The Journey from Two-Step to Multi-Step Phosphorelay Signaling Systems

Deepti       Singh; Priyanka       Gupta; Sneh    Lata    Singla-Pareek; Kadambot    H.M.   Siddique; Ashwani       Pareek
Abstract

Background: The two-component signaling (TCS) system is an important signal transduction machinery in prokaryotes and eukaryotes, excluding animals, that uses a protein phosphorylation mechanism for signal transmission.
Conclusion: Prokaryotes have a primitive type of TCS machinery, which mainly comprises a membrane- bound sensory histidine kinase (HK) and its cognate cytoplasmic response regulator (RR). Hence, it is sometimes referred to as two-step phosphorelay (TSP). Eukaryotes have more sophisticated signaling machinery, with an extra component - a histidine-containing phosphotransfer (HPT) protein that shuttles between HK and RR to communicate signal baggage. As a result, the TSP has evolved from a two-step phosphorelay (His–Asp) in simple prokaryotes to a multi-step phosphorelay (MSP) cascade (His–Asp–His–Asp) in complex eukaryotic organisms, such as plants, to mediate the signaling network. This molecular evolution is also reflected in the form of considerable structural modifications in the domain architecture of the individual components of the TCS system. In this review, we present TCS system's evolutionary journey from the primitive TSP to advanced MSP type across the genera. This information will be highly useful in designing the future strategies of crop improvement based on the individual members of the TCS machinery.
Keywords: Two-component system, histidine kinases, histidine-containing phosphotransfer proteins, response regulators, multi-step phosphorelay, two-step phosphorelay.
Graphical Abstract

[1] 
Boyer, J.S. Plant productivity and environment. Science,  1982, 218(4571), 443-448.
[http://dx.doi.org/10.1126/science.218.4571.443] [PMID: 17808529] 
[2] 
Sahoo, R.K.; Ansari, M.W.; Tuteja, R.; Tuteja, N. OsSUV3 transgenic rice maintains higher endogenous levels of plant hormones that mitigates adverse effects of salinity and sustains crop productivity. Rice (N. Y.),  2014, 7(1), 17.
[http://dx.doi.org/10.1186/s12284-014-0017-2] [PMID: 25184028] 
[3] 
Acquaah, G. Principles of plant genetics and breeding John Wiley & Sons, 2009.
[4] 
Sewelam, N.; Kazan, K.; Schenk, P.M. Global plant stress signaling: reactive oxygen species at the cross-road. Front. Plant Sci.,  2016, 7, 187.
[http://dx.doi.org/10.3389/fpls.2016.00187] [PMID: 26941757] 
[5] 
Hunter, T. Protein kinase classification. In: Methods in enzymology. Academic Press,  1991, pp. 3-37.
[6] 
Stock, A.M.; Robinson, V.L.; Goudreau, P.N. Two-component signal transduction. Annu. Rev. Biochem.,  2000, 69(1), 183-215.
[http://dx.doi.org/10.1146/annurev.biochem.69.1.183] [PMID: 10966457] 
[7] 
Wurgler-Murphy, S.M.; Saito, H. Two-component signal transducers and MAPK cascades. Trends Biochem Sci,  1997, 22(5), 172-176.
[http://dx.doi.org/10.1016/S0968-0004(97)01036-0] [PMID: 9175476] 
[8] 
Loomis, W.F.; Kuspa, A.; Shaulsky, G. Two-component signal transduction systems in eukaryotic microorganisms. Curr. Opin. Microbiol.,  1998, 1(6), 643-648.
[http://dx.doi.org/10.1016/S1369-5274(98)80109-4] [PMID: 10066536] 
[9] 
Zhang, C.C. Bacterial signalling involving eukaryotic-type protein kinases. Mol. Microbiol.,  1996, 20(1), 9-15.
[http://dx.doi.org/10.1111/j.1365-2958.1996.tb02483.x] [PMID: 8861199] 
[10] 
Stock, J.B.; Surette, M.G.; Levit, M.; Park, P. Two-component signal transduction systems: structure-function relationships and mechanisms of catalysis. In: Two-component signal transduction James, A.H.; Thomas, J.S., Eds.; John Wiley & Sons,,  1995, pp. 25-5.
[11] 
Schultz, J.; Copley, R.R.; Doerks, T.; Ponting, C.P.; Bork, P. SMART: a web-based tool for the study of genetically mobile domains. Nucleic Acids Res.,  2000, 28(1), 231-234.
[http://dx.doi.org/10.1093/nar/28.1.231] [PMID: 10592234] 
[12] 
Bekker, M.; Teixeira de Mattos, M.J.; Hellingwerf, K.J. The role of two-component regulation systems in the physiology of the bacterial cell. Sci. Prog.,  2006, 89(Pt 3-4), 213-242.
[http://dx.doi.org/10.3184/003685006783238308] [PMID: 17338439] 
[13] 
Hwang, I.; Chen, H.C.; Sheen, J. Two-component signal transduction pathways in Arabidopsis. Plant Physiol.,  2002, 129(2), 500-515.
[http://dx.doi.org/10.1104/pp.005504] [PMID: 12068096] 
[14] 
Robinson, V.L.; Buckler, D.R.; Stock, A.M. A tale of two components: a novel kinase and a regulatory switch. Nat. Struct. Biol.,  2000, 7(8), 626-633.
[http://dx.doi.org/10.1038/77915] [PMID: 10932244] 
[15] 
Le, D.T.; Nishiyama, R.; Watanabe, Y.; Mochida, K.; Yamaguchi-Shinozaki, K.; Shinozaki, K.; Tran, L.S. Genome-wide expression profiling of soybean two-component system genes in soybean root and shoot tissues under dehydration stress. DNA Res.,  2011, 18(1), 17-29.
[http://dx.doi.org/10.1093/dnares/dsq032] [PMID: 21208938] 
[16] 
Karan, R.; Singla-Pareek, S.L.; Pareek, A. Histidine kinase and response regulator genes as they relate to salinity tolerance in rice. Funct. Integr. Genomics,  2009, 9(3), 411-417.
[http://dx.doi.org/10.1007/s10142-009-0119-x] [PMID: 19277738] 
[17] 
Nishiyama, R.; Watanabe, Y.; Leyva-Gonzalez, M.A.; Ha, C.V.; Fujita, Y.; Tanaka, M.; Seki, M.; Yamaguchi-Shinozaki, K.; Shinozaki, K.; Herrera-Estrella, L.; Tran, L.S. Arabidopsis AHP2, AHP3, and AHP5 histidine phosphotransfer proteins function as redundant negative regulators of drought stress response. Proc. Natl. Acad. Sci. USA,  2013, 110(12), 4840-4845.
[http://dx.doi.org/10.1073/pnas.1302265110] [PMID: 23487796] 
[18] 
Cai, S.J.; Inouye, M. 
                        EnvZ-OmpR interaction and osmoregulation in 
                        Escherichia coli. J. Biol. Chem.,  2002, 277(27), 24155-24161.
[http://dx.doi.org/10.1074/jbc.M110715200] [PMID: 11973328] 
[19] 
Urao, T.; Yakubov, B.; Satoh, R.; Yamaguchi-Shinozaki, K.; Seki, M.; Hirayama, T.; Shinozaki, K. A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell,  1999, 11(9), 1743-1754.
