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Protein Phosphorylation Response to Abiotic Stress in Plants

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Plant Phosphoproteomics

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

Abstract

Plants are an important part of nature because as photoautotrophs, they provide a nutrient source for many other living organisms. Due to their sessile nature, to overcome both biotic and abiotic stresses, plants have developed intricate mechanisms for perception of and reaction to these stresses, both on an external level (perception) and on an internal level (reaction). Specific proteins found within cells play crucial roles in stress mitigation by enhancing cellular processes that facilitate the plants survival during the unfavorable conditions. Well before plants are able to synthesize nascent proteins in response to stress, proteins which already exist in the cell can be subjected to an array of posttranslation modifications (PTMs) that permit a rapid response. These activated proteins can, in turn, aid in further stress responses. Different PTMs have different functions in growth and development of plants. Protein phosphorylation, a reversible form of modification has been well elucidated, and its role in signaling cascades is well documented. In this mini-review, we discuss the integration of protein phosphorylation with other components of abiotic stress–responsive pathways including phytohormones and ion homeostasis. Overall, this review demonstrates the high interconnectivity of the stress response system in plants and how readily plants are able to toggle between various signaling pathways in order to survive harsh conditions. Most notably, fluctuations of the cytosolic calcium levels seem to be a linking component of the various signaling pathways.

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References

  1. Pandey P, Irulappan V, Bagavathiannan MV et al (2017) Impact of combined abiotic and biotic stresses on plant growth and avenues for crop improvement by exploiting physio-morphological traits. Front Plant Sci 8(537). https://doi.org/10.3389/fpls.2017.00537

  2. Sun L, Jing Y, Liu X et al (2020) Heat stress-induced transposon activation correlates with 3D chromatin organization rearrangement in Arabidopsis. Nat Commun 11(1):1886. https://doi.org/10.1038/s41467-020-15809-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Li L, Lyu X, Hou C et al (2015) Widespread rearrangement of 3D chromatin organization underlies polycomb-mediated stress-induced silencing. Mol Cell 58(2):216–231. https://doi.org/10.1016/j.molcel.2015.02.023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Singh K, Foley RC, Oñate-Sánchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5(5):430–436. https://doi.org/10.1016/s1369-5266(02)00289-3

    Article  CAS  PubMed  Google Scholar 

  5. Tang K, Zhao L, Ren Y et al (2020) The transcription factor ICE1 functions in cold stress response by binding to the promoters of CBF and COR genes. J Integr Plant Biol 62(3):258–263. https://doi.org/10.1111/jipb.12918

    Article  CAS  PubMed  Google Scholar 

  6. Woodger FJ, Millar A, Murray F et al (2003) The role of GAMYB transcription factors in GA-regulated gene expression. J Plant Growth Regulat 22(2):176–184. https://doi.org/10.1007/s00344-003-0025-8

    Article  CAS  Google Scholar 

  7. Damaris RN, Lin Z, Yang P et al (2019) The rice alpha-amylase, conserved regulator of seed maturation and germination. Int J Mol Sci 20(2):450. https://doi.org/10.3390/ijms20020450

    Article  CAS  PubMed Central  Google Scholar 

  8. Pincus MR (2001) 2—Physiological structure and function of proteins. In: Sperelakis N (ed) Cell physiology source book, 3rd edn. Academic Press, San Diego, pp 19–42. https://doi.org/10.1016/B978-012656976-6/50094-9

    Chapter  Google Scholar 

  9. Alberts BJA, Lewis J et al (2002) The shape and structure of proteins. In: Molecular biology of the cell, vol 4. Garland Science, New York

    Google Scholar 

  10. Chen F, Nonogaki H, Bradford KJ (2002) A gibberellin-regulated xyloglucan endotransglycosylase gene is expressed in the endosperm cap during tomato seed germination. J Exp Bot 53(367):215–223. https://doi.org/10.1093/jexbot/53.367.215

    Article  CAS  PubMed  Google Scholar 

  11. Smith LM, Kelleher NL (2013) Proteoform: a single term describing protein complexity. Nat Methods 10(3):186–187. https://doi.org/10.1038/nmeth.2369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Aksnes H, Drazic A, Marie M et al (2016) First things first: vital protein marks by N-terminal acetyltransferases. Trends Biochem Sci 41(9):746–760. https://doi.org/10.1016/j.tibs.2016.07.005

    Article  CAS  PubMed  Google Scholar 

  13. Giglione C, Fieulaine S, Meinnel T (2015) N-terminal protein modifications: bringing back into play the ribosome. Biochimie 114:134–146. https://doi.org/10.1016/j.biochi.2014.11.008

    Article  CAS  PubMed  Google Scholar 

  14. Frottin F, Espagne C, Traverso JA et al (2009) Cotranslational proteolysis dominates glutathione homeostasis to support proper growth and development. Plant Cell 21(10):3296–3314. https://doi.org/10.1105/tpc.109.069757

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Traverso JA, Micalella C, Martinez A et al (2013) Roles of N-terminal fatty acid acylations in membrane compartment partitioning: Arabidopsis h-type thioredoxins as a case study. Plant Cell 25(3):1056–1077. https://doi.org/10.1105/tpc.112.106849

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Rips S, Bentley N, Jeong IS et al (2014) Multiple N-glycans cooperate in the subcellular targeting and functioning of Arabidopsis KORRIGAN1. Plant Cell 26(9):3792–3808. https://doi.org/10.1105/tpc.114.129718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Olsen JV, Blagoev B, Gnad F et al (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127(3):635–648

