Signal Integration in Plant Abiotic Stress Responses via Multistep Phosphorelay Signaling
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články, přehledy
PubMed
33679861
PubMed Central
PMC7925916
DOI
10.3389/fpls.2021.644823
Knihovny.cz E-zdroje
- Klíčová slova
- Arabidopsis, abiotic stress, abscisic acid, cytokinin, ethylene, light signaling, multistep phosphorelay (MSP), temperature,
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
Plants growing in any particular geographical location are exposed to variable and diverse environmental conditions throughout their lifespan. The multifactorial environmental pressure resulted into evolution of plant adaptation and survival strategies requiring ability to integrate multiple signals that combine to yield specific responses. These adaptive responses enable plants to maintain their growth and development while acquiring tolerance to a variety of environmental conditions. An essential signaling cascade that incorporates a wide range of exogenous as well as endogenous stimuli is multistep phosphorelay (MSP). MSP mediates the signaling of essential plant hormones that balance growth, development, and environmental adaptation. Nevertheless, the mechanisms by which specific signals are recognized by a commonly-occurring pathway are not yet clearly understood. Here we summarize our knowledge on the latest model of multistep phosphorelay signaling in plants and the molecular mechanisms underlying the integration of multiple inputs including both hormonal (cytokinins, ethylene and abscisic acid) and environmental (light and temperature) signals into a common pathway. We provide an overview of abiotic stress responses mediated via MSP signaling that are both hormone-dependent and independent. We highlight the mutual interactions of key players such as sensor kinases of various substrate specificities including their downstream targets. These constitute a tightly interconnected signaling network, enabling timely adaptation by the plant to an ever-changing environment. Finally, we propose possible future directions in stress-oriented research on MSP signaling and highlight its potential importance for targeted crop breeding.
Zobrazit více v PubMed
Abuelsoud W., Cortleven A., Schmülling T. (2020). Photoperiod stress induces an oxidative burst-like response and is associated with increased apoplastic peroxidase and decreased catalase activities. J. Plant Physiol. 253 153252. 10.1016/j.jplph.2020.153252 PubMed DOI
Ahuja I., de Vos R. C. H., Bones A. M., Hall R. D. (2010). Plant molecular stress responses face climate change. Trends Plant Sci. 15 664–674. 10.1016/j.tplants.2010.08.002 PubMed DOI
Alabadí D., Blázquez M. A. (2008). Integration of light and hormone signals. Plant Signal. Behav. 3 448–449. 10.4161/psb.3.7.5558 PubMed DOI PMC
Allan A. C., Fricker M. D., Ward J. L., Beale M. H., Trewavas A. J. (1994). Two transduction pathways mediate rapid effects of abscisic acid in commelina guard cells. Plant Cell 6 1319–1328. 10.2307/3869829 PubMed DOI PMC
An F., Zhao Q., Ji Y., Li W., Jiang Z., Yu X., et al. (2010). Ethylene-induced stabilization of ETHYLENE INSENSITIVE3 and EIN3-LIKE1 is mediated by proteasomal degradation of EIN3 binding F-box 1 and 2 that requires EIN2 in arabidopsis. Plant Cell 22 2384–2401. 10.1105/tpc.110.076588 PubMed DOI PMC
Antoniadi I., Novák O., Gelová Z., Johnson A., Plíhal O., Simerský R., et al. (2020). Cell-surface receptors enable perception of extracellular cytokinins. Nat. Commun. 11:4284. 10.1038/s41467-020-17700-9 PubMed DOI PMC
Anzalone A. V., Randolph P. B., Davis J. R., Sousa A. A., Koblan L. W., Levy J. M., et al. (2019). Search-and-replace genome editing without double-strand breaks or donor DNA. Nature 576 149–157. 10.1038/s41586-019-1711-4 PubMed DOI PMC
Argueso C. T., Ferreira F. J., Kieber J. J. (2009). Environmental perception avenues: the interaction of cytokinin and environmental response pathways. Plant Cell Environ. 32 1147–1160. 10.1111/j.1365-3040.2009.01940.x PubMed DOI
Baena-González E., Rolland F., Thevelein J. M., Sheen J. (2007). A central integrator of transcription networks in plant stress and energy signalling. Nature 448 938–942. 10.1038/nature06069 PubMed DOI
Baena-González E., Sheen J. (2008). Convergent energy and stress signaling. Trends Plant Sci. 13 474–482. 10.1016/j.tplants.2008.06.006 PubMed DOI PMC
Bakshi A., Piy S., Fernandez J. C., Chervin C., Hewezi T., Binder B. M. (2018). Pethylene receptors signal via a noncanonical pathway to regulate abscisic acid responses. Plant Physiol. 176 910–929. 10.1104/pp.17.01321 PubMed DOI PMC
Bakshi A., Wilson R. L., Lacey R. F., Kim H., Wuppalapati S. K., Binder B. M. (2015). Identification of regions in the receiver domain of the ETHYLENE RESPONSE1 ethylene receptor of arabidopsis important for functional divergence. Plant Physiol. 169 219–232. 10.1104/pp.15.00626 PubMed DOI PMC
Balestrasse K. B., Zilli C. G., Tomaro M. L. (2008). Signal transduction pathways and haem oxygenase induction in soybean leaves subjected to salt stress. Redox Rep. 13 255–262. 10.1179/135100008X308966 PubMed DOI
Ballaré C. L., Pierik R. (2017). The shade-avoidance syndrome: multiple signals and ecological consequences. Plant Cell Environ. 40 2530–2543. 10.1111/pce.12914 PubMed DOI
Belda-Palazón B., Adamo M., Valerio C., Ferreira L. J., Confraria A., Reis-Barata D., et al. (2020). A dual function of SnRK2 kinases in the regulation of SnRK1 and plant growth. Nat. Plants 6 1345–1353. 10.1038/s41477-020-00778-w PubMed DOI
Belin C., De Franco P. O., Bourbousse C., Chaignepain S., Schmitter J. M., Vavasseur A., et al. (2006). Identification of features regulating OST1 kinase activity and OST1 function in guard cells. Plant Physiol. 141 1316–1327. 10.1104/pp.106.079327 PubMed DOI PMC
Bhargava A., Clabaugh I., To J. P., Maxwell B. B., Chiang Y. H., Schaller G. E., et al. (2013). Identification of cytokinin-responsive genes using microarray meta-analysis and RNA-seq in Arabidopsis. Plant Physiol. 162 272–294. 10.1104/pp.113.217026 PubMed DOI PMC
Binder B. M. (2020). Ethylene signaling in plants. J. Biol. Chem. 295 7710–7725. 10.1074/jbc.REV120.010854 PubMed DOI PMC
Binder B. M., Rodríguez F. I., Bleecker A. B. (2010). The copper transporter RAN1 is essential for biogenesis of ethylene receptors in Arabidopsis. J. Biol. Chem. 285 37263–37270. 10.1074/jbc.M110.170027 PubMed DOI PMC
Binder B. M., Walker J. M., Gagne J. M., Emborg T. J., Hemmann G., Bleecker A. B., et al. (2007). The Arabidopsis EIN3 binding F-box proteins EBF1 and EBF2 have distinct but overlapping roles in ethylene signaling. Plant Cell 19 509–523. 10.1105/tpc.106.048140 PubMed DOI PMC
