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Protein Phosphorylation in Plant Cell Signaling

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Plant Phosphoproteomics

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2358))

Abstract

Owing to their sessile nature, plants have evolved sophisticated sensory mechanisms to respond quickly and precisely to the changing environment. The extracellular stimuli are perceived and integrated by diverse receptors, such as receptor-like protein kinases (RLKs) and receptor-like proteins (RLPs), and then transmitted to the nucleus by complex cellular signaling networks, which play vital roles in biological processes including plant growth, development, reproduction, and stress responses. The posttranslational modifications (PTMs) are important regulators for the diversification of protein functions in plant cell signaling. Protein phosphorylation is an important and well-characterized form of the PTMs, which influences the functions of many receptors and key components in cellular signaling. Protein phosphorylation in plants predominantly occurs on serine (Ser) and threonine (Thr) residues, which is dynamically and reversibly catalyzed by protein kinases and protein phosphatases, respectively. In this review, we focus on the function of protein phosphorylation in plant cell signaling, especially plant hormone signaling, and highlight the roles of protein phosphorylation in plant abiotic stress responses.

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References

  1. Zulawski M, Schulze WX (2015) The plant kinome. Methods Mol Biol 1306:1–23. https://doi.org/10.1007/978-1-4939-2648-0_1

    Article  CAS  PubMed  Google Scholar 

  2. Schweighofer A, Meskiene I (2015) Phosphatases in plants. Methods Mol Biol 1306:25–46. https://doi.org/10.1007/978-1-4939-2648-0_2

    Article  CAS  PubMed  Google Scholar 

  3. Zulawski M, Schulze G, Braginets R et al (2014) The Arabidopsis Kinome: phylogeny and evolutionary insights into functional diversification. BMC Genomics 15(1):548. https://doi.org/10.1186/1471-2164-15-548

    Article  PubMed  PubMed Central  Google Scholar 

  4. Millar AH, Heazlewood JL, Giglione C et al (2019) The scope, functions, and dynamics of posttranslational protein modifications. Annu Rev Plant Biol 70:119–151. https://doi.org/10.1146/annurev-arplant-050718-100211

    Article  CAS  PubMed  Google Scholar 

  5. van Wijk KJ, Friso G, Walther D et al (2014) Meta-analysis of Arabidopsis thaliana phospho-proteomics data reveals compartmentalization of phosphorylation motifs. Plant Cell 26(6):2367–2389. https://doi.org/10.1105/tpc.114.125815

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Lohrmann J, Harter K (2002) Plant two-component signaling systems and the role of response regulators. Plant Physiol 128(2):363–369. https://doi.org/10.1104/pp.010907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Trentini DB, Suskiewicz MJ, Heuck A et al (2016) Arginine phosphorylation marks proteins for degradation by a Clp protease. Nature 539(7627):48–53. https://doi.org/10.1038/nature20122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. De Smet I, Voss U, Jürgens G et al (2009) Receptor-like kinases shape the plant. Nat Cell Biol 11(10):1166–1173. https://doi.org/10.1038/ncb1009-1166

    Article  CAS  PubMed  Google Scholar 

  9. Jamieson PA, Shan L, He P (2018) Plant cell surface molecular cypher: receptor-like proteins and their roles in immunity and development. Plant Sci 274:242–251. https://doi.org/10.1016/j.plantsci.2018.05.030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. He Y, Zhou J, Shan L et al (2018) Plant cell surface receptor-mediated signaling—a common theme amid diversity. J Cell Sci 131(2):jcs209353. https://doi.org/10.1242/jcs.209353

  11. Liang X, Zhou JM (2018) Receptor-like cytoplasmic kinases: central players in plant receptor kinase-mediated signaling. Annu Rev Plant Biol 69:267–299. https://doi.org/10.1146/annurev-arplant-042817-040540

    Article  CAS  PubMed  Google Scholar 

  12. Hagihara S, Yamada R, Itami K et al (2019) Dissecting plant hormone signaling with synthetic molecules: perspective from the chemists. Curr Opin Plant Biol 47:32–37. https://doi.org/10.1016/j.pbi.2018.09.002

    Article  CAS  PubMed  Google Scholar 

  13. Shigenaga AM, Berens ML, Tsuda K et al (2017) Towards engineering of hormonal crosstalk in plant immunity. Curr Opin Plant Biol 38:164–172. https://doi.org/10.1016/j.pbi.2017.04.021

    Article  CAS  PubMed  Google Scholar 

  14. Kim TW, Guan S, Sun Y et al (2009) Brassinosteroid signal transduction from cell-surface receptor kinases to nuclear transcription factors. Nat Cell Biol 11(10):1254–1260. https://doi.org/10.1038/ncb1970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Hwang I, Sheen J, Müller B (2012) Cytokinin signaling networks. Annu Rev Plant Biol 63:353–380. https://doi.org/10.1146/annurev-arplant-042811-105503

