Plants are sessile organisms forced to adapt to environmental variations recurring in a day-night cycle. Extensive research has uncovered the transcriptional control of plants' inner clock and has revealed at least some part of the intricate and elaborate regulatory mechanisms that govern plant diel responses and provide adaptation to the ever-changing environment. Here, we analyzed the proteome of the Arabidopsis thaliana mutant genotypes collected in the middle of the day and the middle of the night, including four mutants in the phytochrome (phyA, phyB, phyC, and phyD) and the circadian clock protein LHY. Our approach provided a novel insight into the diel regulations, identifying 640 significant changes in the night-day protein abundance. The comparison with previous studies confirmed that a large portion of identified proteins was a known target of diurnal regulation. However, more than 300 were novel oscillations hidden under standard growth chamber conditions or not manifested in the wild type. Our results indicated a prominent role for ROS metabolism and phytohormone cytokinin in the observed regulations, and the consecutive analyses confirmed that. The cytokinin signaling significantly increased at night, and in the mutants, the hydrogen peroxide content was lower, and the night-day variation seemed to be lost in the phyD genotype. Furthermore, regulations in the lhy and phyB mutants were partially similar to those found in the catalase mutant cat2, indicating shared ROS-mediated signaling pathways. Our data also shed light on the role of the relatively poorly characterized Phytochrome D, pointing to its connection to glutathione metabolism and the regulation of glutathione S-transferases.

Department of Molecular Biology and Radiobiology Faculty of AgriSciences Mendel University in Brno 61300 Brno Czech Republic

Zobrazit více v PubMed

Covington M.F., Maloof J.N., Straume M., Kay S.A., Harmer S.L. Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol. 2008;9:R130. doi: 10.1186/gb-2008-9-8-r130. PubMed DOI PMC

Hazen S.P., Naef F., Quisel T., Gendron J.M., Chen H., Ecker J.R., Borevitz J.O., Kay S.A. Exploring the transcriptional landscape of plant circadian rhythms using genome tiling arrays. Genome Biol. 2009;10:R17. doi: 10.1186/gb-2009-10-2-r17. PubMed DOI PMC

Paajanen P., Lane de Barros Dantas L., Dodd A.N. Layers of crosstalk between circadian regulation and environmental signalling in plants. Curr. Biol. 2021;31:R399–R413. doi: 10.1016/j.cub.2021.03.046. PubMed DOI

Harmer S.L. The Circadian System in Higher Plants. Annu. Rev. Plant Biol. 2009;60:357–377. doi: 10.1146/annurev.arplant.043008.092054. PubMed DOI

Gil K., Park C. Thermal adaptation and plasticity of the plant circadian clock. New Phytol. 2019;221:1215–1229. doi: 10.1111/nph.15518. PubMed DOI

Dubois M., Claeys H., Van den Broeck L., Inzé D. Time of day determines Arabidopsis transcriptome and growth dynamics under mild drought. Plant. Cell Environ. 2017;40:180–189. doi: 10.1111/pce.12809. PubMed DOI

Blair E.J., Bonnot T., Hummel M., Hay E., Marzolino J.M., Quijada I.A., Nagel D.H. Contribution of time of day and the circadian clock to the heat stress responsive transcriptome in Arabidopsis. Sci. Rep. 2019;9:4814. doi: 10.1038/s41598-019-41234-w. PubMed DOI PMC

Hua J. Modulation of plant immunity by light, circadian rhythm, and temperature. Curr. Opin. Plant Biol. 2013;16:406–413. doi: 10.1016/j.pbi.2013.06.017. PubMed DOI

Hermans C., Vuylsteke M., Coppens F., Craciun A., Inzé D., Verbruggen N. Early transcriptomic changes induced by magnesium deficiency in Arabidopsis thaliana reveal the alteration of circadian clock gene expression in roots and the triggering of abscisic acid-responsive genes. New Phytol. 2010;187:119–131. doi: 10.1111/j.1469-8137.2010.03258.x. PubMed DOI

Chen Y.-Y., Wang Y., Shin L.-J., Wu J.-F., Shanmugam V., Tsednee M., Lo J.-C., Chen C.-C., Wu S.-H., Yeh K.-C. Iron Is Involved in the Maintenance of Circadian Period Length in Arabidopsis. Plant Physiol. 2013;161:1409–1420. doi: 10.1104/pp.112.212068. PubMed DOI PMC

