1932

Abstract

The two-component system (TCS), which is one of the most evolutionarily conserved signaling pathway systems, has been known to regulate multiple biological activities and environmental responses in plants. Significant progress has been made in characterizing the biological functions of the TCS components, including signal receptor histidine kinase (HK) proteins, signal transducer histidine-containing phosphotransfer proteins, and effector response regulator proteins. In this review, our scope is focused on the diverse structure, subcellular localization, and interactions of the HK proteins, as well as their signaling functions during development and environmental responses across different plant species. Based on data collected from scientific studies, knowledge about acting mechanisms and regulatory roles of HK proteins is presented. This comprehensive summary ofthe HK-related network provides a panorama of sophisticated modulating activities of HK members and gaps in understanding these activities, as well as the basis for developing biotechnological strategies to enhance the quality of crop plants.

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2021-06-17
2024-04-24
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Literature Cited

  1. 1. 
    Adam K, Hunter T. 2018. Histidine kinases and the missing phosphoproteome from prokaryotes to eukaryotes. Lab. Invest. 98:233–47
    [Google Scholar]
  2. 2. 
    Ahmad B, Azeem F, Ali MA, Nawaz MA, Nadeem H et al. 2020. Genome-wide identification and expression analysis of two component system genes in Cicer arietinum. Genomics 112:1371–83
    [Google Scholar]
  3. 3. 
    Anantharaman V, Aravind L. 2001. The CHASE domain: a predicted ligand-binding module in plant cytokinin receptors and other eukaryotic and bacterial receptors. Trends Biochem. Sci. 26:579–82
    [Google Scholar]
  4. 4. 
    Arico D, Legris M, Castro L, Garcia CF, Laino A et al. 2019. Neighbour signals perceived by phytochrome B increase thermotolerance in Arabidopsis. Plant Cell Environ 42:2554–66This study presents the involvement of phytochrome B in regulating plant resistance to heat stress.
    [Google Scholar]
  5. 5. 
    Bae G, Choi G. 2008. Decoding of light signals by plant phytochromes and their interacting proteins. Annu. Rev. Plant Biol. 59:281–311
    [Google Scholar]
  6. 6. 
    Bakshi A, Piya S, Fernandez JC, Chervin C, Hewezi T, Binder BM. 2018. Ethylene receptors signal via a noncanonical pathway to regulate abscisic acid responses. Plant Physiol 176:910–29
    [Google Scholar]
  7. 7. 
    Barros-Galvão T, Dave A, Gilday AD, Harvey D, Vaistij FE, Graham IA 2020. ABA INSENSITIVE4 promotes rather than represses PHYA-dependent seed germination in Arabidopsis thaliana. New Phytol 226:953–56
    [Google Scholar]
  8. 8. 
    Berleth M, Berleth N, Minges A, Hänsch S, Burkart RC et al. 2019. Molecular analysis of protein-protein interactions in the ethylene pathway in the different ethylene receptor subfamilies. Front. Plant Sci 10:726This study characterizes protein interactions of type II subfamily ethylene receptor ETR2.
    [Google Scholar]
  9. 9. 
    Bhattacharyya D, Garladinne M, Lee YH. 2015. Volatile indole produced by rhizobacterium Proteus vulgaris JBLS202 stimulates growth of Arabidopsis thaliana through auxin, cytokinin, and brassinosteroid pathways. J. Plant Growth Regul. 34:158–68
    [Google Scholar]
  10. 10. 
    Binder BM. 2020. Ethylene signaling in plants. J. Biol. Chem. 295:7710–25
    [Google Scholar]
  11. 11. 
    Binder BM, O'Malley RC, Wang W, Zutz TC, Bleecker AB. 2006. Ethylene stimulates nutations that are dependent on the ETR1 receptor. Plant Physiol 142:1690–700
    [Google Scholar]
  12. 12. 
    Bisson MMA, Groth G. 2010. New insight in ethylene signaling: Autokinase activity of ETR1 modulates the interaction of receptors and EIN2. Mol. Plant 3:882–89
    [Google Scholar]
  13. 13. 
    Boivin S, Kazmierczak T, Brault M, Wen J, Gamas P et al. 2016. Different cytokinin histidine kinase receptors regulate nodule initiation as well as later nodule developmental stages in Medicago truncatula. Plant Cell Environ 39:2198–209
    [Google Scholar]
  14. 14. 
    Caesar K, Thamm AMK, Witthöft J, Elgass K, Huppenberger P et al. 2011. Evidence for the localization of the Arabidopsis cytokinin receptors AHK3 and AHK4 in the endoplasmic reticulum. J. Exp. Bot. 62:5571–80
    [Google Scholar]
  15. 15. 
    Cao K, Yu J, Xu D, Ai K, Bao E, Zou Z 2018. Exposure to lower red to far-red light ratios improve tomato tolerance to salt stress. BMC Plant Biol 18:92
    [Google Scholar]
  16. 16. 
    Carvalho RF, Moda LR, Silva GP, Gavassi MA, Prado RM. 2016. Nutrition in tomato (Solanum lycopersicum L) as affected by light: revealing a new role of phytochrome A. Aust. J. Crop Sci. 10:331–35
    [Google Scholar]
  17. 17. 
    Casteel CL, De Alwis M, Bak A, Dong H, Whitham SA, Jander G. 2015. Disruption of ethylene responses by Turnip mosaic virus mediates suppression of plant defense against the green peach aphid vector. Plant Physiol 169:209–18
    [Google Scholar]
  18. 18. 
    Černý M, Jedelský PL, Novák J, Schlosser A, Brzobohatý B. 2014. Cytokinin modulates proteomic, transcriptomic and growth responses to temperature shocks in Arabidopsis. Plant Cell Environ 37:1641–55
    [Google Scholar]
  19. 19. 