Blatt M. R., Grabov A. (1997). Signal redundancy, gates and integration in the control of ion channels for stomatal movement. J. Exp. Bot. 48 529–537. 10.1093/jxb/48.special_issue.529 PubMed DOI
Boccalandro H. E., Mazza C. A., Mazzella M. A., Casal J. J., Ballaré C. L. (2001). Ultraviolet B radiation enhances a phytochrome-B-mediated photomorphogenic response in Arabidopsis. Plant Physiol. 126 780–788. 10.1104/pp.126.2.780 PubMed DOI PMC
Boudsocq M., Droillard M. J., Barbier-Brygoo H., Laurière C. (2007). Different phosphorylation mechanisms are involved in the activation of sucrose non-fermenting 1 related protein kinases 2 by osmotic stresses and abscisic acid. Plant Mol. Biol. 63 491–503. 10.1007/s11103-006-9103-1 PubMed DOI
Brenner W. G., Ramireddy E., Heyl A., Schmülling T. (2012). Gene regulation by cytokinin in Arabidopsis. Front. Plant Sci. 3:8. 10.3389/fpls.2012.00008 PubMed DOI PMC
Brenner W. G., Romanov G. A., Köllmer I., Bürkle L., Schmülling T. (2005). Immediate-early and delayed cytokinin response genes of Arabidopsis thaliana identified by genome-wide expression profiling reveal novel cytokinin-sensitive processes and suggest cytokinin action through transcriptional cascades. Plant J. 44 314–333. 10.1111/j.1365-313X.2005.02530.x PubMed DOI
Brenner W. G., Schmülling T. (2015). Summarizing and exploring data of a decade of cytokinin-related transcriptomics. Front. Plant Sci. 6:29. 10.3389/fpls.2015.00029 PubMed DOI PMC
Caesar K., Thamm A. M. K., Witthöft J., Elgass K., Huppenberger P., Grefen C., et al. (2011). Evidence for the localization of the Arabidopsis cytokinin receptors AHK3 and AHK4 in the endoplasmic reticulum. J. Exp. Bot. 62 5571–5580. 10.1093/jxb/err238 PubMed DOI PMC
Casal J. J., Candia A. N., Sellaro R. (2014). Light perception and signalling by phytochrome A. J. Exp. Bot. 65 2835–2845. 10.1093/jxb/ert379 PubMed DOI
Castillo M. C., Lozano-Juste J., González-Guzmán M., Rodriguez L., Rodriguez P. L., León J. (2015). Inactivation of PYR/PYL/RCAR ABA receptors by tyrosine nitration may enable rapid inhibition of ABA signaling by nitric oxide in plants. Sci. Signal. 8:ra89. 10.1126/scisignal.aaa7981 PubMed DOI
Černý M., Jedelský P. L., Novák J., Schlosser A., Brzobohatý B. (2014). Cytokinin modulates proteomic, transcriptomic and growth responses to temperature shocks in Arabidopsis. Plant Cell Environ. 37 1641–1655. 10.1111/pce.12270 PubMed DOI
Chang J., Li X., Fu W., Wang J., Yong Y., Shi H., et al. (2019). Asymmetric distribution of cytokinins determines root hydrotropism in Arabidopsis thaliana. Cell Res. 29 984–993. 10.1038/s41422-019-0239-3 PubMed DOI PMC
Cheng M.-C., Liao P.-M., Kuo W.-W., Lin T.-P. (2013). The Arabidopsis ETHYLENE RESPONSE FACTOR1 regulates abiotic stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant Physiol. 162 1566–1582. 10.1104/pp.113.221911 PubMed DOI PMC
Chinnusamy V., Zhu J. K. (2009). Epigenetic regulation of stress responses in plants. Curr. Opin. Plant Biol. 12 133–139. 10.1016/j.pbi.2008.12.006 PubMed DOI PMC
Cho Y. H., Yoo S. D. (2007). ETHYLENE RESPONSE 1 histidine kinase activity of arabidopsis promotes plant growth. Plant Physiol. 143 612–616. 10.1104/pp.106.091504 PubMed DOI PMC
Chung B. Y. W., Balcerowicz M., Di Antonio M., Jaeger K. E., Geng F., Franaszek K., et al. (2020). An RNA thermoswitch regulates daytime growth in Arabidopsis. Nat. Plants 6 522–532. 10.1038/s41477-020-0633-3 PubMed DOI PMC
Claeys H., Inzé D. (2013). The agony of choice: how plants balance growth and survival under water-limiting conditions. Plant Physiol. 162 1768–1779. 10.1104/pp.113.220921 PubMed DOI PMC
Clark K. L., Larsen P. B., Wang X., Chang C. (1998). Association of the Arabidopsis CTR1 Raf-like kinase with the ETR1 and ERS ethylene receptors. Proc. Natl. Acad. Sci. U.S.A. 95 5401–5406. 10.1073/pnas.95.9.5401 PubMed DOI PMC
Cortleven A., Nitschke S., Klaumünzer M., AbdElgawad H., Asard H., Grimm B., 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 1470–1483. 10.1104/pp.113.224667 PubMed DOI PMC
Cortleven A., Schmülling T. (2015). Regulation of chloroplast development and function by cytokinin. J. Exp. Bot. 66 4999–5013. 10.1093/jxb/erv132 PubMed DOI
Cotton J. L. S., Ross C. W., Byrne D. H., Colbert J. T. (1990). Down-regulation of phytochrome mRNA abundance by red light and benzyladenine in etiolated cucumber cotyledons. Plant Mol. Biol. 14 707–714. 10.1007/BF00016503 PubMed DOI
Crosatti C., De Laureto P. P., Bassi R., Cattivelli L. (1999). The interaction between cold and light controls the expression of the cold-regulated barley gene cor14b and the accumulation of the corresponding protein. Plant Physiol. 119 671–680. 10.1104/pp.119.2.671 PubMed DOI PMC
D’Amico-Damião V., Cruz F. J. R., Gavassi M. A., Santos D. M. M., Melo H. C., Carvalho R. F. (2015). Photomorphogenic modulation of water stress in tomato (Solanum lycopersicum L.): the role of phytochromes A, B1, and B2. J. Hortic. Sci. Biotechnol. 90 25–30. 10.1080/14620316.2015.11513149 DOI
Dautel R., Wu X. N., Heunemann M., Schulze W. X., Harter K. (2016). The sensor histidine kinases AHK2 and AHK3 proceed into multiple serine/threonine/tyrosine phosphorylation pathways in Arabidopsis thaliana. Mol. Plant 9 182–186. 10.1016/j.molp.2015.10.002 PubMed DOI
De Wit M., Galvão V. C., Fankhauser C. (2016). Light-mediated hormonal regulation of plant growth and development. Annu. Rev. Plant Biol. 67 513–537. 10.1146/annurev-arplant-043015-112252 PubMed DOI
Dejonghe W., Okamoto M., Cutler S. R. (2018). Small molecule probes of ABA biosynthesis and signaling. Plant Cell Physiol. 59 1490–1499. 10.1093/pcp/pcy126 PubMed DOI
Deng Y., Dong H., Mu J., Ren B., Zheng B., Ji Z., et al. (2010). Arabidopsis histidine kinase CKI1 acts upstream of histidine phosphotransfer proteins to regulate female gametophyte development and vegetative growth. Plant Cell 22 1232–1248. 10.1105/tpc.108.065128 PubMed DOI PMC
Desikan R., Horák J., Chaban C., Mira-Rodado V., Witthöft J., Elgass K., et al. (2008). The histidine kinase AHK5 integrates endogenous and environmental signals in Arabidopsis guard cells. PLoS One 3:e2491. 10.1371/journal.pone.0002491 PubMed DOI PMC
Desikan R., Last K., Harrett-Williams R., Tagliavia C., Harter K., Hooley R., et al. (2006). Ethylene-induced stomatal closure in Arabidopsis occurs via AtrbohF-mediated hydrogen peroxide synthesis. Plant J. 47 907–916. 10.1111/j.1365-313X.2006.02842.x PubMed DOI
Dobisova T., Hrdinova V., Cuesta C., Michlickova S., Urbankova I., Hejatkova R., et al. (2017). Light controls cytokinin signaling via transcriptional regulation of constitutively active sensor histidine kinase CKI1. Plant Physiol. 174 387–404. 10.1104/pp.16.01964 PubMed DOI PMC