Kolmos E., Chow B.Y., Pruneda-Paz J.L., Kay S.A. HsfB2b-mediated repression of PRR7 directs abiotic stress responses of the circadian clock. Proc. Natl. Acad. Sci. USA. 2014;111:16172–16177. doi: 10.1073/pnas.1418483111. PubMed DOI PMC

Marcolino-Gomes J., Rodrigues F.A., Fuganti-Pagliarini R., Bendix C., Nakayama T.J., Celaya B., Molinari H.B.C., de Oliveira M.C.N., Harmon F.G., Nepomuceno A. Diurnal Oscillations of Soybean Circadian Clock and Drought Responsive Genes. PLoS ONE. 2014;9:e86402. doi: 10.1371/journal.pone.0086402. PubMed DOI PMC

Staiger D., Köster T. Spotlight on post-transcriptional control in the circadian system. Cell. Mol. Life Sci. 2011;68:71–83. doi: 10.1007/s00018-010-0513-5. PubMed DOI PMC

Romanowski A., Schlaen R.G., Perez-Santangelo S., Mancini E., Yanovsky M.J. Global transcriptome analysis reveals circadian control of splicing events in Arabidopsis thaliana. Plant J. 2020;103:889–902. doi: 10.1111/tpj.14776. PubMed DOI

Vogel C., Marcotte E.M. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat. Rev. Genet. 2012;13:227–232. doi: 10.1038/nrg3185. PubMed DOI PMC

Hwang H., Cho M.-H., Hahn B.-S., Lim H., Kwon Y.-K., Hahn T.-R., Bhoo S.H. Proteomic identification of rhythmic proteins in rice seedlings. Biochim. Biophys. Acta Proteins Proteom. 2011;1814:470–479. doi: 10.1016/j.bbapap.2011.01.010. PubMed DOI

Choudhary M.K., Nomura Y., Shi H., Nakagami H., Somers D.E. Circadian Profiling of the Arabidopsis Proteome Using 2D-DIGE. Front. Plant Sci. 2016;7:1007. doi: 10.3389/fpls.2016.01007. PubMed DOI PMC

Choudhary M.K., Nomura Y., Wang L., Nakagami H., Somers D.E. Quantitative Circadian Phosphoproteomic Analysis of Arabidopsis Reveals Extensive Clock Control of Key Components in Physiological, Metabolic, and Signaling Pathways. Mol. Cell. Proteom. 2015;14:2243–2260. doi: 10.1074/mcp.M114.047183. PubMed DOI PMC

Graf A., Coman D., Uhrig R.G., Walsh S., Flis A., Stitt M., Gruissem W. Parallel analysis of Arabidopsis circadian clock mutants reveals different scales of transcriptome and proteome regulation. Open Biol. 2017;7:160333. doi: 10.1098/rsob.160333. PubMed DOI PMC

Seaton D.D., Graf A., Baerenfaller K., Stitt M., Millar A.J., Gruissem W. Photoperiodic control of the Arabidopsis proteome reveals a translational coincidence mechanism. Mol. Syst. Biol. 2018;14:e7962. doi: 10.15252/msb.20177962. PubMed DOI PMC

Uhrig R.G., Echevarría-Zomeño S., Schlapfer P., Grossmann J., Roschitzki B., Koerber N., Fiorani F., Gruissem W. Diurnal dynamics of the Arabidopsis rosette proteome and phosphoproteome. Plant. Cell Environ. 2021;44:821–841. doi: 10.1111/pce.13969. PubMed DOI PMC

Verhage L. Isotope labeling to measure protein synthesis rates throughout the diurnal cycle—The technique explained. Plant J. 2022;109:743–744. doi: 10.1111/tpj.15696. PubMed DOI

He Y., Yu Y., Wang X., Qin Y., Su C., Wang L. Aschoff’s rule on circadian rhythms orchestrated by blue light sensor CRY2 and clock component PRR9. Nat. Commun. 2022;13:5869. doi: 10.1038/s41467-022-33568-3. PubMed DOI PMC

Oakenfull R.J., Davis S.J. Shining a light on the Arabidopsis circadian clock. Plant. Cell Environ. 2017;40:2571–2585. doi: 10.1111/pce.13033. PubMed DOI