[http://dx.doi.org/10.1105/tpc.11.9.1743] [PMID: 10488240] 
[20] 
Tran, L.S.; Urao, T.; Qin, F.; Maruyama, K.; Kakimoto, T.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc. Natl. Acad. Sci. USA,  2007, 104(51), 20623-20628.
[http://dx.doi.org/10.1073/pnas.0706547105] [PMID: 18077346] 
[21] 
Sharrock, R.A. The phytochrome red/far-red photoreceptor superfamily. Genome Biol.,  2008, 9(8), 230.
[http://dx.doi.org/10.1186/gb-2008-9-8-230] [PMID: 18771590] 
[22] 
Wang, F.F.; Cheng, S.T.; Wu, Y.; Ren, B.Z.; Qian, W. A bacterial receptor PcrK senses the plant hormone cytokinin to promote adaptation to oxidative stress. Cell Rep.,  2017, 21(10), 2940-2951.
[http://dx.doi.org/10.1016/j.celrep.2017.11.017] [PMID: 29212037] 
[23] 
Capra, E.J.; Laub, M.T. Evolution of two-component signal transduction systems. Annu. Rev. Microbiol.,  2012, 66, 325-347.
[http://dx.doi.org/10.1146/annurev-micro-092611-150039] [PMID: 22746333] 
[24] 
Skerker, J.M.; Perchuk, B.S.; Siryaporn, A.; Lubin, E.A.; Ashenberg, O.; Goulian, M.; Laub, M.T. Rewiring the specificity of two-component signal transduction systems. Cell,  2008, 133(6), 1043-1054.
[http://dx.doi.org/10.1016/j.cell.2008.04.040] [PMID: 18555780] 
[25] 
Sonnenburg, E.D.; Sonnenburg, J.L.; Manchester, J.K.; Hansen, E.E.; Chiang, H.C.; Gordon, J.I. 
                        A hybrid two-component system protein of a prominent human gut symbiont couples glycan sensing 
                        
                            in vivo
                        
                         to carbohydrate metabolism.
                     Proc. Natl. Acad. Sci. USA,  2006, 103(23), 8834-8839.
[http://dx.doi.org/10.1073/pnas.0603249103] [PMID: 16735464] 
[26] 
Alm, E.; Huang, K.; Arkin, A. The evolution of two-component systems in bacteria reveals different strategies for niche adaptation. PLOS Comput. Biol.,  2006, 2(11), e143.
[http://dx.doi.org/10.1371/journal.pcbi.0020143] [PMID: 17083272] 
[27] 
Punwani, J.A.; Hutchison, C.E.; Schaller, G.E.; Kieber, J.J. The subcellular distribution of the Arabidopsis histidine phosphotransfer proteins is independent of cytokinin signaling. Plant J.,  2010, 62(3), 473-482.
[http://dx.doi.org/10.1111/j.1365-313X.2010.04165.x] [PMID: 20136728] 
[28] 
Pils, B.; Heyl, A. Unraveling the evolution of cytokinin signaling. Plant Physiol.,  2009, 151(2), 782-791.
[http://dx.doi.org/10.1104/pp.109.139188] [PMID: 19675156] 
[29] 
Gruhn, N.; Halawa, M.; Snel, B.; Seidl, M.F.; Heyl, A. A subfamily of putative cytokinin receptors is revealed by an analysis of the evolution of the two-component signaling system of plants. Plant Physiol.,  2014, 165(1), 227-237.
[http://dx.doi.org/10.1104/pp.113.228080] [PMID: 24520157] 
[30] 
Fassler, J.S.; West, A.H. Histidine phosphotransfer proteins in fungal two-component signal transduction pathways. Eukaryot. Cell,  2013, 12(8), 1052-1060.
[http://dx.doi.org/10.1128/EC.00083-13] [PMID: 23771905] 
[31] 
MacRitchie, D.M.; Buelow, D.R.; Price, N.L.; Raivio, T.L. Two-component signaling and gram negative envelope stress response systems. In: Bacterial signal transduction: networks and drug targets. ; Utsumi, R., Ed.; Springer: New York,,  2008, pp. 80-110.
[http://dx.doi.org/10.1007/978-0-387-78885-2_6] 
[32] 
Hoch, J.A. 
                        Regulation of the phosphorelay and the initiation of sporulation in 
                        Bacillus subtilis. Annu. Rev. Microbiol.,  1993, 47(1), 441-465.
[http://dx.doi.org/10.1146/annurev.mi.47.100193.002301] [PMID: 8257105] 
[33] 
Tipton, K.A.; Rather, P.N. 
                        An OmpR-EnvZ two-component system ortholog regulates phase variation, osmotic tolerance, motility, and virulence in 
                        Acinetobacter baumannii
                         strain AB5075.
                     J. Bacteriol.,  2017, 199(3), e00705-e00716.
[http://dx.doi.org/10.1128/JB.00705-16] [PMID: 27872182] 
[34] 
Galperin, M.Y.; Nikolskaya, A.N.; Koonin, E.V. Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol. Lett.,  2001, 203(1), 11-21.
[http://dx.doi.org/10.1111/j.1574-6968.2001.tb10814.x] [PMID: 11557134] 
[35] 
Mascher, T.; Helmann, J.D.; Unden, G. Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol. Mol. Biol. Rev.,  2006, 70(4), 910-938.
[http://dx.doi.org/10.1128/MMBR.00020-06] [PMID: 17158704] 
[36] 
Falke, J.J.; Bass, R.B.; Butler, S.L.; Chervitz, S.A.; Danielson, M.A. The two-component signaling pathway of bacterial chemotaxis: a molecular view of signal transduction by receptors, kinases, and adaptation enzymes. Annu. Rev. Cell Dev. Biol.,  1997, 13(1), 457-512.
[http://dx.doi.org/10.1146/annurev.cellbio.13.1.457] [PMID: 9442881] 
[37] 
Bilwes, A.M.; Park, S.Y.; Quezada, C.M.; Simon, M.I.; Crane, B.R. Structure and function of CheA, the histidine kinase central to bacterial chemotaxis. In: Histidine Kinases in Signal Transduction ; Inouye, M.; Dutta, R., Eds.; Academic Press,,  2003, pp. 47-72.
[38] 
Ninfa, A.J.; Jiang, P.; Atkinson, M.R.; Peliska, J.A. Integration of antagonistic signals in the regulation of nitrogen assimilation in Escherichia coli. In: Current topics in cellular regulation ; Stadtman, ER.; Chock, PB., Eds.; Academic Press,,  2001, pp. 31-75.
[39] 
Nagasawa, S.; Tokishita, S.; Aiba, H.; Mizuno, T. 
                        A novel sensor-regulator protein that belongs to the homologous family of signal-transduction proteins involved in adaptive responses in 
                        Escherichia coli. Mol. Microbiol.,  1992, 6(6), 799-807.
[http://dx.doi.org/10.1111/j.1365-2958.1992.tb01530.x] [PMID: 1574005] 
[40] 
Ishige, K.; Nagasawa, S.; Tokishita, S.; Mizuno, T. A novel device of bacterial signal transducers. EMBO J.,  1994, 13(21), 5195-5202.
[http://dx.doi.org/10.1002/j.1460-2075.1994.tb06850.x] [PMID: 7957084] 
[41] 
Sahu, S.N.; Acharya, S.; Tuminaro, H.; Patel, I.; Dudley, K.; LeClerc, J.E.; Cebula, T.A.; Mukhopadhyay, S. 
                        The bacterial adaptive response gene, barA, encodes a novel conserved histidine kinase regulatory switch for adaptation and modulation of metabolism in 
                        Escherichia coli. Mol. Cell. Biochem.,  2003, 253(1-2), 167-177.