Dobrá J., Černý M., Štorchová H., Dobrev P., Skalák J., Jedelský P. L., et al. (2015). The impact of heat stress targeting on the hormonal and transcriptomic response in Arabidopsis. Plant Sci. 231 52–61. 10.1016/j.plantsci.2014.11.005 PubMed DOI
Dobra J., Motyka V., Dobrev P., Malbeck J., Prasil I. T., Haisel D., et al. (2010). Comparison of hormonal responses to heat, drought and combined stress in tobacco plants with elevated proline content. J. Plant Physiol. 167 1360–1370. 10.1016/j.jplph.2010.05.013 PubMed DOI
Dong P., Xiong F., Que Y., Wang K., Yu L., Li Z., et al. (2015). Expression profiling and functional analysis reveals that TOR is a key player in regulating photosynthesis and phytohormone signaling pathways in Arabidopsis. Front. Plant Sci. 6:677. 10.3389/fpls.2015.00677 PubMed DOI PMC
Dubois M., Van den Broeck L., Inzé D. (2018). The pivotal role of ethylene in plant growth. Trends Plant Sci. 23 311–323. 10.1016/j.tplants.2018.01.003 PubMed DOI PMC
Eichmann R., Schäfer P. (2015). Growth versus immunity-a redirection of the cell cycle? Curr. Opin. Plant Biol. 26 106–112. 10.1016/j.pbi.2015.06.006 PubMed DOI
Etheridge N., Hall B. P., Schaller G. E. (2006). Progress report: ethylene signaling and responses. Planta 223 387–391. 10.1007/s00425-005-0163-2 PubMed DOI
Fankhauser C. (2002). Light perception in plants: cytokinins and red light join forces to keep phytochrome B active. Trends Plant Sci. 7 143–145. 10.1016/S1360-1385(02)02228-8 PubMed DOI
Feng J., Wang C., Chen Q., Chen H., Ren B., Li X., et al. (2013). S-nitrosylation of phosphotransfer proteins represses cytokinin signaling. Nat. Commun. 4:1529. 10.1038/ncomms2541 PubMed DOI
Filipe O., De Vleesschauwer D., Haeck A., Demeestere K., Höfte M. (2018). The energy sensor OsSnRK1a confers broad-spectrum disease resistance in rice. Sci. Rep. 8:3864. 10.1038/s41598-018-22101-6 PubMed DOI PMC
Fujii H., Zhu J.-K. (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 8380–8385. 10.1073/pnas.0903144106 PubMed DOI PMC
Fujita Y., Nakashima K., Yoshida T., Katagiri T., Kidokoro S., Kanamori N., et al. (2009). Three SnRK2 protein kinases are the main positive regulators of abscisic acid signaling in response to water stress in Arabidopsis. Plant Cell Physiol. 50 2123–2132. 10.1093/pcp/pcp147 PubMed DOI
Fujita Y., Yoshida T., Yamaguchi-Shinozaki K. (2013). Pivotal role of the AREB/ABF-SnRK2 pathway in ABRE-mediated transcription in response to osmotic stress in plants. Physiol. Plant 147 15–27. 10.1111/j.1399-3054.2012.01635.x PubMed DOI
Gagne J. M., Smalle J., Gingerich D. J., Walker J. M., Yoo S. D., Yanagisawa S., et al. (2004). Arabidopsis EIN3-binding F-box 1 and 2 form ubiquitin-protein ligases that repress ethylene action and promote growth by directing EIN3 degradation. Proc. Natl. Acad. Sci. U.S.A. 101 6803–6808. 10.1073/pnas.0401698101 PubMed DOI PMC
Gangappa S. N., Botto J. F. (2016). The multifaceted roles of HY5 in plant growth and development. Mol. Plant 9 1353–1365. 10.1016/j.molp.2016.07.002 PubMed DOI
González C. V., Ibarra S. E., Piccoli P. N., Botto J. F., Boccalandro H. E. (2012). Phytochrome B increases drought tolerance by enhancing ABA sensitivity in Arabidopsis thaliana. Plant Cell Environ. 35 1958–1968. 10.1111/j.1365-3040.2012.02529.x PubMed DOI
Grefen C., Städele K., Růžiěka K., Obrdlik P., Harter K., Horák J. (2008). Subcellular localization and in vivo interactions of the Arabidopsis thaliana ethylene receptor family members. Mol. Plant 1 308–320. 10.1093/mp/ssm015 PubMed DOI
Guo H., Ecker J. R. (2003). Plant responses to ethylene gas are mediated by SCF(EBF1/EBF2)-dependent proteolysis of EIN3 transcription factor. Cell 115 667–677. 10.1016/s0092-8674(03)00969-3 PubMed DOI
Guo Y., Gan S. (2011). AtMYB2 regulates whole plant senescence by inhibiting cytokinin-mediated branching at late stages of development in Arabidopsis. Plant Physiol. 156 1612–1619. 10.1104/pp.111.177022 PubMed DOI PMC
Gupta S., Rashotte A. M. (2014). Expression patterns and regulation of SlCRF3 and SlCRF5 in response to cytokinin and abiotic stresses in tomato (Solanum lycopersicum). J. Plant Physiol. 171 349–358. 10.1016/j.jplph.2013.09.003 PubMed DOI
Hai N. N., Chuong N. N., Tu N. H. C., Kisiala A., Hoang X. L. T., Thao N. P. (2020). Role and regulation of cytokinins in plant response to drought stress. Plants 9:422. 10.3390/plants9040422 PubMed DOI PMC
Han S. K., Wagner D. (2014). Role of chromatin in water stress responses in plants. J. Exp. Bot. 65 2785–2799. 10.1093/jxb/ert403 PubMed DOI PMC
Han S. K., Wu M. F., Cui S., Wagner D. (2015). Roles and activities of chromatin remodeling ATPases in plants. Plant J. 83 62–77. 10.1111/tpj.12877 PubMed DOI
Hass C., Lohrmann J., Albrecht V., Sweere U., Hummel F., Yoo S. D., et al. (2004). The response regulator 2 mediates ethylene signalling and hormone signal integration in Arabidopsis. Embo J. 23 3290–3302. 10.1038/sj.emboj.7600337 PubMed DOI PMC
Hejátko J., Pernisová M., Eneva T., Palme K., Brzobohatý B. (2003). The putative sensor histidine kinase CKI1 is involved in female gametophyte development in Arabidopsis. Mol. Genet. Genomics 269 443–453. 10.1007/s00438-003-0858-7 PubMed DOI
Hejátko J., Ryu H., Kim G. T., Dobešová R., Choi S., Choi S. M., et al. (2009). The Histidine kinases cytokinin-independent1 and arabidopsis histidine kinase2 and 3 regulate vascular tissue development in arabidopsis shoots. Plant Cell 21 2008–2021. 10.1105/tpc.109.066696 PubMed DOI PMC
Hirayama T., Kieber J. J., Hirayama N., Kogan M., Guzman P., Nourizadeh S., et al. (1999). RESPONSIVE-TO-ANTAGONIST1, a Menkes/Wilson disease-related copper transporter, is required for ethylene signaling in Arabidopsis. Cell 97 383–393. 10.1016/S0092-8674(00)80747-3 PubMed DOI
Horak J., Janda L., Pekarova B., Hejatko J. (2011). Molecular mechanisms of signalling specificity via phosphorelay pathways in Arabidopsis. Curr. Protein Pept. Sci. 12 126–136. 10.2174/1389211213488452037 PubMed DOI
Hothorn M., Dabi T., Chory J. (2011). Structural basis for cytokinin recognition by Arabidopsis thaliana histidine kinase 4. Nat. Chem. Biol. 7 766–768. 10.1038/nchembio.667 PubMed DOI PMC
Huang X., Hou L., Meng J., You H., Li Z., Gong Z., et al. (2018). The antagonistic action of abscisic acid and cytokinin signaling mediates drought stress response in Arabidopsis. Mol. Plant 11 970–982. 10.1016/j.molp.2018.05.001 PubMed DOI
Huang X., Ouyang X., Deng X. W. (2014). Beyond repression of photomorphogenesis: role switching of COP/DET/FUS in light signaling. Curr. Opin. Plant Biol. 21 96–103. 10.1016/j.pbi.2014.07.003 PubMed DOI
