Skip to main content
Log in

Calcium-dependent protein kinases CPK21 and CPK23 phosphorylate and activate the iron-regulated transporter IRT1 to regulate iron deficiency in Arabidopsis

  • Research Paper
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

Iron (Fe) is an essential micronutrient for all organisms. Fe availability in the soil is usually much lower than that required for plant growth, and Fe deficiencies seriously restrict crop growth and yield. Calcium (Ca2+) is a second messenger in all eukaryotes; however, it remains largely unknown how Ca2+ regulates Fe deficiency. In this study, mutations in CPK21 and CPK23, which are two highly homologous calcium-dependent protein kinases, conferredimpaired growth and rootdevelopment under Fe-deficient conditions, whereas constitutively active CPK21 and CPK23 enhanced plant tolerance to Fe-deficient conditions. Furthermore, we found that CPK21 and CPK23 interacted with and phosphorylated the Fe transporter IRON-REGULATED TRANSPORTER1 (IRT1) at the Ser149 residue. Biochemical analyses and complementation of Fe transport in yeast and plants indicated that IRT1 Ser149 is critical for IRT1 transport activity. Taken together, these findings suggest that the CPK21/23-IRT1 signaling pathway is critical for Fe homeostasis in plants and provides targets for improving Fe-deficient environments and breeding crops resistant to Fe-deficient conditions.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Barberon, M., Dubeaux, G., Kolb, C., Isono, E., Zelazny, E., and Vert, G. (2014). Polarization of IRON-REGULATED TRANSPORTER 1 (IRT1) to the plant-soil interface plays crucial role in metal homeostasis. Proc Natl Acad Sci USA 111, 8293–8298.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barberon, M., Zelazny, E., Robert, S., Conéjéro, G., Curie, C., Friml, J., and Vert, G. (2011). Monoubiquitin-dependent endocytosis of the iron-regulated transporter 1 (IRT1) transporter controls iron uptake in plants. Proc Natl Acad Sci USA 108, E450–458.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boudsocq, M., and Sheen, J. (2013). CDPKs in immune and stress signaling. Trends Plant Sci 18, 30–40.

    Article  CAS  PubMed  Google Scholar 

  • Brandt, B., Brodsky, D.E., Xue, S., Negi, J., Iba, K., Kangasjärvi, J., Ghassemian, M., Stephan, A.B., Hu, H., and Schroeder, J.I. (2012). Reconstitution of abscisic acid activation of SLAC1 anion channel by CPK6 and OST1 kinases and branched ABI1 PP2C phosphatase action. Proc Natl Acad Sci USA 109, 10593–10598.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Briat, J.F., Fobis-Loisy, I., Grignon, N., Lobréaux, S., Pascal, N., Savino, G., Thoiron, S., Wirén, N., and Wuytswinkel, O. (1995). Cellular and molecular aspects of iron metabolism in plants. Biol Cell 84, 69–81.

    Article  CAS  Google Scholar 

  • Brumbarova, T., Bauer, P., and Ivanov, R. (2015). Molecular mechanisms governing Arabidopsis iron uptake. Trends Plant Sci 20, 124–133.

    Article  CAS  PubMed  Google Scholar 

  • Chen, X., Ding, Y., Yang, Y., Song, C., Wang, B., Yang, S., Guo, Y., and Gong, Z. (2021). Protein kinases in plant responses to drought, salt, and cold stress. J Integr Plant Biol 63, 53–78.

    Article  CAS  PubMed  Google Scholar 

  • Cheng, S.H., Willmann, M.R., Chen, H.C., and Sheen, J. (2002). Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129, 469–485.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Colangelo, E.P., and Guerinot, M.L. (2004). The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 16, 3400–3412.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Connolly, E.L., Fett, J.P., and Guerinot, M.L. (2002). Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell 14, 1347–1357.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Conte, S.S., and Walker, E.L. (2011). Transporters contributing to iron trafficking in plants. Mol Plant 4, 464–476.

    Article  CAS  PubMed  Google Scholar 

  • D’Angelo, C., Weinl, S., Batistic, O., Pandey, G.K., Cheong, Y.H., Schültke, S., Albrecht, V., Ehlert, B., Schulz, B., Harter, K., et al. (2006). Alternative complex formation of the Ca2+-regulated protein kinase CIPK1 controls abscisic acid-dependent and independent stress responses in Arabidopsis. Plant J 48, 857–872.