    Article  CAS  PubMed  Google Scholar 

  16. Merchante C, Alonso JM, Stepanova AN (2013) Ethylene signaling: simple ligand, complex regulation. Curr Opin Plant Biol 16(5):554–560. https://doi.org/10.1016/j.pbi.2013.08.001

    Article  CAS  PubMed  Google Scholar 

  17. Yao R, Ming Z, Yan L et al (2016) DWARF14 is a non-canonical hormone receptor for strigolactone. Nature 536(7617):469–473. https://doi.org/10.1038/nature19073

    Article  CAS  PubMed  Google Scholar 

  18. Santiago J, Dupeux F, Round A et al (2009) The abscisic acid receptor PYR1 in complex with abscisic acid. Nature 462(7273):665–668. https://doi.org/10.1038/nature08591

    Article  CAS  PubMed  Google Scholar 

  19. Dharmasiri N, Dharmasiri S, Estelle M (2005) The F-box protein TIR1 is an auxin receptor. Nature 435(7041):441–445. https://doi.org/10.1038/nature03543

    Article  CAS  PubMed  Google Scholar 

  20. Murase K, Hirano Y, Sun TP et al (2008) Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456(7221):459–463. https://doi.org/10.1038/nature07519

    Article  CAS  PubMed  Google Scholar 

  21. Sheard LB, Tan X, Mao H et al (2010) Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468(7322):400–405. https://doi.org/10.1038/nature09430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Fu ZQ, Yan S, Saleh A et al (2012) NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 486(7402):228–232. https://doi.org/10.1038/nature11162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Ding Y, Sun T, Ao K et al (2018) Opposite roles of salicylic acid receptors NPR1 and NPR3/NPR4 in transcriptional regulation of plant immunity. Cell 173(6):1454–1467. https://doi.org/10.1016/j.cell.2018.03.044

  24. Santiago J, Brandt B, Wildhagen M et al (2016) Mechanistic insight into a peptide hormone signaling complex mediating floral organ abscission. Elife 5:e15075. https://doi.org/10.7554/eLife.15075

  25. van Zanten M, Snoek LB, Proveniers MC et al (2009) The many functions of ERECTA. Trends Plant Sci 14(4):214–218. https://doi.org/10.1016/j.tplants.2009.01.010

    Article  CAS  PubMed  Google Scholar 

  26. Shen H, Zhong X, Zhao F et al (2015) Overexpression of receptor-like kinase ERECTA improves thermotolerance in rice and tomato. Nat Biotechnol 33(9):996–1003. https://doi.org/10.1038/nbt.3321

    Article  CAS  PubMed  Google Scholar 

  27. Shiu SH, Karlowski WM, Pan R et al (2004) Comparative analysis of the receptor-like kinase family in Arabidopsis and rice. Plant Cell 16(5):1220–1234. https://doi.org/10.1105/tpc.020834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Vij S, Giri J, Dansana PK et al (2008) The receptor-like cytoplasmic kinase (OsRLCK) gene family in rice: organization, phylogenetic relationship, and expression during development and stress. Mol Plant 1(5):732–750. https://doi.org/10.1093/mp/ssn047

    Article  CAS  PubMed  Google Scholar 

  29. Kerk D, Templeton G, Moorhead GB (2008) Evolutionary radiation pattern of novel protein phosphatases revealed by analysis of protein data from the completely sequenced genomes of humans, green algae, and higher plants. Plant Physiol 146(2):351–367. https://doi.org/10.1104/pp.107.111393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Uhrig RG, Labandera AM, Moorhead GB (2013) Arabidopsis PPP family of serine/threonine protein phosphatases: many targets but few engines. Trends Plant Sci 18(9):505–513. https://doi.org/10.1016/j.tplants.2013.05.004

    Article  CAS  PubMed  Google Scholar 

  31. Fuchs S, Grill E, Meskiene I et al (2013) Type 2C protein phosphatases in plants. FEBS J 280(2):681–693. https://doi.org/10.1111/j.1742-4658.2012.08670.x

    Article  CAS  PubMed  Google Scholar 

  32. Wang Q, Qin G, Cao M et al (2020) A phosphorylation-based switch controls TAA1-mediated auxin biosynthesis in plants. Nat Commun 11(1):679. https://doi.org/10.1038/s41467-020-14395-w

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Cao M, Chen R, Li P et al (2019) TMK1-mediated auxin signalling regulates differential growth of the apical hook. Nature 568(7751):240–243. https://doi.org/10.1038/s41586-019-1069-7