    Article  CAS  PubMed  Google Scholar 

  18. Seet BT, Dikic I, Zhou MM et al (2006) Reading protein modifications with interaction domains. Nat Rev Mol Cell Biol 7(7):473–483. https://doi.org/10.1038/nrm1960

    Article  CAS  PubMed  Google Scholar 

  19. Pawson T, Scott JD (1997) Signaling through scaffold, anchoring, and adaptor proteins. Science 278(5346):2075–2080. https://doi.org/10.1126/science.278.5346.2075

    Article  CAS  PubMed  Google Scholar 

  20. Champion A, Kreis M, Mockaitis K et al (2004) Arabidopsis kinome: after the casting. Funct Integr Genomics 4(3):163–187. https://doi.org/10.1007/s10142-003-0096-4

    Article  CAS  PubMed  Google Scholar 

  21. 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 

  22. Yan JX, Packer NH, Gooley AA et al (1998) Protein phosphorylation: technologies for the identification of phosphoamino acids. J Chromatogr A 808(1):23–41. https://doi.org/10.1016/S0021-9673(98)00115-0

    Article  CAS  PubMed  Google Scholar 

  23. Ajadi AA, Cisse A, Ahmad S et al (2020) Protein phosphorylation and phosphoproteome: an overview of rice. Rice Sci 27(3):184–200. https://doi.org/10.1016/j.rsci.2020.04.003

    Article  Google Scholar 

  24. Venter JC, Adams MD, Myers EW et al (2001) The sequence of the human genome. Science 291(5507):1304–1351. https://doi.org/10.1126/science.1058040

    Article  CAS  PubMed  Google Scholar 

  25. Mann M, Ong S-E, Grønborg M et al (2002) Analysis of protein phosphorylation using mass spectrometry: deciphering the phosphoproteome. Trends Biotechnol 20(6):261–268. https://doi.org/10.1016/S0167-7799(02)01944-3

    Article  CAS  PubMed  Google Scholar 

  26. Zulawski M, Braginets R, Schulze WX (2013) PhosPhAt goes kinases—searchable protein kinase target information in the plant phosphorylation site database PhosPhAt. Nucleic Acids Res 41(Database issue):D1176–D1184. https://doi.org/10.1093/nar/gks1081

    Article  CAS  PubMed  Google Scholar 

  27. Wang Y, Liu Z, Cheng H et al (2014) EKPD: a hierarchical database of eukaryotic protein kinases and protein phosphatases. Nucleic Acids Res 42(Database issue):D496–D502. https://doi.org/10.1093/nar/gkt1121

    Article  CAS  PubMed  Google Scholar 

  28. Wang Y, Liu Z, Cheng H et al (2013) EKPD: a hierarchical database of eukaryotic protein kinases and protein phosphatases. Nucleic Acids Res 42(D1):D496–D502. https://doi.org/10.1093/nar/gkt1121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Lin S, Chen L, Tao H et al (2016) Impact of SNPs on protein phosphorylation status in rice (Oryza sativa L.). Int J Mol Sci 17(11). https://doi.org/10.3390/ijms17111738

  30. Cheng H, Deng W, Wang Y et al (2014) dbPPT: a comprehensive database of protein phosphorylation in plants. Database 2014. https://doi.org/10.1093/database/bau121

  31. Zhong M, Li S, Huang F et al (2017) The phosphoproteomic response of rice seedlings to cadmium stress. Int J Mol Sci 18(10):2055

    Article  PubMed Central  Google Scholar 

  32. Chen X, Zhang W, Zhang B et al (2011) Phosphoproteins regulated by heat stress in rice leaves. Proteome Sci 9(1):37

    Article  PubMed  PubMed Central  Google Scholar 

  33. Chen J, Tian L, Xu H et al (2012) Cold-induced changes of protein and phosphoprotein expression patterns from rice roots as revealed by multiplex proteomic analysis. Plant Omics 5(2):194–199

    CAS  Google Scholar 

  34. Chang F, Hsu J-L, Hsu P-H et al (2012) Comparative phosphoproteomic analysis of microsomal fractions of Arabidopsis thaliana and Oryza sativa subjected to high salinity. Plant Sci 185:131–142

    Article  PubMed  Google Scholar 

  35. Yang Y, Guo Y (2018) Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytol 217(2):523–539. https://doi.org/10.1111/nph.14920

    Article  CAS  PubMed  Google Scholar 

  36. 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 

  37. Liu J, Ishitani M, Halfter U et al (2000) The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc Natl Acad Sci U S A 97(7):3730–3734. https://doi.org/10.1073/pnas.060034197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Liu J, Zhu JK (1998) A calcium sensor homolog required for plant salt tolerance. Science 280(5371):1943–1945. https://doi.org/10.1126/science.280.5371.1943

    Article  CAS  PubMed  Google Scholar 

  39. Quan R, Lin H, Mendoza I et al (2007) SCABP8/CBL10, a putative calcium sensor, interacts with the protein kinase SOS2 to protect Arabidopsis shoots from salt stress. Plant Cell 19(4):1415–1431. https://doi.org/10.1105/tpc.106.042291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Shi H, Ishitani M, Kim C et al (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci U S A 97(12):6896–6901. https://doi.org/10.1073/pnas.120170197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. 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 

  42. Kiegle E, Moore CA, Haseloff J et al (2000) Cell-type-specific calcium responses to drought, salt and cold in the Arabidopsis root. Plant J 23(2):267–278. https://doi.org/10.1046/j.1365-313x.2000.00786.x