    Article  PubMed  Google Scholar 

  • Demir, F., Horntrich, C., Blachutzik, J.O., Scherzer, S., Reinders, Y., Kierszniowska, S., Schulze, W.X., Harms, G.S., Hedrich, R., Geiger, D., et al. (2013). Arabidopsis nanodomain-delimited ABA signaling pathway regulates the anion channel SLAH3. Proc Natl Acad Sci USA 110, 8296–8301.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dix, D.R., Bridgham, J.T., Broderius, M.A., Byersdorfer, C.A., and Eide, D.J. (1994). The FET4 gene encodes the low affinity Fe(II) transport protein of Saccharomyces cerevisiae. J Biol Chem 269, 26092–26099.

    Article  CAS  PubMed  Google Scholar 

  • Dong, Q., Bai, B., Almutairi, B.O., and Kudla, J. (2021). Emerging roles of the CBL-CIPK calcium signaling network as key regulatory hub in plant nutrition. J Plant Physiol 257, 153335.

    Article  CAS  PubMed  Google Scholar 

  • Dubeaux, G., Neveu, J., Zelazny, E., and Vert, G. (2018). Metal sensing by the IRT1 transporter-receptor orchestrates its own degradation and plant metal nutrition. Mol Cell 69, 953–964.e5.

    Article  CAS  PubMed  Google Scholar 

  • Eide, D., Broderius, M., Fett, J., and Guerinot, M.L. (1996). A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc Natl Acad Sci USA 93, 5624–5628.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eng, B.H., Guerinot, M.L., Eide, D., and Saier Jr., M.H. (1998). Sequence analyses and phylogenetic characterization of the ZIP family of metal ion transport proteins. J Membr Biol 166, 1–7.

    Article  CAS  PubMed  Google Scholar 

  • Franz, S., Ehlert, B., Liese, A., Kurth, J., Cazalé, A.C., and Romeis, T. (2011). Calcium-dependent protein kinase CPK21 functions in abiotic stress response in Arabidopsis thaliana. Mol Plant 4, 83–96.

    Article  CAS  PubMed  Google Scholar 

  • Fu, D., Zhang, Z., Wallrad, L., Wang, Z., Höller, S., Ju, C.F., Schmitz-Thom, I., Huang, P., Wang, L., Peiter, E., et al. (2022). Ca2+-dependent phosphorylation of NRAMP1 by CPK21 and CPK23 facilitates manganese uptake and homeostasis in Arabidopsis. Proc Natl Acad Sci USA 119, e2204574119.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao, H., Xie, W., Yang, C., Xu, J., Li, J., Wang, H., Chen, X., and Huang, C.F. (2018). NRAMP2, a trans-Golgi network-localized manganese transporter, is required for Arabidopsis root growth under manganese deficiency. New Phytol 217, 179–193.

    Article  CAS  PubMed  Google Scholar 

  • Geiger, D., Maierhofer, T., AL-Rasheid, K.A.S., Scherzer, S., Mumm, P., Liese, A., Ache, P., Wellmann, C., Marten, I., Grill, E., et al. (2011). Stomatal closure by fast abscisic acid signaling is mediated by the guard cell anion channel SLAH3 and the receptor RCAR1. Sci Signal 4, ra32.

    Article  PubMed  Google Scholar 

  • Geiger, D., Scherzer, S., Mumm, P., Marten, I., Ache, P., Matschi, S., Liese, A., Wellmann, C., Al-Rasheid, K.A.S., Grill, E., et al. (2010). Guard cell anion channel SLAC1 is regulated by CDPK protein kinases with distinct Ca2+ affinities. Proc Natl Acad Sci USA 107, 8023–8028.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gratz, R., Manishankar, P., Ivanov, R., Köster, P., Mohr, I., Trofimov, K., Steinhorst, L., Meiser, J., Mai, H.J., Drerup, M., et al. (2019). CIPK11-dependent phosphorylation modulates FIT activity to promote Arabidopsis iron acquisition in response to calcium signaling. Dev Cell 48, 726–740.e10.