    Chang C. 2003. Ethylene signaling: The MAPK module has finally landed. Trends Plant Sci 8:365–68
    [Google Scholar]
  20. 20. 
    Chang C, Kwok SF, Bleecker AB, Meyerowitz EM. 1993. Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. Science 262:539–44
    [Google Scholar]
  21. 21. 
    Chang J, Clay JM, Chang C. 2014. Association of cytochrome b5 with ETR1 ethylene receptor signaling through RTE1 in Arabidopsis. Plant J 77:558–67
    [Google Scholar]
  22. 22. 
    Chen F, Zhou W, Yin H, Luo X, Chen W et al. 2020. Shading of the mother plant during seed development promotes subsequent seed germination in soybean. J. Exp. Bot. 71:2072–84
    [Google Scholar]
  23. 23. 
    Chen Y, Hu G, Rodriguez C, Liu M, Binder BM, Chervin C. 2020. Roles of SlETR7, a newly discovered ethylene receptor, in tomato plant and fruit development. Hortic. Res. 7:17
    [Google Scholar]
  24. 24. 
    Chen Y-F, Gao Z, Kerris RJ III, Wang W, Binder BM, Schaller GE. 2010. Ethylene receptors function as components of high-molecular-mass protein complexes in Arabidopsis. PLOS ONE 5:e8640
    [Google Scholar]
  25. 25. 
    Chen Y-F, Shakeel SN, Bowers J, Zhao X-C, Etheridge N, Schaller GE. 2007. Ligand-induced degradation of the ethylene receptor ETR2 through a proteasome-dependent pathway in Arabidopsis. J. Biol. Chem. 282:24752–58
    [Google Scholar]
  26. 26. 
    Choi J, Huh SU, Kojima M, Sakakibara H, Paek K-H, Hwang I. 2010. The cytokinin-activated transcription factor ARR2 promotes plant immunity via TGA3/NPR1-dependent salicylic acid signaling in Arabidopsis. Dev. Cell 19:284–95
    [Google Scholar]
  27. 27. 
    Chu ZX, Ma Q, Lin YX, Tang XL, Zhou YQ et al. 2011. Genome-wide identification, classification, and analysis of two-component signal system genes in maize. Genet. Mol. Res. 10:3316–30
    [Google Scholar]
  28. 28. 
    Contreras-Cornejo HA, López-Bucio JS, Méndez-Bravo A, Macías-Rodríguez L, Ramos-Vega M et al. 2015. Mitogen-activated protein kinase 6 and ethylene and auxin signaling pathways are involved in Arabidopsis root-system architecture alterations by Trichoderma atroviride. Mol. Plant Microbe Interact. 28:701–10
    [Google Scholar]
  29. 29. 
    Cortés LE, Weldegergis BT, Boccalandro HE, Dicke M, Ballaré CL. 2016. Trading direct for indirect defense? Phytochrome B inactivation in tomato attenuates direct anti-herbivore defenses whilst enhancing volatile-mediated attraction of predators. New Phytol 212:1057–71
    [Google Scholar]
  30. 30. 
    Cortleven A, Nitschke S, Klaumünzer M, Abdelgawad H, Asard H et al. 2014. A novel protective function for cytokinin in the light stress response is mediated by the ARABIDOPSIS HISTIDINE KINASE2 and ARABIDOPSIS HISTIDINE KINASE3 receptors. Plant Physiol 164:1470–83
    [Google Scholar]
  31. 31. 
    Courbier S, Pierik R. 2019. Canopy light quality modulates stress responses in plants. iScience 22:441–52
    [Google Scholar]
  32. 32. 
    D'Amico-Damião V, Cruz FJR, Gavassi MA, Santos DMM, Melo HC, Carvalho RF. 2015. Photomorphogenic modulation of water stress in tomato (Solanum lycopersicum L.): the role of phytochromes A, B1, and B2. J. Hortic. Sci. Biotech. 90:25–30
    [Google Scholar]
  33. 33. 
    Daudu D, Allion E, Liesecke F, Papon N, Courdavault V et al. 2017. CHASE-containing histidine kinase receptors in apple tree: from a common receptor structure to divergent cytokinin binding properties and specific functions. Front. Plant Sci. 8:1614
    [Google Scholar]
  34. 34. 
    Deng Y, Dong H, Mu J, Ren B, Zheng B et al. 2010. Arabidopsis histidine kinase CKI1 acts upstream of histidine phosphotransfer proteins to regulate female gametophyte development and vegetative growth. Plant Cell 22:1232–48
    [Google Scholar]
  35. 35. 
    Desikan R, Hancock JT, Bright J, Harrison J, Weir I et al. 2005. A role for ETR1 in hydrogen peroxide signaling in stomatal guard cells. Plant Physiol 137:831–34
    [Google Scholar]
  36. 36. 
    Desikan R, Horák J, Chaban C, Mira-Rodado V, Witthöft J et al. 2008. The histidine kinase AHK5 integrates endogenous and environmental signals in Arabidopsis guard cells. PLOS ONE 3:e2491
    [Google Scholar]
  37. 37. 
    Dhar YV, Lakhwani D, Pandey A, Singh S, Trivedi PK, Asif MH. 2019. Genome-wide identification and interactome analysis of members of two-component system in Banana. BMC Genom 20:674
    [Google Scholar]
  38. 38. 
    Dinolfo MI, Castañares E, Stenglein SA. 2017. Resistance of Fusarium poae in Arabidopsis leaves requires mainly functional JA and ET signaling pathways. Fungal Biol 121:841–48
    [Google Scholar]
  39. 39. 
    Dobisova T, Hrdinova V, Cuesta C, Michlickova S, Urbankova I et al. 2017. Light controls cytokinin signaling via transcriptional regulation of constitutively active sensor histidine kinase CKI1. Plant Physiol 174:387–404This study demonstrates the link between light- and cytokinin-controlled plant development through regulation of CKI1 expression by phytochrome A.