    Article  CAS  PubMed  Google Scholar 

  34. Huang R, Zheng R, He J et al (2019) Noncanonical auxin signaling regulates cell division pattern during lateral root development. Proc Natl Acad Sci U S A 116(42):21285–21290. https://doi.org/10.1073/pnas.1910916116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Jia W, Li B, Li S et al (2016) Mitogen-activated protein kinase cascade MKK7-MPK6 plays important roles in plant development and regulates shoot branching by phosphorylating PIN1 in Arabidopsis. PLoS Biol 14(9):e1002550. https://doi.org/10.1371/journal.pbio.1002550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Zourelidou M, Absmanner B, Weller B et al (2014) Auxin efflux by PIN-FORMED proteins is activated by two different protein kinases, D6 PROTEIN KINASE and PINOID. Elife 3:e02860. https://doi.org/10.7554/eLife.02860

  37. Yoon GM (2015) New insights into the protein turnover regulation in ethylene biosynthesis. Mol Cells 38(7):597–603. https://doi.org/10.14348/molcells.2015.0152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Hall BP, Shakeel SN, Amir M et al (2012) Histidine kinase activity of the ethylene receptor ETR1 facilitates the ethylene response in Arabidopsis. Plant Physiol 159(2):682–695. https://doi.org/10.1104/pp.112.196790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Qiao H, Shen Z, Huang SS et al (2012) Processing and subcellular trafficking of ER-tethered EIN2 control response to ethylene gas. Science 338(6105):390–393. https://doi.org/10.1126/science.1225974

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Yoo SD, Cho YH, Tena G et al (2008) Dual control of nuclear EIN3 by bifurcate MAPK cascades in C2H4 signalling. Nature 451(7180):789–795. https://doi.org/10.1038/nature06543

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Ishida S, Yuasa T, Nakata M et al (2008) A tobacco calcium-dependent protein kinase, CDPK1, regulates the transcription factor REPRESSION OF SHOOT GROWTH in response to gibberellins. Plant Cell 20(12):3273–3288. https://doi.org/10.1105/tpc.107.057489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Fukazawa J, Nakata M, Ito T et al (2010) The transcription factor RSG regulates negative feedback of NtGA20ox1 encoding GA 20-oxidase. Plant J 62(6):1035–1045. https://doi.org/10.1111/j.1365-313X.2010.04215.x

    Article  CAS  PubMed  Google Scholar 

  43. Qin Q, Wang W, Guo X et al (2014) Arabidopsis DELLA protein degradation is controlled by a type-one protein phosphatase, TOPP4. PLoS Genet 10(7):e1004464. https://doi.org/10.1371/journal.pgen.1004464

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Shen Q, Zhan X, Yang P et al (2019) Dual activities of plant cGMP-dependent protein kinase and its roles in gibberellin signaling and salt stress. Plant Cell 31(12):3073–3091. https://doi.org/10.1105/tpc.19.00510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Yang W, Zhang W, Wang X (2017) Post-translational control of ABA signalling: the roles of protein phosphorylation and ubiquitination. Plant Biotechnol J 15(1):4–14. https://doi.org/10.1111/pbi.12652

    Article  CAS  PubMed  Google Scholar 

  46. Cutler SR, Rodriguez PL, Finkelstein RR et al (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679. https://doi.org/10.1146/annurev-arplant-042809-112122

    Article  CAS  PubMed  Google Scholar 

  47. Wang P, Zhao Y, Li Z et al (2018) Reciprocal regulation of the TOR kinase and ABA receptor balances plant growth and stress response. Mol Cell 69(1):100–112. https://doi.org/10.1016/j.molcel.2017.12.002

  48. Tan W, Zhang D, Zhou H et al (2018) Transcription factor HAT1 is a substrate of SnRK2.3 kinase and negatively regulates ABA synthesis and signaling in Arabidopsis responding to drought. PLoS Genet 14(4):e1007336. https://doi.org/10.1371/journal.pgen.1007336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Lyzenga WJ, Liu H, Schofield A et al (2013) Arabidopsis CIPK26 interacts with KEG, components of the ABA signalling network and is degraded by the ubiquitin-proteasome system. J Exp Bot 64(10):2779–2791. https://doi.org/10.1093/jxb/ert123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Planas-Riverola A, Gupta A, Betegón-Putze I et al (2019) Brassinosteroid signaling in plant development and adaptation to stress. Development 146(5):dev151894. https://doi.org/10.1242/dev.151894

  51. Huang X, Hou L, Meng J et al (2018) The antagonistic action of abscisic acid and cytokinin signaling mediates drought stress response in Arabidopsis. Mol Plant 11(7):970–982. https://doi.org/10.1016/j.molp.2018.05.001

    Article  CAS  PubMed  Google Scholar 

  52. Spoel SH, Mou Z, Tada Y et al (2009) Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity. Cell 137(5):860–872. https://doi.org/10.1016/j.cell.2009.03.038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Saleh A, Withers J, Mohan R et al (2015) Posttranslational modifications of the master transcriptional regulator NPR1 enable dynamic but tight control of plant immune responses. Cell Host Microbe 18(2):169–182. https://doi.org/10.1016/j.chom.2015.07.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Lee HJ, Park YJ, Seo PJ et al (2015) Systemic immunity requires SnRK2.8-mediated nuclear import of NPR1 in Arabidopsis. Plant Cell 27(12):3425–3438. https://doi.org/10.1105/tpc.15.00371