    Article  CAS  PubMed  Google Scholar 

  43. Manishankar P, Wang N, Köster P et al (2018) Calcium signaling during salt stress and in the regulation of ion homeostasis. J Exp Bot 69(17):4215–4226. https://doi.org/10.1093/jxb/ery201

    Article  CAS  Google Scholar 

  44. Tan T, Cai J, Zhan E et al (2016) Stability and localization of 14-3-3 proteins are involved in salt tolerance in Arabidopsis. Plant Mol Biol 92(3):391–400. https://doi.org/10.1007/s11103-016-0520-5

    Article  CAS  PubMed  Google Scholar 

  45. Palmgren MG, Nissen P (2011) P-type ATPases. Annu Rev Biophys 40:243–266. https://doi.org/10.1146/annurev.biophys.093008.131331

    Article  CAS  PubMed  Google Scholar 

  46. Su Y, Luo W, Lin W et al (2015) Model of cation transportation mediated by high-affinity potassium transporters (HKTs) in higher plants. Biol Proced Online 17:1–1. https://doi.org/10.1186/s12575-014-0013-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Bose J, Xie YJ, Shen WB et al (2013) Haem oxygenase modifies salinity tolerance in Arabidopsis by controlling K+ retention via regulation of the plasma membrane H+-ATPase and by altering SOS1 transcript levels in roots. J Exp Bot 64(2):471–481. https://doi.org/10.1093/jxb/ers343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Rudashevskaya EL, Ye JY, Jensen ON et al (2012) Phosphosite mapping of P-type plasma membrane H+-ATPase in homologous and heterologous environments. J Biol Chem 287(7):4904–4913. https://doi.org/10.1074/jbc.M111.307264

    Article  CAS  PubMed  Google Scholar 

  49. Yang YQ, Qin YX, Xie CG et al (2010) The Arabidopsis chaperone J3 regulates the plasma membrane H+-ATPase through interaction with the PKS5 kinase. Plant Cell 22(4):1313–1332. https://doi.org/10.1105/tpc.109.069609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Yang Y, Wu Y, Ma L et al (2019) The Ca(2+) sensor SCaBP3/CBL7 modulates plasma membrane H(+)-ATPase activity and promotes alkali tolerance in Arabidopsis. Plant Cell 31(6):1367–1384. https://doi.org/10.1105/tpc.18.00568

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Krebs EG (1986) 1—The enzymology of control by phosphorylation. In: Boyer PD, Krebs EG (eds) The enzymes, vol 17. Academic Press, San Diego, pp 3–20. https://doi.org/10.1016/S1874-6047(08)60426-6

    Chapter  Google Scholar 

  52. Shin H, Shin H-S, Dewbre GR et al (2004) Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments. Plant J 39(4):629–642. https://doi.org/10.1111/j.1365-313X.2004.02161.x

    Article  CAS  PubMed  Google Scholar 

  53. Chiou TJ, Lin SI (2011) Signaling network in sensing phosphate availability in plants. Annu Rev Plant Biol 62:185–206. https://doi.org/10.1146/annurev-arplant-042110-103849

    Article  CAS  PubMed  Google Scholar 

  54. Liu T-Y, Huang T-K, Tseng C-Y et al (2012) PHO2-dependent degradation of PHO1 modulates phosphate homeostasis in Arabidopsis. Plant Cell 24(5):2168–2183. https://doi.org/10.1105/tpc.112.096636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Huang T-K, Han C-L, Lin S-I et al (2013) Identification of downstream components of ubiquitin-conjugating enzyme PHOSPHATE2 by quantitative membrane proteomics in Arabidopsis roots. Plant Cell 25(10):4044–4060. https://doi.org/10.1105/tpc.113.115998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Park BS, Seo JS, Chua N-H (2014) NITROGEN LIMITATION ADAPTATION recruits PHOSPHATE2 to target the phosphate transporter PT2 for degradation during the regulation of Arabidopsis phosphate homeostasis. Plant Cell 26(1):454–464. https://doi.org/10.1105/tpc.113.120311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Dong B, Rengel Z, Delhaize E (1998) Uptake and translocation of phosphate by pho2 mutant and wild-type seedlings of Arabidopsis thaliana. Planta 205(2):251–256. https://doi.org/10.1007/s004250050318

    Article  CAS  PubMed  Google Scholar 

  58. Delhaize E, Randall PJ (1995) Characterization of a phosphate-accumulator mutant of Arabidopsis thaliana. Plant Physiol 107(1):207–213. https://doi.org/10.1104/pp.107.1.207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Hu B, Zhu C, Li F et al (2011) LEAF TIP NECROSIS1 plays a pivotal role in the regulation of multiple phosphate starvation responses in rice. Plant Physiol 156(3):1101–1115. https://doi.org/10.1104/pp.110.170209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Cao Y, Yan Y, Zhang F et al (2014) Fine characterization of OsPHO2 knockout mutants reveals its key role in Pi utilization in rice. J Plant Physiol 171(3):340–348. https://doi.org/10.1016/j.jplph.2013.07.010

    Article  CAS  PubMed  Google Scholar 

  61. Chen J, Wang Y, Wang F et al (2015) The rice CK2 kinase regulates trafficking of phosphate transporters in response to phosphate levels. Plant Cell 27(3):711–723. https://doi.org/10.1105/tpc.114.135335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Wang F, Deng M, Chen J et al (2020) CASEIN KINASE2-dependent phosphorylation of PHOSPHATE2 fine-tunes phosphate homeostasis in rice. Plant Physiol 183(1):250–262. https://doi.org/10.1104/pp.20.00078

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Clarkson DT, Hanson JB (1980) The mineral nutrition of higher plants. Annu Rev Plant Physiol 31(1):239–298