    [Google Scholar]
  40. 40. 
    Dong C-H, Jang M, Scharein B, Malach A, Rivarola M et al. 2010. Molecular association of the Arabidopsis ETR1 ethylene receptor and a regulator of ethylene signaling, RTE1. J. Biol. Chem. 285:40706–13
    [Google Scholar]
  41. 41. 
    Dong C-H, Rivarola M, Resnick JS, Maggin BD, Chang C. 2008. Subcellular co-localization of Arabidopsis RTE1 and ETR1 supports a regulatory role for RTE1 in ETR1 ethylene signaling. Plant J 53:275–86
    [Google Scholar]
  42. 42. 
    Dowd CD, Chronis D, Radakovic ZS, Siddique S, Schmülling T et al. 2017. Divergent expression of cytokinin biosynthesis, signaling and catabolism genes underlying differences in feeding sites induced by cyst and root-knot nematodes. Plant J 92:211–28
    [Google Scholar]
  43. 43. 
    Ecker JR. 1995. The ethylene signal transduction pathway in plants. Science 268:667–75
    [Google Scholar]
  44. 44. 
    Ermert AL, Mailliet K, Hughes J. 2016. Holophytochrome-interacting proteins in Physcomitrella: putative actors in phytochrome cytoplasmic signaling. Front. Plant Sci. 7:613
    [Google Scholar]
  45. 45. 
    Evans D, Dodds J, Lloyd P, Hall M. 1982. A study of the subcellular localisation of an ethylene binding site in developing cotyledons of Phaseolus vulgaris L. by high resolution autoradiography. Planta 154:48–52
    [Google Scholar]
  46. 46. 
    Fankhauser C, Yeh K-C, Clark J, Zhang H, Elich TD, Chory J. 1999. PKS1, a substrate phosphorylated by phytochrome that modulates light signaling in Arabidopsis. Science 284:1539–41
    [Google Scholar]
  47. 47. 
    Fei C, Chen L, Yang T, Zou W, Lin H, Xi D. 2019. The role of phytochromes in Nicotiana tabacum against Chilli veinal mottle virus. Plant Physiol. Biochem. 139:470–77
    [Google Scholar]
  48. 48. 
    Gahlaut V, Mathur S, Dhariwal R, Khurana JP, Tyagi AK et al. 2014. A multi-step phosphorelay two-component system impacts on tolerance against dehydration stress in common wheat. Funct. Integr. Genom. 14:707–16
    [Google Scholar]
  49. 49. 
    Ganesan M, Lee HY, Kim JI, Song PS. 2017. Development of transgenic crops based on photo-biotechnology. Plant Cell Environ 40:2469–86
    [Google Scholar]
  50. 50. 
    Gao Z, Chen Y-F, Randlett MD, Zhao X-C, Findell JL et al. 2003. Localization of the Raf-like kinase CTR1 to the endoplasmic reticulum of Arabidopsis through participation in ethylene receptor signaling complexes. J. Biol. Chem. 278:34725–32
    [Google Scholar]
  51. 51. 
    Gao Z, Wen C-K, Binder BM, Chen Y-F, Chang J et al. 2008. Heteromeric interactions among ethylene receptors mediate signaling in Arabidopsis. J. Biol. Chem. 283:23801–10
    [Google Scholar]
  52. 52. 
    García A, Aguado E, Martínez C, Loska D, Beltrán S et al. 2020. The ethylene receptors CpETR1A and CpETR2B cooperate in the control of sex determination in Cucurbita pepo. J. Exp. Bot. 71:154–67
    [Google Scholar]
  53. 53. 
    Gavassi MA, Monteiro CC, Campos ML, Melo HC, Carvalho RF. 2017. Phytochromes are key regulators of abiotic stress responses in tomato. Sci. Hortic. 222:126–35
    [Google Scholar]
  54. 54. 
    Giron D, Frago E, Glevarec G, Pieterse CMJ, Dicke M. 2013. Cytokinins as key regulators in plant–microbe–insect interactions: connecting plant growth and defence. Funct. Ecol. 27:599–609
    [Google Scholar]
  55. 55. 
    Gordon SP, Chickarmane VS, Ohno C, Meyerowitz EM. 2009. Multiple feedback loops through cytokinin signaling control stem cell number within the Arabidopsis shoot meristem. PNAS 106:16529–34
    [Google Scholar]
  56. 56. 
    Grefen C, Städele K, Růžička K, Obrdlik P, Harter K, Horák J. 2008. Subcellular localization and in vivo interactions of the Arabidopsis thaliana ethylene receptor family members. Mol. Plant 1:308–20
    [Google Scholar]
  57. 57. 
    Gururani MA, Venkatesh J, Ganesan M, Strasser RJ, Han Y et al. 2015. In vivo assessment of cold tolerance through chlorophyll-a fluorescence in transgenic zoysiagrass expressing mutant phytochrome A. PLOS ONE 10:e0127200
    [Google Scholar]
  58. 58. 
    Hall AE, Bleecker AB. 2003. Analysis of combinatorial loss-of-function mutants in the Arabidopsis ethylene receptors reveals that the ers1 etr1 double mutant has severe developmental defects that are EIN2 dependent. Plant Cell 15:2032–41
    [Google Scholar]
  59. 59. 
    Hall AE, Findell JL, Schaller GE, Sisler EC, Bleecker AB. 2000. Ethylene perception by the ERS1 protein in Arabidopsis. Plant Physiol 123:1449–58
    [Google Scholar]
  60. 60. 
    Han Y, Zhang C, Yang H, Jiao Y. 2014. Cytokinin pathway mediates APETALA1 function in the establishment of determinate floral meristems in Arabidopsis. PNAS 111:6840–45
    [Google Scholar]
  61. 61. 
