Cytokinin is a multifaceted plant hormone that plays major roles not only in diverse plant growth and development processes, but also stress responses. We summarize knowledge of the roles of its metabolism, transport, and signalling in responses to changes in levels of both macronutrients (nitrogen, phosphorus, potassium, sulphur) and micronutrients (boron, iron, silicon, selenium). We comment on cytokinin's effects on plants' xenobiotic resistance, and its interactions with light, temperature, drought, and salinity signals. Further, we have compiled a list of abiotic stress-related genes and demonstrate that their expression patterns overlap with those of cytokinin metabolism and signalling genes.

CEITEC Central European Institute of Technology Faculty of AgriSciences Mendel University in Brno 613 00 Brno Czech Republic

Department of Molecular Biology and Radiobiology Faculty of AgriSciences Mendel University in Brno 613 00 Brno Czech Republic

Institute of Biophysics AS CR 612 00 Brno Czech Republic

Phytophthora Research Centre Faculty of AgriSciences Mendel University in Brno 613 00 Brno Czech Republic

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Suzuki I., Los D.A., Kanesaki Y., Mikami K., Murata N. The pathway for perception and transduction of low-temperature signals in Synechocystis. EMBO J. 2000;19:1327–1334. doi: 10.1093/emboj/19.6.1327. PubMed DOI PMC

Hwang I., Chen H.C., Sheen J. Two-component signal transduction pathways in Arabidopsis. Plant Physiol. 2002;129:500–515. doi: 10.1104/pp.005504. PubMed DOI PMC

Wolanin P.M., Thomason P.A., Stock J.B. Histidine protein kinases: Key signal transducers outside the animal kingdom. Genome Biol. 2002;3 doi: 10.1186/gb-2002-3-10-reviews3013. PubMed DOI PMC

O’Brien J.A., Benková E. Cytokinin cross-talking during biotic and abiotic stress responses. Front. Plant Sci. 2013;4:451. doi: 10.3389/fpls.2013.00451. PubMed DOI PMC

Kieber J.J., Schaller G.E. Cytokinin signaling in plant development. Development. 2018;145:dev149344. doi: 10.1242/dev.149344. PubMed DOI

Krapp A. Plant nitrogen assimilation and its regulation: A complex puzzle with missing pieces. Curr. Opin. Plant Biol. 2015;25:115–122. doi: 10.1016/j.pbi.2015.05.010. PubMed DOI

Gent L., Forde B.G. How do plants sense their nitrogen status? J. Exp. Bot. 2017;68:2531–2539. doi: 10.1093/jxb/erx013. PubMed DOI

Bellegarde F., Gojon A., Martin A. Signals and players in the transcriptional regulation of root responses by local and systemic N signaling in Arabidopsis thaliana. J. Exp. Bot. 2017;68:2553–2565. doi: 10.1093/jxb/erx062. PubMed DOI

Guan P., Ripoll J.J., Wang R., Vuong L., Bailey-Steinitz L.J., Ye D., Crawford N.M. Interacting TCP and NLP transcription factors control plant responses to nitrate availability. Proc. Natl. Acad. Sci. USA. 2017;114:2419–2424. doi: 10.1073/pnas.1615676114. PubMed DOI PMC

Kiba T., Takei K., Kojima M., Sakakibara H. Side-chain modification of cytokinins controls shoot growth in Arabidopsis. Dev. Cell. 2013;27:452–461. doi: 10.1016/j.devcel.2013.10.004. PubMed DOI

Kieber J.J., Schaller G.E. Cytokinins. Arabidopsis Book. 2014;12:e0168. doi: 10.1199/tab.0168. PubMed DOI PMC

Wang R., Tischner R., Gutiérrez R.A., Hoffman M., Xing X., Chen M., Coruzzi G., Crawford N.M. Genomic analysis of the nitrate response using a nitrate reductase-null mutant of Arabidopsis. Plant Physiol. 2004;136:2512–2522. doi: 10.1104/pp.104.044610. PubMed DOI PMC

Ramireddy E., Chang L., Schmülling T. Cytokinin as a mediator for regulating root system architecture in response to environmental cues. Plant Signal. Behav. 2014;9:e27771. doi: 10.4161/psb.27771. PubMed DOI PMC

Menz J., Li Z., Schulze W.X., Ludewig U. Early nitrogen-deprivation responses in Arabidopsis roots reveal distinct differences on transcriptome and (phospho-) proteome levels between nitrate and ammonium nutrition. Plant J. 2016;88:717–734. doi: 10.1111/tpj.13272. PubMed DOI

Liu K.H., Niu Y., Konishi M., Wu Y., Du H., Sun Chung H., Li L., Boudsocq M., McCormack M., Maekawa S., et al. Discovery of nitrate–CPK–NLP signalling in central nutrient–growth networks. Nature. 2017;545:311–316. doi: 10.1038/nature22077. PubMed DOI PMC

Wang R., Xing X., Wang Y., Tran A., Crawford N.M. A Genetic screen for nitrate regulatory mutants captures the nitrate transporter gene NRT1.1. Plant Physiol. 2009;151:472–478. doi: 10.1104/pp.109.140434. PubMed DOI PMC

Maeda Y., Konishi M., Kiba T., Sakuraba Y., Sawaki N., Kurai T., Ueda Y., Sakakibara H., Yanagisawa S. A NIGT1-centred transcriptional cascade regulates nitrate signalling and incorporates phosphorus starvation signals in Arabidopsis. Nat. Commun. 2018;9:1376. doi: 10.1038/s41467-018-03832-6. PubMed DOI PMC

Ruffel S., Krouk G., Ristova D., Shasha D., Birnbaum K.D., Coruzzi G.M. Nitrogen economics of root foraging: Transitive closure of the nitrate-cytokinin relay and distinct systemic signaling for N supply vs. demand. Proc. Natl. Acad. Sci. USA. 2011;108:18524–18529. doi: 10.1073/pnas.1108684108. PubMed DOI PMC

Ruffel S., Poitout A., Krouk G., Coruzzi G.M., Lacombe B. Long-distance nitrate signaling displays cytokinin dependent and independent branches. J. Integr. Plant Biol. 2016;58:226–229. doi: 10.1111/jipb.12453. PubMed DOI

Poitout A., Crabos A., Petřík I., Novák O., Krouk G., Lacombe B., Ruffel S. Responses to Systemic Nitrogen Signaling in Arabidopsis Roots Involve trans-Zeatin in Shoots. Plant Cell. 2018;30:1243–1257. doi: 10.1105/tpc.18.00011. PubMed DOI PMC

Guan P., Wang R., Nacry P., Breton G., Kay S.A., Pruneda-Paz J.L., Davani A., Crawford N.M. Nitrate foraging by Arabidopsis roots is mediated by the transcription factor TCP20 through the systemic signaling pathway. Proc. Natl. Acad. Sci. USA. 2014;111:15267–15272. doi: 10.1073/pnas.1411375111. PubMed DOI PMC

Patterson K., Walters L.A., Cooper A.M., Olvera J.G., Rosas M.A., Rasmusson A.G., Escobar M.A. Nitrate-Regulated Glutaredoxins Control Arabidopsis Primary Root Growth. Plant Physiol. 2016;170:989–999. doi: 10.1104/pp.15.01776. PubMed DOI PMC

Walters L.A., Escobar M.A. The AtGRXS3/4/5/7/8 glutaredoxin gene cluster on Arabidopsis thaliana chromosome 4 is coordinately regulated by nitrate and appears to control primary root growth. Plant Signal. Behav. 2016;11:e1171450. doi: 10.1080/15592324.2016.1171450. PubMed DOI PMC

Walch-Liu P., Neumann G., Bangerth F., Engels C. Rapid effects of nitrogen form on leaf morphogenesis in tobacco. J. Exp. Bot. 2000;51:227–237. doi: 10.1093/jexbot/51.343.227. PubMed DOI

Rahayu Y.S., Walch-Liu P., Neumann G., Römheld V., von Wirén N., Bangerth F. Root-derived cytokinins as long-distance signals for NO3-induced stimulation of leaf growth. J. Exp. Bot. 2005;56:1143–1152. doi: 10.1093/jxb/eri107. PubMed DOI

Müller D., Waldie T., Miyawaki K., To J.P., Melnyk C.W., Kieber J.J., Kakimoto T., Leyser O. Cytokinin is required for escape but not release from auxin mediated apical dominance. Plant J. 2015;82:874–886. doi: 10.1111/tpj.12862. PubMed DOI PMC

Miyawaki K., Matsumoto-Kitano M., Kakimoto T. Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: Tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J. 2004;37:128–138. doi: 10.1046/j.1365-313X.2003.01945.x. PubMed DOI

Takei K., Ueda N., Aoki K., Kuromori T., Hirayama T., Shinozaki K., Yamaya T., Sakakibara H. AtIPT3 is a key determinant of nitrate-dependent cytokinin biosynthesis in Arabidopsis. Plant Cell Physiol. 2004;45:1053–1062. doi: 10.1093/pcp/pch119. PubMed DOI

Sakakibara H., Takei K., Hirose N. Interactions between nitrogen and cytokinin in the regulation of metabolism and development. Trends Plant Sci. 2006;11:440–448. doi: 10.1016/j.tplants.2006.07.004. PubMed DOI

Kiba T., Kudo T., Kojima M., Sakakibara H. Hormonal control of nitrogen acquisition: Roles of auxin, abscisic acid, and cytokinin. J. Exp. Bot. 2011;62:1399–1409. doi: 10.1093/jxb/erq410. PubMed DOI

Osugi A., Kojima M., Takebayashi Y., Ueda N., Kiba T., Sakakibara H. Systemic transport of trans-zeatin and its precursor have differing roles in Arabidopsis shoots. Nat. Plants. 2017;3:17112. doi: 10.1038/nplants.2017.112. PubMed DOI

Landrein B., Formosa-Jordan P., Malivert A., Schuster C., Melnyk C.W., Yang W., Turnbull C., Meyerowitz E.M., Locke J.C.W., Jönsson H. Nitrate modulates stem cell dynamics in Arabidopsis shoot meristems through cytokinins. Proc. Natl. Acad. Sci. USA. 2018;115:1382–1387. doi: 10.1073/pnas.1718670115. PubMed DOI PMC