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Tan S, Abas M, Verstraeten I et al (2020) Salicylic acid targets protein phosphatase 2A to attenuate growth in plants. Curr Biol 30(3):381–395. https://doi.org/10.1016/j.cub.2019.11.058

  56. Prodhan MY, Munemasa S, Nahar MN et al (2018) Guard cell salicylic acid signaling is Iintegrated into abscisic acid signaling via the Ca2+/CPK-dependent pathway. Plant Physiol 178(1):441–450. https://doi.org/10.1104/pp.18.00321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Carvalhais LC, Schenk PM, Dennis PG (2017) Jasmonic acid signalling and the plant holobiont. Curr Opin Microbiol 37:42–47. https://doi.org/10.1016/j.mib.2017.03.009

    Article  CAS  PubMed  Google Scholar 

  58. Kazan K, Manners JM (2013) MYC2: the master in action. Mol Plant 6(3):686–703. https://doi.org/10.1093/mp/sss128

    Article  CAS  PubMed  Google Scholar 

  59. Guo H, Nolan TM, Song G et al (2018) FERONIA receptor kinase contributes to plant immunity by suppressing jasmonic acid signaling in Arabidopsis thaliana. Curr Biol 28(20):3316–3324. https://doi.org/10.1016/j.cub.2018.07.078

  60. Zhai Q, Yan L, Tan D et al (2013) Phosphorylation-coupled proteolysis of the transcription factor MYC2 is important for jasmonate-signaled plant immunity. PLoS Genet 9(4):e1003422. https://doi.org/10.1371/journal.pgen.1003422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Lal NK, Nagalakshmi U, Hurlburt NK et al (2018) The receptor-like cytoplasmic kinase BIK1 localizes to the nucleus and regulates defense hormone expression during plant innate immunity. Cell Host Microbe 23(4):485–497. https://doi.org/10.1016/j.chom.2018.03.010

  62. Yan C, Fan M, Yang M et al (2018) Injury activates Ca2+/calmodulin-dependent phosphorylation of JAV1-JAZ8-WRKY51 complex for jasmonate biosynthesis. Mol Cell 70(1):136–149. https://doi.org/10.1016/j.molcel.2018.03.013

  63. Gong Z, Xiong L, Shi H et al (2020) Plant abiotic stress response and nutrient use efficiency. Sci China Life Sci 63(5):635–674. https://doi.org/10.1007/s11427-020-1683-x

    Article  PubMed  Google Scholar 

  64. Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167(2):313–324. https://doi.org/10.1016/j.cell.2016.08.029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Rampitsch C (2017) Phosphoproteomics analysis for probing plant stress tolerance. Methods Mol Biol 1631:181–193. https://doi.org/10.1007/978-1-4939-7136-7_11

    Article  CAS  PubMed  Google Scholar 

  66. Mithoe SC, Menke FL (2011) Phosphoproteomics perspective on plant signal transduction and tyrosine phosphorylation. Phytochemistry 72(10):997–1006. https://doi.org/10.1016/j.phytochem.2010.12.009

    Article  CAS  PubMed  Google Scholar 

  67. Wu X, Gong F, Cao D et al (2016) Advances in crop proteomics: PTMs of proteins under abiotic stress. Proteomics 16(5):847–865. https://doi.org/10.1002/pmic.201500301

    Article  CAS  PubMed  Google Scholar 

  68. Park CJ, Caddell DF, Ronald PC (2012) Protein phosphorylation in plant immunity: insights into the regulation of pattern recognition receptor-mediated signaling. Front Plant Sci 3:177. https://doi.org/10.3389/fpls.2012.00177

    Article  PubMed  PubMed Central  Google Scholar 

  69. Wu Y, Zhou JM (2013) Receptor-like kinases in plant innate immunity. J Integr Plant Biol 55(12):1271–1286. https://doi.org/10.1111/jipb.12123

    Article  CAS  PubMed  Google Scholar 

  70. Yuan F, Yang H, Xue Y et al (2014) OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature 514(7522):367–371. https://doi.org/10.1038/nature13593

    Article  CAS  PubMed  Google Scholar 

  71. Ma Y, Dai X, Xu Y et al (2015) COLD1 confers chilling tolerance in rice. Cell 160(6):1209–1221. https://doi.org/10.1016/j.cell.2015.01.046

    Article  CAS  PubMed  Google Scholar 

  72. Legris M, Klose C, Burgie ES et al (2016) Phytochrome B integrates light and temperature signals in Arabidopsis. Science 354(6314):897–900. https://doi.org/10.1126/science.aaf5656

    Article  CAS  PubMed  Google Scholar 

  73. Jung JH, Domijan M, Klose C et al (2016) Phytochromes function as thermosensors in Arabidopsis. Science 354(6314):886–889. https://doi.org/10.1126/science.aaf6005