    He Y, Liu X, Ye L, Pan C, Chen L et al. 2016. Genome-wide identification and expression analysis of two-component system genes in tomato. Int. J. Mol. Sci. 17:1204
    [Google Scholar]
  62. 62. 
    He Y, Liu X, Zou T, Pan C, Qin L et al. 2016. Genome-wide identification of two-component system genes in Cucurbitaceae crops and expression profiling analyses in cucumber. Front. Plant Sci. 7:899
    [Google Scholar]
  63. 63. 
    Hejátko J, Pernisova M, Eneva T, Palme K, Brzobohatý B. 2003. The putative sensor histidine kinase CKI1 is involved in female gametophyte development in Arabidopsis. Genet. Mol. Res. 269:443–53
    [Google Scholar]
  64. 64. 
    Hejátko J, Ryu H, Kim G-T, Dobešová R, Choi S et al. 2009. The histidine kinases CYTOKININ-INDEPENDENT1 and ARABIDOPSIS HISTIDINE KINASE2 and 3 regulate vascular tissue development in Arabidopsis shoots. Plant Cell 21:2008–21
    [Google Scholar]
  65. 65. 
    Herivaux A, De Bernonville TD, Roux C, Clastre M, Courdavault V et al. 2017. The identification of phytohormone receptor homologs in early diverging fungi suggests a role for plant sensing in land colonization by fungi. mBio 8:e01739–16
    [Google Scholar]
  66. 66. 
    Hertig C, Melzer M, Rutten T, Erbe S, Hensel G et al. 2020. Barley HISTIDINE KINASE 1 (HvHK1) coordinates transfer cell specification in the young endosperm. Plant J 103:1869–84
    [Google Scholar]
  67. 67. 
    Hoang QT, Han Y-J, Kim J-I. 2019. Plant phytochromes and their phosphorylation. Int. J. Mol. Sci. 20:3450This article is a comprehensive summary of phytochrome structure and action.
    [Google Scholar]
  68. 68. 
    Hoecker U. 2017. The activities of the E3 ubiquitin ligase COP1/SPA, a key repressor in light signaling. Curr. Opin. Plant Biol. 37:63–69
    [Google Scholar]
  69. 69. 
    Hofmann A, Müller S, Drechsler T, Berleth M, Caesar K et al. 2020. High-level expression, purification and initial characterization of recombinant Arabidopsis histidine kinase AHK1. Plants 9:304This work revealed the additional function of AHK1 as a phosphatase enzyme.
    [Google Scholar]
  70. 70. 
    Hoppen C, Müller L, Albrecht AC, Groth G. 2019. The NOP-1 peptide derived from the central regulator of ethylene signaling EIN2 delays floral senescence in cut flowers. Sci. Rep. 9:1287
    [Google Scholar]
  71. 71. 
    Hothorn M, Dabi T, Chory J. 2011. Structural basis for cytokinin recognition by Arabidopsis thaliana histidine kinase 4. Nat. Chem. Biol. 7:766–68
    [Google Scholar]
  72. 72. 
    Hua J, Chang C, Sun Q, Meyerowitz EM. 1995. Ethylene insensitivity conferred by Arabidopsis ERS gene. Science 269:1712–14
    [Google Scholar]
  73. 73. 
    Hua J, Sakai H, Nourizadeh S, Chen QG, Bleecker AB et al. 1998. EIN4 and ERS2 are members of the putative ethylene receptor gene family in Arabidopsis. Plant Cell 10:1321–32
    [Google Scholar]
  74. 74. 
    Hwang I, Chen H-C, Sheen J. 2002. Two-component signal transduction pathways in Arabidopsis. Plant Physiol 129:500–15
    [Google Scholar]
  75. 75. 
    Hwang I, Sheen J. 2001. Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413:383–89
    [Google Scholar]
  76. 76. 
    Iqbal N, Khan NA, Ferrante A, Trivellini A, Francini A, Khan MIR. 2017. Ethylene role in plant growth, development and senescence: interaction with other phytohormones. Front. Plant Sci. 8:475
    [Google Scholar]
  77. 77. 
    Ishida K, Niwa Y, Yamashino T, Mizuno T. 2009. A genome-wide compilation of the two-component systems in Lotus japonicus. DNA Res 16:237–47
    [Google Scholar]
  78. 78. 
    Ishida K, Yamashino T, Nakanishi H, Mizuno T. 2010. Classification of the genes involved in the two-component system of the moss Physcomitrella patens. Biosci. Biotechnol. Biochem. 74:2542–45
    [Google Scholar]
  79. 79. 
    Iwama A, Yamashino T, Tanaka Y, Sakakibara H, Kakimoto T et al. 2007. AHK5 histidine kinase regulates root elongation through an ETR1-dependent abscisic acid and ethylene signaling pathway in Arabidopsis thaliana. Plant Cell Physiol 48:375–80
    [Google Scholar]
  80. 80. 
    Izaguirre MM, Mazza CA, Biondini M, Baldwin IT, Ballaré CL. 2006. Remote sensing of future competitors: impacts on plant defenses. PNAS 103:7170–74
    [Google Scholar]
  81. 81. 
    Jeong AR, Lee S-S, Han Y-J, Shin A-Y, Baek A et al. 2016. New constitutively active phytochromes exhibit light-independent signaling activity. Plant Physiol 171:2826–40
    [Google Scholar]
  82. 82. 
    Jiang L, Cao H, Chen Z, Liu C, Cao S et al. 2018. Cytokinin is involved in TPS22-mediated selenium tolerance in Arabidopsis thaliana. Ann. Bot. 122:501–12
    [Google Scholar]
  83. 83. 