Krishnakumar V., Hanlon M.R., Contrino S., Ferlanti E.S., Karamycheva S., Kim M., Rosen B.D., Cheng C.Y., Moreira W., Mock S.A., et al. Araport: The Arabidopsis Information Portal. Nucleic Acids Res. 2015;43:D1003–D1009. doi: 10.1093/nar/gku1200. PubMed DOI PMC

Rouached H., Arpat A.B., Poirier Y. Regulation of Phosphate Starvation Responses in Plants: Signaling Players and Cross-Talks. Mol. Plant. 2010;3:288–299. doi: 10.1093/mp/ssp120. PubMed DOI

Ham B.K., Chen J., Yan Y., Lucas W.J. Insights into plant phosphate sensing and signaling. Curr. Opin. Biotechnol. 2018;49:1–9. doi: 10.1016/j.copbio.2017.07.005. PubMed DOI

Hirose N., Takei K., Kuroha T., Kamada-Nobusada T., Hayashi H., Sakakibara H. Regulation of cytokinin biosynthesis, compartmentalization and translocation. J. Exp. Bot. 2008;59:75–83. doi: 10.1093/jxb/erm157. PubMed DOI

Franco-Zorrilla J.M., Martin A.C., Solano R., Rubio V., Leyva A., Paz-Ares J. Mutations at CRE1 impair cytokinin-induced repression of phosphate starvation responses in Arabidopsis. Plant J. 2002;32:353–360. doi: 10.1046/j.1365-313X.2002.01431.x. PubMed DOI

Woo J., MacPherson C.R., Liu J., Wang H., Kiba T., Hannah M.A., Wang X.J., Bajic V.B., Chua N.H. The response and recovery of the Arabidopsis thaliana transcriptome to phosphate starvation. BMC Plant Biol. 2012;12:62. doi: 10.1186/1471-2229-12-62. PubMed DOI PMC

Werner T., Nehnevajova E., Köllmer I., Novák O., Strnad M., Krämer U., Schmülling T. Root-Specific Reduction of Cytokinin Causes Enhanced Root Growth, Drought Tolerance, and Leaf Mineral Enrichment in Arabidopsis and Tobacco. Plant Cell. 2010;22:3905–3920. doi: 10.1105/tpc.109.072694. PubMed DOI PMC

Nishiyama R., Le D.T., Watanabe Y., Matsui A., Tanaka M., Seki M., Yamaguchi-Shinozaki K., Shinozaki K., Tran L.S. Transcriptome analyses of a salt-tolerant cytokinin-deficient mutant reveal differential regulation of salt stress response by cytokinin deficiency. PLoS ONE. 2012;7:e32124. doi: 10.1371/journal.pone.0032124. PubMed DOI PMC

Mohan T.C., Castrillo G., Navarro C., Zarco-Fernández S., Ramireddy E., Mateo C., Zamarreño A.M., Paz-Ares J., Muñoz R., García-Mina J.M., et al. Cytokinin Determines Thiol-Mediated Arsenic Tolerance and Accumulation. Plant Physiol. 2016;171:1418–1426. doi: 10.1104/pp.16.00372. PubMed DOI PMC

Jiang L., Cao H., Chen Z., Liu C., Cao S., Wei Z., Han Y., Gao Q., Wang W. Cytokinin is involved in TPS22-mediated selenium tolerance in Arabidopsis thaliana. Ann. Bot. 2018 doi: 10.1093/aob/mcy093. PubMed DOI PMC

Martín A.C., del Pozo J.C., Iglesias J., Rubio V., Solano R., de La Peña A., Leyva A., Paz-Ares J. Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. Plant J. 2000;24:559–567. doi: 10.1046/j.1365-313x.2000.00893.x. PubMed DOI

Franco-Zorrilla J.M., Martín A.C., Leyva A., Paz-Ares J. Interaction between phosphate-starvation, sugar, and cytokinin signaling in Arabidopsis and the roles of cytokinin receptors CRE1/AHK4 and AHK3. Plant Physiol. 2005;138:847–857. doi: 10.1104/pp.105.060517. PubMed DOI PMC

Shin H., Shin H.S., Chen R., Harrison M.J. Loss of At4 function impacts phosphate distribution between the roots and the shoots during phosphate starvation. Plant J. 2006;45:712–726. doi: 10.1111/j.1365-313X.2005.02629.x. PubMed DOI

Wang X., Yi K., Tao Y., Wang F., Wu Z., Jiang D., Chen X., Zhu L., Wu P. Cytokinin represses phosphate-starvation response through increasing of intracellular phosphate level. Plant Cell Environ. 2006;29:1924–1935. doi: 10.1111/j.1365-3040.2006.01568.x. PubMed DOI

Shen C., Yue R., Yang Y., Zhang L., Sun T., Tie S., Wang H. OsARF16 Is Involved in Cytokinin-Mediated Inhibition of Phosphate Transport and Phosphate Signaling in Rice (Oryza sativa L.) PLoS ONE. 2014;9:e112906. doi: 10.1371/journal.pone.0112906. PubMed DOI PMC

Ribot C., Wang Y., Poirier Y. Expression analyses of three members of the AtPHO1 family reveal differential interactions between signaling pathways involved in phosphate deficiency and the responses to auxin, cytokinin, and abscisic acid. Planta. 2008;227:1025–1036. doi: 10.1007/s00425-007-0677-x. PubMed DOI

Lai F., Thacker J., Li Y., Doerner P. Cell division activity determines the magnitude of phosphate starvation responses in Arabidopsis. Plant J. 2007;50:545–556. doi: 10.1111/j.1365-313X.2007.03070.x. PubMed DOI

Schaller G.E., Bishopp A., Kieber J.J. The Yin-Yang of Hormones: Cytokinin and Auxin Interactions in Plant Development. Plant Cell Online. 2015;27:44–63. doi: 10.1105/tpc.114.133595. PubMed DOI PMC

Nam Y.J., Tran L.S.P., Kojima M., Sakakibara H., Nishiyama R., Shin R. Regulatory roles of cytokinins and cytokinin signaling in response to potassium deficiency in Arabidopsis. PLoS ONE. 2012;7:e47797. doi: 10.1371/journal.pone.0047797. PubMed DOI PMC

Schachtman D.P. The Role of Ethylene in Plant Responses to K+ Deficiency. Front. Plant Sci. 2015;6:1153. doi: 10.3389/fpls.2015.01153. PubMed DOI PMC

Rigas S., Ditengou F.A., Ljung K., Daras G., Tietz O., Palme K., Hatzopoulos P. Root gravitropism and root hair development constitute coupled developmental responses regulated by auxin homeostasis in the Arabidopsis root apex. New Phytol. 2013;197:1130–1141. doi: 10.1111/nph.12092. PubMed DOI

Koprivova A., Kopriva S. Sulfur metabolism and its manipulation in crops. J. Genet. Genom. 2016;43:623–629. doi: 10.1016/j.jgg.2016.07.001. PubMed DOI

Honsel A., Kojima M., Haas R., Frank W., Sakakibara H., Herschbach C., Rennenberg H. Sulphur limitation and early sulphur deficiency responses in poplar: Significance of gene expression, metabolites, and plant hormones. J. Exp. Bot. 2012;63:1873–1893. doi: 10.1093/jxb/err365. PubMed DOI PMC

Maruyama-Nakashita A., Nakamura Y., Yamaya T., Takahashi H. A novel regulatory pathway of sulfate uptake in Arabidopsis roots: Implication of CRE1/WOL/AHK4-mediated cytokinin-dependent regulation. Plant J. 2004;38:779–789. doi: 10.1111/j.1365-313X.2004.02079.x. PubMed DOI

Nguyen K.H., Ha C. Van, Nishiyama R., Watanabe Y., Leyva-González M.A., Fujita Y., Tran U.T., Li W., Tanaka M., Seki M., Schaller G.E., et al. Arabidopsis type B cytokinin response regulators ARR1, ARR10, and ARR12 negatively regulate plant responses to drought. Proc. Natl. Acad. Sci. USA. 2016;113:3090–3095. doi: 10.1073/pnas.1600399113. PubMed DOI PMC

Bhargava A., Clabaugh I., To J.P., Maxwell B.B., Chiang Y.H., Schaller G.E., Loraine A., Kieber J.J. Identification of cytokinin-responsive genes using microarray meta-analysis and RNA-Seq in Arabidopsis. Plant Physiol. 2013;162:272–294. doi: 10.1104/pp.113.217026. PubMed DOI PMC

Öztürk S.E., Göktay M., Has C., Babaoğlu M., Allmer J., Doğanlar S., Frary A. Transcriptomic analysis of boron hyperaccumulation mechanisms in Puccinellia distans. Chemosphere. 2018;199:390–401. doi: 10.1016/j.chemosphere.2018.02.070. PubMed DOI

González-Fontes A., Herrera-Rodríguez M.B., Martín-Rejano E.M., Navarro-Gochicoa M.T., Rexach J., Camacho-Cristóbal J.J. Root Responses to Boron Deficiency Mediated by Ethylene. Front. Plant Sci. 2015;6:1103. doi: 10.3389/fpls.2015.01103. PubMed DOI PMC

Yang C.Q., Liu Y.Z., An J.C., Li S., Jin L.F., Zhou G.F., Wei Q.J., Yan H.Q., Wang N.N., Fu L.N., et al. Digital gene expression analysis of corky split vein caused by boron deficiency in “Newhall” Navel Orange (Citrus sinensis Osbeck) for selecting differentially expressed genes related to vascular hypertrophy. PLoS ONE. 2013;8:e65737. doi: 10.1371/journal.pone.0065737. PubMed DOI PMC

Abreu I., Poza L., Bonilla I., Bolaños L. Boron deficiency results in early repression of a cytokinin receptor gene and abnormal cell differentiation in the apical root meristem of Arabidopsis thaliana. Plant Physiol. Biochem. 2014;77:117–121. doi: 10.1016/j.plaphy.2014.02.008. PubMed DOI

Eggert K., von Wirén N. Response of the plant hormone network to boron deficiency. New Phytol. 2017;216:868–881. doi: 10.1111/nph.14731. PubMed DOI

Poza-Viejo L., Abreu I., González-García M.P., Allauca P., Bonilla I., Bolaños L., Reguera M. Boron deficiency inhibits root growth by controlling meristem activity under cytokinin regulation. Plant Sci. 2018;270:176–189. doi: 10.1016/j.plantsci.2018.02.005. PubMed DOI