Legris M., Ince Y.Ç., Fankhauser C. Molecular mechanisms underlying phytochrome-controlled morphogenesis in plants. Nat. Commun. 2019;10:5219. doi: 10.1038/s41467-019-13045-0. PubMed DOI PMC

Schaffer R., Ramsay N., Samach A., Corden S., Putterill J., Carré I.A., Coupland G. The late elongated hypocotyl Mutation of Arabidopsis Disrupts Circadian Rhythms and the Photoperiodic Control of Flowering. Cell. 1998;93:1219–1229. doi: 10.1016/S0092-8674(00)81465-8. PubMed DOI

Park M.-J., Kwon Y.-J., Gil K.-E., Park C.-M. LATE ELONGATED HYPOCOTYL regulates photoperiodic flowering via the circadian clock in Arabidopsis. BMC Plant Biol. 2016;16:114. doi: 10.1186/s12870-016-0810-8. PubMed DOI PMC

Kyung J., Jeon M., Jeong G., Shin Y., Seo E., Yu J., Kim H., Park C.-M., Hwang D., Lee I. The two clock proteins CCA1 and LHY activate VIN3 transcription during vernalization through the vernalization-responsive cis-element. Plant Cell. 2022;34:1020–1037. doi: 10.1093/plcell/koab304. PubMed DOI PMC

Yang S.W., Jang I.-C., Henriques R., Chua N.-H. FAR-RED ELONGATED HYPOCOTYL1 and FHY1-LIKE Associate with the Arabidopsis Transcription Factors LAF1 and HFR1 to Transmit Phytochrome A Signals for Inhibition of Hypocotyl Elongation. Plant Cell. 2009;21:1341–1359. doi: 10.1105/tpc.109.067215. PubMed DOI PMC

Nagatani A., Reed J.W., Chory J. Isolation and Initial Characterization of Arabidopsis Mutants That Are Deficient in Phytochrome A. Plant Physiol. 1993;102:269–277. doi: 10.1104/pp.102.1.269. PubMed DOI PMC

Salomé P.A., Michael T.P., Kearns E.V., Fett-Neto A.G., Sharrock R.A., McClung C.R. The out of phase 1 Mutant Defines a Role for PHYB in Circadian Phase Control in Arabidopsis. Plant Physiol. 2002;129:1674–1685. doi: 10.1104/pp.003418. PubMed DOI PMC

Jung J.-H., Domijan M., Klose C., Biswas S., Ezer D., Gao M., Khattak A.K., Box M.S., Charoensawan V., Cortijo S., et al. Phytochromes function as thermosensors in Arabidopsis. Science. 2016;354:886–889. doi: 10.1126/science.aaf6005. PubMed DOI

Arico D., Legris M., Castro L., Garcia C.F., Laino A., Casal J.J., Mazzella M.A. Neighbour signals perceived by phytochrome B increase thermotolerance in Arabidopsis. Plant. Cell Environ. 2019;42:2554–2566. doi: 10.1111/pce.13575. PubMed DOI

Monte E., Alonso J.M., Ecker J.R., Zhang Y., Li X., Young J., Austin-Phillips S., Quail P.H. Isolation and Characterization of phyC Mutants in Arabidopsis Reveals Complex Crosstalk between Phytochrome Signaling Pathways. Plant Cell. 2003;15:1962–1980. doi: 10.1105/tpc.012971. PubMed DOI PMC

Edwards K.D., Guerineau F., Devlin P.F., Millar A.J. Low-temperature-specific effects of PHYTOCHROME C on the circadian clock in Arabidopsis suggest that PHYC underlies natural variation in biological timing. bioRxiv. 2015:30577. doi: 10.1101/030577. DOI

Devlin P.F., Robson P.R.H., Patel S.R., Goosey L., Sharrock R.A., Whitelam G.C. Phytochrome D Acts in the Shade-Avoidance Syndrome in Arabidopsis by Controlling Elongation Growth and Flowering Time1. Plant Physiol. 1999;119:909–916. doi: 10.1104/pp.119.3.909. PubMed DOI PMC

Aukerman M.J., Hirschfeld M., Wester L., Weaver M., Clack T., Amasino R.M., Sharrock R.A. A deletion in the PHYD gene of the Arabidopsis Wassilewskija ecotype defines a role for phytochrome D in red/far-red light sensing. Plant Cell. 1997;9:1317–1326. doi: 10.1105/tpc.9.8.1317. PubMed DOI PMC