    Jiang L, Liu C, Cao H, Chen Z, Yang J et al. 2019. The role of cytokinin in selenium stress response in Arabidopsis. Plant Sci 281:122–32
    [Google Scholar]
  84. 84. 
    Kakimoto T. 1996. CKI1, a histidine kinase homolog implicated in cytokinin signal transduction. Science 274:982–85
    [Google Scholar]
  85. 85. 
    Karniol B, Wagner JR, Walker JM, Vierstra RD. 2005. Phylogenetic analysis of the phytochrome superfamily reveals distinct microbial subfamilies of photoreceptors. Biochem. J. 392:103–16
    [Google Scholar]
  86. 86. 
    Kessenbrock M, Klein SM, Müller L, Hunsche M, Noga G, Groth G. 2017. Novel protein-protein inhibitor based approach to control plant ethylene responses: synthetic peptides for ripening control. Front. Plant Sci. 8:1528
    [Google Scholar]
  87. 87. 
    Kim HJ, Ryu H, Hong SH, Woo HR, Lim PO et al. 2006. Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis. PNAS 103:814–19
    [Google Scholar]
  88. 88. 
    Kim J-I, Park J-E, Zarate X, Song P-S. 2005. Phytochrome phosphorylation in plant light signaling. Photochem. Photobiol. Sci. 4:681–87
    [Google Scholar]
  89. 89. 
    Klein S, Fiebig A, Neuwald D, Dluhosch D, Müller L et al. 2019. Influence of the ethylene-related signal-inhibiting octapeptide NOP-1 on postharvest ripening and quality of ‘Golden Delicious’ apples. J. Sci. Food Agric. 99:3903–9
    [Google Scholar]
  90. 90. 
    Kong S-G, Lee D-S, Kwak S-N, Kim J-K, Sohn J-K, Kim I-S. 2004. Characterization of sunlight-grown transgenic rice plants expressing Arabidopsis phytochrome A. Mol. Breed. 14:35–46
    [Google Scholar]
  91. 91. 
    Kubiasová K, Montesinos JC, Šamajová O, Nisler J, Mik V et al. 2020. Cytokinin fluoroprobe reveals multiple sites of cytokinin perception at plasma membrane and endoplasmic reticulum. Nat. Commun. 11:4285
    [Google Scholar]
  92. 92. 
    Kundu A, DasGupta M. 2018. Silencing of putative cytokinin receptor histidine kinase1 inhibits both inception and differentiation of root nodules in Arachis hypogaea. Mol. Plant Microbe Interact. 31:187–99
    [Google Scholar]
  93. 93. 
    Laffont C, Rey T, André O, Novero M, Kazmierczak T et al. 2015. The CRE1 cytokinin pathway is differentially recruited depending on Medicago truncatula root environments and negatively regulates resistance to a pathogen. PLOS ONE 10:e0116819
    [Google Scholar]
  94. 94. 
    Lashbrook CC, Tieman DM, Klee HJ. 1998. Differential regulation of the tomato ETR gene family throughout plant development. Plant J 15:243–52
    [Google Scholar]
  95. 95. 
    Legris M, Ince , Fankhauser C. 2019. Molecular mechanisms underlying phytochrome-controlled morphogenesis in plants. Nat. Commun. 10:5219
    [Google Scholar]
  96. 96. 
    Lehotai N, Kolbert Z, Pető A, Feigl G, Ördög A et al. 2012. Selenite-induced hormonal and signalling mechanisms during root growth of Arabidopsis thaliana L. J. Exp. Bot. 63:5677–87
    [Google Scholar]
  97. 97. 
    Lin Z, Zhong S, Grierson D. 2009. Recent advances in ethylene research. J. Exp. Bot. 60:3311–36
    [Google Scholar]
  98. 98. 
    Liu Z, Yuan L, Sundaresan V, Yu X 2018. Arabidopsis CKI1 mediated two-component signaling in the specification of female gametophyte. Plant Signal. Behav. 13:e1469360
    [Google Scholar]
  99. 99. 
    Liu Z, Zhang M, Kong L, Lv Y, Zou M et al. 2014. Genome-wide identification, phylogeny, duplication, and expression analyses of two-component system genes in Chinese cabbage (Brassica rapa ssp. pekinensis). DNA Res 21:379–96
    [Google Scholar]
  100. 100. 
    Lomin SN, Krivosheev DM, Steklov MY, Arkhipov DV, Osolodkin DI et al. 2015. Plant membrane assays with cytokinin receptors underpin the unique role of free cytokinin bases as biologically active ligands. J. Exp. Bot. 66:1851–63
    [Google Scholar]
  101. 101. 
    Lomin SN, Yonekura-Sakakibara K, Romanov GA, Sakakibara H. 2011. Ligand-binding properties and subcellular localization of maize cytokinin receptors. J. Exp. Bot. 62:5149–59
    [Google Scholar]
  102. 102. 
    Lymperopoulos P, Msanne J, Rabara R. 2018. Phytochrome and phytohormones: working in tandem for plant growth and development. Front. Plant Sci 9:1037
    [Google Scholar]
  103. 103. 
    Mähönen AP, Higuchi M, Törmäkangas K, Miyawaki K, Pischke MS et al. 2006. Cytokinins regulate a bidirectional phosphorelay network in Arabidopsis. Current Biol 16:1116–22
    [Google Scholar]
  104. 104. 
    Mani P, Guruprasad KN. 2015. Regulation of growth and development in phytochrome mutants of Arabidopsis thaliana by solar UV. Acta Physiol. Plant. 37:111
    [Google Scholar]
  105. 105. 
    Mathews S. 2006. Phytochrome-mediated development in land plants: red light sensing evolves to meet the challenges of changing light environments. Mol. Ecol. 15:3483–503
    [Google Scholar]
  106. 106. 
