953–10905345 | Nucleus, Cytoplasmic |
AcWNK4 | KAK1313845.1 | 708 | 80.49 | 5.29 | 51.57 | 77.23 | −0.50 | 2127 | Chr06: 29489259–29492655 | Nucleus |
AcWNK5 | KAK1311781.1 | 455 | 51.47 | 8.16 | 45.07 | 75.03 | −0.55 | 1368 | Chr07: 21106937–21109926 | Chloroplast, Nucleus |
AcWNK6 | KAK1311073.1 | 642 | 72.28 | 4.64 | 37.33 | 86.09 | −0.22 | 1929 | Chr08: 22639927–22642439 | Nucleus |
AcWNK7 | KAK1305712.1 | 549 | 62.71 | 5.02 | 42.96 | 80.58 | −0.49 | 1650 | Chr10: 2507487–2511112 | Nucleus |
AcWNK8 | KAK1307206.1 | 645 | 72.89 | 4.84 | 46.28 | 83.12 | −0.44 | 1938 | Chr10: 6894758–6897759 | Nucleus |
AcWNK9 | KAK1295166.1 | 631 | 70.37 | 4.88 | 38.75 | 80.16 | −0.50 | 1896 | Chr16: 5502464–5509085 | Nucleus |
AcWNK10 | KAK1292824.1 | 307 | 34.77 | 5.71 | 33.94 | 76.81 | −0.48 | 924 | Chr17: 27872713–27876323 | Nucleus, Cytoplasmic |
AcWNK11 | KAK1290085.1 | 772 | 86.28 | 5.01 | 46.89 | 81.74 | −0.51 | 2319 | Chr18: 8858348–8866086 | Nucleus |
AcWNK12 | KAK1287662.1 | 707 | 80.25 | 5.21 | 51.54 | 77.33 | −0.50 | 2124 | Chr19: 13748207–13751593 | Nucleus |
AcWNK13 | KAK1286675.1 | 367 | 41.82 | 7.7 | 46.09 | 73.30 | −0.59 | 1104 | Chr20: 1424439–1427077 | Nucleus, Cytoplasmic, Chloroplast |
AcWNK14 | KAK1285712.1 | 645 | 72.83 | 4.89 | 47.97 | 82.51 | −0.451 | 1938 | Chr20: 25344879–25347778 | Nucleus |
AcWNK15 | KAK1284135.1 | 593 | 67.31 | 5.5 | 45.07 | 70.19 | −0.624 | 1782 | Chr21: 25677797–25682792 | Nucleus |
AgWNK1 | KAK1271499.1 | 417 | 46.92 | 6.29 | 33 | 88.8 | −0.326 | 1254 | Chr05: 22931422–22936549 | Nucleus |
AgWNK2 | KAK1271813.1 | 640 | 72.85 | 6.33 | 47.16 | 71.92 | −0.66 | 1923 | Chr05: 29379837–29385258 | Nucleus |
AgWNK3 | KAK1269333.1 | 303 | 34.40 | 5.88 | 35.27 | 77.82 | −0.476 | 912 | Chr06: 5286985–5289995 | Nucleus |
AgWNK4 | KAK1266485.1 | 708 | 80.46 | 5.29 | 49.81 | 76.68 | −0.517 | 2127 | Chr07: 4327250–4330632 | Nucleus |
AgWNK5 | KAK1264485.1 | 536 | 60.80 | 5.68 | 52.28 | 76.04 | −0.545 | 1611 | Chr08: 5773020–5776384 | Nucleus |
AgWNK6 | KAK1264351.1 | 642 | 72.00 | 4.58 | 35.3 | 84.72 | −0.222 | 1929 | Chr09: 3488510–3491022 | Nucleus |
AgWNK7 | KAK1259211.1 | 583 | 66.26 | 4.9 | 44.54 | 81.05 | −0.475 | 1752 | Chr12: 11253328–11256519 | Nucleus |
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Ji, H.; Wu, Y.; Zhao, X.; Miao, J.-L.; Deng, S.; Li, S.; Gao, R.; Liu, Z.-J.; Zhai, J. Genome-Wide Identification and Expression Analysis of WNK Kinase Gene Family in Acorus. Int. J. Mol. Sci. 2023, 24, 17594. https://doi.org/10.3390/ijms242417594
Ji H, Wu Y, Zhao X, Miao J-L, Deng S, Li S, Gao R, Liu Z-J, Zhai J. Genome-Wide Identification and Expression Analysis of WNK Kinase Gene Family in Acorus. International Journal of Molecular Sciences. 2023; 24(24):17594. https://doi.org/10.3390/ijms242417594
Chicago/Turabian StyleJi, Hongyu, You Wu, Xuewei Zhao, Jiang-Lin Miao, Shuwen Deng, Shixing Li, Rui Gao, Zhong-Jian Liu, and Junwen Zhai. 2023. "Genome-Wide Identification and Expression Analysis of WNK Kinase Gene Family in Acorus" International Journal of Molecular Sciences 24, no. 24: 17594. https://doi.org/10.3390/ijms242417594