Tóth R., Kevei E., Hall A., Millar A.J., Nagy F., Kozma-Bognár L. Circadian Clock-Regulated Expression of Phytochrome and Cryptochrome Genes in Arabidopsis. Plant Physiol. 2001;127:1607–1616. doi: 10.1104/pp.010467. PubMed DOI PMC

Ferrari C., Proost S., Janowski M., Becker J., Nikoloski Z., Bhattacharya D., Price D., Tohge T., Bar-Even A., Fernie A., et al. Kingdom-wide comparison reveals the evolution of diurnal gene expression in Archaeplastida. Nat. Commun. 2019;10:737. doi: 10.1038/s41467-019-08703-2. PubMed DOI PMC

Kircher S., Gil P., Kozma-Bognár L., Fejes E., Speth V., Husselstein-Muller T., Bauer D., Ádám É., Schäfer E., Nagy F. Nucleocytoplasmic Partitioning of the Plant Photoreceptors Phytochrome A, B, C, D, and E Is Regulated Differentially by Light and Exhibits a Diurnal Rhythm. Plant Cell. 2002;14:1541–1555. doi: 10.1105/tpc.001156. PubMed DOI PMC

Liu Y., Sun Y., Yao H., Zheng Y., Cao S., Wang H. Arabidopsis Circadian Clock Repress Phytochrome A Signaling. Front. Plant Sci. 2022;13:809563. doi: 10.3389/fpls.2022.809563. PubMed DOI PMC

Pfeiffer A., Nagel M.-K., Popp C., Wüst F., Bindics J., Viczián A., Hiltbrunner A., Nagy F., Kunkel T., Schäfer E. Interaction with plant transcription factors can mediate nuclear import of phytochrome B. Proc. Natl. Acad. Sci. USA. 2012;109:5892–5897. doi: 10.1073/pnas.1120764109. PubMed DOI PMC

Fulton D.C., Stettler M., Mettler T., Vaughan C.K., Li J., Francisco P., Gil M., Reinhold H., Eicke S., Messerli G., et al. β-AMYLASE4, a Noncatalytic Protein Required for Starch Breakdown, Acts Upstream of Three Active β-Amylases in Arabidopsis Chloroplasts. Plant Cell. 2008;20:1040–1058. doi: 10.1105/tpc.107.056507. PubMed DOI PMC

Charron J.-B.F., Ouellet F., Houde M., Sarhan F. The plant Apolipoprotein D ortholog protects Arabidopsis against oxidative stress. BMC Plant Biol. 2008;8:86. doi: 10.1186/1471-2229-8-86. PubMed DOI PMC

Chi W.-T., Fung R.W.M., Liu H.-C., Hsu C.-C., Charng Y.-Y. Temperature-induced lipocalin is required for basal and acquired thermotolerance in Arabidopsis. Plant. Cell Environ. 2009;32:917–927. doi: 10.1111/j.1365-3040.2009.01972.x. PubMed DOI

Lee K.H., Piao H.L., Kim H.-Y., Choi S.M., Jiang F., Hartung W., Hwang I., Kwak J.M., Lee I.-J., Hwang I. Activation of Glucosidase via Stress-Induced Polymerization Rapidly Increases Active Pools of Abscisic Acid. Cell. 2006;126:1109–1120. doi: 10.1016/j.cell.2006.07.034. PubMed DOI

Larkin R.M., Stefano G., Ruckle M.E., Stavoe A.K., Sinkler C.A., Brandizzi F., Malmstrom C.M., Osteryoung K.W. REDUCED CHLOROPLAST COVERAGE genes from Arabidopsis thaliana help to establish the size of the chloroplast compartment. Proc. Natl. Acad. Sci. USA. 2016;113:E1116–E1125. doi: 10.1073/pnas.1515741113. PubMed DOI PMC

Papp I., Mur L., Dalmadi Á., Dulai S., Koncz C. A mutation in the Cap Binding Protein 20 gene confers drought. Plant Mol. Biol. 2004;55:679–686. doi: 10.1007/s11103-004-1680-2. PubMed DOI

Luo Y., Wang Z., Ji H., Fang H., Wang S., Tian L., Li X. An Arabidopsis homolog of importin β1 is required for ABA response and drought tolerance. Plant J. 2013;75:377–389. doi: 10.1111/tpj.12207. PubMed DOI