    Article  CAS  PubMed  Google Scholar 

  74. Saidi Y, Finka A, Muriset M et al (2009) The heat shock response in moss plants is regulated by specific calcium-permeable channels in the plasma membrane. Plant Cell 21(9):2829–2843. https://doi.org/10.1105/tpc.108.065318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Kumar SV, Wigge PA (2010) H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140(1):136–147. https://doi.org/10.1016/j.cell.2009.11.006

    Article  CAS  PubMed  Google Scholar 

  76. Jiang Z, Zhou X, Tao M et al (2019) Plant cell-surface GIPC sphingolipids sense salt to trigger Ca2+ influx. Nature 572(7769):341–346. https://doi.org/10.1038/s41586-019-1449-z

    Article  CAS  PubMed  Google Scholar 

  77. Viczián A, Ádám É, Staudt AM et al (2020) Differential phosphorylation of the N-terminal extension regulates phytochrome B signaling. New Phytol 225(4):1635–1650. https://doi.org/10.1111/nph.16243

    Article  CAS  PubMed  Google Scholar 

  78. Su Y, Wang S, Zhang F et al (2017) Phosphorylation of histone H2A at serine 95: a plant-specific mark involved in flowering time regulation and H2A.Z deposition. Plant Cell 29(9):2197–2213. https://doi.org/10.1105/tpc.17.00266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Gao F, Han X, Wu J et al (2012) A heat-activated calcium-permeable channel—Arabidopsis cyclic nucleotide-gated ion channel 6—is involved in heat shock responses. Plant J 70(6):1056–1069. https://doi.org/10.1111/j.1365-313X.2012.04969.x

    Article  CAS  PubMed  Google Scholar 

  80. Tian W, Hou C, Ren Z et al (2019) A calmodulin-gated calcium channel links pathogen patterns to plant immunity. Nature 572(7767):131–135. https://doi.org/10.1038/s41586-019-1413-y

    Article  CAS  PubMed  Google Scholar 

  81. Toyota M, Spencer D, Sawai-Toyota S et al (2018) Glutamate triggers long-distance, calcium-based plant defense signaling. Science 361(6407):1112–1115. https://doi.org/10.1126/science.aat7744

    Article  CAS  PubMed  Google Scholar 

  82. Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61:593–620. https://doi.org/10.1146/annurev-arplant-070109-104628

    Article  CAS  PubMed  Google Scholar 

  83. Drerup MM, Schlücking K, Hashimoto K et al (2013) The Calcineurin B-like calcium sensors CBL1 and CBL9 together with their interacting protein kinase CIPK26 regulate the Arabidopsis NADPH oxidase RBOHF. Mol Plant 6(2):559–569. https://doi.org/10.1093/mp/sst009

    Article  CAS  PubMed  Google Scholar 

  84. Latz A, Mehlmer N, Zapf S et al (2013) Salt stress triggers phosphorylation of the Arabidopsis vacuolar K+ channel TPK1 by calcium-dependent protein kinases (CDPKs). Mol Plant 6(4):1274–1289. https://doi.org/10.1093/mp/sss158

    Article  CAS  PubMed  Google Scholar 

  85. Liu J, Feng L, Li J et al (2015) Genetic and epigenetic control of plant heat responses. Front Plant Sci 6:267. https://doi.org/10.3389/fpls.2015.00267

    Article  PubMed  PubMed Central  Google Scholar 

  86. Busch W, Wunderlich M, Schöffl F (2005) Identification of novel heat shock factor-dependent genes and biochemical pathways in Arabidopsis thaliana. Plant J 41(1):1–14. https://doi.org/10.1111/j.1365-313X.2004.02272.x

    Article  CAS  PubMed  Google Scholar 

  87. Evrard A, Kumar M, Lecourieux D et al (2013) Regulation of the heat stress response in Arabidopsis by MPK6-targeted phosphorylation of the heat stress factor HsfA2. PeerJ 1:e59. https://doi.org/10.7717/peerj.59

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Liu HT, Gao F, Li GL et al (2008) The calmodulin-binding protein kinase 3 is part of heat-shock signal transduction in Arabidopsis thaliana. Plant J 55(5):760–773. https://doi.org/10.1111/j.1365-313X.2008.03544.x

    Article  CAS  PubMed  Google Scholar 

  89. Andrási N, Rigó G, Zsigmond L et al (2019) The mitogen-activated protein kinase 4-phosphorylated heat shock factor A4A regulates responses to combined salt and heat stresses. J Exp Bot 70(18):4903–4918. https://doi.org/10.1093/jxb/erz217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Nguyen XC, Kim SH, Lee K et al (2012) Identification of a C2H2-type zinc finger transcription factor (ZAT10) from Arabidopsis as a substrate of MAP kinase. Plant Cell Rep 31(4):737–745. https://doi.org/10.1007/s00299-011-1192-x