Séguéla M., Briat J.F., Vert G., Curie C. Cytokinins negatively regulate the root iron uptake machinery in Arabidopsis through a growth-dependent pathway. Plant J. 2008;55:289–300. doi: 10.1111/j.1365-313X.2008.03502.x. PubMed DOI

Shen C., Yue R., Sun T., Zhang L., Yang Y., Wang H. OsARF16, a transcription factor regulating auxin redistribution, is required for iron deficiency response in rice (Oryza sativa L.) Plant Sci. 2015;231:148–158. doi: 10.1016/j.plantsci.2014.12.003. PubMed DOI

Yin L., Wang S., Liu P., Wang W., Cao D., Deng X., Zhang S. Silicon-mediated changes in polyamine and 1-aminocyclopropane-1-carboxylic acid are involved in silicon-induced drought resistance in Sorghum bicolor L. Plant Physiol. Biochem. 2014;80:268–277. doi: 10.1016/j.plaphy.2014.04.014. PubMed DOI

Kim Y.H., Khan A.L., Waqas M., Jeong H.J., Kim D.H., Shin J.S., Kim J.G., Yeon M.H., Lee I.J. Regulation of jasmonic acid biosynthesis by silicon application during physical injury to Oryza sativa L. J. Plant Res. 2014;127:525–532. doi: 10.1007/s10265-014-0641-3. PubMed DOI

Hosseini S.A., Maillard A., Hajirezaei M.R., Ali N., Schwarzenberg A., Jamois F., Yvin J.C. Induction of Barley Silicon Transporter HvLsi1 and HvLsi2, increased silicon concentration in the shoot and regulated Starch and ABA Homeostasis under Osmotic stress and Concomitant Potassium Deficiency. Front. Plant Sci. 2017;8:1359. doi: 10.3389/fpls.2017.01359. PubMed DOI PMC

Markovich O., Steiner E., Kouřil Š., Tarkowski P., Aharoni A., Elbaum R. Silicon promotes cytokinin biosynthesis and delays senescence in Arabidopsis and Sorghum. Plant Cell Environ. 2017;40:1189–1196. doi: 10.1111/pce.12913. PubMed DOI

Hartikainen H. Biogeochemistry of selenium and its impact on food chain quality and human health. J. Trace Elem. Med. Biol. 2005;18:309–318. doi: 10.1016/j.jtemb.2005.02.009. PubMed DOI

Pilon-Smits E.A., Quinn C.F., Tapken W., Malagoli M., Schiavon M. Physiological functions of beneficial elements. Curr. Opin. Plant Biol. 2009;12:267–274. doi: 10.1016/j.pbi.2009.04.009. PubMed DOI

Schiavon M., Pilon-Smits E.A. The fascinating facets of plant selenium accumulation—Biochemistry, physiology, evolution and ecology. New Phytol. 2017;213:1582–1596. doi: 10.1111/nph.14378. PubMed DOI

Shibagaki N., Rose A., McDermott J.P., Fujiwara T., Hayashi H., Yoneyama T., Davies J.P. Selenate-resistant mutants of Arabidopsis thaliana identify Sultr1;2, a sulfate transporter required for efficient transport of sulfate into roots. Plant J. 2002;29:475–486. doi: 10.1046/j.0960-7412.2001.01232.x. PubMed DOI

Lehotai N., Kolbert Z., Peto A., Feigl G., Ördög A., Kumar D., Tari I., Erdei L. Selenite-induced hormonal and signalling mechanisms during root growth of Arabidopsis thaliana L. J. Exp. Bot. 2012;63:5677–5687. doi: 10.1093/jxb/ers222. PubMed DOI

Kolbert Z., Lehotai N., Molnár Á., Feigl G. “The roots” of selenium toxicity: A new concept. Plant Signal. Behav. 2016;11:e1241935. doi: 10.1080/15592324.2016.1241935. PubMed DOI PMC

Lehotai N., Feigl G., Koós Á., Molnár Á., Ördög A., Pető A., Erdei L., Kolbert Z. Nitric oxide–cytokinin interplay influences selenite sensitivity in Arabidopsis. Plant Cell Rep. 2016;35:2181–2195. doi: 10.1007/s00299-016-2028-5. PubMed DOI

Bruno L., Pacenza M., Forgione I., Lamerton L.R., Greco M., Chiappetta A., Bitonti M.B. In Arabidopsis thaliana Cadmium Impact on the Growth of Primary Root by Altering SCR Expression and Auxin-Cytokinin Cross-Talk. Front. Plant Sci. 2017;8:1323. doi: 10.3389/fpls.2017.01323. PubMed DOI PMC

Yang Z., Liu G., Liu J., Zhang B., Meng W., Müller B., Hayashi K., Zhang X., Zhao Z., De Smet I., Ding Z. Synergistic action of auxin and cytokinin mediates aluminum-induced root growth inhibition in Arabidopsis. EMBO Rep. 2017;18:1213–1230. doi: 10.15252/embr.201643806. PubMed DOI PMC

Gemrotová M., Kulkarni M.G., Stirk W.A., Strnad M., Van Staden J., Spíchal L. Seedlings of medicinal plants treated with either a cytokinin antagonist (PI-55) or an inhibitor of cytokinin degradation (INCYDE) are protected against the negative effects of cadmium. Plant Growth Regul. 2013;71:137–145. doi: 10.1007/s10725-013-9813-8. DOI

Fukudome A., Aksoy E., Wu X., Kumar K., Jeong I.S., May K., Russell W.K., Koiwa H. Arabidopsis CPL4 is an essential C-terminal domain phosphatase that suppresses xenobiotic stress responses. Plant J. 2014;80:27–39. doi: 10.1111/tpj.12612. PubMed DOI

Ramel F., Sulmon C., Cabello-Hurtado F., Taconnat L., Martin-Magniette M.L., Renou J.P., El Amrani A., Couée I., Gouesbet G. Genome-wide interacting effects of sucrose and herbicide-mediated stress in Arabidopsis thaliana: Novel insights into atrazine toxicity and sucrose-induced tolerance. BMC Genom. 2007;8:450. doi: 10.1186/1471-2164-8-450. PubMed DOI PMC

Ramel F., Sulmon C., Serra A.A., Gouesbet G., Couée I. Xenobiotic sensing and signalling in higher plants. J. Exp. Bot. 2012;63:3999–4014. doi: 10.1093/jxb/ers102. PubMed DOI

Brenner W.G., Schmulling T. Transcript profiling of cytokinin action in Arabidopsis roots and shoots discovers largely similar but also organ-specific responses. BMC Plant Biol. 2012;12:112. doi: 10.1186/1471-2229-12-112. PubMed DOI PMC

Brenner W.G., Schmülling T. Summarizing and exploring data of a decade of cytokinin-related transcriptomics. Front. Plant Sci. 2015;6:29. doi: 10.3389/fpls.2015.00029. PubMed DOI PMC

Daryanto S., Wang L., Jacinthe P.A. Global Synthesis of Drought Effects on Maize and Wheat Production. PLoS ONE. 2016;11:e0156362. doi: 10.1371/journal.pone.0156362. PubMed DOI PMC

Clauw P., Coppens F., De Beuf K., Dhondt S., Van Daele T., Maleux K., Storme V., Clement L., Gonzalez N., Inzé D. Leaf Responses to Mild Drought Stress in Natural Variants of Arabidopsis. Plant Physiol. 2015;167:800–816. doi: 10.1104/pp.114.254284. PubMed DOI PMC

Xu Y., Huang B. Effects of foliar-applied ethylene inhibitor and synthetic cytokinin on creeping bentgrass to enhance heat tolerance. Crop Sci. 2009;49:1876–1884. doi: 10.2135/cropsci2008.07.0441. DOI

Xu S., Brockmöller T., Navarro-Quezada A., Kuhl H., Gase K., Ling Z., Zhou W., Kreitzer C., Stanke M., Tang H., et al. Wild tobacco genomes reveal the evolution of nicotine biosynthesis. Proc. Natl. Acad. Sci. USA. 2017;114:6133–6138. doi: 10.1073/pnas.1700073114. PubMed DOI PMC

Le D.T., Nishiyama R., Watanabe Y., Vankova R., Tanaka M., Seki M., Ham L.H., Yamaguchi-Shinozaki K., Shinozaki K., Tran L.S.P. Identification and expression analysis of cytokinin metabolic genes in soybean under normal and drought conditions in relation to cytokinin levels. PLoS ONE. 2012;7:e42411. doi: 10.1371/journal.pone.0042411. PubMed DOI PMC

Dobra J., Motyka V., Dobrev P., Malbeck J., Prasil I.T., Haisel D., Gaudinova A., Havlova M., Gubis J., Vankova R. Comparison of hormonal responses to heat, drought and combined stress in tobacco plants with elevated proline content. J. Plant Physiol. 2010;167:1360–1370. doi: 10.1016/j.jplph.2010.05.013. PubMed DOI

Nishiyama R., Watanabe Y., Fujita Y., Le D.T., Kojima M., Werner T., Vankova R., Yamaguchi-Shinozaki K., Shinozaki K., Kakimoto T., et al. 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. 2011;23:2169–2183. doi: 10.1105/tpc.111.087395. PubMed DOI PMC

Bano A., Dorffling K., Bettin D., Hahn H. Abscisic acid and cytokinins as possible root-to-shoot signals in xylem sap of rice plants in drying soils. Funct. Plant Biol. 1993;20:109–115. doi: 10.1071/PP9930109. DOI

Argueso C.T., Ferreira F.J., Kieber J.J. Environmental perception avenues: The interaction of cytokinin and environmental response pathways. Plant Cell Environ. 2009;32:1147–1160. doi: 10.1111/j.1365-3040.2009.01940.x. PubMed DOI

Tran L.S., Urao T., Qin F., Maruyama K., Kakimoto T., Shinozaki K., Yamaguchi-Shinozaki K. Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2007;104:20623–20628. doi: 10.1073/pnas.0706547105. PubMed DOI PMC

Jang G., Chang S.H., Um T.Y., Lee S., Kim J.K., Choi Y.D. Antagonistic interaction between jasmonic acid and cytokinin in xylem development. Sci. Rep. 2017;7:10212. doi: 10.1038/s41598-017-10634-1. PubMed DOI PMC