[http://dx.doi.org/10.1023/A:1026028930203] [PMID: 14619967] 
[42] 
Kato, M.; Mizuno, T.; Shimizu, T.; Hakoshima, T. Insights into multistep phosphorelay from the crystal structure of the C-terminal HPt domain of ArcB. Cell,  1997, 88(5), 717-723.
[http://dx.doi.org/10.1016/S0092-8674(00)81914-5] [PMID: 9054511] 
[43] 
Bilwes, A.M.; Alex, L.A.; Crane, B.R.; Simon, M.I. Structure of CheA, a signal-transducing histidine kinase. Cell,  1999, 96(1), 131-141.
[http://dx.doi.org/10.1016/S0092-8674(00)80966-6] [PMID: 9989504] 
[44] 
Gonzalez-Rizzo, S.; Crespi, M.; Frugier, F. 
                        The 
                        Medicago truncatula
                         CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with 
                        Sinorhizobium meliloti. Plant Cell,  2006, 18(10), 2680-2693.
[http://dx.doi.org/10.1105/tpc.106.043778] [PMID: 17028204] 
[45] 
Salah Ud-Din, A.I.M.; Roujeinikova, A. Methyl-accepting chemotaxis proteins: a core sensing element in prokaryotes and archaea. Cell. Mol. Life Sci.,  2017, 74(18), 3293-3303.
[http://dx.doi.org/10.1007/s00018-017-2514-0] [PMID: 28409190] 
[46] 
Rudolph, J.; Tolliday, N.; Schmitt, C.; Schuster, S.C.; Oesterhelt, D. Phosphorylation in halobacterial signal transduction. EMBO J.,  1995, 14(17), 4249-4257.
[http://dx.doi.org/10.1002/j.1460-2075.1995.tb00099.x] [PMID: 7556066] 
[47] 
Klare, J.P.; Bordignon, E.; Engelhard, M.; Steinhoff, H.J. Transmembrane signal transduction in archaeal phototaxis: the sensory rhodopsin II-transducer complex studied by electron paramagnetic resonance spectroscopy. Eur. J. Cell Biol.,  2011, 90(9), 731-739.
[http://dx.doi.org/10.1016/j.ejcb.2011.04.013] [PMID: 21684631] 
[48] 
Inoue, K.; Tsukamoto, T.; Sudo, Y. Molecular and evolutionary aspects of microbial sensory rhodopsins. Biochim. Biophys. Acta,  2014, 1837(5), 562-577.
[http://dx.doi.org/10.1016/j.bbabio.2013.05.005] [PMID: 23732219] 
[49] 
Koretke, K.K.; Lupas, A.N.; Warren, P.V.; Rosenberg, M.; Brown, J.R. Evolution of two-component signal transduction. Mol. Biol. Evol.,  2000, 17(12), 1956-1970.
[http://dx.doi.org/10.1093/oxfordjournals.molbev.a026297] [PMID: 11110912] 
[50] 
Ashby, M.K. Distribution, structure and diversity of “bacterial” genes encoding two-component proteins in the Euryarchaeota. Archaea,  2006, 2(1), 11-30.
[http://dx.doi.org/10.1155/2006/562404] [PMID: 16877318] 
[51] 
Papon, N.; Stock, A.M. What do archaeal and eukaryotic histidine kinases sense? F1000 Res.,  2019, 8, 8.
[http://dx.doi.org/10.12688/f1000research.20094.1] [PMID: 31942238] 
[52] 
Anantharaman, V.; Aravind, L. MEDS and PocR are novel domains with a predicted role in sensing simple hydrocarbon derivatives in prokaryotic signal transduction systems. Bioinformatics,  2005, 21(12), 2805-2811.
[http://dx.doi.org/10.1093/bioinformatics/bti418] [PMID: 15814558] 
[53] 
Cheung, J.; Hendrickson, W.A. Sensor domains of two-component regulatory systems. Curr. Opin. Microbiol.,  2010, 13(2), 116-123.
[http://dx.doi.org/10.1016/j.mib.2010.01.016] [PMID: 20223701] 
[54] 
Perry, J.; Koteva, K.; Wright, G. Receptor domains of two-component signal transduction systems. Mol. Biosyst.,  2011, 7(5), 1388-1398.
[http://dx.doi.org/10.1039/c0mb00329h] [PMID: 21347487] 
[55] 
Najnin, T.; Siddiqui, K.S.; Elkaid, N.; Kornfeld, G.; Curmi, P.M.; Cavicchioli, R. 
                        Characterization of a temperature-responsive two component regulatory system from the Antarctic archaeon, 
                        Methanococcoides burtonii.
                     Sci. Rep.,  2016, 6(1), 1-5.
[PMID: 28442746] 
[56] 
Li, J.; Zheng, X.; Guo, X.; Qi, L.; Dong, X. 
                        Characterization of an archaeal two-component system that regulates methanogenesis in 
                        Methanosaeta harundinacea. PLoS One,  2014, 9(4), e95502.
[http://dx.doi.org/10.1371/journal.pone.0095502] [PMID: 24748383] 
[57] 
Galperin, M.Y.; Makarova, K.S.; Wolf, Y.I.; Koonin, E.V. Phyletic distribution and lineage-specific domain architectures of archaeal two-component signal transduction systems. J. Bacteriol.,  2018, 200(7), e00681-e17.
[http://dx.doi.org/10.1128/JB.00681-17] [PMID: 29263101] 
[58] 
Wuichet, K.; Cantwell, B.J.; Zhulin, I.B. Evolution and phyletic distribution of two-component signal transduction systems. Curr. Opin. Microbiol.,  2010, 13(2), 219-225.
[http://dx.doi.org/10.1016/j.mib.2009.12.011] [PMID: 20133179] 
[59] 
Galperin, M.Y. Diversity of structure and function of response regulator output domains. Curr. Opin. Microbiol.,  2010, 13(2), 150-159.
[http://dx.doi.org/10.1016/j.mib.2010.01.005] [PMID: 20226724] 
[60] 
Mizuno, T.; Kaneko, T.; Tabata, S. 
                        Compilation of all genes encoding bacterial two-component signal transducers in the genome of the cyanobacterium, 
                        Synechocystis
                         sp. strain PCC 6803.
                     DNA Res.,  1996, 3(6), 407-414.
[http://dx.doi.org/10.1093/dnares/3.6.407] [PMID: 9097043] 
[61] 
Ashby, M.K.; Houmard, J. Cyanobacterial two-component proteins: structure, diversity, distribution, and evolution. Microbiol. Mol. Biol. Rev.,  2006, 70(2), 472-509.
[http://dx.doi.org/10.1128/MMBR.00046-05] [PMID: 16760311] 
[62] 
Hsiao, H.Y.; He, Q.; Van Waasbergen, L.G.; Grossman, A.R. Control of photosynthetic and high-light-responsive genes by the histidine kinase DspA: negative and positive regulation and interactions between signal transduction pathways. J. Bacteriol.,  2004, 186(12), 3882-3888.
[http://dx.doi.org/10.1128/JB.186.12.3882-3888.2004] [PMID: 15175302] 
[63] 
Cadoret, J.C.; Rousseau, B.; Perewoska, I.; Sicora, C.; Cheregi, O.; Vass, I.; Houmard, J. 