    Mayerhofer H, Panneerselvam S, Kaljunen H, Tuukkanen A, Mertens HD, Mueller-Dieckmann J. 2015. Structural model of the cytosolic domain of the plant ethylene receptor 1 (ETR1). J. Biol. Chem. 290:2644–58
    [Google Scholar]
  107. 107. 
    Milić D, Dick M, Mulnaes D, Pfleger C, Kinnen A et al. 2018. Recognition motif and mechanism of ripening inhibitory peptides in plant hormone receptor ETR1. Sci. Rep. 8:3890
    [Google Scholar]
  108. 108. 
    Mira-Rodado V. 2019. New insights into multistep-phosphorelay (MSP)/two-component system (TCS) regulation: Are plants and bacteria that different?. Plants 8:590
    [Google Scholar]
  109. 109. 
    Mira-Rodado V, Veerabagu M, Witthöft J, Teply J, Harter K, Desikan R. 2012. Identification of two-component system elements downstream of AHK5 in the stomatal closure response of Arabidopsis thaliana. Plant Signal. Behav 7:1467–76This study presents AHP1, AHP2, AHP5, ARR4, and ARR7 as AHK5 downstream partners.
    [Google Scholar]
  110. 110. 
    Miri M, Janakirama P, Huebert T, Ross L, McDowell T et al. 2019. Inside out: root cortex-localized LHK1 cytokinin receptor limits epidermal infection of Lotus japonicus roots by Mesorhizobium loti. New Phytol 222:1523–37
    [Google Scholar]
  111. 111. 
    Miyata K, Nakagawa T. 2016. The Lotus intrinsic ethylene receptor regulates both symbiotic and non-symbiotic responses. Plant Biotechnol 33:27–32
    [Google Scholar]
  112. 112. 
    Mizuno T. 2005. Two-component phosphorelay signal transduction systems in plants: from hormone responses to circadian rhythms. Biosci. Biotechnol. Biochem. 69:2263–76
    [Google Scholar]
  113. 113. 
    Mochida K, Yoshida T, Sakurai T, Yamaguchi-Shinozaki K, Shinozaki K, Tran L-SP. 2010. Genome-wide analysis of two-component systems and prediction of stress-responsive two-component system members in soybean. DNA Res 17:303–24
    [Google Scholar]
  114. 114. 
    Mougel C, Zhulin IB. 2001. CHASE: an extracellular sensing domain common to transmembrane receptors from prokaryotes, lower eukaryotes and plants. Trends Biochem. Sci. 26:582–84
    [Google Scholar]
  115. 115. 
    Moussatche P, Klee HJ. 2004. Autophosphorylation activity of the Arabidopsis ethylene receptor multigene family. J. Biol. Chem. 279:48734–41
    [Google Scholar]
  116. 116. 
    Müller-Dieckmann H-J, Grantz AA, Kim S-H. 1999. The structure of the signal receiver domain of the Arabidopsis thaliana ethylene receptor ETR1. Structure 7:1547–56
    [Google Scholar]
  117. 117. 
    Nguyen D, Rieu I, Mariani C, van Dam NM. 2016. How plants handle multiple stresses: hormonal interactions underlying responses to abiotic stress and insect herbivory. Plant Mol. Biol. 91:727–40
    [Google Scholar]
  118. 118. 
    Nitschke S, Cortleven A, Iven T, Feussner I, Havaux M et al. 2016. Circadian stress regimes affect the circadian clock and cause jasmonic acid-dependent cell death in cytokinin-deficient Arabidopsis plants. Plant Cell 28:1616–39
    [Google Scholar]
  119. 119. 
    Nongpiur R, Soni P, Karan R, Singla-Pareek SL, Pareek A 2012. Histidine kinases in plants: cross talk between hormone and stress responses. Plant Signal. Behav. 7:1230–37
    [Google Scholar]
  120. 120. 
    Ortiz-Castro R, Pelagio-Flores R, Méndez-Bravo A, Ruiz-Herrera LF, Campos-García J, López-Bucio J. 2014. Pyocyanin, a virulence factor produced by Pseudomonas aeruginosa, alters root development through reactive oxygen species and ethylene signaling in Arabidopsis. Mol. Plant Microbe Interact. 27:364–78
    [Google Scholar]
  121. 121. 
    Pareek A, Singh A, Kumar M, Kushwaha HR, Lynn AM, Singla-Pareek SL. 2006. Whole-genome analysis of Oryza sativa reveals similar architecture of two-component signaling machinery with Arabidopsis. Plant Physiol 142:380–97
    [Google Scholar]
  122. 122. 
    Pekárová B, Klumpler T, Třísková O, Horák J, Jansen S et al. 2011. Structure and binding specificity of the receiver domain of sensor histidine kinase CKI1 from Arabidopsis thaliana. Plant J 67:827–39
    [Google Scholar]
  123. 123. 
    Pham J, Desikan R. 2012. Modulation of ROS production and hormone levels by AHK5 during abiotic and biotic stress signaling. Plant Signal. Behav. 7:893–97
    [Google Scholar]
  124. 124. 
    Pham J, Liu J, Bennett MH, Mansfield JW, Desikan R. 2012. Arabidopsis histidine kinase 5 regulates salt sensitivity and resistance against bacterial and fungal infection. New Phytol 194:168–80
    [Google Scholar]
  125. 125. 
    Plett JM, Mathur J, Regan S 2009. Ethylene receptor ETR2 controls trichome branching by regulating microtubule assembly in Arabidopsis thaliana. J. Exp. Bot. 60:3923–33
    [Google Scholar]
  126. 126. 
    Qiu Y, Pasoreck EK, Reddy AK, Nagatani A, Ma W et al. 2017. Mechanism of early light signaling by the carboxy-terminal output module of Arabidopsis phytochrome B. Nat. Commun. 8:1905
    [Google Scholar]
  127. 127. 