Huang X., Hou L., Meng J., You H., Li Z., Gong Z., Yang S., Shi Y. The Antagonistic Action of Abscisic Acid and Cytokinin Signaling Mediates Drought Stress Response in Arabidopsis. Mol. Plant. 2018;11:970–982. doi: 10.1016/j.molp.2018.05.001. PubMed DOI

Rivero R.M., Ruiz J.M., García P.C., López-Lefebre L.R., Sánchez E., Romero L. Resistance to cold and heat stress: Accumulation of phenolic compounds in tomato and watermelon plants. Plant Sci. 2001;160:315–321. doi: 10.1016/S0168-9452(00)00395-2. PubMed DOI

Ghanem M.E., Albacete A., Smigocki A.C., Frébort I., Pospísilová H., Martínez-Andújar C., Acosta M., Sánchez-Bravo J., Lutts S., Dodd I.C., Pérez-Alfocea F. Root-synthesized cytokinins improve shoot growth and fruit yield in salinized tomato (Solanum lycopersicum L.) plants. J. Exp. Bot. 2011;62:125–140. doi: 10.1093/jxb/erq266. PubMed DOI PMC

Rivero R.M., Kojima M., Gepstein A., Sakakibara H., Mittler R., Gepstein S., Blumwald E. Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc. Natl. Acad. Sci. USA. 2007;104:19631–19636. doi: 10.1073/pnas.0709453104. PubMed DOI PMC

Rivero R.M., Gimeno J., Van Deynze A., Walia H., Blumwald E. Enhanced Cytokinin Synthesis in Tobacco Plants Expressing PSARK::IPT Prevents the Degradation of Photosynthetic Protein Complexes During Drought. Plant Cell Physiol. 2010;51:1929–1941. doi: 10.1093/pcp/pcq143. PubMed DOI

Reguera M., Peleg Z., Abdel-Tawab Y.M., Tumimbang E.B., Delatorre C.A., Blumwald E. Stress-Induced Cytokinin Synthesis Increases Drought Tolerance through the Coordinated Regulation of Carbon and Nitrogen Assimilation in Rice. Plant Physiol. 2013;163:1609–1622. doi: 10.1104/pp.113.227702. PubMed DOI PMC

Ma X., Zhang J., Huang B. Cytokinin-mitigation of salt-induced leaf senescence in perennial ryegrass involving the activation of antioxidant systems and ionic balance. Environ. Exp. Bot. 2016;125:1–11. doi: 10.1016/j.envexpbot.2016.01.002. DOI

Décima Oneto C., Otegui M.E., Baroli I., Beznec A., Faccio P., Bossio E., Blumwald E., Lewi D. Water deficit stress tolerance in maize conferred by expression of an isopentenyltransferase (IPT) gene driven by a stress- and maturation-induced promoter. J. Biotechnol. 2016;220:66–77. doi: 10.1016/j.jbiotec.2016.01.014. PubMed DOI

Vojta P., Kokáš F., Husičková A., Grúz J., Bergougnoux V., Marchetti C.F., Jiskrová E., Ježilová E., Mik V., Ikeda Y., Galuszka P. Whole transcriptome analysis of transgenic barley with altered cytokinin homeostasis and increased tolerance to drought stress. New Biotechnol. 2016;33:676–691. doi: 10.1016/j.nbt.2016.01.010. PubMed DOI

Ramireddy E., Hosseini S.A., Eggert K., Gillandt S., Gnad H., von Wirén N., Schmülling T. Root Engineering in Barley: Increasing Cytokinin Degradation Produces a Larger Root System, Mineral Enrichment in the Shoot and Improved Drought Tolerance. Plant Physiol. 2018;177:1078–1095. doi: 10.1104/pp.18.00199. PubMed DOI PMC

Černý M., Kuklová A., Hoehenwarter W., Fragner L., Novák O., Rotková G., Jedelský P.L.P. L., Žáková K. K., Šmehilová M., Strnad M., et al. Proteome and metabolome profiling of cytokinin action in Arabidopsis identifying both distinct and similar responses to cytokinin down- and up-regulation. J. Exp. Bot. 2013;64:4193–4206. doi: 10.1093/jxb/ert227. PubMed DOI PMC

Zavaleta-Mancera H.A., López-Delgado H., Loza-Tavera H., Mora-Herrera M., Trevilla-García C., Vargas-Suárez M., Ougham H. Cytokinin promotes catalase and ascorbate peroxidase activities and preserves the chloroplast integrity during dark-senescence. J. Plant Physiol. 2007;164:1572–1582. doi: 10.1016/j.jplph.2007.02.003. PubMed DOI

Ma X., Zhang J., Burgess P., Rossi S., Huang B. Interactive effects of melatonin and cytokinin on alleviating drought-induced leaf senescence in creeping bentgrass (Agrostis stolonifera) Environ. Exp. Bot. 2018;145:1–11. doi: 10.1016/j.envexpbot.2017.10.010. DOI

Liao X., Guo X., Wang Q., Wang Y., Zhao D., Yao L., Wang S., Liu G., Li T. Overexpression of MsDREB6.2 results in cytokinin-deficient developmental phenotypes and enhances drought tolerance in transgenic apple plants. Plant J. 2017;89:510–526. doi: 10.1111/tpj.13401. PubMed DOI

Nakabayashi R., Yonekura-Sakakibara K., Urano K., Suzuki M., Yamada Y., Nishizawa T., Matsuda F., Kojima M., Sakakibara H., Shinozaki K., et al. Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. Plant J. 2014;77:367–379. doi: 10.1111/tpj.12388. PubMed DOI PMC

Novák J., Pavlů J., Novák O., Nožková-Hlaváčková V., Špundová M., Hlavinka J., Koukalová Š., Skalák J., Černý M., Brzobohatý B. High cytokinin levels induce a hypersensitive-like response in tobacco. Ann. Bot. 2013;112:41–55. doi: 10.1093/aob/mct092. PubMed DOI PMC

White R.G., Kirkegaard J.A. The distribution and abundance of wheat roots in a dense, structured subsoil—Implications for water uptake. Plant Cell Environ. 2010;33:133–148. doi: 10.1111/j.1365-3040.2009.02059.x. PubMed DOI

Novák J., Černý M., Pavlů J., Zemánková J., Skalák J., Plačková L., Brzobohatý B. Roles of proteome dynamics and cytokinin signaling in root to hypocotyl ratio changes induced by shading roots of Arabidopsis seedlings. Plant Cell Physiol. 2015;56:1006–1018. doi: 10.1093/pcp/pcv026. PubMed DOI

Laplaze L., Benkova E., Casimiro I., Maes L., Vanneste S., Swarup R., Weijers D., Calvo V., Parizot B., Herrera-Rodriguez M.B., et al. Cytokinins act directly on lateral root founder cells to inhibit root initiation. Plant Cell. 2007;19:3889–3900. doi: 10.1105/tpc.107.055863. PubMed DOI PMC

Pospíšilová H., Jiskrová E., Vojta P., Mrízová K., Kokáš F., Čudejková M.M., Bergougnoux V., Plíhal O., Klimešová J., Novák O., et al. Transgenic barley overexpressing a cytokinin dehydrogenase gene shows greater tolerance to drought stress. New Biotechnol. 2016;33:692–705. doi: 10.1016/j.nbt.2015.12.005. PubMed DOI

Jang G., Choi Y.D. Drought stress promotes xylem differentiation by modulating the interaction between cytokinin and jasmonic acid. Plant Signal. Behav. 2018;13:e1451707. doi: 10.1080/15592324.2018.1451707. PubMed DOI PMC

Guan C., Wang X., Feng J., Hong S., Liang Y., Ren B., Zuo J. Cytokinin Antagonizes Abscisic Acid-Mediated Inhibition of Cotyledon Greening by Promoting the Degradation of ABSCISIC ACID INSENSITIVE5 Protein in Arabidopsis. Plant Physiol. 2014;164:1515–1526. doi: 10.1104/pp.113.234740. PubMed DOI PMC

Huang Y., Sun M.M., Ye Q., Wu X.Q., Wu W.H., Chen Y.F. Abscisic Acid Modulates Seed Germination via ABA INSENSITIVE5-Mediated PHOSPHATE1. Plant Physiol. 2017;175:1661–1668. doi: 10.1104/pp.17.00164. PubMed DOI PMC

Yang C.Y., Huang Y.C., Ou S.L. ERF73/HRE1 is involved in H2O2 production via hypoxia-inducible Rboh gene expression in hypoxia signaling. Protoplasma. 2017;254:1705–1714. doi: 10.1007/s00709-016-1064-x. PubMed DOI

Nguyen T.Q., Emery R.J.N. Is ABA the earliest upstream inhibitor of apical dominance? J. Exp. Bot. 2017;68:881–884. doi: 10.1093/jxb/erx028. DOI

Prerostova S., Dobrev P.I., Gaudinova A., Knirsch V., Körber N., Pieruschka R., Fiorani F., Brzobohatý B., Černý M., Spichal L., et al. Cytokinins: Their Impact on Molecular and Growth Responses to Drought Stress and Recovery in Arabidopsis. Front. Plant Sci. 2018;9:655. doi: 10.3389/fpls.2018.00655. PubMed DOI PMC

Fu J., Wu H., Ma S., Xiang D., Liu R., Xiong L. OsJAZ1 Attenuates Drought Resistance by Regulating JA and ABA Signaling in Rice. Front. Plant Sci. 2017;8:2108. doi: 10.3389/fpls.2017.02108. PubMed DOI PMC

Ahmad P., Rasool S., Gul A., Sheikh S.A., Akram N.A., Ashraf M., Kazi A.M., Gucel S. Jasmonates: Multifunctional Roles in Stress Tolerance. Front. Plant Sci. 2016;7:813. doi: 10.3389/fpls.2016.00813. PubMed DOI PMC

Veselova S.V., Farhutdinov R.G., Veselov S.Y., Kudoyarova G.R., Veselov D.S., Hartung W. The effect of root cooling on hormone content, leaf conductance and root hydraulic conductivity of durum wheat seedlings (Triticum durum L.) J. Plant Physiol. 2005;162:21–26. doi: 10.1016/j.jplph.2004.06.001. PubMed DOI

Ntatsi G., Savvas D., Papasotiropoulos V., Katsileros A., Zrenner R.M., Hincha D.K., Zuther E., Schwarz D. Rootstock Sub-Optimal Temperature Tolerance Determines Transcriptomic Responses after Long-Term Root Cooling in Rootstocks and Scions of Grafted Tomato Plants. Front. Plant Sci. 2017;8:911. doi: 10.3389/fpls.2017.00911. PubMed DOI PMC