    Article  CAS  PubMed  Google Scholar 

  • Gratz, R., von der Mark, C., Ivanov, R., and Brumbarova, T. (2021). Fe acquisition at the crossroad of calcium and reactive oxygen species signaling. Curr Opin Plant Biol 63, 102048.

    Article  CAS  PubMed  Google Scholar 

  • Guerinot, M.L. (2000). The ZIP family of metal transporters. Biochim Biophys Acta 1465, 190–198.

    Article  CAS  PubMed  Google Scholar 

  • Guerinot, M.L., and Yi, Y. (1994). Iron: nutritious, noxious, and not readily available. Plant Physiol 104, 815–820.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gutermuth, T., Herbell, S., Lassig, R., Brosché, M., Romeis, T., Feijó, J.A., Hedrich, R., and Konrad, K.R. (2018). Tip-localized Ca2+-permeable channels control pollen tube growth via kinase-dependent R- and S-type anion channel regulation. New Phytol 218, 1089–1105.

    Article  CAS  PubMed  Google Scholar 

  • Hamel, L.P., Sheen, J., and Séguin, A. (2014). Ancient signals: comparative genomics of green plant CDPKs. Trends Plant Sci 19, 79–89.

    Article  CAS  PubMed  Google Scholar 

  • Harmon, A.C., Gribskov, M., Gubrium, E., and Harper, J.F. (2001). The CDPK superfamily of protein kinases. New Phytol 151, 175–183.

    Article  CAS  PubMed  Google Scholar 

  • Hashimoto, K., and Kudla, J. (2011). Calcium decoding mechanisms in plants. Biochimie 93, 2054–2059.

    Article  CAS  PubMed  Google Scholar 

  • Hua, D., Wang, C., He, J., Liao, H., Duan, Y., Zhu, Z., Guo, Y., Chen, Z., and Gong, Z. (2012). A plasma membrane receptor kinase, GHR1, mediates abscisic acid- and hydrogen peroxide-regulated stomatal movement in Arabidopsis. Plant Cell 24, 2546–2561.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ivanov, R., Brumbarova, T., and Bauer, P. (2012). Fitting into the harsh reality: regulation of iron-deficiency responses in dicotyledonous plants. Mol Plant 5, 27–42.

    Article  CAS  PubMed  Google Scholar 

  • Ivanov, R., Brumbarova, T., Blum, A., Jantke, A.M., Fink-Straube, C., and Bauer, P. (2014). SORTING NEXIN1 is required for modulating the trafficking and stability of the Arabidopsis IRON-REGULATED TRANSPORTER1. Plant Cell 26, 1294–1307.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jakoby, M., Wang, H.Y., Reidt, W., Weisshaar, B., and Bauer, P. (2004). FRU (BHLH029) is required for induction of iron mobilization genes in Arabidopsis thaliana. FEBS Lett 577, 528–534.

    Article  CAS  PubMed  Google Scholar 

  • Jiang, Y., Chen, X., Chai, S., Sheng, H., Sha, L., Fan, X., Zeng, J., Kang, H., Zhang, H., Xiao, X., et al. (2021). TpIRT1 from Polish wheat (Triticum polonicum L.) enhances the accumulation of Fe, Mn, Co, and Cd in Arabidopsis. Plant Sci 312, 111058.

    Article  CAS  PubMed  Google Scholar 

  • Ju, C., Zhang, Z., Deng, J., Miao, C., Wang, Z., Wallrad, L., Javed, L., Fu, D., Zhang, T., Kudla, J., et al. (2022). Ca2+-dependent successive phosphorylation of vacuolar transporter MTP8 by CBL2/3-CIPK3/9/26 and CPK5 is critical for manganese homeostasis in Arabidopsis. Mol Plant 15, 419–437.

    Article  CAS  PubMed  Google Scholar 

  • Kawamoto, N., Sasabe, M., Endo, M., Machida, Y., and Araki, T. (2015). Calcium-dependent protein kinases responsible for the phosphorylation of a bZIP transcription factor FD crucial for the florigen complex formation. Sci Rep 5, 8341.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Khan, I., Gratz, R., Denezhkin, P., Schott-Verdugo, S.N., Angrand, K., Genders, L., Basgaran, R.M., Fink-Straube, C., Brumbarova, T., Gohlke, H., et al. (2019). Calcium-promoted interaction between the C2-domain protein EHB1 and metal transporter IRT1 inhibits Arabidopsis iron acquisition. Plant Physiol 180, 1564–1581.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi, T., and Nishizawa, N.K. (2012). Iron uptake, translocation, and regulation in higher plants. Annu Rev Plant Biol 63, 131–152.