Huang X., Zhang X., Gong Z., Yang S., Shi Y. (2017). ABI4 represses the expression of type-A ARRs to inhibit seed germination in Arabidopsis. Plant J. 89 354–365. 10.1111/tpj.13389 PubMed DOI
Huang Y., Li H., Hutchison C. E., Laskey J., Kieber J. J. (2003). Biochemical and functional analysis of CTR1, a protein kinase that negatively regulates ethylene signaling in Arabidopsis. Plant J. 33 221–233. 10.1046/j.1365-313X.2003.01620.x PubMed DOI
Hutchison C. E., Kieber J. J. (2002). Cytokinin signaling in Arabidopsis. Plant Cell 14 S47–S59. 10.1105/tpc.010444 PubMed DOI PMC
Hutchison C. E., Li J., Argueso C., Gonzalez M., Lee E., Lewis M. W., et al. (2006). The Arabidopsis histidine phosphotransfer proteins are redundant positive regulators of cytokinin signaling. Plant Cell 18 3073–3087. 10.1105/tpc.106.045674 PubMed DOI PMC
Hwang I., Sheen J. (2001). Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413 383–389. 10.1038/35096500 PubMed DOI
Inzé A., Vanderauwera S., Hoeberichts F. A., Vandorpe M., van Gaever T., van Breusegem F. (2012). A subcellular localization compendium of hydrogen peroxide-induced proteins. Plant Cell Environ. 35 308–320. 10.1111/j.1365-3040.2011.02323.x PubMed DOI
Iwama A., Yamashino T., Tanaka Y., Sakakibara H., Kakimoto T., Sato S., 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. 48 375–380. 10.1093/pcp/pcl065 PubMed DOI
Jamsheer M. K., Jindal S., Laxmi A. (2019). Evolution of TOR–SnRK dynamics in green plants and its integration with phytohormone signaling networks. J. Exp. Bot. 70 2239–2259. 10.1093/jxb/erz107 PubMed DOI
Jeon J., Cho C., Lee M. R., Van Binh N., Kim J. (2016). CYTOKININ RESPONSE FACTOR2 (CRF2) and CRF3 regulate lateral root development in response to cold stress in Arabidopsis. Plant Cell 28 1828–1843. 10.1105/tpc.15.00909 PubMed DOI PMC
Jeon J., Kim J. (2013). Arabidopsis response regulator1 and arabidopsis histidine phosphotransfer protein2 (AHP2), AHP3, and AHP5 function in cold signaling. Plant Physiol. 161 408–424. 10.1104/pp.112.207621 PubMed DOI PMC
Jeon J., Kim N. Y., Kim S., Kang N. Y., Novák O., Ku S. J., et al. (2010). A subset of cytokinin two-component signaling system plays a role in cold temperature stress response in Arabidopsis. J. Biol. Chem. 285 23371–23386. 10.1074/jbc.M109.096644 PubMed DOI PMC
Jiang B., Shi Y., Peng Y., Jia Y., Yan Y., Dong X., et al. (2020). Cold-Induced CBF–PIF3 interaction enhances freezing tolerance by stabilizing the phyB thermosensor in Arabidopsis. Mol. Plant 13 894–906. 10.1016/j.molp.2020.04.006 PubMed DOI
Jinek M., Chylinski K., Fonfara I., Hauer M., Doudna J. A., Charpentier E. (2012). A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337 816–821. 10.1126/science.1225829 PubMed DOI PMC
Johnová P., Skalák J., Saiz-Fernández I., Brzobohatý B. (2016). Plant responses to ambient temperature fluctuations and water-limiting conditions: a proteome-wide perspective. Biochim. Biophys. Acta Proteins Proteomics 1864 916–931. 10.1016/j.bbapap.2016.02.007 PubMed DOI
Ju C., Yoon G. M., Shemansky J. M., Lin D. Y., Ying Z. I., Chang J., et al. (2012). CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from the ER membrane to the nucleus in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 109 19486–19491. 10.1073/pnas.1214848109 PubMed DOI PMC
Jung J. H., Domijan M., Klose C., Biswas S., Ezer D., Gao M., et al. (2016). Phytochromes function as thermosensors in Arabidopsis. Science 354 886–889. 10.1126/science.aaf6005 PubMed DOI
Kakimoto T. (1996). CKI1, a histidine kinase homolog implicated in cytokinin signal transduction. Science 274 982–985. 10.1126/science.274.5289.982 PubMed DOI
Kang N. Y., Cho C., Kim N. Y., Kim J. (2012). Cytokinin receptor-dependent and receptor-independent pathways in the dehydration response of Arabidopsis thaliana. J. Plant Physiol. 169 1382–1391. 10.1016/j.jplph.2012.05.007 PubMed DOI
Kaplan F., Kopka J., Haskell D. W., Zhao W., Schiller K. C., Gatzke N., et al. (2004). Exploring the temperature-stress metabolome. Plant Physiol. 136 4159–4168. 10.1104/pp.104.052142.1 PubMed DOI PMC
Katsuta S., Masuda G., Bak H., Shinozawa A., Kamiyama Y., Umezawa T., et al. (2020). Arabidopsis Raf-like kinases act as positive regulators of subclass III SnRK2 in osmostress signaling. Plant J. 103 634–644. 10.1111/tpj.14756 PubMed DOI PMC
Kidokoro S., Maruyama K., Nakashima K., Imura Y., Narusaka Y., Shinwari Z. K., et al. (2009). The phytochrome-interacting factor PIF7 negatively regulates dreb1 expression under circadian control in Arabidopsis. Plant Physiol. 151 2046–2057. 10.1104/pp.109.147033 PubMed DOI PMC
Kieber J. J., Rothenberg M., Roman G., Feldmann K. A., Ecker J. R. (1993). CTR1, a negative regulator of the ethylene response pathway in arabidopsis, encodes a member of the Raf family of protein kinases. Cell 72 427–441. 10.1016/0092-8674(93)90119-B PubMed DOI
Kieber J. J., Schaller G. E. (2018). Cytokinin signaling in plant development. Development 145:dev149344. 10.1242/dev.149344 PubMed DOI
Kim G. D., Cho Y. H., Yoo S. D. (2017). Regulatory functions of cellular energy sensor SNF1-Related Kinase1 for leaf senescence delay through ETHYLENE- INSENSITIVE3 repression. Sci. Rep. 7:3193. 10.1038/s41598-017-03506-1 PubMed DOI PMC
Kosová K., Prášil I. T., Vítámvás P., Dobrev P., Motyka V., Floková K., et al. (2012). Complex phytohormone responses during the cold acclimation of two wheat cultivars differing in cold tolerance, winter Samanta and spring Sandra. J. Plant Physiol. 169 567–576. 10.1016/j.jplph.2011.12.013 PubMed DOI
Kubiasová K., Montesinos J. C., Šamajová O., Nisler J., Mik V., Semerádová H., et al. (2020). Cytokinin fluoroprobe reveals multiple sites of cytokinin perception at plasma membrane and endoplasmic reticulum. Nat. Commun. 11:4285. 10.1038/s41467-020-17949-0 PubMed DOI PMC
Kumar M., Kesawat M. S., Ali A., Lee S. C., Gill S. S., Kim H. U. (2019). Integration of abscisic acid signaling with other signaling pathways in plant stress responses and development. Plants 8:592. 10.3390/plants8120592 PubMed DOI PMC
Kumar M. N., Jane W. N., Verslues P. E. (2013). Role of the putative osmosensor Arabidopsis histidine kinase1 in dehydration avoidance and low-water-potential response. Plant Physiol. 161 942–953. PubMed PMC
Kumar M. N., Verslues P. E. (2015). Stress physiology functions of the Arabidopsis histidine kinase cytokinin receptors. Physiol. Plant 154 369–380. 10.1111/ppl.12290 PubMed DOI
Larkindale J., Mishkind M., Vierling E. (2007). “Plant responses to high temperature,” in Plant Abiotic Stress, eds Muhammed A., Aksel R., von Borstel R. C. (Boston, MA: Springer; ).