Maruyama K., Urano K., Yoshiwara K., Morishita Y., Sakurai N., Suzuki H., Kojima M., Sakakibara H., Shibata D., Saito K., et al. Integrated Analysis of the Effects of Cold and Dehydration on Rice Metabolites, Phytohormones, and Gene Transcripts. Plant Physiol. 2014;164:1759–1771. doi: 10.1104/pp.113.231720. PubMed DOI PMC

Li S., Yang Y., Zhang Q., Liu N., Xu Q., Hu L. Differential physiological and metabolic response to low temperature in two zoysiagrass genotypes native to high and low latitude. PLoS ONE. 2018;13:e0198885. doi: 10.1371/journal.pone.0198885. PubMed DOI PMC

Jeon J., Kim N.Y., Kim S., Kang N.Y., Novák O., Ku S.J., Cho C., Lee D.J., Lee E.J., Strnad M., Kim J. A subset of cytokinin two-component signaling system plays a role in cold temperature stress response in Arabidopsis. J. Biol. Chem. 2010;285:23371–23386. doi: 10.1074/jbc.M109.096644. PubMed DOI PMC

Shi Y., Tian S., Hou L., Huang X., Zhang X., Guo H., Yang S. Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-A ARR genes in Arabidopsis. Plant Cell. 2012;24:2578–2595. doi: 10.1105/tpc.112.098640. PubMed DOI PMC

Kang N.Y., Cho C., Kim J. Inducible Expression of Arabidopsis Response Regulator 22 (ARR22), a Type-C ARR, in Transgenic Arabidopsis Enhances Drought and Freezing Tolerance. PLoS ONE. 2013;8:e79248. doi: 10.1371/journal.pone.0079248. PubMed DOI PMC

Zwack P.J., Compton M.A., Adams C.I., Rashotte A.M. Cytokinin response factor 4 (CRF4) is induced by cold and involved in freezing tolerance. Plant Cell Rep. 2016;35:573–584. doi: 10.1007/s00299-015-1904-8. PubMed DOI

Jeon J., Cho C., Lee M.R., Van Binh N., Kim J. CYTOKININ RESPONSE FACTOR2 (CRF2) and CRF3 Regulate Lateral Root Development in Response to Cold Stress in Arabidopsis. Plant Cell. 2016;28:1828–1843. doi: 10.1105/tpc.15.00909. PubMed DOI PMC

Dobrá J., Černý M., Štorchová H., Dobrev P., Skalák J., Jedelský P.L., Lukšanová H., Gaudinová A., Pešek B., Malbecka J., et al. The impact of heat stress targeting on the hormonal and transcriptomic response in Arabidopsis. Plant Sci. 2015;231:52–61. doi: 10.1016/j.plantsci.2014.11.005. PubMed DOI

Skalák J., Černý M., Jedelský P., Dobrá J., Ge E., Novák J., Hronková M., Dobrev P., Vanková R., Brzobohatý B. Stimulation of ipt overexpression as a tool to elucidate the role of cytokinins in high temperature responses of Arabidopsis thaliana. J. Exp. Bot. 2016;67:2861–2873. doi: 10.1093/jxb/erw129. PubMed DOI PMC

Černý M., Jedelský P.L., Novák J., Schlosser A., Brzobohatý B. Cytokinin modulates proteomic, transcriptomic and growth responses to temperature shocks in Arabidopsis. Plant Cell Environ. 2014;37:1641–1655. doi: 10.1111/pce.12270. PubMed DOI

Escandón M., Cañal M.J., Pascual J., Pinto G., Correia B., Amaral J., Meijón M. Integrated physiological and hormonal profile of heat-induced thermotolerance in Pinus radiata. Tree Physiol. 2016;36:63–77. doi: 10.1093/treephys/tpv127. PubMed DOI

Escandón M., Meijón M., Valledor L., Pascual J., Pinto G., Cañal M.J. Metabolome Integrated Analysis of High-Temperature Response in Pinus radiata. Front. Plant Sci. 2018;9:485. doi: 10.3389/fpls.2018.00485. PubMed DOI PMC

Lochmanová G., Zdráhal Z., Konečná H., Koukalová Š., Malbeck J., Souček P., Válková M., Kiran N.S., Brzobohatý B. Cytokinin-induced photomorphogenesis in dark-grown Arabidopsis: A proteomic analysis. J. Exp. Bot. 2008;59:3705–3719. doi: 10.1093/jxb/ern220. PubMed DOI

Černý M., Dyčka F., Bobáľová J., Brzobohatý B. Early cytokinin response proteins and phosphoproteins of Arabidopsis thaliana identified by proteome and phosphoproteome profiling. J. Exp. Bot. 2011;62:921–937. doi: 10.1093/jxb/erq322. PubMed DOI PMC

Macková H., Hronková M., Dobrá J., Turečková V., Novák O., Lubovská Z., Motyka V., Haisel D., Hájek T., Prášil I.T., et al. Enhanced drought and heat stress tolerance of tobacco plants with ectopically enhanced cytokinin oxidase/dehydrogenase gene expression. J. Exp. Bot. 2013;64:2805–2815. doi: 10.1093/jxb/ert131. PubMed DOI PMC

Danilova M.N., Kudryakova N.V., Doroshenko A.S., Zabrodin D.A., Vinogradov N.S., Kuznetsov V.V. Molecular and physiological responses of Arabidopsis thaliana plants deficient in the genes responsible for ABA and cytokinin reception and metabolism to heat shock. Russ. J. Plant Physiol. 2016;63:308–318. doi: 10.1134/S1021443716030043. DOI

Yang Y., Jiang Y., Mi X., Gan L., Gu T., Ding J., Li Y. Identification and expression analysis of cytokinin response regulators in Fragaria vesca. Acta Physiol. Plant. 2016;38:198. doi: 10.1007/s11738-016-2213-8. DOI

Mi X., Wang X., Wu H., Gan L., Ding J., Li Y. Characterization and expression analysis of cytokinin biosynthesis genes in Fragaria vesca. Plant Growth Regul. 2017;82:139–149. doi: 10.1007/s10725-016-0246-z. DOI

Cortleven A., Schmülling T. Regulation of chloroplast development and function by cytokinin. J. Exp. Bot. 2015;66:4999–5013. doi: 10.1093/jxb/erv132. PubMed DOI

Sweere U., Eichenberg K., Lohrmann J., Mira-Rodado V., Bäurle I., Kudla J., Nagy F., Schafer E., Harter K. Interaction of the response regulator ARR4 with phytochrome B in modulating red light signaling. Science. 2001;294:1108–1111. doi: 10.1126/science.1065022. PubMed DOI

Chi W., Li J., He B., Chai X., Xu X., Sun X., Jiang J., Feng P., Zuo J., Lin R., et al. DEG9, a serine protease, modulates cytokinin and light signaling by regulating the level of ARABIDOPSIS RESPONSE REGULATOR 4. Proc. Natl. Acad. Sci. USA. 2016;113:E3568–E3576. doi: 10.1073/pnas.1601724113. PubMed DOI PMC

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

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

Edwards K.D., Takata N., Johansson M., Jurca M., Novák O., Hényková E., Liverani S., Kozarewa I., Strnad M., Millar A.J., et al. Circadian clock components control daily growth activities by modulating cytokinin levels and cell division-associated gene expression in Populus trees. Plant Cell Environ. 2018;41:1468–1482. doi: 10.1111/pce.13185. 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

Janečková H., Husičková A., Ferretti U., Prčina M., Pilařová E., Plačková L., Pospíšil P., Doležal K., Špundová M. The interplay between cytokinins and light during senescence in detached Arabidopsis leaves. Plant Cell Environ. 2018;41:1870–1885. doi: 10.1111/pce.13329. PubMed DOI

Vandenbussche F., Habricot Y., Condiff A.S., Maldiney R., Van der Straeten D., Ahmad M. HY5 is a point of convergence between cryptochrome and cytokinin signalling pathways in Arabidopsis thaliana. Plant J. 2007;49:428–441. doi: 10.1111/j.1365-313X.2006.02973.x. PubMed DOI

Cortleven A., Nitschke S., Klaumunzer M., AbdElgawad H., Asard H., Grimm B., Riefler M., Schmulling T. 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. 2014;164:1470–1483. doi: 10.1104/pp.113.224667. PubMed DOI PMC

Danilova M.N., Kudryakova N.V., Voronin P.Y., Oelmüller R., Kusnetsov V.V., Kulaeva O.N. Membrane receptors of cytokinin and their regulatory role in Arabidopsis thaliana plant response to photooxidative stress under conditions of water deficit. Russ. J. Plant Physiol. 2014;61:434–442. doi: 10.1134/S1021443714040062. DOI

Bashri G., Singh M., Mishra R.K., Kumar J., Singh V.P., Prasad S.M. Kinetin Regulates UV-B-Induced Damage to Growth, Photosystem II Photochemistry, and Nitrogen Metabolism in Tomato Seedlings. J. Plant Growth Regul. 2018;37:233–245. doi: 10.1007/s00344-017-9721-7. DOI

Patterson K., Cakmak T., Cooper A., Lager I., Rasmusson A.G., Escobar M.A. Distinct signalling pathways and transcriptome response signatures differentiate ammonium- and nitrate-supplied plants. Plant Cell Environ. 2010;33:1486–14501. doi: 10.1111/j.1365-3040.2010.02158.x. PubMed DOI PMC

Canales J., Moyano T.C., Villarroel E., Gutiérrez R.A. Systems analysis of transcriptome data provides new hypotheses about Arabidopsis root response to nitrate treatments. Front. Plant Sci. 2014;5:22. doi: 10.3389/fpls.2014.00022. PubMed DOI PMC

Krapp A., Berthome R., Orsel M., Mercey-Boutet S., Yu A., Castaings L., Elftieh S., Major H., Renou J.-P., Daniel-Vedele F. Arabidopsis Roots and Shoots Show Distinct Temporal Adaptation Patterns toward Nitrogen Starvation. Plant Physiol. 2011;157:1255–1282. doi: 10.1104/pp.111.179838. PubMed DOI PMC

