Cytokinin and Ethylene Cell Signaling Pathways from Prokaryotes to Eukaryotes
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem, Research Support, U.S. Gov't, Non-P.H.S., přehledy
PubMed
33238457
PubMed Central
PMC7700396
DOI
10.3390/cells9112526
PII: cells9112526
Knihovny.cz E-zdroje
- Klíčová slova
- cell signaling, cytokinins, ethylene, histidine kinases, receptors,
- MeSH
- cytokininy metabolismus MeSH
- ethyleny metabolismus MeSH
- Eukaryota metabolismus MeSH
- lidé MeSH
- prokaryotické buňky metabolismus MeSH
- signální transdukce fyziologie MeSH
- Check Tag
- lidé MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
- Research Support, U.S. Gov't, Non-P.H.S. MeSH
- Názvy látek
- cytokininy MeSH
- ethylene MeSH Prohlížeč
- ethyleny MeSH
Cytokinins (CKs) and ethylene (ET) are among the most ancient organic chemicals on Earth. A wide range of organisms including plants, algae, fungi, amoebae, and bacteria use these substances as signaling molecules to regulate cellular processes. Because of their ancestral origin and ubiquitous occurrence, CKs and ET are also considered to be ideal molecules for inter-kingdom communication. Their signal transduction pathways were first historically deciphered in plants and are related to the two-component systems, using histidine kinases as primary sensors. Paradoxically, although CKs and ET serve as signaling molecules in different kingdoms, it has been supposed for a long time that the canonical CK and ET signaling pathways are restricted to terrestrial plants. These considerations have now been called into question following the identification over recent years of genes encoding CK and ET receptor homologs in many other lineages within the tree of life. These advances shed new light on the dissemination and evolution of these hormones as both intra- and inter-specific communication molecules in prokaryotic and eukaryotic organisms.
Biochemistry and Cellular and Molecular Biology University of Tennessee Knoxville TN 37996 USA
Biomolécules et Biotechnologies Végétales BBV EA2106 Université de Tours F 37200 Tours France
LBLGC University of Orléans EA1207 INRA USC1328 F 45000 Orléans France
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Kieber J.J., Schaller G.E. Cytokinins. Arab. Book. 2014;12:e0168. doi: 10.1199/tab.0168. PubMed DOI PMC
Abeles F., Morgan P., Saltveit M.J. Ethylene in Plant Biology. 2nd ed. Academic Press; San Diego, CA, USA: 1992.
Rashotte A.M. The evolution of cytokinin signaling and its role in development before Angiosperms. Semin. Cell Dev. Biol. 2020;29 doi: 10.1016/j.semcdb.2020.06.010. PubMed DOI
Binder B.M. Ethylene signaling in plants. J. Biol. Chem. 2020;295:7710–7725. doi: 10.1074/jbc.REV120.010854. PubMed DOI PMC
Schaller G.E., Shiu S.-H., Armitage J.P. Two-Component Systems and Their Co-Option for Eukaryotic Signal Transduction. Curr. Biol. 2011;21:R320–R330. doi: 10.1016/j.cub.2011.02.045. PubMed DOI
Papon N., Stock A.M. Two-component systems. Curr. Biol. 2019;29:R724–R725. doi: 10.1016/j.cub.2019.06.010. PubMed DOI
Inoue T., Higuchi M., Hashimoto Y., Seki M., Kobayashi M., Kato T., Tabata S., Shinozaki K., Kakimoto T. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nat. Cell Biol. 2001;409:1060–1063. doi: 10.1038/35059117. PubMed DOI
Chang C., Kwok S.F., Bleecker A.B., Meyerowitz E.M. Arabidopsis ethylene-response gene ETR1: Similarity of product to two-component regulators. Science. 1993;262:539–544. doi: 10.1126/science.8211181. PubMed DOI