    Article  CAS  Google Scholar 

  64. Zhao S, Zhang M-L, Ma T-L et al (2016) Phosphorylation of ARF2 relieves its repression of transcription of the K+ transporter gene HAK5 in response to low potassium stress. Plant Cell 28(12):3005–3019. https://doi.org/10.1105/tpc.16.00684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399. https://doi.org/10.1146/annurev.arplant.55.031903.141701

    Article  CAS  PubMed  Google Scholar 

  66. Miller G, Suzuki N, Ciftci-Yilmaz S et al (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33(4):453–467. https://doi.org/10.1111/j.1365-3040.2009.02041.x

    Article  CAS  PubMed  Google Scholar 

  67. Mittler R, Vanderauwera S, Gollery M et al (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9(10):490–498. https://doi.org/10.1016/j.tplants.2004.08.009

    Article  CAS  PubMed  Google Scholar 

  68. Oberschall A, Deák M, Török K et al (2000) A novel aldose/aldehyde reductase protects transgenic plants against lipid peroxidation under chemical and drought stresses. Plant Journal 24(4):437–446. https://doi.org/10.1111/j.1365-313X.2000.00885.x

    Article  CAS  Google Scholar 

  69. Suzuki N, Koussevitzky S, Mittler R et al (2012) ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environ 35(2):259–270. https://doi.org/10.1111/j.1365-3040.2011.02336.x

    Article  CAS  PubMed  Google Scholar 

  70. 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 

  71. Ye W, Muroyama D, Munemasa S et al (2013) Calcium-dependent protein kinase CPK6 positively functions in induction by yeast elicitor of stomatal closure and inhibition by yeast elicitor of light-induced stomatal opening in Arabidopsis. Plant Physiol 163(2):591–599. https://doi.org/10.1104/pp.113.224055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Chandran V, Stollar EJ, Lindorff-Larsen K et al (2006) Structure of the regulatory apparatus of a calcium-dependent protein kinase (CDPK): a novel mode of calmodulin-target recognition. J Mol Biol 357(2):400–410. https://doi.org/10.1016/j.jmb.2005.11.093

    Article  CAS  PubMed  Google Scholar 

  73. Harper JF, Breton G, Harmon A (2004) Decoding Ca(2+) signals through plant protein kinases. Annu Rev Plant Biol 55:263–288. https://doi.org/10.1146/annurev.arplant.55.031903.141627

    Article  CAS  PubMed  Google Scholar 

  74. Harper JF, Harmon A (2005) Plants, symbiosis and parasites: a calcium signalling connection. Nat Rev Mol Cell Biol 6(7):555–566. https://doi.org/10.1038/nrm1679

    Article  CAS  PubMed  Google Scholar 

  75. Asano T, Tanaka N, Yang G et al (2005) Genome-wide identification of the rice calcium-dependent protein kinase and its closely related kinase gene families: comprehensive analysis of the CDPKs gene family in rice. Plant Cell Physiol 46(2):356–366. https://doi.org/10.1093/pcp/pci035

    Article  CAS  PubMed  Google Scholar 

  76. Hrabak EM, Chan CW, Gribskov M et al (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132(2):666–680. https://doi.org/10.1104/pp.102.011999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Cheng SH, Willmann MR, Chen HC et al (2002) Calcium signaling through protein kinases. The Arabidopsis calcium-dependent protein kinase gene family. Plant Physiol 129(2):469–485. https://doi.org/10.1104/pp.005645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Kobayashi M, Ohura I, Kawakita K et al (2007) Calcium-dependent protein kinases regulate the production of reactive oxygen species by potato NADPH oxidase. Plant Cell 19(3):1065–1080. https://doi.org/10.1105/tpc.106.048884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Dubiella U, Seybold H, Durian G et al (2013) Calcium-dependent protein kinase/NADPH oxidase activation circuit is required for rapid defense signal propagation. Proc Natl Acad Sci U S A 110(21):8744–8749. https://doi.org/10.1073/pnas.1221294110

    Article  PubMed  PubMed Central  Google Scholar 

  80. Sirichandra C, Gu D, Hu HC et al (2009) Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase. FEBS Lett 583(18):2982–2986. https://doi.org/10.1016/j.febslet.2009.08.033

    Article  CAS  PubMed  Google Scholar 

  81. Duan Z-Q, Bai L, Zhao Z-G et al (2009) Drought-stimulated activity of plasma membrane nicotinamide adenine dinucleotide phosphate oxidase and its catalytic properties in rice. J Integr Plant Biol 51(12):1104–1115. https://doi.org/10.1111/j.1744-7909.2009.00879.x

    Article  CAS  PubMed  Google Scholar 

  82. Kovtun Y, Chiu WL, Tena G et al (2000) Functional analysis of oxidative stress-activated mitogen-activated protein kinase cascade in plants. Proc Natl Acad Sci U S A 97(6):2940–2945. https://doi.org/10.1073/pnas.97.6.2940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Pitzschke A, Hirt H (2006) Mitogen-activated protein kinases and reactive oxygen species signaling in plants. Plant Physiol 141(2):351–356. https://doi.org/10.1104/pp.106.079160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Pitzschke A, Djamei A, Bitton F et al (2009) A major role of the MEKK1-MKK1/2-MPK4 pathway in ROS signalling. Mol Plant 2(1):120–137. https://doi.org/10.1093/mp/ssn079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. 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.e634. https://doi.org/10.1016/j.devcel.2017.09.025