Lee C.-M., Thomashow M. F. (2012). Photoperiodic regulation of the C-repeat binding factor (CBF) cold acclimation pathway and freezing tolerance in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 109 15054–15059. 10.1073/pnas.1211295109 PubMed DOI PMC
Legris M., Klose C., Burgie E. S., Rojas C. C., Neme M., Hiltbrunner A., et al. (2016). Phytochrome B integrates light and temperature signals in Arabidopsis. Science 354 897–900. 10.1126/science.aaf5656 PubMed DOI
Li J., Li G., Wang H., Wang Deng X. (2011). Phytochrome signaling mechanisms. Arab. B. 9 e0148. 10.1199/tab.0148 PubMed DOI PMC
Li W., Herrera-Estrella L., Tran L.-S. P. (2016). The Yin–Yang of cytokinin homeostasis and drought acclimation/adaptation. Trends Plant Sci. 21 548–550. 10.1016/j.tplants.2016.05.006 PubMed DOI
Li W., Ma M., Feng Y., Li H., Wang Y., Ma Y., et al. (2015). EIN2-directed translational regulation of ethylene signaling in Arabidopsis. Cell 163 670–683. 10.1016/j.cell.2015.09.037 PubMed DOI
Lin Z., Li Y., Zhang Z., Liu X., Hsu C. C., Du Y., et al. (2020). A RAF-SnRK2 kinase cascade mediates early osmotic stress signaling in higher plants. Nat. Commun. 11:613. 10.1038/s41467-020-14477-9 PubMed DOI PMC
Liu J., Zhang F., Zhou J., Chen F., Wang B., Xie X. (2012). Phytochrome B control of total leaf area and stomatal density affects drought tolerance in rice. Plant Mol. Biol. 78 289–300. 10.1007/s11103-011-9860-3 PubMed DOI
Liu Z., Yuan L., Song X., Yu X., Sundaresan V. (2017). AHP2, AHP3, and AHP5 act downstream of CKI1 in Arabidopsis female gametophyte development. J. Exp. Bot. 68 3365–3373. 10.1093/jxb/erx181 PubMed DOI PMC
Lozano-Juste J., Alrefaei A. F., Rodriguez P. L. (2020). Plant osmotic stress signaling: MAPKKKs Meet SnRK2s. Trends Plant Sci. 25 1179–1182. 10.1016/j.tplants.2020.09.003 PubMed DOI
Lozano-Juste J., León J. (2010a). Enhanced abscisic acid-mediated responses in nia1nia2noa1-2 triple mutant impaired in NIA/NR- and AtNOA1-dependent nitric oxide biosynthesis in Arabidopsis. Plant Physiol. 152 891–903. 10.1104/pp.109.148023 PubMed DOI PMC
Lozano-Juste J., León J. (2010b). Nitric oxide modulates sensitivity to ABA. Plant Signal. Behav. 5 314–316. 10.4161/psb.5.3.11235 PubMed DOI PMC
Lu X. D., Zhou C. M., Xu P. B., Luo Q., Lian H. L., Yang H. Q. (2015). Red-light-dependent interaction of phyB with SPA1 promotes COP1-SPA1 dissociation and photomorphogenic development in Arabidopsis. Mol. Plant 8 467–478. 10.1016/j.molp.2014.11.025 PubMed DOI
Ma Y., Szostkiewicz I., Korte A., Moes D., Yang Y., Christmann A., et al. (2009). Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324 1064–1068. 10.1126/science.1172408 PubMed DOI
Macková H., Hronková M., Dobrá J., Turečková V., Novák O., Lubovská Z., et al. (2013). Enhanced drought and heat stress tolerance of tobacco plants with ectopically enhanced cytokinin oxidase/dehydrogenase gene expression. J. Exp. Bot. 64 2805–2815. 10.1093/jxb/ert131 PubMed DOI PMC
Marchadier E., Hetherington A. M. (2014). Involvement of two-component signalling systems in the regulation of stomatal aperture by light in Arabidopsis thaliana. New Phytol. 203 462–468. 10.1111/nph.12813 PubMed DOI
Maruyama K., Urano K., Yoshiwara K., Morishita Y., Sakurai N., Suzuki H., et al. (2014). Integrated analysis of the effects of cold and dehydration on rice metabolites, phytohormones, and gene transcripts. Plant Physiol. 164 1759–1771. 10.1104/pp.113.231720 PubMed DOI PMC
Mason M. G., Jha D., Salt D. E., Tester M., Hill K., Kieber J. J., et al. (2010). Type-B response regulators ARR1 and ARR12 regulate expression of AtHKT1;1 and accumulation of sodium in Arabidopsis shoots. Plant J. 64 753–763. 10.1111/j.1365-313X.2010.04366.x PubMed DOI
McAinsh M. R., Hetherington A. M. (1998). Encoding specificity in Ca2+ signalling systems. Trends Plant Sci. 3 32–36. 10.1016/S1360-1385(97)01150-3 DOI
Merchante C., Brumos J., Yun J., Hu Q., Spencer K. R., Enríquez P., et al. (2015). Gene-specific translation regulation mediated by the hormone-signaling molecule EIN2. Cell 163 684–697. 10.1016/j.cell.2015.09.036 PubMed DOI
Mira-Rodado V., Sweere U., Grefen C., Kunkel T., Fejes E., Nagy F., et al. (2007). Functional cross-talk between two-component and phytochrome B signal transduction in Arabidopsis. J. Exp. Bot. 58 2595–2607. 10.1093/jxb/erm087 PubMed DOI
Mittler R., Finka A., Goloubinoff P. (2012). How do plants feel the heat? Trends Biochem. Sci. 37 118–125. 10.1016/j.tibs.2011.11.007 PubMed DOI
Miura K., Furumoto T. (2013). Cold signaling and cold response in plants. Int. J. Mol. Sci. 14 5312–5337. 10.3390/ijms14035312 PubMed DOI PMC
Müller B., Sheen J. (2007). Arabidopsis cytokinin signaling pathway. Sci. STKE 2007:cm5. 10.1126/stke.4072007cm5 PubMed DOI
Müller M., Munné-Bosch S. (2015). Ethylene response factors: a key regulatory hub in hormone and stress signaling. Plant Physiol. 169 32–41. 10.1104/pp.15.00677 PubMed DOI PMC
Nakashima K., Fujita Y., Kanamori N., Katagiri T., Umezawa T., Kidokoro S., et al. (2009). Three arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant Cell Physiol. 50 1345–1363. 10.1093/pcp/pcp083 PubMed DOI
Nakashima K., Yamaguchi-Shinozaki K. (2013). ABA signaling in stress-response and seed development. Plant Cell Rep. 32 959–970. 10.1007/s00299-013-1418-1 PubMed DOI
Ng L. M., Melcher K., Teh B. T., Xu H. E. (2014). Abscisic acid perception and signaling: structural mechanisms and applications. Acta Pharmacol. Sin. 35 567–584. 10.1038/aps.2014.5 PubMed DOI PMC
Nguyen K. H., Ha C., Van, Nishiyama R., Watanabe Y., Leyva-González M. A., et al. (2016). Arabidopsis type B cytokinin response regulators ARR1, ARR10, and ARR12 negatively regulate plant responses to drought. Proc. Natl. Acad. Sci. U.S.A. 113 3090–3095. 10.1073/pnas.1600399113 PubMed DOI PMC
Nishiyama R., Watanabe Y., Fujita Y., Le D. T., Kojima M., Werner T., et al. (2011). Analysis of cytokinin mutants and regulation of cytokinin metabolic genes reveals important regulatory roles of cytokinins in drought, salt and abscisic acid responses, and abscisic acid biosynthesis. Plant Cell 23 2169–2183. 10.1105/tpc.111.087395 PubMed DOI PMC
Nitschke S., Cortleven A., Iven T., Feussner I., Havaux M., Riefler 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 1616–1639. 10.1105/tpc.16.00016 PubMed DOI PMC
Nitschke S., Cortleven A., Schmülling T. (2017). Novel stress in plants by altering the photoperiod. Trends Plant Sci. 22 913–916. 10.1016/j.tplants.2017.09.005 PubMed DOI