    Article  CAS  PubMed  Google Scholar 

  91. Wang F, Yang Y, Wang Z et al (2015) A critical role of lyst-interacting protein 5, a positive regulator of multivesicular body biogenesis, in plant responses to heat and salt stresses. Plant Physiol 169(1):497–511. https://doi.org/10.1104/pp.15.00518

  92. Samakovli D, Tichá T, Vavrdová T et al (2020) YODA-HSP90 module regulates phosphorylation-dependent inactivation of SPEECHLESS to control stomatal development under acute heat stress in Arabidopsis. Mol Plant 13(4):612–633. https://doi.org/10.1016/j.molp.2020.01.001

    Article  CAS  PubMed  Google Scholar 

  93. Link V, Sinha AK, Vashista P et al (2002) A heat-activated MAP kinase in tomato: a possible regulator of the heat stress response. FEBS Lett 531(2):179–183. https://doi.org/10.1016/s0014-5793(02)03498-1

    Article  CAS  PubMed  Google Scholar 

  94. Ding H, He J, Wu Y et al (2018) The tomato mitogen-activated protein kinase SlMPK1 is as a negative regulator of the high-temperature stress response. Plant Physiol 177(2):633–651. https://doi.org/10.1104/pp.18.00067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Chan A, Carianopol C, Tsai AY et al (2017) SnRK1 phosphorylation of FUSCA3 positively regulates embryogenesis, seed yield, and plant growth at high temperature in Arabidopsis. J Exp Bot 68(15):4219–4231. https://doi.org/10.1093/jxb/erx233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Mizoi J, Kanazawa N, Kidokoro S et al (2019) Heat-induced inhibition of phosphorylation of the stress-protective transcription factor DREB2A promotes thermotolerance of Arabidopsis thaliana. J Biol Chem 294(3):902–917. https://doi.org/10.1074/jbc.RA118.002662

    Article  CAS  PubMed  Google Scholar 

  97. Li H, Ding Y, Shi Y et al (2017) MPK3- and MPK6-mediated ICE1 phosphorylation negatively regulates ICE1 stability and freezing tolerance in Arabidopsis. Dev Cell 43(5):630–642. https://doi.org/10.1016/j.devcel.2017.09.025

  98. Zhao C, Wang P, Si T et al (2017) MAP kinase cascades regulate the cold response by modulating ICE1 protein stability. Dev Cell 43(5):618–629. https://doi.org/10.1016/j.devcel.2017.09.024

  99. Ye K, Li H, Ding Y et al (2019) BRASSINOSTEROID-INSENSITIVE2 negatively regulates the stability of transcription factor ICE1 in response to cold stress in Arabidopsis. Plant Cell 31(11):2682–2696. https://doi.org/10.1105/tpc.19.00058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Ding Y, Li H, Zhang X et al (2015) OST1 kinase modulates freezing tolerance by enhancing ICE1 stability in Arabidopsis. Dev Cell 32(3):278–289. https://doi.org/10.1016/j.devcel.2014.12.023

    Article  CAS  PubMed  Google Scholar 

  101. Ding Y, Lv J, Shi Y et al (2019) EGR2 phosphatase regulates OST1 kinase activity and freezing tolerance in Arabidopsis. EMBO J 38(1):e99819. https://doi.org/10.15252/embj.201899819

  102. Zhang Z, Li J, Li F et al (2017) OsMAPK3 phosphorylates OsbHLH002/OsICE1 and inhibits its ubiquitination to activate OsTPP1 and enhances rice chilling tolerance. Dev Cell 43(6):731–743. https://doi.org/10.1016/j.devcel.2017.11.016

  103. Ding Y, Jia Y, Shi Y et al (2018) OST1-mediated BTF3L phosphorylation positively regulates CBFs during plant cold responses. EMBO J 37(8):e98228. https://doi.org/10.15252/embj.201798228

  104. Wang X, Ding Y, Li Z et al (2019) PUB25 and PUB26 promote plant freezing tolerance by degrading the cold signaling negative regulator MYB15. Dev Cell 51(2):222–235. https://doi.org/10.1016/j.devcel.2019.08.008

  105. Kim SH, Kim HS, Bahk S et al (2017) Phosphorylation of the transcriptional repressor MYB15 by mitogen-activated protein kinase 6 is required for freezing tolerance in Arabidopsis. Nucleic Acids Res 45(11):6613–6627. https://doi.org/10.1093/nar/gkx417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Liu Z, Jia Y, Ding Y et al (2017) Plasma membrane CRPK1-mediated phosphorylation of 14-3-3 proteins induces their nuclear import to fine-tune CBF signaling during cold response. Mol Cell 66(1):117–128. https://doi.org/10.1016/j.molcel.2017.02.016

  107. Feng W, Kita D, Peaucelle A et al (2018) The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca2+ signaling. Curr Biol 28(5):666–675. https://doi.org/10.1016/j.cub.2018.01.023