                        Cyclic nucleotides, the photosynthetic apparatus and response to a UV-B stress in the Cyanobacterium 
                        Synechocystis
                         sp. PCC 6803.
                     J. Biol. Chem.,  2005, 280(40), 33935-33944.
[http://dx.doi.org/10.1074/jbc.M503153200] [PMID: 16096278] 
[64] 
Mikami, K.; Kanesaki, Y.; Suzuki, I.; Murata, N. The histidine kinase Hik33 perceives osmotic stress and cold stress in Synechocystis sp PCC 6803. Mol. Microbiol.,  2002, 46(4), 905-915.
[http://dx.doi.org/10.1046/j.1365-2958.2002.03202.x] [PMID: 12421299] 
[65] 
Ohmori, M.; Ikeuchi, M.; Sato, N.; Wolk, P.; Kaneko, T.; Ogawa, T.; Kanehisa, M.; Goto, S.; Kawashima, S.; Okamoto, S.; Yoshimura, H.; Katoh, H.; Fujisawa, T.; Ehira, S.; Kamei, A.; Yoshihara, S.; Narikawa, R.; Tabat, S. 
                        Characterization of genes encoding multi-domain proteins in the genome of the filamentous nitrogen-fixing Cyanobacterium 
                        anabaena
                         sp. strain PCC 7120.
                     DNA Res.,  2001, 8(6), 271-284.
[http://dx.doi.org/10.1093/dnares/8.6.271] [PMID: 11858227] 
[66] 
Liang, J.; Scappino, L.; Haselkorn, R. 
                        The patA gene product, which contains a region similar to CheY of 
                        Escherichia coli
                        , controls heterocyst pattern formation in the cyanobacterium 
                        Anabaena
                         7120.
                     Proc. Natl. Acad. Sci. USA,  1992, 89(12), 5655-5659.
[http://dx.doi.org/10.1073/pnas.89.12.5655] [PMID: 1608976] 
[67] 
Galperin, M.Y. A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts. BMC Microbiol.,  2005, 5(1), 35.
[http://dx.doi.org/10.1186/1471-2180-5-35] [PMID: 15955239] 
[68] 
Armbrust, E.V. The life of diatoms in the world’s oceans. Nature,  2009, 459(7244), 185-192.
[http://dx.doi.org/10.1038/nature08057] [PMID: 19444204] 
[69] 
Douzery, E.J.; Snell, E.A.; Bapteste, E.; Delsuc, F.; Philippe, H. The timing of eukaryotic evolution: does a relaxed molecular clock reconcile proteins and fossils? Proc. Natl. Acad. Sci. USA,  2004, 101(43), 15386-15391.
[http://dx.doi.org/10.1073/pnas.0403984101] [PMID: 15494441] 
[70] 
Yoon, H.S.; Hackett, J.D.; Ciniglia, C.; Pinto, G.; Bhattacharya, D. A molecular timeline for the origin of photosynthetic eukaryotes. Mol. Biol. Evol.,  2004, 21(5), 809-818.
[http://dx.doi.org/10.1093/molbev/msh075] [PMID: 14963099] 
[71] 
Zimmer, A.; Lang, D.; Richardt, S.; Frank, W.; Reski, R.; Rensing, S.A. Dating the early evolution of plants: detection and molecular clock analyses of orthologs. Mol. Genet. Genomics,  2007, 278(4), 393-402.
[http://dx.doi.org/10.1007/s00438-007-0257-6] [PMID: 17593393] 
[72] 
Kabbara, S.; Bidon, B.; Kilani, J.; Dugé de Bernonville, T.; Clastre, M.; Courdavault, V.; Cock, J.M.; Papon, N. Megaviruses: an involvement in phytohormone receptor gene transfer in brown algae? Gene,  2019, 704, 149-151.
[http://dx.doi.org/10.1016/j.gene.2019.04.055] [PMID: 31009683] 
[73] 
Defosse, T.A.; Sharma, A.; Mondal, A.K.; Dugé de Bernonville, T.; Latgé, J.P.; Calderone, R.; Giglioli-Guivarc’h, N.; Courdavault, V.; Clastre, M.; Papon, N. Hybrid histidine kinases in pathogenic fungi. Mol. Microbiol.,  2015, 95(6), 914-924.
[http://dx.doi.org/10.1111/mmi.12911] [PMID: 25560420] 
[74] 
Yu, Z.; Armant, O.; Fischer, R. Fungi use the SakA (HogA) pathway for phytochrome-dependent light signalling. Nat. Microbiol.,  2016, 1(5), 16019.
[http://dx.doi.org/10.1038/nmicrobiol.2016.19] [PMID: 27572639] 
[75] 
Catlett, N.L.; Yoder, O.C.; Turgeon, B.G. Whole-genome analysis of two-component signal transduction genes in fungal pathogens. Eukaryot. Cell,  2003, 2(6), 1151-1161.
[http://dx.doi.org/10.1128/EC.2.6.1151-1161.2003] [PMID: 14665450] 
[76] 
Dongo, A.; Bataillé-Simoneau, N.; Campion, C.; Guillemette, T.; Hamon, B.; Iacomi-Vasilescu, B.; Katz, L.; Simoneau, P. The group III two-component histidine kinase of filamentous fungi is involved in the fungicidal activity of the bacterial polyketide ambruticin. Appl. Environ. Microbiol.,  2009, 75(1), 127-134.
[http://dx.doi.org/10.1128/AEM.00993-08] [PMID: 19011080] 
[77] 
Chauhan, N.; Latge, J.P.; Calderone, R. 
                        Signalling and oxidant adaptation in 
                        Candida albicans
                         and 
                        Aspergillus fumigatus. Nat. Rev. Microbiol.,  2006, 4(6), 435-444.
[http://dx.doi.org/10.1038/nrmicro1426] [PMID: 16710324] 
[78] 
Loomis, W.F.; Shaulsky, G.; Wang, N. Histidine kinases in signal transduction pathways of eukaryotes. J. Cell Sci.,  1997, 110(Pt 10), 1141-1145.
[PMID: 9191038] 
[79] 
Schuster, S.C.; Noegel, A.A.; Oehme, F.; Gerisch, G.; Simon, M.I. 
                        The hybrid histidine kinase DokA is part of the osmotic response system of 
                        Dictyostelium. EMBO J.,  1996, 15(15), 3880-3889.
[http://dx.doi.org/10.1002/j.1460-2075.1996.tb00762.x] [PMID: 8670893] 
[80] 
Singleton, C.K.; Zinda, M.J.; Mykytka, B.; Yang, P. 
                        The histidine kinase dhkC regulates the choice between migrating slugs and terminal differentiation in 
                        Dictyostelium discoideum. Dev. Biol.,  1998, 203(2), 345-357.
[http://dx.doi.org/10.1006/dbio.1998.9049] [PMID: 9808785] 
[81] 
Wang, N.; Söderbom, F.; Anjard, C.; Shaulsky, G.; Loomis, W.F. 
                        SDF-2 induction of terminal differentiation in 
                        Dictyostelium discoideum
                         is mediated by the membrane-spanning sensor kinase DhkA.
                     Mol. Cell. Biol.,  1999, 19(7), 4750-4756.
[http://dx.doi.org/10.1128/MCB.19.7.4750] [PMID: 10373524] 
[82] 
Ryo, M.; Yamashino, T.; Nomoto, Y.; Goto, Y.; Ichinose, M.; Sato, K.; Sugita, M.; Aoki, S. 