Njimona I., Yang R., Lamparter T. (2014). Temperature effects on bacterial phytochrome. PLoS One 9:e109794. 10.1371/journal.pone.0109794 PubMed DOI PMC
Nukarinen E., Ngele T., Pedrotti L., Wurzinger B., Mair A., Landgraf R., et al. (2016). Quantitative phosphoproteomics reveals the role of the AMPK plant ortholog SnRK1 as a metabolic master regulator under energy deprivation. Sci. Rep. 6:31697. 10.1038/srep31697 PubMed DOI PMC
O’Brien J. A., Benková E. (2013). Cytokinin cross-talking during biotic and abiotic stress responses. Front. Plant Sci. 4:451. 10.3389/fpls.2013.00451 PubMed DOI PMC
Park S.-Y., Fung P., Nishimura N., Jensen D. R., Fujii H., Zhao Y., et al. (2009). Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science 324 1068–1071. 10.1126/science.1173041 PubMed DOI PMC
Peirats-Llobet M., Han S. K., Gonzalez-Guzman M., Jeong C. W., Rodriguez L., Belda-Palazon B., et al. (2016). A direct link between abscisic acid sensing and the chromatin-remodeling ATPase BRAHMA via Core ABA signaling pathway components. Mol. Plant 9 136–147. 10.1016/j.molp.2015.10.003 PubMed DOI
Pham J., Desikan R. (2012). Modulation of ROS production and hormone levels by AHK5 during abiotic and biotic stress signaling. Plant Signal. Behav. 7 893–897. 10.4161/psb.20692 PubMed DOI PMC
Pham J., Liu J., Bennett M. H., Mansfield J. W., Desikan R. (2012). Arabidopsis histidine kinase 5 regulates salt sensitivity and resistance against bacterial and fungal infection. New Phytol. 194 168–180. 10.1111/j.1469-8137.2011.04033.x PubMed DOI
Pischke M. S., Jones L. G., Otsuga D., Fernandez D. E., Drews G. N., Sussman M. R. (2002). An Arabidopsis histidine kinase is essential for megagametogenesis. Proc. Natl. Acad. Sci. U.S.A. 99 15800–15805. 10.1073/pnas.232580499 PubMed DOI PMC
Potter K. C., Wang J., Schaller G. E., Kieber J. J. (2018). Cytokinin modulates context-dependent chromatin accessibility through the type-B response regulators. Nat. Plants 4 1102–1111. 10.1038/s41477-018-0290-y PubMed DOI
Potuschak T., Lechner E., Parmentier Y., Yanagisawa S., Grava S., Koncz C., et al. (2003). EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F box proteins: EBF1 and EBF2. Cell 115 679–689. 10.1016/S0092-8674(03)00968-1 PubMed DOI
Qiao H., Chang K. N., Yazaki J., Ecker J. R. (2009). Interplay between ethylene, ETP1/ETP2 F-box proteins, and degradation of EIN2 triggers ethylene responses in Arabidopsis. Genes Dev. 23 512–521. 10.1101/gad.1765709 PubMed DOI PMC
Qiao H., Shen Z., Huang S. S. C., Schmitz R. J., Urich M. A., Briggs S. P., et al. (2012). Processing and subcellular trafficking of ER-tethered EIN2 control response to ethylene gas. Science 338 390–393. 10.1126/science.1225974 PubMed DOI PMC
Quail P. H., Boylan M. T., Parks B. M., Short T. W., Xu Y., Wagner D. (1995). Phytochromes: photosensory perception and signal transduction. Science 268 675–680. 10.1126/science.7732376 PubMed DOI
Radchuk R., Radchuk V., Weschke W., Borisjuk L., Weber H. (2006). Repressing the expression of the SUCROSE NONFERMENTING-1-RELATED PROTEIN KINASE gene in pea embryo causes pleiotropic defects of maturation similar to an abscisic acid-insensitive phenotype. Plant Physiol. 140 263–278. 10.1104/pp.105.071167 PubMed DOI PMC
Raines T., Blakley I. C., Tsai Y. C., Worthen J. M., Franco-Zorrilla J. M., Solano R., et al. (2016). Characterization of the cytokinin-responsive transcriptome in rice. BMC Plant Biol. 16:260. 10.1186/s12870-016-0932-z PubMed DOI PMC
Rashotte A. M., Mason M. G., Hutchison C. E., Ferreira F. J., Schaller G. E., Kieber J. J. (2006). A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a two-component pathway. Proc. Natl. Acad. Sci. U.S.A. 103 11081–11085. 10.1073/pnas.0602038103 PubMed DOI PMC
Rockwell N. C., Su Y. S., Lagarias J. C. (2006). Phytochrome structure and signaling mechanisms. Annu. Rev. Plant Biol. 57 837–858. 10.1146/annurev.arplant.56.032604.144208 PubMed DOI PMC
Rodríguez-Gacio Mdel C., Matilla-Vázquez M. A., Matilla A. J. (2009). Seed dormancy and ABA signaling: the breakthrough goes on. Plant Signal. Behav. 4 1035–1049. 10.4161/psb.4.11.9902 PubMed DOI PMC
Roeber V. M., Bajaj I., Rohde M., Schmülling T., Cortleven A. (2020). Light acts as a stressor and influences abiotic and biotic stress responses in plants. Plant. Cell Environ. 1–20. 10.1111/pce.13948 PubMed DOI
Rusaczonek A., Czarnocka W., Kacprzak S., Witoń D., Ślesak I., Szechyńska-Hebda M., 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. 6679–6695. 10.1093/jxb/erv375 PubMed DOI PMC
Sah S. K., Reddy K. R., Li J. (2016). Abscisic acid and abiotic stress tolerance in crop plants. Front. Plant Sci. 7:571. 10.3389/fpls.2016.00571 PubMed DOI PMC
Salomé P. A., To J. P. C., Kieber J. J., McClung C. R. (2006). Arabidopsis response regulators ARR3 and ARR4 play cytokinin-independent roles in the control of circadian period. Plant Cell 18 55–69. 10.1105/tpc.105.037994 PubMed DOI PMC
Sami F., Faizan M., Faraz A., Siddiqui H., Yusuf M., Hayat S. (2018). Nitric oxide-mediated integrative alterations in plant metabolism to confer abiotic stress tolerance, NO crosstalk with phytohormones and NO-mediated post translational modifications in modulating diverse plant stress. Nitric Oxide Biol. Chem. 73 22–38. 10.1016/j.niox.2017.12.005 PubMed DOI
Samsonová Z., Kiran N. S., Novák O., Spyroglou I., Skalák J., Hejátko J., et al. (2020). Steady-state levels of cytokinins and their derivatives may serve as a unique classifier of arabidopsis ecotypes. Plants 9:116. 10.3390/plants9010116 PubMed DOI PMC
Schaller G. E., Bleecker A. B. (1995). Ethylene-binding sites generated in yeast expressing the Arabidopsis ETR1 gene. Science 270 1809–1811. 10.1126/science.270.5243.1809 PubMed DOI
Scharein B., Voet-van-Vormizeele J., Harter K., Groth G. (2008). Ethylene signaling: identification of a putative ETR1-AHP1 phosphorelay complex by fluorescence spectroscopy. Anal. Biochem. 377 72–76. 10.1016/j.ab.2008.03.015 PubMed DOI
Schepetilnikov M., Ryabova L. A. (2018). Recent discoveries on the role of tor (Target of rapamycin) signaling in translation in plants. Plant Physiol. 176 1095–1105. 10.1104/pp.17.01243 PubMed DOI PMC
Sharp R. E., Lenoble M. E. (2002). ABA, ethylene and the control of shoot and root growth under water stress. J. Exp. Bot. 53 33–37. 10.1093/jxb/53.366.33 PubMed DOI
Sheerin D. J., Menon C., zur Oven-Krockhaus S., Enderle B., Zhu L., Johnen P., et al. (2015). Light-activated Phytochrome A and B interact with members of the SPA family to promote photomorphogenesis in Arabidopsis by reorganizing the COP1/SPA complex. Plant Cell 27 189–201. 10.1105/tpc.114.134775 PubMed DOI PMC