Zheng B.S., Rönnberg E., Viitanen L., Salminen T.A., Lundgren K., Moritz T., Edqvist J. Arabidopsis sterol carrier protein-2 is required for normal development of seeds and seedlings. J. Exp. Bot. 2008;59:3485–3499. doi: 10.1093/jxb/ern201. PubMed DOI PMC

Diaz C., Kusano M., Sulpice R., Araki M., Redestig H., Saito K., Stitt M., Shin R. Determining novel functions of Arabidopsis14-3-3 proteins in central metabolic processes. BMC Syst. Biol. 2011;5:192. doi: 10.1186/1752-0509-5-192. PubMed DOI PMC

Link S., Engelmann K., Meierhoff K., Westhoff P. The Atypical Short-Chain Dehydrogenases HCF173 and HCF244 Are Jointly Involved in Translational Initiation of the psbA mRNA of Arabidopsis. Plant Physiol. 2012;160:2202–2218. doi: 10.1104/pp.112.205104. PubMed DOI PMC

Christians M.J., Larsen P.B. Mutational loss of the prohibitin AtPHB3 results in an extreme constitutive ethylene response phenotype coupled with partial loss of ethylene-inducible gene expression in Arabidopsis seedlings. J. Exp. Bot. 2007;58:2237–2248. doi: 10.1093/jxb/erm086. PubMed DOI

Wang Y., Ries A., Wu K., Yang A., Crawford N.M. The Arabidopsis Prohibitin Gene PHB3 Functions in Nitric Oxide–Mediated Responses and in Hydrogen Peroxide–Induced Nitric Oxide Accumulation. Plant Cell. 2010;22:249–259. doi: 10.1105/tpc.109.072066. PubMed DOI PMC

Clark S.M., Di Leo R., Dhanoa P.K., Van Cauwenberghe O.R., Mullen R.T., Shelp B.J. Biochemical characterization, mitochondrial localization, expression, and potential functions for an Arabidopsis γ-aminobutyrate transaminase that utilizes both pyruvate and glyoxylate. J. Exp. Bot. 2009;60:1743–1757. doi: 10.1093/jxb/erp044. PubMed DOI PMC

Ahn G., Kim H., Kim D.H., Hanh H., Yoon Y., Singaram I., Wijesinghe K.J., Johnson K.A., Zhuang X., Liang Z., et al. SH3 Domain-Containing Protein 2 Plays a Crucial Role at the Step of Membrane Tubulation during Cell Plate Formation. Plant Cell. 2017;29:1388–1405. doi: 10.1105/tpc.17.00108. PubMed DOI PMC

Niehaus T.D., Patterson J.A., Alexander D.C., Folz J.S., Pyc M., MacTavish B.S., Bruner S.D., Mullen R.T., Fiehn O., Hanson A.D. The metabolite repair enzyme Nit1 is a dual-targeted amidase that disposes of damaged glutathione in Arabidopsis. Biochem. J. 2019;476:683–697. doi: 10.1042/BCJ20180931. PubMed DOI

Sibout R., Eudes A., Mouille G., Pollet B., Lapierre C., Jouanin L., Séguin A. CINNAMYL ALCOHOL DEHYDROGENASE-C and -D Are the Primary Genes Involved in Lignin Biosynthesis in the Floral Stem of Arabidopsis. Plant Cell. 2005;17:2059–2076. doi: 10.1105/tpc.105.030767. PubMed DOI PMC

Burow M., Zhang Z.-Y., Ober J.A., Lambrix V.M., Wittstock U., Gershenzon J., Kliebenstein D.J. ESP and ESM1 mediate indol-3-acetonitrile production from indol-3-ylmethyl glucosinolate in Arabidopsis. Phytochemistry. 2008;69:663–671. doi: 10.1016/j.phytochem.2007.08.027. PubMed DOI

Černý M., Novák J., Habánová H., Cerna H., Brzobohatý B. Role of the proteome in phytohormonal signaling. Biochim. Biophys. Acta Proteins Proteom. 2016;1864:1003–1015. doi: 10.1016/j.bbapap.2015.12.008. PubMed DOI

Ancín M., Fernandez-Irigoyen J., Santamaria E., Larraya L., Fernández-San Millán A., Veramendi J., Farran I. New In Vivo Approach to Broaden the Thioredoxin Family Interactome in Chloroplasts. Antioxidants. 2022;11:1979. doi: 10.3390/antiox11101979. PubMed DOI PMC