                        Light-regulated PAS-containing histidine kinases delay gametophore formation in the moss 
                        Physcomitrella patens. J. Exp. Bot.,  2018, 69(20), 4839-4851.
[http://dx.doi.org/10.1093/jxb/ery257] [PMID: 29992239] 
[83] 
Möglich, A.; Ayers, R.A.; Moffat, K. Structure and signaling mechanism of Per-ARNT-Sim domains. Structure,  2009, 17(10), 1282-1294.
[http://dx.doi.org/10.1016/j.str.2009.08.011] [PMID: 19836329] 
[84] 
Rensing, S.A.; Lang, D.; Zimmer, A.D.; Terry, A.; Salamov, A.; Shapiro, H.; Nishiyama, T.; Perroud, P.F.; Lindquist, E.A.; Kamisugi, Y.; Tanahashi, T.; Sakakibara, K.; Fujita, T.; Oishi, K.; Shin-I, T.; Kuroki, Y.; Toyoda, A.; Suzuki, Y.; Hashimoto, S.; Yamaguchi, K.; Sugano, S.; Kohara, Y.; Fujiyama, A.; Anterola, A.; Aoki, S.; Ashton, N.; Barbazuk, W.B.; Barker, E.; Bennetzen, J.L.; Blankenship, R.; Cho, S.H.; Dutcher, S.K.; Estelle, M.; Fawcett, J.A.; Gundlach, H.; Hanada, K.; Heyl, A.; Hicks, K.A.; Hughes, J.; Lohr, M.; Mayer, K.; Melkozernov, A.; Murata, T.; Nelson, D.R.; Pils, B.; Prigge, M.; Reiss, B.; Renner, T.; Rombauts, S.; Rushton, P.J.; Sanderfoot, A.; Schween, G.; Shiu, S.H.; Stueber, K.; Theodoulou, F.L.; Tu, H.; Van de Peer, Y.; Verrier, P.J.; Waters, E.; Wood, A.; Yang, L.; Cove, D.; Cuming, A.C.; Hasebe, M.; Lucas, S.; Mishler, B.D.; Reski, R.; Grigoriev, I.V.; Quatrano, R.S.; Boore, J.L. 
                        The 
                        Physcomitrella
                         genome reveals evolutionary insights into the conquest of land by plants.
                     Science,  2008, 319(5859), 64-69.
[http://dx.doi.org/10.1126/science.1150646] [PMID: 18079367] 
[85] 
Ishida, K.; Yamashino, T.; Nakanishi, H.; Mizuno, T. Classification of the genes involved in the two-component system of the moss Physcomitrella patens. Biosci. Biotechnol. Biochem.,  2010, 74(12), 2542-2545.
[http://dx.doi.org/10.1271/bbb.100623] [PMID: 21150091] 
[86] 
Schaller, G.E.; Kieber, J.J.; Shiu, S.H. Two-component signaling elements and histidyl-aspartyl phosphorelays. Arabidopsis Book,  2008, 6, e0112.
[http://dx.doi.org/10.1199/tab.0112] [PMID: 22303237] 
[87] 
Ding, Y.; Kalo, P.; Yendrek, C.; Sun, J.; Liang, Y.; Marsh, J.F.; Harris, J.M.; Oldroyd, G.E. 
                        Abscisic acid coordinates nod factor and cytokinin signaling during the regulation of nodulation in 
                        Medicago truncatula.
                     Plant Cell,  2008, 20(10), 2681-2695.
[http://dx.doi.org/10.1105/tpc.108.061739] [PMID: 18931020] 
[88] 
Murray, J.D.; Karas, B.J.; Sato, S.; Tabata, S.; Amyot, L.; Szczyglowski, K. 
                        A cytokinin perception mutant colonized by 
                        Rhizobium
                         in the absence of nodule organogenesis.
                     Science,  2007, 315(5808), 101-104.
[http://dx.doi.org/10.1126/science.1132514] [PMID: 17110535] 
[89] 
Paul, S.; Wildhagen, H.; Janz, D.; Teichmann, T.; Hänsch, R.; Polle, A. 
                        Tissue-and cell-specific cytokinin activity in 
                        Populus× canescens
                         monitored by ARR5: GUS reporter lines in summer and winter.
                     Front. Plant Sci.,  2016, 7, 652.
[http://dx.doi.org/10.3389/fpls.2016.00652] [PMID: 27242853] 
[90] 
Papon, N.; Vansiri, A.; Gantet, P.; Chénieux, J.C.; Rideau, M.; Crèche, J. 
                        Histidine-containing phosphotransfer domain extinction by RNA interference turns off a cytokinin signalling circuitry in 
                        Catharanthus roseus
                         suspension cells.
                     FEBS Lett.,  2004, 558(1-3), 85-88.
[http://dx.doi.org/10.1016/S0014-5793(03)01522-9] [PMID: 14759521] 
[91] 
Nongpiur, R.; Soni, P.; Karan, R.; Singla-Pareek, S.L.; Pareek, A. Histidine kinases in plants: cross talk between hormone and stress responses. Plant Signal. Behav.,  2012, 7(10), 1230-1237.
[http://dx.doi.org/10.4161/psb.21516] [PMID: 22902699] 
[92] 
Pareek, A.; Singh, A.; Kumar, M.; Kushwaha, H.R.; Lynn, A.M.; Singla-Pareek, S.L. 
                        Whole-genome analysis of 
                        Oryza sativa
                         reveals similar architecture of two-component signaling machinery with Arabidopsis.
                     Plant Physiol.,  2006, 142(2), 380-397.
[http://dx.doi.org/10.1104/pp.106.086371] [PMID: 16891544] 
[93] 
Singh, G.; Kumar, R. 
                        Genome-wide 
                        
                            in silico
                        
                         analysis of plant two component signaling system in woody model plant 
                        
                            Populus trichocarpa
                        
                        .
                     Res Plant Biol.,  2012, 2(2), 13-23.
[94] 
Stock, J.B.; Ninfa, A.J.; Stock, A.M. Protein phosphorylation and regulation of adaptive responses in bacteria. Microbiol. Rev.,  1989, 53(4), 450-490.
[http://dx.doi.org/10.1128/MR.53.4.450-490.1989] [PMID: 2556636] 
[95] 
Schaller, G.E.; Shiu, S.H.; Armitage, J.P. Two-component systems and their co-option for eukaryotic signal transduction. Curr. Biol.,  2011, 21(9), R320-R330.
[http://dx.doi.org/10.1016/j.cub.2011.02.045] [PMID: 21549954] 
[96] 
Hughes, J.; Lamparter, T. Prokaryotes and phytochrome. The connection to chromophores and signaling. Plant Physiol.,  1999, 121(4), 1059-1068.
[http://dx.doi.org/10.1104/pp.121.4.1059] [PMID: 10594094] 
[97] 
Bleecker, A.B.; Kende, H. Ethylene: a gaseous signal molecule in plants. Annu. Rev. Cell Dev. Biol.,  2000, 16(1), 1-18.
[http://dx.doi.org/10.1146/annurev.cellbio.16.1.1] [PMID: 11031228] 
[98] 
Inoue, T.; Higuchi, M.; Hashimoto, Y.; Seki, M.; Kobayashi, M.; Kato, T.; Tabata, S.; Shinozaki, K.; Kakimoto, T. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature,  2001, 409(6823), 1060-1063.