Shi X., Gupta S., Rashotte A. M. (2014). Characterization of two tomato AP2/ERF genes, SlCRF1 and SlCRF2 in hormone and stress responses. Plant Cell Rep. 33 35–45. 10.1007/s00299-013-1510-6 PubMed DOI
Shi Y., Tian S., Hou L., Huang X., Zhang X., Guo H., et al. (2012). Ethylene signaling negatively regulates freezing tolerance by repressing expression of and Type-A genes in Arabidopsis. Plant Cell 24 2578–2595. 10.1105/tpc.112.098640 PubMed DOI PMC
Shin D. H., Choi M., Kim K., Bang G., Cho M., Choi S.-B., et al. (2013). HY5 regulates anthocyanin biosynthesis by inducing the transcriptional activation of the MYB75/PAP1 transcription factor in Arabidopsis. FEBS Lett. 587 1543–1547. 10.1016/j.febslet.2013.03.037 PubMed DOI
Shin J., Park E., Choi G. (2007). PIF3 regulates anthocyanin biosynthesis in an HY5-dependent manner with both factors directly binding anthocyanin biosynthetic gene promoters in Arabidopsis. Plant J. 49 981–994. 10.1111/j.1365-313X.2006.03021.x PubMed DOI
Siegel R. S., Xue S., Murata Y., Yang Y., Nishimura N., Wang A., et al. (2009). Calcium elevation-dependent and attenuated resting calcium-dependent abscisic acid induction of stomatal closure and abscisic acid-induced enhancement of calcium sensitivities of S-type anion and inward-rectifying K+ channels in Arabidopsis guard cells. Plant J. 59 207–220. 10.1111/j.1365-313X.2009.03872.x PubMed DOI PMC
Skalák J., Černý M., Jedelský P., Dobrá J., Ge E., Novák J., et al. (2016). Stimulation of ipt overexpression as a tool for elucidation of the role of cytokinins in high temperature responses of Arabidopsis thaliana. J. Exp. Bot. 67 2861–2873. 10.1093/jxb/erw129 PubMed DOI PMC
Skirycz A., Claeys H., De Bodt S., Oikawa A., Shinoda S., Andriankaja M., et al. (2011). Pause-and-stop: the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest. Plant Cell 23 1876–1888. 10.1105/tpc.111.084160 PubMed DOI PMC
Soma F., Takahashi F., Suzuki T., Shinozaki K., Yamaguchi-Shinozaki K. (2020). Plant Raf-like kinases regulate the mRNA population upstream of ABA-unresponsive SnRK2 kinases under drought stress. Nat. Commun. 11:1373. 10.1038/s41467-020-15239-3 PubMed DOI PMC
Soto-Burgos J., Bassham D. C. (2017). SnRK1 activates autophagy via the TOR signaling pathway in Arabidopsis thaliana. PLoS One 12:e0182591. 10.1371/journal.pone.0182591 PubMed DOI PMC
Srivastava A. K., Senapati D., Srivastava A. K., Chakraborty M., Gangappa S. N., Chattopadhyay S. (2015). SHW1 interacts with HY5 and COP1, and promotes COP1-mediated degradation of HY5 during Arabidopsis seedling development. Plant Physiol. 169 2922–2934. 10.1104/pp.15.01184 PubMed DOI PMC
Stavang J. A., Gallego-Bartolomé J., Gómez M. D., Yoshida S., Asami T., Olsen J. E., et al. (2009). Hormonal regulation of temperature-induced growth in Arabidopsis. Plant J. 60 589–601. 10.1111/j.1365-313X.2009.03983.x PubMed DOI
Street I. H., Aman S., Zubo Y., Ramzan A., Wang X., Shakeel S. N., et al. (2015). Ethylene inhibits cell proliferation of the Arabidopsis root meristem. Plant Physiol. 169 338–350. 10.1104/pp.15.00415 PubMed DOI PMC
Sung D. Y., Kaplan F., Lee K. J., Guy C. L. (2003). Acquired tolerance to temperature extremes. Trends Plant Sci. 8 179–187. 10.1016/S1360-1385(03)00047-5 PubMed DOI
Sweere U., Eichenberg K., Lohrmann J., Mira-Rodado V., Bäurle I., Kudla J., et al. (2001). Interaction of the response regulator ARR4 with phytochrome B in modulating red light signaling. Science 294 1108–1111. 10.1126/science.1065022 PubMed DOI
Takatsuka H., Umeda M. (2019). ABA inhibits root cell elongation through repressing the cytokinin signaling. Plant Signal. Behav. 14:e1578632. 10.1080/15592324.2019.1578632 PubMed DOI PMC
Terry M. J., Linley P. J., Kohchi T. (2002). Making light of it: the role of plant haem oxygenases in phytochrome chromophore synthesis. Biochem. Soc. Trans. 30 604–609. 10.1042/bst0300604 PubMed DOI
Todaka D., Zhao Y., Yoshida T., Kudo M., Kidokoro S., Mizoi J., et al. (2017). Temporal and spatial changes in gene expression, metabolite accumulation and phytohormone content in rice seedlings grown under drought stress conditions. Plant J. 90 61–78. 10.1111/tpj.13468 PubMed DOI
Tran L. S. P., Shinozaki K., Yamaguchi-Shinozaki K. (2010). Role of cytokinin responsive two-component system in ABA and osmotic stress signalings. Plant Signal. Behav. 5 148–150. 10.4161/psb.5.2.10411 PubMed DOI PMC
Tran L.-S. P., Urao T., Qin F., Maruyama K., Kakimoto T., Shinozaki K., et al. (2007). 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. U.S.A. 104 20623–20628. 10.1073/pnas.0706547105 PubMed DOI PMC
Tun N. N., Livaja M., Kieber J. J., Scherer G. F. E. (2008). Zeatin-induced nitric oxide (NO) biosynthesis in Arabidopsis thaliana mutants of NO biosynthesis and of two-component signaling genes. New Phytol. 178 515–531. 10.1111/j.1469-8137.2008.02383.x PubMed DOI
Urao T., Miyata S., Yamaguchi-Shinozaki K., Shinozaki K. (2000). Possible his to Asp phosphorelay signaling in an Arabidopsis two- component system. FEBS Lett. 478 227–232. 10.1016/S0014-5793(00)01860-3 PubMed DOI
Urao T., Yakubov B., Satoh R., Yamaguchi-Shinozaki K., Seki M., Hirayama T., et al. (1999). A transmembrane hybrid-type histidine kinase in Arabidopsis functions as an osmosensor. Plant Cell 11 1743–1754. 10.1105/tpc.11.9.1743 PubMed DOI PMC
Vandenbussche F., Habricot Y., Condiff A. S., Maldiney R., Van Der Straeten D., Ahmad M. (2007). HY5 is a point of convergence between cryptochrome and cytokinin signalling pathways in Arabidopsis thaliana. Plant J. 49 428–441. 10.1111/j.1365-313X.2006.02973.x PubMed DOI
Vishwakarma K., Upadhyay N., Kumar N., Yadav G., Singh J., Mishra R. K., et al. (2017). Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front. Plant Sci. 8:161. 10.3389/fpls.2017.00161 PubMed DOI PMC
Waidyarathne P., Samarasinghe S. (2018). Boolean calcium signalling model predicts calcium role in acceleration and stability of abscisic acid-mediated stomatal closure. Sci. Rep. 8:17635. 10.1038/s41598-018-35872-9 PubMed DOI PMC
Wang F., Guo Z., Li H., Wang M., Onac E., Zhou J., et al. (2016). Phytochrome A and B function antagonistically to regulate cold tolerance via abscisic acid-dependent jasmonate signaling. Plant Physiol. 170 459–471. 10.1104/pp.15.01171 PubMed DOI PMC
Wang H. (2015). Phytochrome signaling: time to tighten up the loose ends. Mol. Plant 8 540–551. 10.1016/j.molp.2014.11.021 PubMed DOI