    Article  CAS  PubMed  Google Scholar 

  86. Kocsy G, Tóth B, Berzy T et al (2001) Glutathione reductase activity and chilling tolerance are induced by a hydroxylamine derivative BRX-156 in maize and soybean. Plant Sci 160(5):943–950. https://doi.org/10.1016/s0168-9452(01)00333-8

    Article  CAS  PubMed  Google Scholar 

  87. Liu Y, He C (2017) A review of redox signaling and the control of MAP kinase pathway in plants. Redox Biol 11:192–204. https://doi.org/10.1016/j.redox.2016.12.009

    Article  CAS  PubMed  Google Scholar 

  88. Waszczak C, Akter S, Jacques S et al (2015) Oxidative post-translational modifications of cysteine residues in plant signal transduction. J Exp Bot 66(10):2923–2934. https://doi.org/10.1093/jxb/erv084

    Article  CAS  PubMed  Google Scholar 

  89. Jarvis RM, Hughes SM, Ledgerwood EC (2012) Peroxiredoxin 1 functions as a signal peroxidase to receive, transduce, and transmit peroxide signals in mammalian cells. Free Radic Biol Med 53(7):1522–1530. https://doi.org/10.1016/j.freeradbiomed.2012.08.001

    Article  CAS  PubMed  Google Scholar 

  90. 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 

  91. Mongrand S, Hare PD, Chua N-H (2003) Abscisic acid. In: Henry HL, Norman AW (eds) Encyclopedia of hormones. Academic Press, New York, pp 1–10. https://doi.org/10.1016/B0-12-341103-3/00245-X

    Chapter  Google Scholar 

  92. Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58(2):221–227. https://doi.org/10.1093/jxb/erl164

    Article  CAS  PubMed  Google Scholar 

  93. Fujita Y, Fujita M, Shinozaki K et al (2011) ABA-mediated transcriptional regulation in response to osmotic stress in plants. J Plant Res 124(4):509–525. https://doi.org/10.1007/s10265-011-0412-3

    Article  CAS  PubMed  Google Scholar 

  94. Kirchler T, Briesemeister S, Singer M et al (2010) The role of phosphorylatable serine residues in the DNA-binding domain of Arabidopsis bZIP transcription factors. Eur J Cell Biol 89(2):175–183. https://doi.org/10.1016/j.ejcb.2009.11.023

    Article  CAS  PubMed  Google Scholar 

  95. Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61(6):1041–1052. https://doi.org/10.1111/j.1365-313X.2010.04124.x

    Article  CAS  PubMed  Google Scholar 

  96. Jia W, Wang Y, Zhang S et al (2002) Salt-stress-induced ABA accumulation is more sensitively triggered in roots than in shoots. J Exp Bot 53(378):2201–2206. https://doi.org/10.1093/jxb/erf079

    Article  CAS  PubMed  Google Scholar 

  97. Raghavendra AS, Gonugunta VK, Christmann A et al (2010) ABA perception and signalling. Trends Plant Sci 15(7):395–401. https://doi.org/10.1016/j.tplants.2010.04.006

    Article  CAS  PubMed  Google Scholar 

  98. Qiu JH, Hou YX, Wang YF et al (2017) A comprehensive proteomic survey of ABA-induced protein phosphorylation in rice (Oryza sativa L.). Int J Mol Sci 18(1). https://doi.org/10.3390/ijms18010060

  99. Nijhawan A, Jain M, Tyagi AK et al (2008) Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol 146(2):333–350. https://doi.org/10.1104/pp.107.112821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Jakoby M, Weisshaar B, Dröge-Laser W et al (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7(3):106–111. https://doi.org/10.1016/S1360-1385(01)02223-3

    Article  CAS  PubMed  Google Scholar 

  101. Schütze K, Harter K, Chaban C (2008) Post-translational regulation of plant bZIP factors. Trends Plant Sci 13(5):247–255. https://doi.org/10.1016/j.tplants.2008.03.002

    Article  CAS  PubMed  Google Scholar 

  102. Liu C, Mao B, Ou S et al (2014) OsbZIP71, a bZIP transcription factor, confers salinity and drought tolerance in rice. Plant Mol Biol 84(1):19–36. https://doi.org/10.1007/s11103-013-0115-3

    Article  CAS  PubMed  Google Scholar 

  103. Nutan KK, Kushwaha HR, Singla-Pareek SL et al (2017) Transcription dynamics of Saltol QTL localized genes encoding transcription factors, reveals their differential regulation in contrasting genotypes of rice. Funct Integr Genomics 17(1):69–83. https://doi.org/10.1007/s10142-016-0529-5

    Article  CAS  PubMed  Google Scholar 

  104. Das P, Lakra N, Nutan KK et al (2019) A unique bZIP transcription factor imparting multiple stress tolerance in Rice. Rice 12(1):58. https://doi.org/10.1186/s12284-019-0316-8

    Article  PubMed  PubMed Central  Google Scholar 

  105. Tang N, Zhang H, Li XH et al (2012) Constitutive activation of transcription factor OsbZIP46 improves drought tolerance in rice. Plant Physiol 158(4):1755–1768. https://doi.org/10.1104/pp.111.190389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Lopez-Molina L, Mongrand S, Chua NH (2001) A postgermination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc Natl Acad Sci U S A 98(8):4782–4787. https://doi.org/10.1073/pnas.081594298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Uno Y, Furihata T, Abe H et al (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci U S A 97(21):11632–11637. https://doi.org/10.1073/pnas.190309197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Furihata T, Maruyama K, Fujita Y et al (2006) Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc Natl Acad Sci U S A 103(6):1988–1993. https://doi.org/10.1073/pnas.0505667103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Fujii H, Zhu JK (2009) Arabidopsis mutant deficient in 3 abscisic acid-activated protein kinases reveals critical roles in growth, reproduction, and stress. Proc Natl Acad Sci U S A 106(20):8380–8385. https://doi.org/10.1073/pnas.0903144106