[http://dx.doi.org/10.1038/35059117] [PMID: 11234017] 
[99] 
Yeh, K.C.; Lagarias, J.C. Eukaryotic phytochromes: light-regulated serine/threonine protein kinases with histidine kinase ancestry. Proc. Natl. Acad. Sci. USA,  1998, 95(23), 13976-13981.
[http://dx.doi.org/10.1073/pnas.95.23.13976] [PMID: 9811911] 
[100] 
Salas-Delgado, G.; Ongay-Larios, L.; Kawasaki-Watanabe, L.; López-Villaseñor, I.; Coria, R. The yeasts phosphorelay systems: a comparative view. World J. Microbiol. Biotechnol.,  2017, 33(6), 111.
[http://dx.doi.org/10.1007/s11274-017-2272-z] [PMID: 28470426] 
[101] 
Lomin, S.N.; Yonekura-Sakakibara, K.; Romanov, G.A.; Sakakibara, H. Ligand-binding properties and subcellular localization of maize cytokinin receptors. J. Exp. Bot.,  2011, 62(14), 5149-5159.
[http://dx.doi.org/10.1093/jxb/err220] [PMID: 21778179] 
[102] 
Wulfetange, K.; Lomin, S.N.; Romanov, G.A.; Stolz, A.; Heyl, A.; Schmülling, T. The cytokinin receptors of Arabidopsis are located mainly to the endoplasmic reticulum. Plant Physiol.,  2011, 156(4), 1808-1818.
[http://dx.doi.org/10.1104/pp.111.180539] [PMID: 21709172] 
[103] 
Romanov, G.A.; Lomin, S.N.; Schmülling, T. Biochemical characteristics and ligand-binding properties of Arabidopsis cytokinin receptor AHK3 compared to CRE1/AHK4 as revealed by a direct binding assay. J. Exp. Bot.,  2006, 57(15), 4051-4058.
[http://dx.doi.org/10.1093/jxb/erl179] [PMID: 17075078] 
[104] 
Surette, M.G.; Levit, M.; Liu, Y.; Lukat, G.; Ninfa, E.G.; Ninfa, A.; Stock, J.B. Dimerization is required for the activity of the protein histidine kinase CheA that mediates signal transduction in bacterial chemotaxis. J. Biol. Chem.,  1996, 271(2), 939-945.
[http://dx.doi.org/10.1074/jbc.271.2.939] [PMID: 8557708] 
[105] 
Rivera-Cancel, G.; Ko, W.H.; Tomchick, D.R.; Correa, F.; Gardner, K.H. Full-length structure of a monomeric histidine kinase reveals basis for sensory regulation. Proc. Natl. Acad. Sci. USA,  2014, 111(50), 17839-17844.
[http://dx.doi.org/10.1073/pnas.1413983111] [PMID: 25468971] 
[106] 
Ueguchi, C.; Koizumi, H.; Suzuki, T.; Mizuno, T. 
                        Novel family of sensor histidine kinase genes in 
                        Arabidopsis thaliana. Plant Cell Physiol.,  2001, 42(2), 231-235.
[http://dx.doi.org/10.1093/pcp/pce015] [PMID: 11230578] 
[107] 
Yamada, H.; Suzuki, T.; Terada, K.; Takei, K.; Ishikawa, K.; Miwa, K.; Yamashino, T.; Mizuno, T. The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol.,  2001, 42(9), 1017-1023.
[http://dx.doi.org/10.1093/pcp/pce127] [PMID: 11577198] 
[108] 
Pas, J.; von Grotthuss, M.; Wyrwicz, L.S.; Rychlewski, L.; Barciszewski, J. Structure prediction, evolution and ligand interaction of CHASE domain. FEBS Lett.,  2004, 576(3), 287-290.
[http://dx.doi.org/10.1016/j.febslet.2004.09.020] [PMID: 15498549] 
[109] 
Mougel, C.; Zhulin, I.B. CHASE: an extracellular sensing domain common to transmembrane receptors from prokaryotes, lower eukaryotes and plants. Trends Biochem. Sci.,  2001, 26(10), 582-584.
[http://dx.doi.org/10.1016/S0968-0004(01)01969-7] [PMID: 11590001] 
[110] 
Anantharaman, V.; Aravind, L. The CHASE domain: a predicted ligand-binding module in plant cytokinin receptors and other eukaryotic and bacterial receptors. Trends Biochem. Sci.,  2001, 26(10), 579-582.
[http://dx.doi.org/10.1016/S0968-0004(01)01968-5] [PMID: 11590000] 
[111] 
Heyl, A.; Wulfetange, K.; Pils, B.; Nielsen, N.; Romanov, G.A.; Schmülling, T. Evolutionary proteomics identifies amino acids essential for ligand-binding of the cytokinin receptor CHASE domain. BMC Evol. Biol.,  2007, 7(1), 62.
[http://dx.doi.org/10.1186/1471-2148-7-62] [PMID: 17439640] 
[112] 
Zhang, W.; Shi, L. Distribution and evolution of multiple-step phosphorelay in prokaryotes: lateral domain recruitment involved in the formation of hybrid-type histidine kinases. Microbiology (Reading),  2005, 151(Pt 7), 2159-2173.
[http://dx.doi.org/10.1099/mic.0.27987-0] [PMID: 16000707] 
[113] 
Tsuzuki, M.; Ishige, K.; Mizuno, T. 
                        Phosphotransfer circuitry of the putative multi-signal transducer, ArcB, of 
                        Escherichia coli
                        : 
                        
                            in vitro
                        
                         studies with mutants.
                     Mol. Microbiol.,  1995, 18(5), 953-962.
[http://dx.doi.org/10.1111/j.1365-2958.1995.18050953.x] [PMID: 8825099] 
[114] 
Rashotte, A.M.; Goertzen, L.R. The CRF domain defines cytokinin response factor proteins in plants. BMC Plant Biol.,  2010, 10(1), 74.
[http://dx.doi.org/10.1186/1471-2229-10-74] [PMID: 20420680] 
[115] 
Scharein, B.; Voet-van-Vormizeele, J.; Harter, K.; Groth, G. Ethylene signaling: identification of a putative ETR1-AHP1 phosphorelay complex by fluorescence spectroscopy. Anal. Biochem.,  2008, 377(1), 72-76.
[http://dx.doi.org/10.1016/j.ab.2008.03.015] [PMID: 18384742] 
[116] 
West, A.H.; Stock, A.M. Histidine kinases and response regulator proteins in two-component signaling systems. Trends Biochem. Sci.,  2001, 26(6), 369-376.
[http://dx.doi.org/10.1016/S0968-0004(01)01852-7] [PMID: 11406410] 
[117] 
Burbulys, D.; Trach, K.A.; Hoch, J.A. 
                        Initiation of sporulation in 
                        B. subtilis
                         is controlled by a multicomponent phosphorelay.
                     Cell,  1991, 64(3), 545-552.
[http://dx.doi.org/10.1016/0092-8674(91)90238-T] [PMID: 1846779] 
[118] 
Banno, S.; Noguchi, R.; Yamashita, K.; Fukumori, F.; Kimura, M.; Yamaguchi, I.; Fujimura, M. 
                        Roles of putative His-to-Asp signaling modules HPT-1 and RRG-2, on viability and sensitivity to osmotic and oxidative stresses in 
                        Neurospora crassa. Curr. Genet.,  2007, 51(3), 197-208.
[http://dx.doi.org/10.1007/s00294-006-0116-8] [PMID: 17211673] 
[119] 
Mavrianos, J.; Desai, C.; Chauhan, N. 