Wang P., Zhao Y., Li Z., Hsu C. C., Liu X., Fu L., et al. (2018). Reciprocal regulation of the TOR Kinase and ABA receptor balances plant growth and stress response. Mol. Cell 69 100.e10–112.e10. 10.1016/j.molcel.2017.12.002 PubMed DOI PMC
Wang Q., Liu Q., Wang X., Zuo Z., Oka Y., Lin C. (2018). New insights into the mechanisms of phytochrome–cryptochrome coaction. New Phytol. 217 547–551. 10.1111/nph.14886 PubMed DOI PMC
Wang Y., Li L., Ye T., Zhao S., Liu Z., Feng Y. Q., et al. (2011). Cytokinin antagonizes ABA suppression to seed germination of Arabidopsis by downregulating ABI5 expression. Plant J. 68 249–261. 10.1111/j.1365-313X.2011.04683.x PubMed DOI
Webb A. A. R., Larman M. G., Montgomery L. T., Taylor J. E., Hetherington A. M. (2001). The role of calcium in ABA-induced gene expression and stomatal movements. Plant J. 26 351–362. 10.1046/j.1365-313X.2001.01032.x PubMed DOI
Wen X., Zhang C., Ji Y., Zhao Q., He W., An F., et al. (2012). Activation of ethylene signaling is mediated by nuclear translocation of the cleaved EIN2 carboxyl terminus. Cell Res. 22 1613–1616. 10.1038/cr.2012.145 PubMed DOI PMC
Wilson R. L., Bakshi A., Binder B. M. (2014a). Loss of the ETR1 ethylene receptor reduces the inhibitory effect of far-red light and darkness on seed germination of Arabidopsis thaliana. Front. Plant Sci. 5:433. 10.3389/fpls.2014.00433 PubMed DOI PMC
Wilson R. L., Kim H., Bakshi A., Binder B. M. (2014b). The ethylene receptors ethylene response1 and ethylene response2 have contrasting roles in seed germination of arabidopsis during salt stress. Plant Physiol. 165 1353–1366. 10.1104/pp.114.241695 PubMed DOI PMC
Wright S. T. C. (1977). The relationship between leaf water potential ψleaf and the levels of abscisic acid and ethylene in excised wheat leaves. Planta 134 183–189. 10.1007/BF00384969 PubMed DOI
Wulfetange K., Lomin S. N., Romanov G. A., Stolz A., Heyl A., Schmülling T. (2011). The cytokinin receptors of arabidopsis are located mainly to the endoplasmic reticulum. Plant Physiol. 156 1808–1818. 10.1104/pp.111.180539 PubMed DOI PMC
Xiong L., Schumaker K. S., Zhu J.-K. (2002). Cell signaling during cold, drought, and salt stress. Plant Cell 14 S165–S183. 10.1105/tpc.000596 PubMed DOI PMC
Xu X., Paik I., Zhu L., Huq E. (2015). Illuminating progress in phytochrome-mediated light signaling pathways. Trends Plant Sci. 20 641–650. 10.1016/j.tplants.2015.06.010 PubMed DOI
Yaish M. W., Colasanti J., Rothstein S. J. (2011). The role of epigenetic processes in controlling flowering time in plants exposed to stress. J. Exp. Bot. 62 3727–3735. 10.1093/jxb/err177 PubMed DOI
Yamada H., Suzuki T., Terada K., Takei K., Ishikawa K., Miwa 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 1017–1023. 10.1093/pcp/pce127 PubMed DOI
Yu F., Wu Y., Xie Q. (2016). Ubiquitin-proteasome system in ABA signaling: from perception to action. Mol. Plant 9 21–33. 10.1016/j.molp.2015.09.015 PubMed DOI
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. 10.1016/j.devcel.2016.03.009 PubMed DOI
Zdarska M., Cuyacot A. R., Tarr P. T., Yamoune A., Szmitkowska A., Hrdinová V., et al. (2019). ETR1 integrates response to ethylene and cytokinins into a single multistep phosphorelay pathway to control root growth. Mol. Plant 12 1338–1352. 10.1016/j.molp.2019.05.012 PubMed DOI PMC
Zdarska M., Dobisová T., Gelová Z., Pernisová M., Dabravolski S., Hejátko J. (2015). Illuminating light, cytokinin, and ethylene signalling crosstalk in plant development. J. Exp. Bot. 66 4913–4931. 10.1093/jxb/erv261 PubMed DOI
Zhang F., Wang L., Qi B., Zhao B., Ko E. E., Riggan N. D., et al. (2017). EIN2 mediates direct regulation of histone acetylation in the ethylene response. Proc. Natl. Acad. Sci. U.S.A. 114 10274–10279. 10.1073/pnas.1707937114 PubMed DOI PMC
Zhao H., Duan K.-X., Ma B., Yin C.-C., Hu Y., Tao J.-J., et al. (2020). Histidine kinase MHZ1/OsHK1 interacts with ethylene receptors to regulate root growth in rice. Nat. Commun. 11:518. 10.1038/s41467-020-14313-0 PubMed DOI PMC
Zhao X. C., Schaller G. E. (2004). Effect of salt and osmotic stress upon expression of the ethylene receptor ETR1 in Arabidopsis thaliana. FEBS Lett. 562 189–192. 10.1016/S0014-5793(04)00238-8 PubMed DOI
Zhong S., Zhao M., Shi T., Shi H., An F., Zhao Q., et al. (2009). EIN3/EIL1 cooperate with PIF1 to prevent photo-oxidation and to promote greening of Arabidopsis seedlings. Proc. Natl. Acad. Sci. U.S.A. 106 21431–21436. 10.1073/pnas.0907670106 PubMed DOI PMC
Zhou W., Lozano-Torres J. L., Blilou I., Zhang X., Zhai Q., Smant G., et al. (2019). A jasmonate signaling network activates root stem cells and promotes regeneration. Cell 177 942.e14–956.e14. 10.1016/j.cell.2019.03.006 PubMed DOI
Zhu L., Bu Q., Xu X., Paik I., Huang X., Hoecker U., et al. (2015). CUL4 forms an E3 ligase with COP1 and SPA to promote light-induced degradation of PIF1. Nat. Commun. 6:7245. 10.1038/ncomms8245 PubMed DOI
Źróbek-Sokolnik A. (2012). Temperature stress and responses of plants, eds Ahmad P., Prasad M. N. V. (Berlin: Springer; ).
Zubo Y. O., Blakley I. C., Yamburenko M. V., Worthen J. M., Street I. H., Franco-Zorrilla J. M., et al. (2017). Cytokinin induces genome-wide binding of the type-B response regulator ARR10 to regulate growth and development in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 114 E5995–E6004. 10.1073/pnas.1620749114 PubMed DOI PMC
Zürcher E., Müller B. (2016). Cytokinin synthesis, signaling, and function-advances and new insights. Int. Rev. Cell Mol. Biol. 324 1–38. 10.1016/bs.ircmb.2016.01.001 PubMed DOI
Zwack P. J., De Clercq I., Howton T. C., Hallmark H. T., Hurny A., Keshishian E. A., et al. (2016). Cytokinin response factor 6 represses cytokinin-associated genes during oxidative stress. Plant Physiol. 172 1249–1258. 10.1104/pp.16.00415 PubMed DOI PMC
Zwack P. J., Rashotte A. M. (2015). Interactions between cytokinin signalling and abiotic stress responses. J. Exp. Bot. 66 4863–4871. 10.1093/jxb/erv172 PubMed DOI
Zwack P. J., Robinson B. R., Risley M. G., Rashotte A. M. (2013). Cytokinin response factor 6 negatively regulates leaf senescence and is induced in response to cytokinin and numerous abiotic stresses. Plant Cell Physiol. 54 971–981. 10.1093/pcp/pct049 PubMed DOI
Cytokinins regulate spatially specific ethylene production to control root growth in Arabidopsis
Epigenetics and plant hormone dynamics: a functional and methodological perspective
Small signaling peptides mediate plant adaptions to abiotic environmental stress