Anantharaman V., Aravind L. The CHASE domain: A predicted ligand-binding module in plant cytokinin receptors and other eukaryotic and bacterial receptors. Trends Biochem. Sci. 2001;26:579–582. doi: 10.1016/S0968-0004(01)01968-5. PubMed DOI
Mougel C., Zhulin I.B. CHASE: An extracellular sensing domain common to transmembrane receptors from prokaryotes, lower eukaryotes and plants. Trends Biochem. Sci. 2001;26:582–584. doi: 10.1016/S0968-0004(01)01969-7. PubMed DOI
Wang W., Esch J.J., Shiu S.-H., Agula H., Binder B.M., Chang C., Patterson S.E., Bleecker A.B. Identification of Important Regions for Ethylene Binding and Signaling in the Transmembrane Domain of the ETR1 Ethylene Receptor of Arabidopsis. Plant Cell. 2006;18:3429–3442. doi: 10.1105/tpc.106.044537. PubMed DOI PMC
Ju C., Van De Poel B., Cooper E.D., Thierer J.H., Gibbons T.R., Delwiche C.F., Chang C. Conservation of ethylene as a plant hormone over 450 million years of evolution. Nat. Plants. 2015;1:14004. doi: 10.1038/nplants.2014.4. PubMed DOI
Cheng S., Xian W., Fu Y., Marin B., Keller J., Wu T., Sun W., Li X., Xu Y., Zhang Y., et al. Genomes of Subaerial Zygnematophyceae Provide Insights into Land Plant Evolution. Cell. 2019;179:1057–1067.e14. doi: 10.1016/j.cell.2019.10.019. PubMed DOI
Wang S., Li L., Li H., Sahu S.K., Wang H., Xu Y., Xian W., Song B., Liang H., Cheng S., et al. Genomes of early-diverging streptophyte algae shed light on plant terrestrialization. Nat. Plants. 2020;6:95–106. doi: 10.1038/s41477-019-0560-3. PubMed DOI PMC
Li L., Wang S., Wang H., Sahu S.K., Marin B., Li H., Xu Y., Liang H., Li Z., Cheng S., et al. The genome of Prasinoderma coloniale unveils the existence of a third phylum within green plants. Nat. Ecol. Evol. 2020;4:1220–1231. doi: 10.1038/s41559-020-1221-7. PubMed DOI PMC
Nishiyama T., Sakayama H., De Vries J., Buschmann H., Saint-Marcoux D., Ullrich K.K., Haas F.B., Vanderstraeten L., Becker D., Lang D., et al. The Chara Genome: Secondary Complexity and Implications for Plant Terrestrialization. Cell. 2018;174:448–464.e24. doi: 10.1016/j.cell.2018.06.033. PubMed DOI
Papon N., Binder B.M. An Evolutionary Perspective on Ethylene Sensing in Microorganisms. Trends Microbiol. 2019;27:193–196. doi: 10.1016/j.tim.2018.12.002. PubMed DOI
Kabbara S., Schmülling T., Papon N. CHASEing Cytokinin Receptors in Plants, Bacteria, Fungi, and Beyond. Trends Plant Sci. 2018;23:179–181. doi: 10.1016/j.tplants.2018.01.001. PubMed DOI
Spíchal L. Cytokinins—Recent news and views of evolutionally old molecules. Funct. Plant Biol. 2012;39:267–284. doi: 10.1071/fp11276. PubMed DOI
Lacey R.F., Binder B.M. Ethylene Regulates the Physiology of the Cyanobacterium Synechocystis sp. PCC 6803 via an Ethylene Receptor. Plant Physiol. 2016;171:2798–2809. doi: 10.1104/pp.16.00602. PubMed DOI PMC
Wang F.-F., Cheng S.-T., Wu Y., Ren B.-Z., Qian W. A Bacterial Receptor PcrK Senses the Plant Hormone Cytokinin to Promote Adaptation to Oxidative Stress. Cell Rep. 2017;21:2940–2951. doi: 10.1016/j.celrep.2017.11.017. PubMed DOI
Wang F.-F., Qian W. The roles of histidine kinases in sensing host plant and cell–cell communication signal in a phytopathogenic bacterium. Philos. Trans. R. Soc. B Biol. Sci. 2019;374:20180311. doi: 10.1098/rstb.2018.0311. PubMed DOI PMC