                        Two-component histidine phosphotransfer protein Ypd1 is not essential for viability in 
                        Candida albicans. Eukaryot. Cell,  2014, 13(4), 452-460.
[http://dx.doi.org/10.1128/EC.00243-13] [PMID: 24489039] 
[120] 
Heyl, A.; Brault, M.; Frugier, F.; Kuderova, A.; Lindner, A.C.; Motyka, V.; Rashotte, A.M.; Schwartzenberg, K.V.; Vankova, R.; Schaller, G.E. Nomenclature for members of the two-component signaling pathway of plants. Plant Physiol.,  2013, 161(3), 1063-1065.
[http://dx.doi.org/10.1104/pp.112.213207] [PMID: 23324541] 
[121] 
Hutchison, C.E.; Kieber, J.J. Cytokinin signaling in Arabidopsis. Plant Cell,  2002, 14(Suppl.), S47-S59.
[http://dx.doi.org/10.1105/tpc.010444] [PMID: 12045269] 
[122] 
To, J.P.; Haberer, G.; Ferreira, F.J.; Deruère, J.; Mason, M.G.; Schaller, G.E.; Alonso, J.M.; Ecker, J.R.; Kieber, J.J. Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling. Plant Cell,  2004, 16(3), 658-671.
[http://dx.doi.org/10.1105/tpc.018978] [PMID: 14973166] 
[123] 
Rashotte, A.M.; Mason, M.G.; Hutchison, C.E.; Ferreira, F.J.; Schaller, G.E.; Kieber, J.J. A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a two-component pathway. Proc. Natl. Acad. Sci. USA,  2006, 103(29), 11081-11085.
[http://dx.doi.org/10.1073/pnas.0602038103] [PMID: 16832061] 
[124] 
Hosoda, K.; Imamura, A.; Katoh, E.; Hatta, T.; Tachiki, M.; Yamada, H.; Mizuno, T.; Yamazaki, T. Molecular structure of the GARP family of plant Myb-related DNA binding motifs of the Arabidopsis response regulators. Plant Cell,  2002, 14(9), 2015-2029.
[http://dx.doi.org/10.1105/tpc.002733] [PMID: 12215502] 
[125] 
Sakai, H.; Aoyama, T.; Oka, A. Arabidopsis ARR1 and ARR2 response regulators operate as transcriptional activators. Plant J.,  2000, 24(6), 703-711.
[http://dx.doi.org/10.1046/j.1365-313x.2000.00909.x] [PMID: 11135105] 
[126] 
Riaño-Pachón, D.M.; Corrêa, L.G.; Trejos-Espinosa, R.; Mueller-Roeber, B. Green transcription factors: a chlamydomonas overview. Genetics,  2008, 179(1), 31-39.
[http://dx.doi.org/10.1534/genetics.107.086090] [PMID: 18493038] 
[127] 
Mizuno, T. Plant response regulators implicated in signal transduction and circadian rhythm. Curr. Opin. Plant Biol.,  2004, 7(5), 499-505.
[http://dx.doi.org/10.1016/j.pbi.2004.07.015] [PMID: 15337091] 
[128] 
Kiba, T.; Aoki, K.; Sakakibara, H.; Mizuno, T. Arabidopsis response regulator, ARR22, ectopic expression of which results in phenotypes similar to the 
                        wol
                         cytokinin-receptor mutant.
                     Plant Cell Physiol.,  2004, 45(8), 1063-1077.
[http://dx.doi.org/10.1093/pcp/pch128] [PMID: 15356332] 
[129] 
Schaller, G.E.; Doi, K.; Hwang, I.; Kieber, J.J.; Khurana, J.P.; Kurata, N.; Mizuno, T.; Pareek, A.; Shiu, S.H.; Wu, P.; Yip, W.K. Nomenclature for two-component signaling elements of rice. Plant Physiol.,  2007, 143(2), 555-557.
[http://dx.doi.org/10.1104/pp.106.093666] [PMID: 17284581] 
[130] 
Horák, J.; Grefen, C.; Berendzen, K.W.; Hahn, A.; Stierhof, Y.D.; Stadelhofer, B.; Stahl, M.; Koncz, C.; Harter, K. 
                        The Arabidopsis thaliana
                         response regulator ARR22 is a putative AHP phospho-histidine phosphatase expressed in the chalaza of developing seeds.
                     BMC Plant Biol.,  2008, 8(1), 77.
[http://dx.doi.org/10.1186/1471-2229-8-77] [PMID: 18625081] 
[131] 
Mähönen, A.P.; Bishopp, A.; Higuchi, M.; Nieminen, K.M.; Kinoshita, K.; Törmäkangas, K.; Ikeda, Y.; Oka, A.; Kakimoto, T.; Helariutta, Y. Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science,  2006, 311(5757), 94-98.
[http://dx.doi.org/10.1126/science.1118875] [PMID: 16400151] 
[132] 
Gattolin, S.; Alandete-Saez, M.; Elliott, K.; Gonzalez-Carranza, Z.; Naomab, E.; Powell, C.; Roberts, J.A. 
                        Spatial and temporal expression of the response regulators ARR22 and ARR24 in 
                        Arabidopsis thaliana. J. Exp. Bot.,  2006, 57(15), 4225-4233.
[http://dx.doi.org/10.1093/jxb/erl205] [PMID: 17099079] 
[133] 
Mizuno, T.; Nakamichi, N. Pseudo-response regulators (PRRs) or true oscillator components (TOCs). Plant Cell Physiol.,  2005, 46(5), 677-685.
[http://dx.doi.org/10.1093/pcp/pci087] [PMID: 15767264] 
[134] 
Mizuno, T. Two-component phosphorelay signal transduction systems in plants: from hormone responses to circadian rhythms. Biosci. Biotechnol. Biochem.,  2005, 69(12), 2263-2276.
[http://dx.doi.org/10.1271/bbb.69.2263] [PMID: 16377883] 
[135] 
Song, Y.H.; Ito, S.; Imaizumi, T. Similarities in the circadian clock and photoperiodism in plants. Curr. Opin. Plant Biol.,  2010, 13(5), 594-603.
[http://dx.doi.org/10.1016/j.pbi.2010.05.004] [PMID: 20620097] 
[136] 
Liu, T.; Carlsson, J.; Takeuchi, T.; Newton, L.; Farré, E.M. Direct regulation of abiotic responses by the Arabidopsis circadian clock component PRR7. Plant J.,  2013, 76(1), 101-114.
[http://dx.doi.org/10.1111/tpj.12276] [PMID: 23808423] 
[137] 
Nakamichi, N.; Takao, S.; Kudo, T.; Kiba, T.; Wang, Y.; Kinoshita, T.; Sakakibara, H. Improvement of Arabidopsis biomass and cold, drought and salinity stress tolerance by modified circadian clock-associated PSEUDO-RESPONSE REGULATORs. Plant Cell Physiol.,  2016, 57(5), 1085-1097.
[http://dx.doi.org/10.1093/pcp/pcw057] [PMID: 27012548] 
[138] 
Fukushima, A.; Kusano, M.; Nakamichi, N.; Kobayashi, M.; Hayashi, N.; Sakakibara, H.; Mizuno, T.; Saito, K. Impact of clock-associated Arabidopsis pseudo-response regulators in metabolic coordination. Proc. Natl. Acad. Sci. USA,  2009, 106(17), 7251-7256.