  108. Zhu JK (2000) Genetic analysis of plant salt tolerance using Arabidopsis. Plant Physiol 124(3):941–948. https://doi.org/10.1104/pp.124.3.941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Lin H, Yang Y, Quan R et al (2009) Phosphorylation of SOS3-LIKE CALCIUM BINDING PROTEIN8 by SOS2 protein kinase stabilizes their protein complex and regulates salt tolerance in Arabidopsis. Plant Cell 21(5):1607–1619. https://doi.org/10.1105/tpc.109.066217

    Article  PubMed  PubMed Central  Google Scholar 

  110. Yang Z, Wang C, Xue Y et al (2019) Calcium-activated 14-3-3 proteins as a molecular switch in salt stress tolerance. Nat Commun 10(1):1199. https://doi.org/10.1038/s41467-019-09181-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Zhou H, Lin H, Chen S et al (2014) Inhibition of the Arabidopsis salt overly sensitive pathway by 14-3-3 proteins. Plant Cell 26(3):1166–1182. https://doi.org/10.1105/tpc.113.117069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Ma L, Ye J, Yang Y et al (2019) The SOS2-SCaBP8 complex generates and fine-tunes an AtANN4-dependent calcium signature under salt stress. Dev Cell 48(5):697–709. https://doi.org/10.1016/j.devcel.2019.02.010

  113. Shen L, Zhuang B, Wu Q et al (2019) Phosphatidic acid promotes the activation and plasma membrane localization of MKK7 and MKK9 in response to salt stress. Plant Sci 287:110190. https://doi.org/10.1016/j.plantsci.2019.110190

    Article  CAS  PubMed  Google Scholar 

  114. Wang P, Shen L, Guo J et al (2019) Phosphatidic acid directly regulates PINOID-dependent phosphorylation and activation of the PIN-FORMED2 auxin efflux transporter in response to salt stress. Plant Cell 31(1):250–271. https://doi.org/10.1105/tpc.18.00528

    Article  CAS  PubMed  Google Scholar 

  115. Wang PH, Lee CE, Lin YS et al (2019) The glutamate receptor-like protein GLR3.7 interacts with 14-3-3ω and participates in salt stress response in Arabidopsis thaliana. Front Plant Sci 10:1169. https://doi.org/10.3389/fpls.2019.01169

    Article  PubMed  PubMed Central  Google Scholar 

  116. Zhou YB, Liu C, Tang DY et al (2018) The receptor-like cytoplasmic kinase STRK1 phosphorylates and activates CatC, thereby regulating H2O2 homeostasis and improving salt tolerance in rice. Plant Cell 30(5):1100–1118. https://doi.org/10.1105/tpc.17.01000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Mu C, Zhou L, Shan L et al (2019) Phosphatase GhDsPTP3a interacts with annexin protein GhANN8b to reversely regulate salt tolerance in cotton (Gossypium spp.). New Phytol 223(4):1856–1872. https://doi.org/10.1111/nph.15850

    Article  CAS  PubMed  Google Scholar 

  118. Ma QJ, Sun MH, Kang H et al (2019) A CIPK protein kinase targets sucrose transporter MdSUT2.2 at Ser(254) for phosphorylation to enhance salt tolerance. Plant Cell Environ 42(3):918–930. https://doi.org/10.1111/pce.13349

    Article  CAS  PubMed  Google Scholar 

  119. Zhao Y, Chan Z, Gao J et al (2016) ABA receptor PYL9 promotes drought resistance and leaf senescence. Proc Natl Acad Sci U S A 113(7):1949–1954. https://doi.org/10.1073/pnas.1522840113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Wong MM, Bhaskara GB, Wen TN et al (2019) Phosphoproteomics of Arabidopsis highly ABA-Induced1 identifies AT-Hook-Like10 phosphorylation required for stress growth regulation. Proc Natl Acad Sci U S A 116(6):2354–2363. https://doi.org/10.1073/pnas.1819971116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Jiang H, Tang B, Xie Z et al (2019) GSK3-like kinase BIN2 phosphorylates RD26 to potentiate drought signaling in Arabidopsis. Plant J 100(5):923–937. https://doi.org/10.1111/tpj.14484

    Article  CAS  PubMed  Google Scholar 

  122. Xie Z, Nolan T, Jiang H et al (2019) The AP2/ERF transcription factor TINY modulates brassinosteroid-regulated plant growth and drought responses in Arabidopsis. Plant Cell 31(8):1788–1806. https://doi.org/10.1105/tpc.18.00918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Nolan TM, Brennan B, Yang M et al (2017) Selective autophagy of BES1 mediated by DSK2 balances plant growth and survival. Dev Cell 41(1):33–46. https://doi.org/10.1016/j.devcel.2017.03.013

  124. Fang Y, Xiong L (2015) General mechanisms of drought response and their application in drought resistance improvement in plants. Cell Mol Life Sci 72(4):673–689. https://doi.org/10.1007/s00018-014-1767-0