Kiba T., Inaba J., Kudo T., Ueda N., Konishi M., Mitsuda N., Takiguchi Y., Kondou Y., Yoshizumi T., Ohme-Takagi M., et al. Repression of Nitrogen Starvation Responses by Members of the Arabidopsis GARP-Type Transcription Factor NIGT1/HRS1 Subfamily. Plant Cell. 2018;30:925–945. doi: 10.1105/tpc.17.00810. PubMed DOI PMC

Pant B.D., Musialak-Lange M., Nuc P., May P., Buhtz A., Kehr J., Walther D., Scheible W.-R. Identification of Nutrient-Responsive Arabidopsis and Rapeseed MicroRNAs by Comprehensive Real-Time Polymerase Chain Reaction Profiling and Small RNA Sequencing. Plant Physiol. 2009;150:1541–1555. doi: 10.1104/pp.109.139139. PubMed DOI PMC

Zhao M., Ding H., Zhu J.K., Zhang F., Li W.X. Involvement of miR169 in the nitrogen-starvation responses in Arabidopsis. New Phytol. 2011;190:906–915. doi: 10.1111/j.1469-8137.2011.03647.x. PubMed DOI PMC

Konishi N., Ishiyama K., Matsuoka K., Maru I., Hayakawa T., Yamaya T., Kojima S. NADH-dependent glutamate synthase plays a crucial role in assimilating ammonium in the Arabidopsis root. Physiol. Plant. 2014;152:138–151. doi: 10.1111/ppl.12177. PubMed DOI

Bi Y.M., Wang R.L., Zhu T., Rothstein S.J. Global transcription profiling reveals differential responses to chronic nitrogen stress and putative nitrogen regulatory components in Arabidopsis. BMC Genom. 2007;8:281. doi: 10.1186/1471-2164-8-281. PubMed DOI PMC

Canales J., Rueda-López M., Craven-Bartle B., Avila C., Cánovas F.M. Novel Insights into Regulation of Asparagine Synthetase in Conifers. Front. Plant Sci. 2012;3:100. doi: 10.3389/fpls.2012.00100. PubMed DOI PMC

Alvarez J.M., Riveras E., Vidal E.A., Gras D.E., Contreras-López O., Tamayo K.P., Aceituno F., Gómez I., Ruffel S., Lejay L., et al. Systems approach identifies TGA1 and TGA4 transcription factors as important regulatory components of the nitrate response of Arabidopsis thaliana roots. Plant J. 2014;80:1–13. doi: 10.1111/tpj.12618. PubMed DOI

Konishi M., Yanagisawa S. Arabidopsis NIN-like transcription factors have a central role in nitrate signalling. Nat. Commun. 2013;4:1617. doi: 10.1038/ncomms2621. PubMed DOI

Rubin G., Tohge T., Matsuda F., Saito K., Scheible W.R. Members of the LBD Family of Transcription Factors Repress Anthocyanin Synthesis and Affect Additional Nitrogen Responses in Arabidopsis. Plant Cell. 2009;21:3567–3584. doi: 10.1105/tpc.109.067041. PubMed DOI PMC

Jost R., Pharmawati M., Lapis-Gaza H.R., Rossig C., Berkowitz O., Lambers H., Finnegan P.M. Differentiating phosphate-dependent and phosphate-independent systemic phosphate-starvation response networks in Arabidopsis thaliana through the application of phosphite. J. Exp. Bot. 2015;66:2501–2514. doi: 10.1093/jxb/erv025. PubMed DOI PMC

Hammond J.P., Bennett M.J., Bowen H.C., Broadley M.R., Eastwood D.C., May S.T., Rahn C., Swarup R., Woolaway K.E., White P.J. Changes in Gene Expression in Arabidopsis Shoots during Phosphate Starvation and the Potential for Developing Smart Plants. Plant Physiol. 2003;132:578–596. doi: 10.1104/pp.103.020941. PubMed DOI PMC

Ayadi A., David P., Arrighi J.F., Chiarenza S., Thibaud M.C., Nussaume L., Marin E. Reducing the Genetic Redundancy of Arabidopsis PHOSPHATE TRANSPORTER1 Transporters to Study Phosphate Uptake and Signaling. Plant Physiol. 2015;167:1511–1526. doi: 10.1104/pp.114.252338. PubMed DOI PMC

Gu M., Chen A., Sun S., Xu G. Complex Regulation of Plant Phosphate Transporters and the Gap between Molecular Mechanisms and Practical Application: What Is Missing? Mol. Plant. 2016;9:396–416. doi: 10.1016/j.molp.2015.12.012. PubMed DOI

Lapis-Gaza H.R., Jost R., Finnegan P.M. Arabidopsis PHOSPHATE TRANSPORTER1 genes PHT1;8 and PHT1;9 are involved in root-to-shoot translocation of orthophosphate. BMC Plant Biol. 2014;14:334. doi: 10.1186/s12870-014-0334-z. PubMed DOI PMC

Puga M.I., Mateos I., Charukesi R., Wang Z., Franco-Zorrilla J.M., de Lorenzo L., Irigoyen M.L., Masiero S., Bustos R., Rodriguez J., et al. SPX1 is a phosphate-dependent inhibitor of PHOSPHATE STARVATION RESPONSE 1 in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2014;111:14947–14952. doi: 10.1073/pnas.1404654111. PubMed DOI PMC

Maruyama-Nakashita A., Nakamura Y., Tohge T., Saito K., Takahashi H. Arabidopsis SLIM1 is a central transcriptional regulator of plant sulfur response and metabolism. Plant Cell. 2006;18:3235–3251. doi: 10.1105/tpc.106.046458. PubMed DOI PMC

Bielecka M., Watanabe M., Morcuende R., Scheible W.R., Hawkesford M.J., Hesse H., Hoefgen R. Transcriptome and metabolome analysis of plant sulfate starvation and resupply provides novel information on transcriptional regulation of metabolism associated with sulfur, nitrogen and phosphorus nutritional responses in Arabidopsis. Front. Plant Sci. 2014;5:805. doi: 10.3389/fpls.2014.00805. PubMed DOI PMC

Nikiforova V., Freitag J., Kempa S., Adamik M., Hesse H., Hoefgen R. Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: Interlacing of biosynthetic pathways provides response specificity. Plant J. 2003;33:633–650. doi: 10.1046/j.1365-313X.2003.01657.x. PubMed DOI

Kopriva S., Calderwood A., Weckopp S.C., Koprivova A. Plant sulfur and Big Data. Plant Sci. 2015;241:1–10. doi: 10.1016/j.plantsci.2015.09.014. PubMed DOI

Zhang B., Pasini R., Dan H., Joshi N., Zhao Y., Leustek T., Zheng Z.L. Aberrant gene expression in the Arabidopsis SULTR1;2 mutants suggests a possible regulatory role for this sulfate transporter in response to sulfur nutrient status. Plant J. 2014;77:185–197. doi: 10.1111/tpj.12376. PubMed DOI

Henríquez-Valencia C., Arenas-M A., Medina J., Canales J. Integrative Transcriptomic Analysis Uncovers Novel Gene Modules That Underlie the Sulfate Response in Arabidopsis thaliana. Front. Plant Sci. 2018;9:470. doi: 10.3389/fpls.2018.00470. PubMed DOI PMC

Kawashima C.G., Berkowitz O., Hell R., Noji M., Saito K. Characterization and expression analysis of a serine acetyltransferase gene family involved in a key step of the sulfur assimilation pathway in Arabidopsis. Plant Physiol. 2005;137:220–230. doi: 10.1104/pp.104.045377. PubMed DOI PMC

Forieri I., Sticht C., Reichelt M., Gretz N., Hawkesford M.J., Malagoli M., Wirtz M., Hell R. System analysis of metabolism and the transcriptome in Arabidopsis thaliana roots reveals differential co-regulation upon iron, sulfur and potassium deficiency. Plant Cell Environ. 2017;40:95–107. doi: 10.1111/pce.12842. PubMed DOI

Chen D., Cao B., Wang S., Liu P., Deng X., Yin L., Zhang S. Silicon moderated the K deficiency by improving the plant-water status in sorghum. Sci. Rep. 2016;6:22882. doi: 10.1038/srep22882. PubMed DOI PMC

Gierth M., Mäser P., Schroeder J.I. The Potassium Transporter AtHAK5 Functions in K+ Deprivation-Induced High-Affinity K+ Uptake and AKT1 K+ Channel Contribution to K+ Uptake Kinetics in Arabidopsis Roots. Plant Physiol. 2005;137:1105–1114. doi: 10.1104/pp.104.057216. PubMed DOI PMC

Pyo Y.J., Gierth M., Schroeder J.I., Cho M.H. High-Affinity K+ Transport in Arabidopsis: AtHAK5 and AKT1 Are Vital for Seedling Establishment and Postgermination Growth under Low-Potassium Conditions. Plant Physiol. 2010;153:863–875. doi: 10.1104/pp.110.154369. PubMed DOI PMC

Ragel P., Ródenas R., García-Martín E., Andrés Z., Villalta I., Nieves-Cordones M., Rivero R.M., Martínez V., Pardo J.M., Quintero F.J., Rubio F. CIPK23 regulates HAK5-mediated high-affinity K+ uptake in Arabidopsis roots. Plant Physiol. 2015;169:01401.2015. doi: 10.1104/pp.15.01401. PubMed DOI PMC

Osakabe Y., Arinaga N., Umezawa T., Katsura S., Nagamachi K., Tanaka H., Ohiraki H., Yamada K., Seo S.-U., Abo M., et al. Osmotic Stress Responses and Plant Growth Controlled by Potassium Transporters in Arabidopsis. Plant Cell. 2013;25:609–624. doi: 10.1105/tpc.112.105700. PubMed DOI PMC

Pilot G., Gaymard F., Mouline K., Chérel I., Sentenac H. Regulated expression of Arabidopsis shaker K+ channel genes involved in K+ uptake and distribution in the plant. Plant Mol. Biol. 2003;51:773–787. doi: 10.1023/A:1022597102282. PubMed DOI

Wang Y., Wu W.H. Regulation of potassium transport and signaling in plants. Curr. Opin. Plant Biol. 2017;39:123–128. doi: 10.1016/j.pbi.2017.06.006. PubMed DOI

Rigas S., Debrosses G., Haralampidis K., Vicente-Agullo F., Feldmann K.A., Grabov A., Dolan L., Hatzopoulos P. TRH1 encodes a potassium transporter required for tip growth in Arabidopsis root hairs. Plant Cell. 2001;13:139–151. doi: 10.1105/tpc.13.1.139. PubMed DOI PMC