Mergner J., Frejno M., List M., Papacek M., Chen X., Chaudhary A., Samaras P., Richter S., Shikata H., Messerer M., et al. Mass-spectrometry-based draft of the Arabidopsis proteome. Nature. 2020;579:409–414. doi: 10.1038/s41586-020-2094-2. PubMed DOI

Stewart J.L., Nemhauser J.L. Do Trees Grow on Money? Auxin as the Currency of the Cellular Economy. Cold Spring Harb. Perspect. Biol. 2010;2:a001420. doi: 10.1101/cshperspect.a001420. PubMed DOI PMC

Singh M., Mas P. A Functional Connection between the Circadian Clock and Hormonal Timing in Arabidopsis. Genes. 2018;9:567. doi: 10.3390/genes9120567. PubMed DOI PMC

Rawat R., Schwartz J., Jones M.A., Sairanen I., Cheng Y., Andersson C.R., Zhao Y., Ljung K., Harmer S.L. REVEILLE1, a Myb-like transcription factor, integrates the circadian clock and auxin pathways. Proc. Natl. Acad. Sci. USA. 2009;106:16883–16888. doi: 10.1073/pnas.0813035106. PubMed DOI PMC

Covington M.F., Harmer S.L. The Circadian Clock Regulates Auxin Signaling and Responses in Arabidopsis. PLoS Biol. 2007;5:e222. doi: 10.1371/journal.pbio.0050222. PubMed DOI PMC

Voß U., Wilson M.H., Kenobi K., Gould P.D., Robertson F.C., Peer W.A., Lucas M., Swarup K., Casimiro I., Holman T.J., et al. The circadian clock rephases during lateral root organ initiation in Arabidopsis thaliana. Nat. Commun. 2015;6:7641. doi: 10.1038/ncomms8641. PubMed DOI PMC

Adams S., Grundy J., Veflingstad S.R., Dyer N.P., Hannah M.A., Ott S., Carré I.A. Circadian control of abscisic acid biosynthesis and signalling pathways revealed by genome-wide analysis of LHY binding targets. New Phytol. 2018;220:893–907. doi: 10.1111/nph.15415. PubMed DOI

Li B., Takahashi D., Kawamura Y., Uemura M. Comparison of Plasma Membrane Proteomic Changes of Arabidopsis Suspension-Cultured Cells (T87 Line) after Cold and ABA Treatment in Association with Freezing Tolerance Development. Plant Cell Physiol. 2012;53:543–554. doi: 10.1093/pcp/pcs010. PubMed DOI

Ezer D., Jung J.-H., Lan H., Biswas S., Gregoire L., Box M.S., Charoensawan V., Cortijo S., Lai X., Stöckle D., et al. The evening complex coordinates environmental and endogenous signals in Arabidopsis. Nat. Plants. 2017;3:17087. doi: 10.1038/nplants.2017.87. PubMed DOI PMC

Nováková M., Motyka V., Dobrev P.I., Malbeck J., Gaudinová A., Vanková R. Diurnal variation of cytokinin, auxin and abscisic acid levels in tobacco leaves. J. Exp. Bot. 2005;56:2877–2883. doi: 10.1093/jxb/eri282. PubMed DOI

Hanano S., Domagalska M.A., Nagy F., Davis S.J. Multiple phytohormones influence distinct parameters of the plant circadian clock. Genes Cells. 2006;11:1381–1392. doi: 10.1111/j.1365-2443.2006.01026.x. PubMed DOI

Salome P.A., To J.P.C., Kieber J.J., McClung R. Arabidopsis Response Regulators ARR3 and ARR4 Play Cytokinin-Independent Roles in the Control of Circadian Period. Plant Cell Online. 2006;18:55–69. doi: 10.1105/tpc.105.037994. PubMed DOI PMC

Nitschke S., Cortleven A., Iven T., Feussner I., Havaux M., Riefler M., Schmülling T. Circadian Stress Regimes Affect the Circadian Clock and Cause Jasmonic Acid-Dependent Cell Death in Cytokinin-Deficient Arabidopsis Plants. Plant Cell. 2016;28:1616–1639. doi: 10.1105/tpc.16.00016. PubMed DOI PMC