    Article  CAS  PubMed  Google Scholar 

  125. Li F, Li M, Wang P et al (2017) Regulation of cotton (Gossypium hirsutum) drought responses by mitogen-activated protein (MAP) kinase cascade-mediated phosphorylation of GhWRKY59. New Phytol 215(4):1462–1475. https://doi.org/10.1111/nph.14680

    Article  CAS  PubMed  Google Scholar 

  126. Chen L, Sun H, Wang F et al (2020) Genome-wide identification of MAPK cascade genes reveals the GhMAP3K14-GhMKK11-GhMPK31 pathway is involved in the drought response in cotton. Plant Mol Biol 103(1–2):211–223. https://doi.org/10.1007/s11103-020-00986-0

    Article  CAS  PubMed  Google Scholar 

  127. Ma H, Chen J, Zhang Z et al (2017) MAPK kinase 10.2 promotes disease resistance and drought tolerance by activating different MAPKs in rice. Plant J 92(4):557–570. https://doi.org/10.1111/tpj.13674

    Article  CAS  PubMed  Google Scholar 

  128. Ning J, Li X, Hicks LM et al (2010) A Raf-like MAPKKK gene DSM1 mediates drought resistance through reactive oxygen species scavenging in rice. Plant Physiol 152(2):876–890. https://doi.org/10.1104/pp.109.149856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Li Y, Cai H, Liu P et al (2017) Arabidopsis MAPKKK18 positively regulates drought stress resistance via downstream MAPKK3. Biochem Biophys Res Commun 484(2):292–297. https://doi.org/10.1016/j.bbrc.2017.01.104

    Article  CAS  PubMed  Google Scholar 

  130. Wu L, Zu X, Zhang H et al (2015) Overexpression of ZmMAPK1 enhances drought and heat stress in transgenic Arabidopsis thaliana. Plant Mol Biol 88(4–5):429–443. https://doi.org/10.1007/s11103-015-0333-y

    Article  CAS  PubMed  Google Scholar 

  131. Zhu D, Chang Y, Pei T et al (2019) MAPK-like protein 1 positively regulates maize seedling drought sensitivity by suppressing ABA biosynthesis. Plant J 104(4):747–760. https://doi.org/10.1111/tpj.14660

    Article  CAS  Google Scholar 

  132. Ma Y, Cao J, Chen Q et al (2019) The kinase CIPK11 functions as a negative regulator in drought stress response in Arabidopsis. Int J Mol Sci 20(10):2422. https://doi.org/10.3390/ijms20102422

  133. Ma QJ, Sun MH, Lu J et al (2019) An apple sucrose transporter MdSUT2.2 is a phosphorylation target for protein kinase MdCIPK22 in response to drought. Plant Biotechnol J 17(3):625–637. https://doi.org/10.1111/pbi.13003

    Article  CAS  PubMed  Google Scholar 

  134. Huang K, Peng L, Liu Y et al (2018) Arabidopsis calcium-dependent protein kinase AtCPK1 plays a positive role in salt/drought-stress response. Biochem Biophys Res Commun 498(1):92–98. https://doi.org/10.1016/j.bbrc.2017.11.175

    Article  CAS  PubMed  Google Scholar 

  135. Bundó M, Coca M (2017) Calcium-dependent protein kinase OsCPK10 mediates both drought tolerance and blast disease resistance in rice plants. J Exp Bot 68(11):2963–2975. https://doi.org/10.1093/jxb/erx145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Cieśla A, Mituła F, Misztal L et al (2016) A role for barley calcium-dependent protein kinase CPK2a in the response to drought. Front Plant Sci 7:1550. https://doi.org/10.3389/fpls.2016.01550

    Article  PubMed  PubMed Central  Google Scholar 

  137. Mergner J, Frejno M, List M et al (2020) Mass-spectrometry-based draft of the Arabidopsis proteome. Nature 579(7799):409–414. https://doi.org/10.1038/s41586-020-2094-2

    Article  CAS  PubMed  Google Scholar 

  138. Wang P, Hsu CC, Du Y et al (2020) Mapping proteome-wide targets of protein kinases in plant stress responses. Proc Natl Acad Sci U S A 117(6):3270–3280. https://doi.org/10.1073/pnas.1919901117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This work was supported by funding from the National Natural Science Foundation of China (32070564 and 31600207) and Yunnan Fundamental Research Projects. Due to space limitations, we apologize to our colleagues whose important work are not cited in this review.

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  1. State Key Laboratory of Conservation and Utilization of Bio-Resources in Yunnan and Center for Life Science, School of Life Sciences, Yunnan University, Kunming, China

    Ping Li & Junzhong Liu

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    Xu Na Wu

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Li, P., Liu, J. (2021). Protein Phosphorylation in Plant Cell Signaling. In: Wu, X.N. (eds) Plant Phosphoproteomics. Methods in Molecular Biology, vol 2358. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-1625-3_3

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