Han M., Wu W., Wu W.-H., Wang Y. Potassium Transporter KUP7 Is Involved in K+ Acquisition and Translocation in Arabidopsis Root under K+ -Limited Conditions. Mol. Plant. 2016;9:437–446. doi: 10.1016/j.molp.2016.01.012. PubMed DOI

Armengaud P., Breitling R., Amtmann A. The Potassium-Dependent Transcriptome of Arabidopsis Reveals a Prominent Role of Jasmonic Acid in Nutrient Signaling. Plant Physiol. 2004;136:2556–2576. doi: 10.1104/pp.104.046482. PubMed DOI PMC

Li W., Lan P. The Understanding of the Plant Iron Deficiency Responses in Strategy I Plants and the Role of Ethylene in This Process by Omic Approaches. Front. Plant Sci. 2017;8:40. doi: 10.3389/fpls.2017.00040. PubMed DOI PMC

Mai H.J., Pateyron S., Bauer P. Iron homeostasis in Arabidopsis thaliana: Transcriptomic analyses reveal novel FIT-regulated genes, iron deficiency marker genes and functional gene networks. BMC Plant Biol. 2016;16:211. doi: 10.1186/s12870-016-0899-9. PubMed DOI PMC

Stein R.J., Waters B.M. Use of natural variation reveals core genes in the transcriptome of iron-deficient Arabidopsis thaliana roots. J. Exp. Bot. 2012;63:1039–1055. doi: 10.1093/jxb/err343. PubMed DOI PMC

Mendoza-Cózatl D.G., Xie Q., Akmakjian G.Z., Jobe T.O., Patel A., Stacey M.G., Song L., Demoin D.W., Jurisson S.S., Stacey G., Schroeder J.I. OPT3 Is a Component of the Iron-Signaling Network between Leaves and Roots and Misregulation of OPT3 Leads to an Over-Accumulation of Cadmium in Seeds. Mol. Plant. 2014;7:1455–1469. doi: 10.1093/mp/ssu067. PubMed DOI PMC

Takano J., Noguchi K., Yasumori M., Kobayashi M., Gajdos Z., Miwa K., Hayashi H., Yoneyama T., Fujiwara T. Arabidopsis boron transporter for xylem loading. Nature. 2002;420:337–340. doi: 10.1038/nature01139. PubMed DOI

Miwa K., Aibara I., Fujiwara T. Arabidopsis thaliana BOR4 is upregulated under high boron conditions and confers tolerance to high boron. Soil Sci. Plant Nutr. 2014;60:349–355. doi: 10.1080/00380768.2013.866524. DOI

Msanne J., Lin J., Stone J.M., Awada T. Characterization of abiotic stress-responsive Arabidopsis thaliana RD29A and RD29B genes and evaluation of transgenes. Planta. 2011;234:97–107. doi: 10.1007/s00425-011-1387-y. PubMed DOI

Huang K.C., Lin W.C., Cheng W.H. Salt hypersensitive mutant 9, a nucleolar APUM23 protein, is essential for salt sensitivity in association with the ABA signaling pathway in Arabidopsis. BMC Plant Biol. 2018;18:40. doi: 10.1186/s12870-018-1255-z. PubMed DOI PMC

Vogel J.T., Zarka D.G., Van Buskirk H.A., Fowler S.G., Thomashow M.F. Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J. 2005;41:195–211. doi: 10.1111/j.1365-313X.2004.02288.x. PubMed DOI

Lee B., Henderson D.A., Zhu J.K. The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell. 2005;17:3155–3175. doi: 10.1105/tpc.105.035568. PubMed DOI PMC

Maruyama K., Sakuma Y., Kasuga M., Ito Y., Seki M., Goda H., Shimada Y., Yoshida S., Shinozaki K., Yamaguchi-Shinozaki K. Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. Plant J. 2004;38:982–993. doi: 10.1111/j.1365-313X.2004.02100.x. PubMed DOI

Nakaminami K., Matsui A., Nakagami H., Minami A., Nomura Y., Tanaka M., Morosawa T., Ishida J., Takahashi S., Uemura M., et al. Analysis of differential expression patterns of mRNA and protein during cold-acclimation and de-acclimation in Arabidopsis. Mol. Cell. Proteom. 2014;13:3602–3611. doi: 10.1074/mcp.M114.039081. PubMed DOI PMC

Janská A., Aprile A., Zámečník J., Cattivelli L., Ovesná J. Transcriptional responses of winter barley to cold indicate nucleosome remodelling as a specific feature of crown tissues. Funct. Integr. Genom. 2011;11:307–325. doi: 10.1007/s10142-011-0213-8. PubMed DOI PMC

Teige M., Scheikl E., Eulgem T., Dóczi R., Ichimura K., Shinozaki K., Dangl J.L., Hirt H. The MKK2 Pathway Mediates Cold and Salt Stress Signaling in Arabidopsis. Mol. Cell. 2004;15:141–152. doi: 10.1016/j.molcel.2004.06.023. PubMed DOI

Guo W.L., Chen R.-G., Du X.H., Zhang Z., Yin Y.X., Gong Z.H., Wang G.Y. Reduced tolerance to abiotic stress in transgenic Arabidopsis overexpressing a Capsicum annuum multiprotein bridging factor 1. BMC Plant Biol. 2014;14:138. doi: 10.1186/1471-2229-14-138. PubMed DOI PMC

Cho S.M., Kang B.R., Kim Y.C. Transcriptome Analysis of Induced Systemic Drought Tolerance Elicited by Pseudomonas chlororaphis O6 in Arabidopsis thaliana. Plant Pathol. J. 2013;29:209–220. doi: 10.5423/PPJ.SI.07.2012.0103. PubMed DOI PMC

Rest J.S., Wilkins O., Yuan W., Purugganan M.D., Gurevitch J. Meta-analysis and meta-regression of transcriptomic responses to water stress in Arabidopsis. Plant J. 2016;85:548–560. doi: 10.1111/tpj.13124. PubMed DOI PMC

MacGregor D.R., Penfield S. Exploring the pleiotropy of hos1. J. Exp. Bot. 2015;66:1661–1671. doi: 10.1093/jxb/erv022. PubMed DOI

Simpson S.D., Nakashima K., Narusaka Y., Seki M., Shinozaki K., Yamaguchi-Shinozaki K. Two different novel cis-acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence. Plant J. 2003;33:259–270. doi: 10.1046/j.1365-313X.2003.01624.x. PubMed DOI

Sakuma Y., Maruyama K., Qin F., Osakabe Y., Shinozaki K., Yamaguchi-Shinozaki K. Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc. Natl. Acad. Sci. USA. 2006;103:18822–18827. doi: 10.1073/pnas.0605639103. PubMed DOI PMC

Baek D., Chun H.J., Kang S., Shin G., Park S.J., Hong H., Kim C., Kim D.H., Lee S.Y., Kim M.C., et al. A Role for Arabidopsis miR399f in Salt, Drought, and ABA Signaling. Mol. Cells. 2016;39:111–118. doi: 10.14348/molcells.2016.2188. PubMed DOI PMC

Kuhn J.M., Boisson-Dernier A., Dizon M.B., Maktabi M.H., Schroeder J.I. The protein phosphatase AtPP2CA negatively regulates abscisic acid signal transduction in Arabidopsis, and effects of abh1 on AtPP2CA mRNA. Plant Physiol. 2006;140:127–139. doi: 10.1104/pp.105.070318. PubMed DOI PMC

Zhang L., Zhang X., Fan S. Meta-analysis of salt-related gene expression profiles identifies common signatures of salt stress responses in Arabidopsis. Plant Syst. Evol. 2017;303:757–774. doi: 10.1007/s00606-017-1407-x. DOI

Yamada K., Fukao Y., Hayashi M., Fukazawa M., Suzuki I., Nishimura M. Cytosolic HSP90 Regulates the Heat Shock Response That Is Responsible for Heat Acclimation in Arabidopsis thaliana. J. Biol. Chem. 2007;282:37794–37804. doi: 10.1074/jbc.M707168200. PubMed DOI

Larkindale J., Vierling E. Core genome responses involved in acclimation to high temperature. Plant Physiol. 2008;146:748–761. doi: 10.1104/pp.107.112060. PubMed DOI PMC

Charng Y.Y., Liu H.C., Liu N.Y., Chi W.T., Wang C.N., Chang S.H., Wang T.T. A Heat-Inducible Transcription Factor, HsfA2, Is Required for Extension of Acquired Thermotolerance in Arabidopsis. Plant Physiol. 2007;143:251–262. doi: 10.1104/pp.106.091322. PubMed DOI PMC

Lin K.F., Tsai M.Y., Lu C.A., Wu S.J., Yeh C.H. The roles of Arabidopsis HSFA2, HSFA4a, and HSFA7a in the heat shock response and cytosolic protein response. Bot. Stud. 2018;59:15. doi: 10.1186/s40529-018-0231-0. PubMed DOI PMC

Sung D.Y., Vierling E., Guy C.L. Comprehensive expression profile analysis of the Arabidopsis Hsp70 gene family. Plant Physiol. 2001;126:789–800. doi: 10.1104/pp.126.2.789. PubMed DOI PMC

Guo J., Dai X., Xu W., Ma M. Overexpressing GSH1 and AsPCS1 simultaneously increases the tolerance and accumulation of cadmium and arsenic in Arabidopsis thaliana. Chemosphere. 2008;72:1020–1026. doi: 10.1016/j.chemosphere.2008.04.018. PubMed DOI

Song J., Feng S.J., Chen J., Zhao W.T., Yang Z.M. A cadmium stress-responsive gene AtFC1 confers plant tolerance to cadmium toxicity. BMC Plant Biol. 2017;17:187. doi: 10.1186/s12870-017-1141-0. PubMed DOI PMC

Chen J., Yang L., Yan X., Liu Y., Wang R., Fan T., Ren Y., Tang X., Xiao F., Liu Y., et al. Zinc-Finger Transcription Factor ZAT6 Positively Regulates Cadmium Tolerance through the Glutathione-Dependent Pathway in Arabidopsis. Plant Physiol. 2016;171:707–719. doi: 10.1104/pp.15.01882. PubMed DOI PMC