    Article  PubMed  PubMed Central  Google Scholar 

  110. Chae MJ, Lee JS, Nam MH et al (2007) A rice dehydration-inducible SNF1-related protein kinase 2 phosphorylates an abscisic acid responsive element-binding factor and associates with ABA signaling. Plant Mol Biol 63(2):151–169. https://doi.org/10.1007/s11103-006-9079-x

    Article  CAS  PubMed  Google Scholar 

  111. Hong JY, Chae MJ, Lee IS et al (2011) Phosphorylation-mediated regulation of a rice ABA responsive element binding factor. Phytochemistry 72(1):27–36. https://doi.org/10.1016/j.phytochem.2010.10.005

    Article  CAS  PubMed  Google Scholar 

  112. Kobayashi Y, Murata M, Minami H et al (2005) Abscisic acid-activated SNRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors. Plant J 44(6):939–949. https://doi.org/10.1111/j.1365-313X.2005.02583.x

    Article  CAS  PubMed  Google Scholar 

  113. Muniz Garcia MN, Giammaria V, Grandellis C et al (2012) Characterization of StABF1, a stress-responsive bZIP transcription factor from Solanum tuberosum L. that is phosphorylated by StCDPK2 in vitro. Planta 235(4):761–778. https://doi.org/10.1007/s00425-011-1540-7

    Article  CAS  PubMed  Google Scholar 

  114. H-i C, Park H-J, Park JH et al (2005) Arabidopsis calcium-dependent protein kinase AtCPK32 interacts with ABF4, a transcriptional regulator of abscisic acid-responsive gene expression, and modulates its activity. Plant Physiol 139(4):1750–1761. https://doi.org/10.1104/pp.105.069757

    Article  CAS  Google Scholar 

  115. Chang H-C, Tsai M-C, Wu S-S et al (2019) Regulation of ABI5 expression by ABF3 during salt stress responses in Arabidopsis thaliana. Bot Stud 60(1):16. https://doi.org/10.1186/s40529-019-0264-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Geiger D, Maierhofer T, AL-Rasheid KAS 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(173):ra32. https://doi.org/10.1126/scisignal.2001346

    Article  CAS  PubMed  Google Scholar 

  117. Lee SC, Lim CW, Lan W et al (2013) ABA signaling in guard cells entails a dynamic protein–protein interaction relay from the PYL-RCAR family receptors to ion channels. Mol Plant 6(2):528–538. https://doi.org/10.1093/mp/sss078

    Article  CAS  PubMed  Google Scholar 

  118. Zhang T, Chen S, Harmon AC (2014) Protein phosphorylation in stomatal movement. Plant Signal Behav 9(11):e972845. https://doi.org/10.4161/15592316.2014.972845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Acharya BR, Jeon BW, Zhang W et al (2013) Open stomata 1 (OST1) is limiting in abscisic acid responses of Arabidopsis guard cells. New Phytol 200(4):1049–1063. https://doi.org/10.1111/nph.12469

    Article  CAS  PubMed  Google Scholar 

  120. Vahisalu T, Kollist H, Wang YF et al (2008) SLAC1 is required for plant guard cell S-type anion channel function in stomatal signalling. Nature 452(7186):487–491. https://doi.org/10.1038/nature06608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Imes D, Mumm P, Böhm J et al (2013) Open stomata 1 (OST1) kinase controls R-type anion channel QUAC1 in Arabidopsis guard cells. Plant J 74(3):372–382. https://doi.org/10.1111/tpj.12133

    Article  CAS  PubMed  Google Scholar 

  122. Sato A, Sato Y, Fukao Y et al (2009) Threonine at position 306 of the KAT1 potassium channel is essential for channel activity and is a target site for ABA-activated SnRK2/OST1/SnRK2.6 protein kinase. Biochem J 424(3):439–448. https://doi.org/10.1042/bj20091221

    Article  CAS  PubMed  Google Scholar 

  123. Takahashi Y, Ebisu Y, Kinoshita T et al (2013) bHLH transcription factors that facilitate K+ uptake during stomatal opening are repressed by abscisic acid through phosphorylation. Sci Signal 6(280):ra48. https://doi.org/10.1126/scisignal.2003760

    Article  CAS  PubMed  Google Scholar 

  124. Grondin A, Rodrigues O, Verdoucq L et al (2015) Aquaporins contribute to ABA-triggered stomatal closure through OST1-mediated phosphorylation. Plant Cell 27(7):1945–1954. https://doi.org/10.1105/tpc.15.00421

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Ueguchi-Tanaka M, Ashikari M, Nakajima M et al (2005) GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437(7059):693–698. https://doi.org/10.1038/nature04028

    Article  CAS  PubMed  Google Scholar 

  126. Hauvermale AL, Ariizumi T, Steber CM (2012) Gibberellin signaling: a theme and variations on DELLA repression. Plant Physiol 160(1):83–92. https://doi.org/10.1104/pp.112.200956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Qin F, Kodaira KS, Maruyama K et al (2011) SPINDLY, a negative regulator of gibberellic acid signaling, is involved in the plant abiotic stress response. Plant Physiol 157(4):1900–1913. https://doi.org/10.1104/pp.111.187302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Hamayun M, Hussain A, Khan SA et al (2017) Gibberellins producing endophytic fungus Porostereum spadiceum AGH786 rescues growth of salt affected soybean. Front Microbiol 8:686. https://doi.org/10.3389/fmicb.2017.00686