    Riefler M, Novak O, Strnad M, Schmülling T. 2006. Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18:40–54
    [Google Scholar]
  128. 128. 
    Rockwell NC, Lagarias JC. 2020. Phytochrome evolution in 3D: deletion, duplication, and diversification. New Phytol 225:2283–300
    [Google Scholar]
  129. 129. 
    Romanov GA, Lomin SN, Schmülling T. 2018. Cytokinin signaling: from the ER or from the PM? That is the question!. New Phytol 218:41–53This article provides current understandings of the subcellular localization of cytokinin receptors.
    [Google Scholar]
  130. 130. 
    Rusaczonek A, Czarnocka W, Kacprzak S, Witoń D, Ślesak I et al. 2015. Role of phytochromes A and B in the regulation of cell death and acclimatory responses to UV stress in Arabidopsis thaliana. J. Exp. Bot. 66:6679–95
    [Google Scholar]
  131. 131. 
    Sakai H, Hua J, Chen QG, Chang C, Medrano LJ et al. 1998. ETR2 is an ETR1-like gene involved in ethylene signaling in Arabidopsis. PNAS 95:5812–17
    [Google Scholar]
  132. 132. 
    Sánchez-López ÁM, Baslam M, De Diego N, Muñoz FJ, Bahaji A et al. 2016. Volatile compounds emitted by diverse phytopathogenic microorganisms promote plant growth and flowering through cytokinin action. Plant Cell Environ 39:2592–608This work demonstrates the positive effects on plant development of volatile compounds from not only beneficial but also pathogenic microorganisms.
    [Google Scholar]
  133. 133. 
    Sardesai N, Lee L-Y, Chen H, Yi H, Olbricht GR et al. 2013. Cytokinins secreted by Agrobacterium promote transformation by repressing a plant myb transcription factor. Sci. Signal. 6:ra100
    [Google Scholar]
  134. 134. 
    Sasaki T, Suzaki T, Soyano T, Kojima M, Sakakibara H, Kawaguchi M. 2014. Shoot-derived cytokinins systemically regulate root nodulation. Nat. Commun. 5:4983
    [Google Scholar]
  135. 135. 
    Schäfer M, Meza-Canales ID, Brütting C, Baldwin IT, Meldau S. 2015. Cytokinin concentrations and CHASE-DOMAIN CONTAINING HIS KINASE 2 (NaCHK2)- and NaCHK3-mediated perception modulate herbivory-induced defense signaling and defenses in Nicotiana attenuata. New Phytol 207:645–58
    [Google Scholar]
  136. 136. 
    Schaller GE, Kieber JJ, Shiu S-H. 2008. Two-component signaling elements and histidyl-aspartyl phosphorelays. Arabidopsis Book 6:e0112This work summarizes the knowledge of the structural diversity of two-component system elements and their phosphorelay in Arabidopsis.
    [Google Scholar]
  137. 137. 
    Schaller GE, Ladd AN, Lanahan MB, Spanbauer JM, Bleecker AB. 1995. The ethylene response mediator ETR1 from Arabidopsis forms a disulfide-linked dimer. J. Biol. Chem. 270:12526–30
    [Google Scholar]
  138. 138. 
    Schott-Verdugo S, Müller L, Classen E, Gohlke H, Groth G. 2019. Structural model of the ETR1 ethylene receptor transmembrane sensor domain. Sci. Rep. 9:8869
    [Google Scholar]
  139. 139. 
    Sharrock RA, Quail PH. 1989. Novel phytochrome sequences in Arabidopsis thaliana: structure, evolution, and differential expression of a plant regulatory photoreceptor family. Gene Dev 3:1745–57
    [Google Scholar]
  140. 140. 
    Shin A-Y, Han Y-J, Baek A, Ahn T, Kim SY et al. 2016. Evidence that phytochrome functions as a protein kinase in plant light signalling. Nat. Commun. 7:11545
    [Google Scholar]
  141. 141. 
    Siddique S, Radakovic ZS, Carola M, Chronis D, Novák O et al. 2015. A parasitic nematode releases cytokinin that controls cell division and orchestrates feeding site formation in host plants. PNAS 112:12669–74
    [Google Scholar]
  142. 142. 
    Singh A, Kushwaha HR, Soni P, Gupta H, Singla-Pareek SL, Pareek A 2015. Tissue specific and abiotic stress regulated transcription of histidine kinases in plants is also influenced by diurnal rhythm. Front. Plant Sci 6:711
    [Google Scholar]
  143. 143. 
    Singh G, Kumar R. 2012. Genome-wide in silico analysis of plant two component signaling system in woody model plant Populus trichocarpa. Res. Plant Biol. 2:13–22
    [Google Scholar]
  144. 144. 
    Spallek T, Melnyk CW, Wakatake T, Zhang J, Sakamoto Y et al. 2017. Interspecies hormonal control of host root morphology by parasitic plants. PNAS 114:5283–88
    [Google Scholar]
  145. 145. 
    Spíchal L, Rakova NY, Riefler M, Mizuno T, Romanov GA et al. 2004. Two cytokinin receptors of Arabidopsis thaliana, CRE1/AHK4 and AHK3, differ in their ligand specificity in a bacterial assay. Plant Cell Physiol 45:1299–305
    [Google Scholar]
  146. 146. 
    Suzuki I, Cretin C, Omata T, Sugiyama T. 1994. Transcriptional and posttranscriptional regulation of nitrogen-responding expression of phosphoenolpyruvate carboxylase gene in maize. Plant Physiol 105:1223–29
    [Google Scholar]
  147. 147. 
    Sweere U, Eichenberg K, Lohrmann J, Mira-Rodado V, Bäurle I et al. 2001. Interaction of the response regulator ARR4 with phytochrome B in modulating red light signaling. Science 294:1108–11
    [Google Scholar]
  148. 148. 