Pavlů J., Novák J., Koukalová V., Luklová M., Brzobohatý B., Černý M. Cytokinin at the Crossroads of Abiotic Stress Signalling Pathways. Int. J. Mol. Sci. 2018;19:2450. doi: 10.3390/ijms19082450. PubMed DOI PMC

Zheng B., Deng Y., Mu J., Ji Z., Xiang T., Niu Q.-W., Chua N.-H., Zuo J. Cytokinin affects circadian-clock oscillation in a phytochrome B- and Arabidopsis response regulator 4-dependent manner. Physiol. Plant. 2006;127:277–292. doi: 10.1111/j.1399-3054.2006.00660.x. DOI

Dobisova T., Hrdinova V., Cuesta C., Michlickova S., Urbankova I., Hejatkova R., Zadnikova P., Pernisova M., Benkova E., Hejatko J. Light Controls Cytokinin Signaling via Transcriptional Regulation of Constitutively Active Sensor Histidine Kinase CKI1. Plant Physiol. 2017;174:387–404. doi: 10.1104/pp.16.01964. PubMed DOI PMC

Mizoguchi T., Wheatley K., Hanzawa Y., Wright L., Mizoguchi M., Song H.-R., Carré I.A., Coupland G. LHY and CCA1 Are Partially Redundant Genes Required to Maintain Circadian Rhythms in Arabidopsis. Dev. Cell. 2002;2:629–641. doi: 10.1016/S1534-5807(02)00170-3. PubMed DOI

Černý M., Habánová H., Berka M., Luklová M., Brzobohatý B. Hydrogen Peroxide: Its Role in Plant Biology and Crosstalk with Signalling Networks. Int. J. Mol. Sci. 2018;19:2812. doi: 10.3390/ijms19092812. PubMed DOI PMC

Lai A.G., Doherty C.J., Mueller-Roeber B., Kay S.A., Schippers J.H.M., Dijkwel P.P. CIRCADIAN CLOCK-ASSOCIATED 1 regulates ROS homeostasis and oxidative stress responses. Proc. Natl. Acad. Sci. USA. 2012;109:17129–17134. doi: 10.1073/pnas.1209148109. PubMed DOI PMC

Román Á., Li X., Deng D., Davey J.W., James S., Graham I.A., Haydon M.J. Superoxide is promoted by sucrose and affects amplitude of circadian rhythms in the evening. Proc. Natl. Acad. Sci. USA. 2021;118:e2020646118. doi: 10.1073/pnas.2020646118. PubMed DOI PMC

Gallé Á., Czékus Z., Bela K., Horváth E., Ördög A., Csiszár J., Poór P. Plant Glutathione Transferases and Light. Front. Plant Sci. 2019;9:1944. doi: 10.3389/fpls.2018.01944. PubMed DOI PMC

Gallé Á., Czékus Z., Bela K., Horváth E., Csiszár J., Poór P. Diurnal changes in tomato glutathione transferase activity and expression. Acta Biol. Hung. 2018;69:505–509. doi: 10.1556/018.69.2018.4.11. PubMed DOI

Jiang H.-W., Liu M.-J., Chen I.-C., Huang C.-H., Chao L.-Y., Hsieh H.-L. A Glutathione S -Transferase Regulated by Light and Hormones Participates in the Modulation of Arabidopsis Seedling Development. Plant Physiol. 2010;154:1646–1658. doi: 10.1104/pp.110.159152. PubMed DOI PMC

Zechmann B. Diurnal changes of subcellular glutathione content in Arabidopsis thaliana. Biol. Plant. 2017;61:791–796. doi: 10.1007/s10535-017-0729-4. DOI

Pavlů J., Kerchev P., Černý M., Novák J., Berka M., Jobe T.O., López Ramos J.M., Saiz-Fernández I., Michael Rashotte A., Kopriva S., et al. Cytokinin modulates sulfur and glutathione metabolic network. J. Exp. Bot. 2022 doi: 10.1093/jxb/erac391. PubMed DOI

van Zanten M., Snoek L.B., Proveniers M.C.G., Peeters A.J.M. The many functions of ERECTA. Trends Plant Sci. 2009;14:214–218. doi: 10.1016/j.tplants.2009.01.010. PubMed DOI

McCarthy A., Chung M., Ivanov A.G., Krol M., Inman M., Maxwell D.P., Hüner N.P.A. An established Arabidopsis thaliana var. Landsberg erecta cell suspension culture accumulates chlorophyll and exhibits a stay-green phenotype in response to high external sucrose concentrations. J. Plant Physiol. 2016;199:40–51. doi: 10.1016/j.jplph.2016.05.008. PubMed DOI