    Article  PubMed  PubMed Central  Google Scholar 

  129. Urano K, Maruyama K, Jikumaru Y et al (2017) Analysis of plant hormone profiles in response to moderate dehydration stress. Plant J 90(1):17–36. https://doi.org/10.1111/tpj.13460

    Article  CAS  PubMed  Google Scholar 

  130. Wang B, Wei H, Xue Z et al (2017) Gibberellins regulate iron deficiency-response by influencing iron transport and translocation in rice seedlings (Oryza sativa). Ann Bot 119(6):945–956. https://doi.org/10.1093/aob/mcw250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Schwechheimer C (2012) Gibberellin signaling in plants – the extended version. Front Plant Sci 2(107). https://doi.org/10.3389/fpls.2011.00107

  132. Achard P, Cheng H, De Grauwe L et al (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311(5757):91–94. https://doi.org/10.1126/science.1118642

    Article  CAS  PubMed  Google Scholar 

  133. Magome H, Yamaguchi S, Hanada A et al (2008) The DDF1 transcriptional activator upregulates expression of a gibberellin-deactivating gene, GA2ox7, under high-salinity stress in Arabidopsis. Plant J 56(4):613–626. https://doi.org/10.1111/j.1365-313X.2008.03627.x

    Article  CAS  PubMed  Google Scholar 

  134. Dai C, Xue H-W (2010) Rice early flowering1, a CKI, phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signalling. EMBO J 29(11):1916–1927. https://doi.org/10.1038/emboj.2010.75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Griffiths J, Murase K, Rieu I et al (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18(12):3399–3414. https://doi.org/10.1105/tpc.106.047415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Silverstone AL, Ciampaglio CN, Sun T (1998) The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell 10(2):155–169. https://doi.org/10.1105/tpc.10.2.155

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Nemoto K, Ramadan A, Arimura G-I et al (2017) Tyrosine phosphorylation of the GARU E3 ubiquitin ligase promotes gibberellin signalling by preventing GID1 degradation. Nat Commun 8(1):1004–1004. https://doi.org/10.1038/s41467-017-01005-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. 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 

  139. Sun TP (2011) The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr Biol 21(9):R338–R345. https://doi.org/10.1016/j.cub.2011.02.036

    Article  CAS  PubMed  Google Scholar 

  140. Xu H, Liu Q, Yao T et al (2014) Shedding light on integrative GA signaling. Curr Opin Plant Biol 21:89–95. https://doi.org/10.1016/j.pbi.2014.06.010

    Article  CAS  PubMed  Google Scholar 

  141. Davière JM, Achard P (2016) A pivotal role of DELLAs in regulating multiple hormone signals. Mol Plant 9(1):10–20. https://doi.org/10.1016/j.molp.2015.09.011

    Article  CAS  PubMed  Google Scholar 

  142. Verma V, Ravindran P, Kumar PP (2016) Plant hormone-mediated regulation of stress responses. BMC Plant Biol 16:86–86. https://doi.org/10.1186/s12870-016-0771-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. Shiu S-H, 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 

  144. Shi C-C, Feng C-C, Yang M-M et al (2014) Overexpression of the receptor-like protein kinase genes AtRPK1 and OsRPK1 reduces the salt tolerance of Arabidopsis thaliana. Plant Sci 217-218:63–70. https://doi.org/10.1016/j.plantsci.2013.12.002

    Article  CAS  PubMed  Google Scholar 

  145. Stone JM, Walker JC (1995) Plant protein kinase families and signal transduction. Plant Physiol 108(2):451–457. https://doi.org/10.1104/pp.108.2.451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Niu J (2003) Studies on plant and wheat protein kinases. Acta Bot Sin 23(1):143–150

    CAS  Google Scholar 

  147. Shiu SH, Bleecker AB (2001) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci U S A 98(19):10763–10768. https://doi.org/10.1073/pnas.181141598

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Gish LA, Clark SE (2011) The RLK/Pelle family of kinases. Plant J 66(1):117–127. https://doi.org/10.1111/j.1365-313X.2011.04518.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Wang H, Wei Z, Li J et al (2017) 9—Brassinosteroids. In: Li J, Li C, Smith SM (eds) Hormone metabolism and signaling in plants. Academic Press, San Diego, pp 291–326. https://doi.org/10.1016/B978-0-12-811562-6.00009-8

    Chapter  Google Scholar 

  150. Kim SY, Kim BH, Lim CJ et al (2010) Constitutive activation of stress-inducible genes in a brassinosteroid-insensitive 1 (bri1) mutant results in higher tolerance to cold. Physiol Plant 138(2):191–204. https://doi.org/10.1111/j.1399-3054.2009.01304.x

    Article  PubMed  Google Scholar 

  151. Gruszka D (2018) Crosstalk of the brassinosteroid signalosome with phytohormonal and stress signaling components maintains a balance between the processes of growth and stress tolerance. Int J Mol Sci 19(9):2675

    Article  PubMed Central  Google Scholar 

  152. Hou Y, Qiu J, Wang Y et al (2017) A quantitative proteomic analysis of brassinosteroid-induced protein phosphorylation in rice (Oryza sativa L.). Front Plant Sci 8(514). https://doi.org/10.3389/fpls.2017.00514

  153. Wang Z-Y, Bai M-Y, Oh E et al (2012) Brassinosteroid signaling network and regulation of photomorphogenesis. Annu Rev Genet 46(1):701–724. https://doi.org/10.1146/annurev-genet-102209-163450