    Article  CAS  PubMed  Google Scholar 

  • Kudla, J., Becker, D., Grill, E., Hedrich, R., Hippler, M., Kummer, U., Parniske, M., Romeis, T., and Schumacher, K. (2018). Advances and current challenges in calcium signaling. New Phytol 218, 414–431.

    Article  PubMed  Google Scholar 

  • Lee, S., and An, G. (2009). Over-expression of OsIRT1 leads to increased iron and zinc accumulations in rice. Plant Cell Environ 32, 408–416.

    Article  CAS  PubMed  Google Scholar 

  • Liang, X., and Zhou, J.M. (2018). Receptor-like cytoplasmic kinases: central players in plant receptor kinase-mediated signaling. Annu Rev Plant Biol 69, 267–299.

    Article  CAS  PubMed  Google Scholar 

  • Lingam, S., Mohrbacher, J., Brumbarova, T., Potuschak, T., Fink-Straube, C., Blondet, E., Genschik, P., and Bauer, P. (2011). Interaction between the bHLH transcription factor FIT and ETHYLENE INSENSITIVE3/ETHYLENE INSENSITIVE3-LIKE1 reveals molecular linkage between the regulation of iron acquisition and ethylene signaling in Arabidopsis. Plant Cell 23, 1815–1829.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu, K.H., Niu, Y., Konishi, M., Wu, Y., Du, H., Sun Chung, H., Li, L., Boudsocq, M., McCormack, M., Maekawa, S., et al. (2017). Discovery of nitrate-CPK-NLP signalling in central nutrient-growth networks. Nature 545, 311–316.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luan, S., and Wang, C. (2021). Calcium signaling mechanisms across kingdoms. Annu Rev Cell Dev Biol 37, 311–340.

    Article  CAS  PubMed  Google Scholar 

  • Ma, S.Y., and Wu, W.H. (2007). AtCPK23 functions in Arabidopsis responses to drought and salt stresses. Plant Mol Biol 65, 511–518.

    Article  CAS  PubMed  Google Scholar 

  • Manishankar, P., Wang, N., Köster, P., Alatar, A.A., and Kudla, J. (2018). Calcium signaling during salt stress and in the regulation of ion homeostasis. J Exp Bot 69, 4215–4226.

    Article  CAS  Google Scholar 

  • Marschner, H., and Römheld, V. (1994). Strategies of plants for acquisition of iron. Plant Soil 165, 261–274.

    Article  CAS  Google Scholar 

  • Martha-Paz, A.M., Eide, D., Mendoza-Cózatl, D., Castro-Guerrero, N.A., and Aréchiga-Carvajal, E.T. (2019). Zinc uptake in the Basidiomycota: characterization of zinc transporters in Ustilago maydis. Mol Membr Biol 35, 39–50.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meiser, J., Lingam, S., and Bauer, P. (2011). Posttranslational regulation of the iron deficiency basic helix-loop-helix transcription factor FIT is affected by iron and nitric oxide. Plant Physiol 157, 2154–2166.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mori, I.C., Murata, Y., Yang, Y., Munemasa, S., Wang, Y.F., Andreoli, S., Tiriac, H., Alonso, J.M., Harper, J.F., Ecker, J.R., et al. (2006). CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion- and Ca2+ permeable channels and stomatal closure. PLoS Biol 4, 327–341.

    Article  Google Scholar 

  • Perochon, A., Aldon, D., Galaud, J.P., and Ranty, B. (2011). Calmodulin and calmodulin-like proteins in plant calcium signaling. Biochimie 93, 2048–2053.