Li X., Wang H., Wang Y., Zhang L., Wang Y. Comparison of Metabolic Profiling of Arabidopsis Inflorescences Between Landsberg erecta and Columbia, and Meiosis-Defective Mutants by 1H-NMR Spectroscopy. Phenomics. 2021;1:73–89. doi: 10.1007/s43657-021-00012-3. PubMed DOI PMC

Burgie E.S., Gannam Z.T.K., McLoughlin K.E., Sherman C.D., Holehouse A.S., Stankey R.J., Vierstra R.D. Differing biophysical properties underpin the unique signaling potentials within the plant phytochrome photoreceptor families. Proc. Natl. Acad. Sci. USA. 2021;118:e2105649118. doi: 10.1073/pnas.2105649118. PubMed DOI PMC

Ha J.-H., Kim J.-H., Kim S.-G., Sim H.-J., Lee G., Halitschke R., Baldwin I.T., Kim J.-I., Park C.-M. Shoot phytochrome B modulates reactive oxygen species homeostasis in roots via abscisic acid signaling in Arabidopsis. Plant J. 2018;94:790–798. doi: 10.1111/tpj.13902. PubMed DOI

Berka M., Luklová M., Dufková H., Malých V., Novák J., Saiz-Fernández I., Rashotte A.M., Brzobohaty B., Cerny M. Barley root proteome and metabolome in response to cytokinin and abiotic stimuli. Front. Plant Sci. 2020;11:1647. doi: 10.3389/fpls.2020.590337. PubMed DOI PMC

Dufková H., Berka M., Luklová M., Rashotte A.M., Brzobohatý B., Černý M. Eggplant Germination is Promoted by Hydrogen Peroxide and Temperature in an Independent but Overlapping Manner. Molecules. 2019;24:4270. doi: 10.3390/molecules24234270. PubMed DOI PMC

Berková V., Kameniarová M., Ondrisková V., Berka M., Menšíková S., Kopecká R., Luklová M., Novák J., Spíchal L., Rashotte A.M., et al. Arabidopsis Response to Inhibitor of Cytokinin Degradation INCYDE: Modulations of Cytokinin Signaling and Plant Proteome. Plants. 2020;9:1563. doi: 10.3390/plants9111563. PubMed DOI PMC

Krishnakumar V., Contrino S., Cheng C.Y., Belyaeva I., Ferlanti E.S., Miller J.R., Vaughn M.W., Micklem G., Town C.D., Chan A.P. Thalemine: A warehouse for Arabidopsis data integration and discovery. Plant Cell Physiol. 2017;58:e4. doi: 10.1093/pcp/pcw200. PubMed DOI

Schneider C.A., Rasband W.S., Eliceiri K.W. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods. 2012;9:671–675. doi: 10.1038/nmeth.2089. PubMed DOI PMC

Béziat C., Kleine-Vehn J., Feraru E. Histochemical staining of β-glucuronidase and its spatial quantification. Methods Mol. Biol. 2017;1497:73–80. doi: 10.1007/978-1-4939-6469-7_8. PubMed DOI

Pang Z., Chong J., Zhou G., De Lima Morais D.A., Chang L., Barrette M., Gauthier C., Jacques P.É., Li S., Xia J. MetaboAnalyst 5.0: Narrowing the gap between raw spectra and functional insights. Nucleic Acids Res. 2021;49:W388–W396. doi: 10.1093/nar/gkab382. PubMed DOI PMC

Liebermeister W., Noor E., Flamholz A., Davidi D., Bernhardt J., Milo R. Visual account of protein investment in cellular functions. Proc. Natl. Acad. Sci. USA. 2014;111:8488–8493. doi: 10.1073/pnas.1314810111. PubMed DOI PMC

Sun L., Dong S., Ge Y., Fonseca J.P., Robinson Z.T., Mysore K.S., Mehta P. DiVenn: An interactive and integrated web-based visualization tool for comparing gene lists. Front. Genet. 2021;10:421. doi: 10.3389/fgene.2019.00421. PubMed DOI PMC

Salicylic Acid Treatment and Its Effect on Seed Yield and Seed Molecular Composition of Pisum sativum under Abiotic Stress