Frébortová J., Plíhal O., Florová V., Kokáš F., Kubiasová K., Greplová M., Šimura J., Novák O., Frébort I. Light influences cytokinin biosynthesis and sensing in Nostoc (cyanobacteria) J. Phycol. 2017;53:703–714. doi: 10.1111/jpy.12538. PubMed DOI
Allen C.J., Lacey R.F., Bickford A.B.B., Beshears C.P., Gilmartin C.J., Binder B.M. Cyanobacteria Respond to Low Levels of Ethylene. Front. Plant Sci. 2019;10:950. doi: 10.3389/fpls.2019.00950. PubMed DOI PMC
Lacey R.F., Allen C.J., Bakshi A., Binder B.M. Ethylene causes transcriptomic changes inSynechocystisduring phototaxis. Plant Direct. 2018;2:e00048. doi: 10.1002/pld3.48. PubMed DOI PMC
Mount S.M., Chang C. Evidence for a Plastid Origin of Plant Ethylene Receptor Genes. Plant Physiol. 2002;130:10–14. doi: 10.1104/pp.005397. PubMed DOI PMC
Kabbara S., Bidon B., Kilani J., Osman M., Hamze M., Stock A.M., Papon N., Sun Y., Jiang X., Lv Y., et al. Cytokinin Sensing in Bacteria. Biomolecules. 2020;10:186. doi: 10.3390/biom10020186. PubMed DOI PMC
Grant J.R., Katz L.A. Building a Phylogenomic Pipeline for the Eukaryotic Tree of Life—Addressing Deep Phylogenies with Genome-Scale Data. PLoS Curr. 2014;6 doi: 10.1371/currents.tol.c24b6054aebf3602748ac042ccc8f2e9. PubMed DOI PMC
Kabbara S., Hérivaux A., De Bernonville T.D., Courdavault V., Clastre M., Gastebois A., Osman M., Hamze M., Cock J.M., Schaap P., et al. Diversity and Evolution of Sensor Histidine Kinases in Eukaryotes. Genome Biol. Evol. 2019;11:86–108. doi: 10.1093/gbe/evy213. PubMed DOI PMC
Defosse T.A., Sharma A., Mondal A.K., De Bernonville T.D., Latgé J.-P., Calderone R., Giglioli-Guivarc’H N., Courdavault V., Clastre M., Papon N. Hybrid histidine kinases in pathogenic fungi. Mol. Microbiol. 2015;95:914–924. doi: 10.1111/mmi.12911. PubMed DOI
Hérivaux A., So Y.-S., Gastebois A., Latgé J.-P., Bouchara J.-P., Bahn Y.-S., Papon N. Major Sensing Proteins in Pathogenic Fungi: The Hybrid Histidine Kinase Family. PLOS Pathog. 2016;12:e1005683. doi: 10.1371/journal.ppat.1005683. PubMed DOI PMC
Foo E., McAdam E.L., Weller J.L., Reid J.B. Interactions between ethylene, gibberellins, and brassinosteroids in the development of rhizobial and mycorrhizal symbioses of pea. J. Exp. Bot. 2016;67:2413–2424. doi: 10.1093/jxb/erw047. PubMed DOI PMC
Santos R.T.D.L., Vierheilig H., Ocampo J.A., Garcia-Garrido J.M. Altered pattern of arbuscular mycorrhizal formation in tomato ethylene mutants. Plant Signal. Behav. 2011;6:755–758. doi: 10.4161/psb.6.5.15415. PubMed DOI PMC
Chanclud E., Kisiala A., Emery N.R.J., Chalvon V., Ducasse A., Romiti-Michel C., Gravot A., Kroj T., Morel J.-B. Cytokinin Production by the Rice Blast Fungus Is a Pivotal Requirement for Full Virulence. PLoS Pathog. 2016;12:e1005457. doi: 10.1371/journal.ppat.1005457. PubMed DOI PMC
Cosme M., Ramireddy E., Franken P., Schmülling T., Wurst S. Shootand root-borne cytokinin influences arbuscular mycorrhizal symbiosis. Mycorrhiza. 2016;26:709–720. doi: 10.1007/s00572-016-0706-3. PubMed DOI PMC
Laffont C., Rey T., André O., Novero M., Kazmierczak T., Debelle F., Bonfante P., Jacquet C., Frugier F. The CRE1 Cytokinin Pathway Is Differentially Recruited Depending on Medicago truncatula Root Environments and Negatively Regulates Resistance to a Pathogen. PLoS ONE. 2015;10:e0116819. doi: 10.1371/journal.pone.0116819. PubMed DOI PMC
Hinsch J., Galuszka P., Tudzynski P. Functional characterization of the first filamentous fungal tRNA -isopentenyltransferase and its role in the virulence of Claviceps purpurea. New Phytol. 2016;211:980–992. doi: 10.1111/nph.13960. PubMed DOI