    Takano M, Inagaki N, Xie X, Yuzurihara N, Hihara F et al. 2005. Distinct and cooperative functions of phytochromes A, B, and C in the control of deetiolation and flowering in rice. Plant Cell 17:3311–25
    [Google Scholar]
  149. 149. 
    Toledo-Ortiz G, Johansson H, Lee KP, Bou-Torrent J, Stewart K et al. 2014. The HY5-PIF regulatory module coordinates light and temperature control of photosynthetic gene transcription. PLOS Genet 10:e1004416
    [Google Scholar]
  150. 150. 
    Tran L-SP, Urao T, Qin F, Maruyama K, Kakimoto T et al. 2007. Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. PNAS 104:20623–28
    [Google Scholar]
  151. 151. 
    Ueguchi C, Koizumi H, Suzuki T, Mizuno T. 2001. Novel family of sensor histidine kinase genes in Arabidopsis thaliana. Plant Cell Physiol 42:231–35
    [Google Scholar]
  152. 152. 
    Urao T, Miyata S, Yamaguchi-Shinozaki K, Shinozaki K. 2000. Possible His to Asp phosphorelay signaling in an Arabidopsis two-component system. FEBS Lett 478:227–32
    [Google Scholar]
  153. 153. 
    Urao T, Yakubov B, Satoh R, Yamaguchi-Shinozaki K, Seki M et al. 1999. A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell 11:1743–54
    [Google Scholar]
  154. 154. 
    Velez-Ramirez AI, Vreugdenhil D, Millenaar FF, van Ieperen W. 2019. Phytochrome A protects tomato plants from injuries induced by continuous light. Front. Plant Sci. 10:19
    [Google Scholar]
  155. 155. 
    Viczián A, Ádám É, Staudt AM, Lambert D, Klement E et al. 2020. Differential phosphorylation of the N-terminal extension regulates phytochrome B signaling. New Phytol 225:1635–50
    [Google Scholar]
  156. 156. 
    Voitsekhovskaja OV. 2019. Phytochromes and other (photo) receptors of information in plants. Russ. J. Plant Physiol. 66:351–64
    [Google Scholar]
  157. 157. 
    Wang F, Guo Z, Li H, Wang M, Onac E et al. 2016. Phytochrome A and B function antagonistically to regulate cold tolerance via abscisic acid-dependent jasmonate signaling. Plant Physiol 170:459–71
    [Google Scholar]
  158. 158. 
    Wang F, Wang L, Qiao L, Chen J, Pappa MB et al. 2017. Arabidopsis CPR5 regulates ethylene signaling via molecular association with the ETR1 receptor. J. Integr. Plant Biol. 59:810–24
    [Google Scholar]
  159. 159. 
    Wang Y, Zhang X, Cui Y, Li L, Wang D et al. 2019. AHK3-mediated cytokinin signaling is required for the delayed leaf senescence induced by SSPP. Int. J. Mol. Sci. 20:2043
    [Google Scholar]
  160. 160. 
    Wen F, Qin T, Wang Y, Dong W, Zhang A et al. 2015. OsHK3 is a crucial regulator of abscisic acid signaling involved in antioxidant defense in rice. J. Integr. Plant Biol. 57:213–28
    [Google Scholar]
  161. 161. 
    Wohlbach DJ, Quirino BF, Sussman MR. 2008. Analysis of the Arabidopsis histidine kinase ATHK1 reveals a connection between vegetative osmotic stress sensing and seed maturation. Plant Cell 20:1101–17
    [Google Scholar]
  162. 162. 
    Wuriyanghan H, Zhang B, Cao W-H, Ma B, Lei G et al. 2009. The ethylene receptor ETR2 delays floral transition and affects starch accumulation in rice. Plant Cell 21:1473–94
    [Google Scholar]
  163. 163. 
    Yamada H, Suzuki T, Terada K, Takei K, Ishikawa K et al. 2001. The Arabidopsis AHK4 histidine kinase is a cytokinin-binding receptor that transduces cytokinin signals across the membrane. Plant Cell Physiol 42:1017–23
    [Google Scholar]
  164. 164. 
    Yang T, Lv R, Li J, Lin H, Xi D. 2018. Phytochrome A and B negatively regulate salt stress tolerance of Nicotiana tabacum via ABA–jasmonic acid synergistic cross-talk. Plant Cell Physiol 59:2381–93
    [Google Scholar]
  165. 165. 
    Yang Y-X, Wang M-M, Yin Y-L, Onac E, Zhou G-F et al. 2015. RNA-seq analysis reveals the role of red light in resistance against Pseudomonas syringae pv. tomato DC3000 in tomato plants. BMC Genom 16:120
    [Google Scholar]
  166. 166. 
    Yuan L, Liu Z, Song X, Johnson C, Yu X, Sundaresan V 2016. The CKI1 histidine kinase specifies the female gametic precursor of the endosperm. Dev. Cell 37:34–46
    [Google Scholar]
  167. 167. 
    Zdarska M, Cuyacot AR, Tarr PT, Yamoune A, Szmitkowska A et al. 2019. ETR1 integrates response to ethylene and cytokinins into a single multistep phosphorelay pathway to control root growth. Mol. Plant 12:1338–52This study examines the noncanonical pathway in ethylene signaling.
    [Google Scholar]
  168. 168. 
    Zhao H, Duan K-X, Ma B, Yin C-C, Hu Y et al. 2020. Histidine kinase MHZ1/OsHK1 interacts with ethylene receptors to regulate root growth in rice. Nat. Commun. 11:518
    [Google Scholar]
  169. 169. 
    Zürcher E, Liu J, di Donato M, Geisler M, Müller B 2016. Plant development regulated by cytokinin sinks. Science 353:1027–30
    [Google Scholar]
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