    Article  CAS  PubMed  Google Scholar 

  • Prodhan, M.Y., Munemasa, S., Nahar, M.N.E.N., Nakamura, Y., and Murata, Y. (2018). Guard cell salicylic acid signaling is integrated into abscisic acid signaling via the Ca2+/CPK-dependent pathway. Plant Physiol 178, 441–450.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robinson, N.J., Procter, C.M., Connolly, E.L., and Guerinot, M.L. (1999). A ferric-chelate reductase for iron uptake from soils. Nature 397, 694–697.

    Article  CAS  PubMed  Google Scholar 

  • Santi, S., and Schmidt, W. (2009). Dissecting iron deficiency-induced proton extrusion in Arabidopsis roots. New Phytol 183, 1072–1084.

    Article  CAS  PubMed  Google Scholar 

  • Scherzer, S., Maierhofer, T., Al-Rasheid, K.A.S., Geiger, D., and Hedrich, R. (2012). Multiple calcium-dependent kinases modulate ABA-activated guard cell anion channels. Mol Plant 5, 1409–1412.

    Article  CAS  PubMed  Google Scholar 

  • Shi, S., Li, S., Asim, M., Mao, J., Xu, D., Ullah, Z., Liu, G., Wang, Q., and Liu, H. (2018). The Arabidopsis calcium-dependent protein kinases (CDPKs) and their roles in plant growth regulation and abiotic stress responses. Int J Mol Sci 19, 1900.

    Article  PubMed  PubMed Central  Google Scholar 

  • Shin, L.J., Lo, J.C., Chen, G.H., Callis, J., Fu, H., and Yeh, K.C. (2013). IRT1 DEGRADATION FACTOR1, a RING E3 ubiquitin ligase, regulates the degradation of IRON-REGULATED TRANSPORTER1 in Arabidopsis. Plant Cell 25, 3039–3051.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steinhorst, L., He, G., Moore, L.K., Schültke, S., Schmitz-Thom, I., Cao, Y., Hashimoto, K., Andrés, Z., Piepenburg, K., Ragel, P., et al. (2022). A Ca2+-sensor switch for tolerance to elevated salt stress in Arabidopsis. Dev Cell 57, 2081–2094.e7.

    Article  CAS  PubMed  Google Scholar 

  • Su, H., Wang, T., Ju, C., Deng, J., Zhang, T., Li, M., Tian, H., and Wang, C. (2021). Abscisic acid signaling negatively regulates nitrate uptake via phosphorylation of NRT1.1 by SnRK2s in Arabidopsis. J Integr Plant Biol 63, 597–610.

    Article  CAS  Google Scholar 

  • Supek, F., Supekova, L., Nelson, H., and Nelson, N. (1996). A yeast manganese transporter related to the macrophage protein involved in conferring resistance to mycobacteria. Proc Natl Acad Sci USA 93, 5105–5110.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Valmonte, G.R., Arthur, K., Higgins, C.M., and MacDiarmid, R.M. (2014). Calcium-dependent protein kinases in plants: evolution, expression and function. Plant Cell Physiol 55, 551–569.

    Article  CAS  PubMed  Google Scholar 

  • van Kleeff, P.J.M., Gao, J., Mol, S., Zwart, N., Zhang, H., Li, K.W., and de Boer, A.H. (2018). The Arabidopsis GORK K+-channel is phosphorylated by calcium-dependent protein kinase 21 (CPK21), which in turn is activated by 14–3-3 proteins. Plant Physiol Biochem 125, 219–231.

    Article  CAS  PubMed  Google Scholar 

  • Vert, G., Grotz, N., Dédaldéchamp, F., Gaymard, F., Guerinot, M.L., Briat, J.F., and Curie, C. (2002). IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14, 1223–1233.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, J. P., Xu, Y. P., Munyampundu, J. P., Liu, T. Y., and Cai, X.Z. (2016). Calcium-dependent protein kinase (CDPK) and CDPK-related kinase (CRK) gene families in tomato: genome-wide identification and functional analyses in disease resistance. Mol Genet Genomics 291, 661–676.

    Article  CAS  PubMed  Google Scholar 

  • Waters, B.M., Chu, H.H., DiDonato, R.J., Roberts, L.A., Eisley, R.B., Lahner, B., Salt, D.E., and Walker, E.L. (2006). Mutations in Arabidopsis Yellow Stripe-Likel and Yellow Stripe-Like3 reveal their roles in metal ion homeostasis and loading of metal ions in seeds. Plant Physiol 141, 1446–1458.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wild, M., Davière, J.M., Regnault, T., Sakvarelidze-Achard, L., Carrera, E., Lopez Diaz, I., Cayrel, A., Dubeaux, G., Vert, G., and Achard, P. (2016). Tissue-specific regulation of gibberellin signaling fine-tunes Arabidopsis iron-deficiency responses. Dev Cell 37, 190–200.