    Article  CAS  PubMed  Google Scholar 

  154. Wang W, Bai M-Y, Wang Z-Y (2014) The brassinosteroid signaling network—a paradigm of signal integration. Curr Opin Plant Biol 21:147–153. https://doi.org/10.1016/j.pbi.2014.07.012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Santiago J, Henzler C, Hothorn M (2013) Molecular mechanism for plant steroid receptor activation by somatic embryogenesis co-receptor kinases. Science 341(6148):889–892

    Article  CAS  PubMed  Google Scholar 

  156. Sun Y, Han Z, Tang J et al (2013) Structure reveals that BAK1 as a co-receptor recognizes the BRI1-bound brassinolide. Cell Res 23(11):1326–1329. https://doi.org/10.1038/cr.2013.131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Oh M-H, Bender K, Kim SY et al (2015) Functional analysis of the BRI1 receptor kinase by Thr-for-Ser substitution in a regulatory autophosphorylation site. Front Plant Sci 6(562). https://doi.org/10.3389/fpls.2015.00562

  158. Tang W, Kim T-W, Oses-Prieto JA et al (2008) BSKs mediate signal transduction from the receptor kinase BRI1 in Arabidopsis. Science 321(5888):557–560. https://doi.org/10.1126/science.1156973

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Kim T-W, 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 

  160. He J-X, Gendron JM, Yang Y et al (2002) The GSK3-like kinase BIN2 phosphorylates and destabilizes BZR1, a positive regulator of the brassinosteroid signaling pathway in Arabidopsis. Proc Natl Acad Sci U S A 99(15):10185–10190. https://doi.org/10.1073/pnas.152342599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Wang Z-Y, Nakano T, Gendron J et al (2002) Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev Cell 2(4):505–513. https://doi.org/10.1016/S1534-5807(02)00153-3

    Article  CAS  PubMed  Google Scholar 

  162. Yin Y, Wang Z-Y, Mora-Garcia S et al (2002) BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109(2):181–191. https://doi.org/10.1016/S0092-8674(02)00721-3

    Article  CAS  PubMed  Google Scholar 

  163. Koh S, Lee S-C, Kim M-K et al (2007) T-DNA tagged knockout mutation of rice OsGSK1, an orthologue of Arabidopsis BIN2, with enhanced tolerance to various abiotic stresses. Plant Mol Biol 65(4):453–466. https://doi.org/10.1007/s11103-007-9213-4

    Article  CAS  PubMed  Google Scholar 

  164. Gampala SS, Kim T-W, He J-X et al (2007) An essential role for 14-3-3 proteins in brassinosteroid signal transduction in Arabidopsis. Dev Cell 13(2):177–189. https://doi.org/10.1016/j.devcel.2007.06.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  165. Bai M-Y, Zhang L-Y, Gampala SS et al (2007) Functions of OsBZR1 and 14-3-3 proteins in brassinosteroid signaling in rice. Proc Natl Acad Sci U S A 104(34):13839–13844. https://doi.org/10.1073/pnas.0706386104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  166. Ryu H, Cho Y-G (2015) Plant hormones in salt stress tolerance. J Plant Biol 58(3):147–155. https://doi.org/10.1007/s12374-015-0103-z

    Article  CAS  Google Scholar 

  167. Wu W, Zhang Q, Ervin EH et al (2017) Physiological mechanism of enhancing salt stress tolerance of perennial ryegrass by 24-epibrassinolide. Front Plant Sci 8(1017). https://doi.org/10.3389/fpls.2017.01017

  168. Savas S, Ozcelik H (2005) Phosphorylation states of cell cycle and DNA repair proteins can be altered by the nsSNPs. BMC Cancer 5(1):107. https://doi.org/10.1186/1471-2407-5-107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. Ryu GM, Song P, Kim KW et al (2009) Genome-wide analysis to predict protein sequence variations that change phosphorylation sites or their corresponding kinases. Nucleic Acids Res 37(4):1297–1307. https://doi.org/10.1093/nar/gkn1008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Trusov Y, Botella JR (2016) Plant G-proteins come of age: breaking the bond with animal models. Front Chem 4(24). https://doi.org/10.3389/fchem.2016.00024

  171. Halford NG, Hey SJ (2009) Snf1-related protein kinases (SnRKs) act within an intricate network that links metabolic and stress signalling in plants. Biochemical J 419(2):247–259. https://doi.org/10.1042/bj20082408

    Article  CAS  Google Scholar 

  172. Droillard MJ, Boudsocq M, Barbier-Brygoo H et al (2004) Involvement of MPK4 in osmotic stress response pathways in cell suspensions and plantlets of Arabidopsis thaliana: activation by hypoosmolarity and negative role in hyperosmolarity tolerance. FEBS Lett 574(1-3):42–48. https://doi.org/10.1016/j.febslet.2004.08.001

    Article  CAS  PubMed  Google Scholar 

  173. Teige M, Scheikl E, Eulgem T et al (2004) The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol Cell 15(1):141–152. https://doi.org/10.1016/j.molcel.2004.06.023

    Article  CAS  PubMed  Google Scholar 

  174. Ichimura K, Mizoguchi T, Yoshida R et al (2000) Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATMPK4 and ATMPK6. Plant J 24(5):655–665. https://doi.org/10.1046/j.1365-313x.2000.00913.x

    Article  CAS  PubMed  Google Scholar 

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This work is supported by the National Natural Science Foundation of China (NSFC, No. 31271805).

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Damaris, R.N., Yang, P. (2021). Protein Phosphorylation Response to Abiotic Stress in Plants. 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_2

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