Goh D.M., Cosme M., Kisiala A., Mulholland S., Said Z.M.F., Spíchal L., Emery R.N., Declerck S., Guinel F. A Stimulatory Role for Cytokinin in the Arbuscular Mycorrhizal Symbiosis of Pea. Front. Plant Sci. 2019;10 doi: 10.3389/fpls.2019.00262. PubMed DOI PMC
Hérivaux A., De Bernonville T.D., Le Roux C., Clastre M., Courdavault V., Gastebois A., Bouchara J.-P., James T.Y., Latgé J.-P., Martin F., et al. The Identification of Phytohormone Receptor Homologs in Early Diverging Fungi Suggests a Role for Plant Sensing in Land Colonization by Fungi. mBio. 2017;8:e01739-16. doi: 10.1128/mBio.01739-16. PubMed DOI PMC
Genre A., Lanfranco L., Perotto S., Bonfante P. Unique and common traits in mycorrhizal symbioses. Nat. Rev. Genet. 2020:1–12. doi: 10.1038/s41579-020-0402-3. PubMed DOI
Pons S., Fournier S., Chervin C., Bécard G., Rochange S., Frey N.F.D., Pagès V.P. Phytohormone production by the arbuscular mycorrhizal fungus Rhizophagus irregularis. PLoS ONE. 2020;15:e0240886. doi: 10.1371/journal.pone.0240886. PubMed DOI PMC
Aoki M., Kisiala A., Li S., Stock N.L., Brunetti C.R., Huber R.J., Emery R.N. Cytokinin Detection during the Dictyostelium discoideum Life Cycle: Profiles Are Dynamic and Affect Cell Growth and Spore Germination. Biomolecules. 2019;9:702. doi: 10.3390/biom9110702. PubMed DOI PMC
Aoki M.M., Emery R.J.N., Anjard C., Brunetti C.R., Huber R.J. Cytokinins in Dictyostelia—A Unique Model for Studying the Functions of Signaling Agents From Species to Kingdoms. Front. Cell Dev. Biol. 2020;8:511. doi: 10.3389/fcell.2020.00511. PubMed DOI PMC
Anjard C., Loomis W.F. Cytokinins induce sporulation in Dictyostelium. Development. 2008;135:819–827. doi: 10.1242/dev.018051. PubMed DOI
Loomis W.F. Cell signaling during development of Dictyostelium. Dev. Biol. 2014;391:1–16. doi: 10.1016/j.ydbio.2014.04.001. PubMed DOI PMC
Wang N., Shaulsky G., Escalante R., Loomis W.F. A two-component histidine kinase gene that functions in Dictyostelium development. EMBO J. 1996;15:3890–3898. doi: 10.1002/j.1460-2075.1996.tb00763.x. PubMed DOI PMC
Kabbara S., Bidon B., Kilani J., De Bernonville T.D., Clastre M., Courdavault V., Cock J.M., Papon N. Megaviruses: An involvement in phytohormone receptor gene transfer in brown algae? Gene. 2019;704:149–151. doi: 10.1016/j.gene.2019.04.055. PubMed DOI
North J.A., Narrowe A.B., Xiong W., Byerly K.M., Zhao G., Young S.J., Murali S., Wildenthal J.A., Cannon W.R., Wrighton K.C., et al. A nitrogenase-like enzyme system catalyzes methionine, ethylene, and methane biogenesis. Science. 2020;369:1094–1098. doi: 10.1126/science.abb6310. PubMed DOI
North J.A., Miller A.R., Wildenthal J.A., Young S.J., Tabita F.R. Microbial pathway for anaerobic 5’-methylthioadenosine metabolism coupled to ethylene formation. Proc. Natl. Acad. Sci. USA. 2017;114:E10455–E10464. doi: 10.1073/pnas.1711625114. PubMed DOI PMC
Amagai A. Ethylene as a potent inducer of sexual development. Dev. Growth Differ. 2011;53:617–623. doi: 10.1111/j.1440-169X.2011.01273.x. PubMed DOI
Daudu D., Kisiala A., Ribeiro C.W., Mélin C., Perrot L., Clastre M., Courdavault V., Papon N., Oudin A., Courtois M., et al. Setting-up a fast and reliable cytokinin biosensor based on a plant histidine kinase receptor expressed in Saccharomyces cerevisiae. J. Biotechnol. 2019;289:103–111. doi: 10.1016/j.jbiotec.2018.11.013. PubMed DOI