[http://dx.doi.org/10.1073/pnas.0900952106] [PMID: 19359492] 
[139] 
Hayama, R.; Sarid-Krebs, L.; Richter, R.; Fernández, V.; Jang, S.; Coupland, G. PSEUDO RESPONSE REGULATORs stabilize CONSTANS protein to promote flowering in response to day length. EMBO J.,  2017, 36(7), 904-918.
[http://dx.doi.org/10.15252/embj.201693907] [PMID: 28270524] 
[140] 
Satbhai, S.B.; Yamashino, T.; Okada, R.; Nomoto, Y.; Mizuno, T.; Tezuka, Y.; Itoh, T.; Tomita, M.; Otsuki, S.; Aoki, S. 
                        Pseudo-response regulator (PRR) homologues of the moss 
                        Physcomitrella patens
                        : insights into the evolution of the PRR family in land plants.
                     DNA Res.,  2011, 18(1), 39-52.
[http://dx.doi.org/10.1093/dnares/dsq033] [PMID: 21186242] 
[141] 
Serrano-Bueno, G.; Romero-Campero, F.J.; Lucas-Reina, E.; Romero, J.M.; Valverde, F. Evolution of photoperiod sensing in plants and algae. Curr. Opin. Plant Biol.,  2017, 37, 10-17.
[http://dx.doi.org/10.1016/j.pbi.2017.03.007] [PMID: 28391047] 
[142] 
Pin, P.A.; Zhang, W.; Vogt, S.H.; Dally, N.; Büttner, B.; Schulze-Buxloh, G.; Jelly, N.S.; Chia, T.Y.; Mutasa-Göttgens, E.S.; Dohm, J.C.; Himmelbauer, H.; Weisshaar, B.; Kraus, J.; Gielen, J.J.; Lommel, M.; Weyens, G.; Wahl, B.; Schechert, A.; Nilsson, O.; Jung, C.; Kraft, T.; Müller, A.E. The role of a pseudo-response regulator gene in life cycle adaptation and domestication of beet. Curr. Biol.,  2012, 22(12), 1095-1101.
[http://dx.doi.org/10.1016/j.cub.2012.04.007] [PMID: 22608508] 
[143] 
Haydon, M.J.; Mielczarek, O.; Robertson, F.C.; Hubbard, K.E.; Webb, A.A. 
                        Photosynthetic entrainment of the 
                        Arabidopsis thaliana
                         circadian clock.
                     Nature,  2013, 502(7473), 689-692.
[http://dx.doi.org/10.1038/nature12603] [PMID: 24153186] 
[144] 
Makino, S.; Kiba, T.; Imamura, A.; Hanaki, N.; Nakamura, A.; Suzuki, T.; Taniguchi, M.; Ueguchi, C.; Sugiyama, T.; Mizuno, T. 
                        Genes encoding pseudo-response regulators: insight into His-to-Asp phosphorelay and circadian rhythm in 
                        Arabidopsis thaliana. Plant Cell Physiol.,  2000, 41(6), 791-803.
[http://dx.doi.org/10.1093/pcp/41.6.791] [PMID: 10945350] 
[145] 
Takata, N.; Saito, S.; Saito, C.T.; Uemura, M. Phylogenetic footprint of the plant clock system in angiosperms: evolutionary processes of pseudo-response regulators. BMC Evol. Biol.,  2010, 10(1), 126.
[http://dx.doi.org/10.1186/1471-2148-10-126] [PMID: 20433765] 
[146] 
Farré, E.M.; Liu, T. The PRR family of transcriptional regulators reflects the complexity and evolution of plant circadian clocks. Curr. Opin. Plant Biol.,  2013, 16(5), 621-629.
[http://dx.doi.org/10.1016/j.pbi.2013.06.015] [PMID: 23856081] 
[147] 
Bartrina, I.; Jensen, H.; Novák, O.; Strnad, M.; Werner, T.; Schmülling, T. Gain-of-function mutants of the cytokinin receptors AHK2 and AHK3 regulate plant organ size, flowering time and plant longevity. Plant Physiol.,  2017, 173(3), 1783-1797.
[http://dx.doi.org/10.1104/pp.16.01903] [PMID: 28096190] 
[148] 
Müller, B.; Sheen, J. Arabidopsis cytokinin signaling pathway. Sci. STKE,  2007, 2007(407), cm5.
[PMID: 17925576] 
[149] 
Singh, A.; Kushwaha, H.R.; Soni, P.; Gupta, H.; Singla-Pareek, S.L.; Pareek, A. Tissue specific and abiotic stress regulated transcription of histidine kinases in plants is also influenced by diurnal rhythm. Front. Plant Sci.,  2015, 6, 711.
[http://dx.doi.org/10.3389/fpls.2015.00711] [PMID: 26442025] 
[150] 
Nongpiur, R.C.; Singla-Pareek, S.L.; Pareek, A. The quest for osmosensors in plants. J. Exp. Bot.,  2020, 71(2), 595-607.
[http://dx.doi.org/10.1093/jxb/erz263] [PMID: 31145792] 
[151] 
Nongpiur, R.C.; Gupta, P.; Sharan, A.; Singh, D.; Singla-Pareek, S.L.; Pareek, A. The two-component system: transducing environmental and hormonal signals. In: Sensory Biology of Plants Springer: Singapore,  2019, pp. 247-278.
[152] 
Gupta, P.; Nongpiur, R.C.; Singla-Pareek, S.L.; Pareek, A. Plant histidine kinases: Targets for crop improvement. In: Advancement in Crop Improvement Techniques ; Tuteja, N.; Tuteja, R.; Passricha, N.; Saifi, SK., Eds.; Woodhead Publishing,,  2020, pp. 101-109.
[153] 
Sharan, A.; Soni, P.; Nongpiur, R.C.; Singla-Pareek, S.L.; Pareek, A. Mapping the ‘Two-component system’network in rice. Sci. Rep.,  2017, 7(1), 1-3.
[http://dx.doi.org/10.1038/s41598-017-08076-w] [PMID: 28127051] 
[154] 
Kushwaha, H.R.; Singla-Pareek, S.L.; Pareek, A. Putative osmosensor--OsHK3b--a histidine kinase protein from rice shows high structural conservation with its ortholog AtHK1 from Arabidopsis. J. Biomol. Struct. Dyn.,  2014, 32(8), 1318-1332.
[http://dx.doi.org/10.1080/07391102.2013.818576] [PMID: 23869567] 
[155] 
Sun, L.; Zhang, Q.; Wu, J.; Zhang, L.; Jiao, X.; Zhang, S.; Zhang, Z.; Sun, D.; Lu, T.; Sun, Y. Two rice authentic histidine phosphotransfer proteins, OsAHP1 and OsAHP2, mediate cytokinin signaling and stress responses in rice. Plant Physiol.,  2014, 165(1), 335-345.
[http://dx.doi.org/10.1104/pp.113.232629] [PMID: 24578505] 
[156] 
Wang, B.; Chen, Y.; Guo, B.; Kabir, M.R.; Yao, Y.; Peng, H.; Xie, C.; Zhang, Y.; Sun, Q.; Ni, Z. Expression and functional analysis of genes encoding cytokinin receptor-like histidine kinase in maize (Zea mays L.). Mol. Genet. Genomics,  2014, 289(4), 501-512.
[http://dx.doi.org/10.1007/s00438-014-0821-9] [PMID: 24585212] 
Cite As
Current Genomics

The Journey from Two-Step to Multi-Step Phosphorelay Signaling Systems

Abstract

Graphical Abstract