    Article  CAS  PubMed  Google Scholar 

  • Yang, Z., Wang, C., Xue, Y., Liu, X., Chen, S., Song, C.P., Yang, Y., and Guo, Y. (2019). Calcium-activated 14–3-3 proteins as a molecular switch in salt stress tolerance. Nat Commun 10, 1199.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yip Delormel, T., and Boudsocq, M. (2019). Properties and functions of calcium-dependent protein kinases and their relatives in Arabidopsis thaliana. New Phytol 224, 585–604.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, B., Zhang, C., Liu, C., Fu, A., and Luan, S. (2021a). A Golgi-localized manganese transporter functions in pollen tube tip growth to control male fertility in Arabidopsis. Plant Commun 2, 100178.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, Z., Fu, D., Sun, Z., Ju, C., Miao, C., Wang, Z., Xie, D., Ma, L., Gong, Z., and Wang, C. (2021b). Tonoplast-associated calcium signaling regulates manganese homeostasis in Arabidopsis. Mol Plant 14, 805–819.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, Z., Hu, X., Zhang, Y., Miao, Z., Xie, C., Meng, X., Deng, J., Wen, J., Mysore, K.S., Frugier, F., et al. (2016). Opposing control by transcription factors MYB61 and MYB3 increases freezing tolerance by relieving C-repeat binding factor suppression. Plant Physiol 172, 1306–1323.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou, L., Lan, W., Jiang, Y., Fang, W., and Luan, S. (2014). A calcium-dependent protein kinase interacts with and activates a calcium channel to regulate pollen tube growth. Mol Plant 7, 369–376.

    Article  CAS  PubMed  Google Scholar 

  • Zhou, J., Wang, X., He, Y., Sang, T., Wang, P., Dai, S., Zhang, S., and Meng, X. (2020). Differential phosphorylation of the transcription factor WRKY33 by the protein kinases CPK5/CPK6 and MPK3/MPK6 cooperatively regulates camalexin biosynthesis in Arabidopsis. Plant Cell 32, 2621–2638.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu, S.Y., Yu, X.C., Wang, X.J., Zhao, R., Li, Y., Fan, R.C., Shang, Y., Du, S.Y., Wang, X.F., Wu, F.Q., et al. (2007). Two calcium-dependent protein kinases, CPK4 and CPK11, regulate abscisic acid signal transduction in Arabidopsis. Plant Cell 19, 3019–3036.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (32222008, 32100215, 31900236), Northwest A&F University (Z111021604), the open funds of China Postdoctoral Science Foundation (2018M643740), and Natural Science Basic Research Plan in Shaanxi Province of China (2019JQ-150). We thank Dr. Chao-feng Huang (National Key Laboratory of Plant Molecular Genetics) for yeast strain Δfet3/fet4, Dr. Hua Zhao, Dr. Xue-ling Huang and Feng-ping Yuan (State Key Laboratory of Crop Stress Biology in Arid Areas) for providing Olympus IX83-FV3000, CFX connect, and other platforms, Dr. Xiao-han Li (College of Natural Resources and Environment, Northwest A&F University) for providing technical support with ICP-MS.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Cun Wang.

Ethics declarations

The author(s) declare that they have no conflict of interest.

Electronic Supplementary Material

11427_2022_2330_MOESM1_ESM.pdf

Calcium-dependent protein kinases CPK21 and CPK23 phosphorylate and activate IRT1 to regulate iron deficiency in Arabidopsis

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, Z., Zhang, Y., Liu, Y. et al. Calcium-dependent protein kinases CPK21 and CPK23 phosphorylate and activate the iron-regulated transporter IRT1 to regulate iron deficiency in Arabidopsis. Sci. China Life Sci. 66, 2646–2662 (2023). https://doi.org/10.1007/s11427-022-2330-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-022-2330-4

Keywords