Song W.Y., Martinoia E., Lee J., Kim D., Kim D.Y., Vogt E., Shim D., Choi K.S., Hwang I., Lee Y. A Novel Family of Cys-Rich Membrane Proteins Mediates Cadmium Resistance in Arabidopsis. Plant Physiol. 2004;135:1027–1039. doi: 10.1104/pp.103.037739. PubMed DOI PMC

Morel M., Crouzet J., Gravot A., Auroy P., Leonhardt N., Vavasseur A., Richaud P. AtHMA3, a P1B-ATPase Allowing Cd/Zn/Co/Pb Vacuolar Storage in Arabidopsis. Plant Physiol. 2008;149:894–904. doi: 10.1104/pp.108.130294. PubMed DOI PMC

Zhang J., Martinoia E., Lee Y. Vacuolar Transporters for Cadmium and Arsenic in Plants and their Applications in Phytoremediation and Crop Development. Plant Cell Physiol. 2018;59:1317–1325. doi: 10.1093/pcp/pcy006. PubMed DOI

Mills R.F., Krijger G.C., Baccarini P.J., Hall J.L., Williams L.E. Functional expression of AtHMA4, a P1B-type ATPase of the Zn/Co/Cd/Pb subclass. Plant J. 2003;35:164–176. doi: 10.1046/j.1365-313X.2003.01790.x. PubMed DOI

Van Hoewyk D., Takahashi H., Inoue E., Hess A., Tamaoki M., Pilon-Smits E.A.H. Transcriptome analyses give insights into selenium-stress responses and selenium tolerance mechanisms in Arabidopsis. Physiol. Plant. 2008;132:236–253. doi: 10.1111/j.1399-3054.2007.01002.x. PubMed DOI

Huang J., Zhang Y., Peng J.S., Zhong C., Yi H.Y., Ow D.W., Gong J.M. Fission Yeast HMT1 Lowers Seed Cadmium through Phytochelatin-Dependent Vacuolar Sequestration in Arabidopsis. Plant Physiol. 2012;158:1779–1788. doi: 10.1104/pp.111.192872. PubMed DOI PMC

Kim Y.O., Kang H. Comparative expression analysis of genes encoding metallothioneins in response to heavy metals and abiotic stresses in rice (Oryza sativa) and Arabidopsis thaliana. Biosci. Biotechnol. Biochem. 2018:1–10. doi: 10.1080/09168451.2018.1486177. PubMed DOI

Sanz-Fernández M., Rodríguez-Serrano M., Sevilla-Perea A., Pena L., Mingorance M.D., Sandalio L.M., Romero-Puertas M.C. Screening Arabidopsis mutants in genes useful for phytoremediation. J. Hazard. Mater. 2017;335:143–151. doi: 10.1016/j.jhazmat.2017.04.021. PubMed DOI

Kim D.Y., Bovet L., Maeshima M., Martinoia E., Lee Y. The ABC transporter AtPDR8 is a cadmium extrusion pump conferring heavy metal resistance. Plant J. 2007;50:207–218. doi: 10.1111/j.1365-313X.2007.03044.x. PubMed DOI

Kim D.Y., Bovet L., Kushnir S., Noh E.W., Martinoia E., Lee Y. AtATM3 Is Involved in Heavy Metal Resistance in Arabidopsis. Plant Physiol. 2006;140:922–932. doi: 10.1104/pp.105.074146. PubMed DOI PMC

Park J., Song W.Y., Ko D., Eom Y., Hansen T.H., Schiller M., Lee T.G., Martinoia E., Lee Y. The phytochelatin transporters AtABCC1 and AtABCC2 mediate tolerance to cadmium and mercury. Plant J. 2012;69:278–288. doi: 10.1111/j.1365-313X.2011.04789.x. PubMed DOI

Song W.Y., Park J., Mendoza-Cozatl D.G., Suter-Grotemeyer M., Shim D., Hortensteiner S., Geisler M., Weder B., Rea P.A., Rentsch D., et al. Arsenic tolerance in Arabidopsis is mediated by two ABCC-type phytochelatin transporters. Proc. Natl. Acad. Sci. USA. 2010;107:21187–21192. doi: 10.1073/pnas.1013964107. PubMed DOI PMC

Sánchez-Bermejo E., Castrillo G., del Llano B., Navarro C., Zarco-Fernández S., Martinez-Herrera D.J., Leo-del Puerto Y., Muñoz R., Cámara C., Paz-Ares J., et al. Natural variation in arsenate tolerance identifies an arsenate reductase in Arabidopsis thaliana. Nat. Commun. 2014;5:4617. doi: 10.1038/ncomms5617. PubMed DOI

Sawaki Y., Iuchi S., Kobayashi Y., Kobayashi Y., Ikka T., Sakurai N., Fujita M., Shinozaki K., Shibata D., Kobayashi M., et al. STOP1 regulates multiple genes that protect arabidopsis from proton and aluminum toxicities. Plant Physiol. 2009;150:281–294. doi: 10.1104/pp.108.134700. PubMed DOI PMC

Iuchi S., Koyama H., Iuchi A., Kobayashi Y., Kitabayashi S., Kobayashi Y., Ikka T., Hirayama T., Shinozaki K., Kobayashi M. Zinc finger protein STOP1 is critical for proton tolerance in Arabidopsis and coregulates a key gene in aluminum tolerance. Proc. Natl. Acad. Sci. USA. 2007;104:9900–9905. doi: 10.1073/pnas.0700117104. PubMed DOI PMC

Larsen P.B., Geisler M.J.B., Jones C.A., Williams K.M., Cancel J.D. ALS3 encodes a phloem-localized ABC transporter-like protein that is required for aluminum tolerance in Arabidopsis. Plant J. 2004;41:353–363. doi: 10.1111/j.1365-313X.2004.02306.x. PubMed DOI

Skipsey M., Knight K.M., Brazier-Hicks M., Dixon D.P., Steel P.G., Edwards R. Xenobiotic Responsiveness of Arabidopsis thaliana to a Chemical Series Derived from a Herbicide Safener. J. Biol. Chem. 2011;286:32268–32276. doi: 10.1074/jbc.M111.252726. PubMed DOI PMC

Gandia-Herrero F., Lorenz A., Larson T., Graham I.A., Bowles D.J., Rylott E.L., Bruce N.C. Detoxification of the explosive 2,4,6-trinitrotoluene in Arabidopsis: Discovery of bifunctional O- and C-glucosyltransferases. Plant J. 2008;56:963–974. doi: 10.1111/j.1365-313X.2008.03653.x. PubMed DOI

Landa P., Prerostova S., Langhansova L., Marsik P., Vanek T. Transcriptomic response of Arabidopsis thaliana (L.) Heynh. roots to ibuprofen. Int. J. Phytoremediation. 2017;19:695–700. doi: 10.1080/15226514.2016.1267697. PubMed DOI

Weisman D., Alkio M., Colón-Carmona A. Transcriptional responses to polycyclic aromatic hydrocarbon-induced stress in Arabidopsis thaliana reveal the involvement of hormone and defense signaling pathways. BMC Plant Biol. 2010;10:59. doi: 10.1186/1471-2229-10-59. PubMed DOI PMC

Behringer C., Bartsch K., Schaller A. Safeners recruit multiple signalling pathways for the orchestrated induction of the cellular xenobiotic detoxification machinery in Arabidopsis. Plant Cell Environ. 2011;34:1970–1985. doi: 10.1111/j.1365-3040.2011.02392.x. PubMed DOI

Manabe Y., Tinker N., Colville A., Miki B. CSR1, the Sole Target of Imidazolinone Herbicide in Arabidopsis thaliana. Plant Cell Physiol. 2007;48:1340–1358. doi: 10.1093/pcp/pcm105. PubMed DOI

Subramanian S., Schnoor J.L., Van Aken B. Effects of Polychlorinated Biphenyls (PCBs) and Their Hydroxylated Metabolites (OH-PCBs) on Arabidopsis thaliana. Environ. Sci. Technol. 2017;51:7263–7270. doi: 10.1021/acs.est.7b01538. PubMed DOI PMC

DeRidder B.P., Dixon D.P., Beussman D.J., Edwards R., Goldsbrough P.B. Induction of Glutathione S-Transferases in Arabidopsis by Herbicide Safeners. Plant Physiol. 2002;130:1497–1505. doi: 10.1104/pp.010066. PubMed DOI PMC

Nutricati E., Miceli A., Blando F., De Bellis L. Characterization of two Arabidopsis thaliana glutathione S-transferases. Plant Cell Rep. 2006;25:997–1005. doi: 10.1007/s00299-006-0146-1. PubMed DOI

Grzam A., Martin M.N., Hell R., Meyer A.J. γ-Glutamyl transpeptidase GGT4 initiates vacuolar degradation of glutathione S -conjugates in Arabidopsis. FEBS Lett. 2007;581:3131–3138. doi: 10.1016/j.febslet.2007.05.071. PubMed DOI

Merewitz E. Drought Stress Tolerance in Plants. Volume 1. Springer International Publishing; Cham, Switzerland: 2016. Chemical Priming-Induced Drought Stress Tolerance in Plants; pp. 77–103.

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

Šimura J., Antoniadi I., Široká J., Tarkowská D., Strnad M., Ljung K., Novák O. Plant Hormonomics: Multiple Phytohormone Profiling by Targeted Metabolomics. Plant Physiol. 2018;177:476–489. doi: 10.1104/pp.18.00293. PubMed DOI PMC

Černý M., Skalák J., Cerna H., Brzobohatý B. Advances in purification and separation of posttranslationally modified proteins. J. Proteom. 2013;92:2–27. doi: 10.1016/j.jprot.2013.05.040. PubMed DOI

Hsu C.C., Zhu Y., Arrington J. V, Paez J.S., Wang P., Zhu P., Chen I.H., Zhu J.K., Tao W.A. Universal plant phosphoproteomics workflow and its application to tomato signaling in response to cold stress. Mol. Cell. Proteom. 2018:mcp.TIR118.000702. doi: 10.1074/mcp.TIR118.000702. PubMed DOI PMC

Vandereyken K., Van Leene J., De Coninck B., Cammue B.P.A. Hub Protein Controversy: Taking a Closer Look at Plant Stress Response Hubs. Front. Plant Sci. 2018;9:694. doi: 10.3389/fpls.2018.00694. PubMed DOI PMC

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