Andreas P., Kisiala A., Emery R.N., De Clerck-Floate R., Tooker J.F., Price P.W., Miller D.G., Chen M.-S., Connor E.F. Cytokinins Are Abundant and Widespread among Insect Species. Plants. 2020;9:208. doi: 10.3390/plants9020208. PubMed DOI PMC
Kisiala A., Kambhampati S., Stock N.L., Aoki M., Emery R.N. Quantification of Cytokinins Using High-Resolution Accurate-Mass Orbitrap Mass Spectrometry and Parallel Reaction Monitoring (PRM) Anal. Chem. 2019;91:15049–15056. doi: 10.1021/acs.analchem.9b03728. PubMed DOI
Seegobin M., Kisiala A., Noble A., Kaplan D., Brunetti C., Emery R.J.N. Canis familiaris tissues are characterized by different profiles of cytokinins typical of the tRNA degradation pathway. FASEB J. 2018;32:6575–6581. doi: 10.1096/fj.201800347. PubMed DOI
Mizuno T., Yamashino T. Biochemical Characterization of Plant Hormone Cytokinin-Receptor Histidine Kinases Using Microorganisms. Methods Enzymol. 2010;471:335–356. doi: 10.1016/s0076-6879(10)71018-1. PubMed DOI
Schaller G.E., Binder B.M. Biochemical Characterization of Plant Ethylene Receptors Following Transgenic Expression in Yeast. Methods Enzymol. 2007;422:270–287. doi: 10.1016/s0076-6879(06)22013-5. PubMed DOI
Daudu D., Allion E., Liesecke F., Papon N., Courdavault V., De Bernonville T.D., Mélin C., Oudin A., Clastre M., LaNoue A., et al. CHASE-Containing Histidine Kinase Receptors in Apple Tree: From a Common Receptor Structure to Divergent Cytokinin Binding Properties and Specific Functions. Front. Plant Sci. 2017;8:1614. doi: 10.3389/fpls.2017.01614. PubMed DOI PMC
Kubiasová K., Montesinos J.C., Šamajová O., Nisler J., Mik V., Semerádová H., Plíhalová L., Novak O., Marhavý P., Cavallari N., et al. Cytokinin fluoroprobe reveals multiple sites of cytokinin perception at plasma membrane and endoplasmic reticulum. Nat. Commun. 2020;11:1–11. doi: 10.1038/s41467-020-17949-0. PubMed DOI PMC
Brütting C., Crava C.M., Schäfer M., Schuman M.C., Meldau S., Adam N., Baldwin I.T. Cytokinin transfer by a free-living mirid to Nicotiana attenuata recapitulates a strategy of endophytic insects. eLife. 2018;7 doi: 10.7554/eLife.36268. PubMed DOI PMC
Body M.J.A., Appel H.M., Edger P.P., Schultz J.C. A gall-forming insect manipulates hostplant phytohormone synthesis, concentrations, and signaling. bioRxiv. 2019:658823. doi: 10.1101/658823. DOI
Siddique S., Radakovic Z.S., De La Torre C.M., Chronis D., Novák O., Ramireddy E., Holbein J., Matera C., Hütten M., Gutbrod P., et al. A parasitic nematode releases cytokinin that controls cell division and orchestrates feeding site formation in host plants. Proc. Natl. Acad. Sci. USA. 2015;112:12669–12674. doi: 10.1073/pnas.1503657112. PubMed DOI PMC
Siddique S., Grundler F.M. Parasitic nematodes manipulate plant development to establish feeding sites. Curr. Opin. Microbiol. 2018;46:102–108. doi: 10.1016/j.mib.2018.09.004. PubMed DOI
Ku Y.-S., Sintaha M., Cheung M.-Y., Lam H.-M. Plant Hormone Signaling Crosstalks between Biotic and Abiotic Stress Responses. Int. J. Mol. Sci. 2018;19:3206. doi: 10.3390/ijms19103206. PubMed DOI PMC
Bedini A., Mercy L., Schneider C., Franken P., Lucic-Mercy E. Unraveling the Initial Plant Hormone Signaling, Metabolic Mechanisms and Plant Defense Triggering the Endomycorrhizal Symbiosis Behavior. Front. Plant Sci. 2018;9:1800. doi: 10.3389/fpls.2018.01800. PubMed DOI PMC