Cytokinin Deficiency Alters Leaf Proteome and Metabolome during Effector-Triggered Immunity in Arabidopsis thaliana Plants
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
322QN248
Hainan Provincial Natural Science Foundation of China
CZ.02.1.01/0.0/0.0/16_019/0000738
Ministry of Education, Youth and Sports of the Czech Republic
Project 'Centre for Experimental Plant Biology'
European Regional Development Fund
PubMed
36015426
PubMed Central
PMC9415597
DOI
10.3390/plants11162123
PII: plants11162123
Knihovny.cz E-zdroje
- Klíčová slova
- Arabidopsis thaliana, Flg22 peptide, cytokinin, defence response, metabolome, proteome,
- Publikační typ
- časopisecké články MeSH
The involvement of cytokinins (CK) in biotic stresses has been recognized, while knowledge regarding the effects of CK deficiency on plant response against pathogens is less abundant. Thus, the purpose of this study was to reveal the effects of CK deficiency on proteomics and metabolomic responses of flg22-triggered immunity. We conducted a series of histochemical assays to investigate the activity of the downstream pathways caused by flg22, such as accumulation of ROS, induction of defence genes, and callose deposition, that occurred in Arabidopsis thaliana transgenic lines overexpressing the Hordeum vulgare CKX2 gene (HvCKX2), which are therefore CK-deficient. We also used GC and LC-MS-based technology to quantify variations in stress hormone levels and metabolomic and proteomic responses in flg22-treated HvCKX2 and wild-type Arabidopsis plants. We found that CK deficiency alters the flg22-triggered plant defence response, especially through induction of callose deposition, upregulation of defence response-related proteins, increased amino acid biosynthesis, and regulation of plant photosynthesis. We also indicated that JA might be an important contributor to immune response in plants deficient in CKs. The present study offers new evidence on the fundamental role of endogenous CK in the response to pathogens, as well as the possibility of altering plant biotic tolerance by manipulating CK pools.
Zobrazit více v PubMed
Choi J., Choi D., Lee S., Ryu C.-M., Hwang I. Cytokinins and plant immunity: Old foes or new friends? Trends Plant Sci. 2011;16:388–394. doi: 10.1016/j.tplants.2011.03.003. PubMed DOI
Li S.M., Zheng H.X., Zhang X.S., Sui N. Cytokinins as central regulators during plant growth and stress response. Plant Cell Rep. 2021;40:271–282. doi: 10.1007/s00299-020-02612-1. PubMed DOI
Gupta R., Pizarro L., Leibman-Markus M., Marash I., Bar M. Cytokinin response induces immunity and fungal pathogen resistance, and modulates trafficking of the PRR LeEIX2 in tomato. Mol. Plant Pathol. 2020;21:1287–1306. doi: 10.1111/mpp.12978. PubMed DOI PMC
Amasino R.J.P.P. 1955: Kinetin arrives. The 50th anniversary of a new plant hormone. Plant Physiol. 2005;138:1177–1184. doi: 10.1104/pp.104.900160. PubMed DOI PMC
Schmülling T., Werner T., Riefler M., Krupková E., Manns I.B.Y. Structure and function of cytokinin oxidase/dehydrogenase genes of maize, rice, Arabidopsis and other species. J. Plant Res. 2003;116:241–252. doi: 10.1007/s10265-003-0096-4. PubMed DOI
Trifunović M., Cingel A., Simonović A., Jevremović S., Petrić M., Dragićević I.Č., Motyka V., Dobrev P.I., Zahajská L., Subotić A. Overexpression of Arabidopsis cytokinin oxidase/dehydrogenase genes AtCKX1 and AtCKX2 in transgenic Centaurium erythraea Rafn. Plant Cell Tissue Organ Cult. 2013;115:139–150. doi: 10.1007/s11240-013-0347-6. DOI
Černý M., Kuklová A., Hoehenwarter W., Fragner L., Novák O., Rotková G., Jedelský P.L., Žáková 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
Galuszka P., Frébortová J., Werner T., Yamada M., Strnad M., Schmülling T., Frébort I. Cytokinin oxidase/dehydrogenase genes in barley and wheat. Eur. J. Biochem. 2004;271:3990–4002. doi: 10.1111/j.1432-1033.2004.04334.x. 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
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
Skalák J., Vercruyssen L., Claeys H., Hradilová J., Černý M., Novák O., Plačková L., Saiz-Fernández I., Skaláková P., Coppens F., et al. Multifaceted activity of cytokinin in leaf development shapes its size and structure in Arabidopsis. Plant J. 2019;97:805–824. doi: 10.1111/tpj.14285. PubMed DOI
Cortleven A., Leuendorf J.E., Frank M., Pezzetta D., Bolt S., Schmülling T. Cytokinin action in response to abiotic and biotic stresses in plants. Plant Cell Environ. 2019;42:998–1018. doi: 10.1111/pce.13494. PubMed DOI
Argueso C.T., Ferreira F.J., Epple P., To J.P.C., Hutchison C.E., Schaller G.E., Dangl J.L., Kieber J.J. Two-Component Elements Mediate Interactions between Cytokinin and Salicylic Acid in Plant Immunity. PLoS Genet. 2012;8:e1002448. doi: 10.1371/journal.pgen.1002448. PubMed DOI PMC
Baillie A.L., Fleming A.J. The developmental relationship between stomata and mesophyll airspace. New Phytol. 2020;225:1120–1126. doi: 10.1111/nph.16341. PubMed DOI
Gupta R., Leibman-Markus M., Pizarro L., Bar M. Cytokinin induces bacterial pathogen resistance in tomato. Plant Pathol. 2021;70:318–325. doi: 10.1111/ppa.13279. DOI
Großkinsky D.K., Naseem M., Abdelmohsen U.R., Plickert N., Engelke T., Griebel T., Zeier J., Novák O., Strnad M., Pfeifhofer H., et al. Cytokinins Mediate Resistance against Pseudomonas syringae in Tobacco through Increased Antimicrobial Phytoalexin Synthesis Independent of Salicylic Acid Signaling. Plant Physiol. 2011;157:815–830. doi: 10.1104/pp.111.182931. 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
Barna B., Smigocki A.C., Baker J.C. Transgenic Production of Cytokinin Suppresses Bacterially Induced Hypersensitive Response Symptoms and Increases Antioxidative Enzyme Levels in Nicotiana spp. Phytopathology. 2008;98:1242–1247. doi: 10.1094/PHYTO-98-11-1242. PubMed DOI
Zhang X., Liu D., Gao D., Zhao W., Du H., Qiu Z., Huang J., Wen P., Wang Y., Li Q., et al. Cytokinin Confers Brown Planthopper Resistance by Elevating Jasmonic Acid Pathway in Rice. Int. J. Mol. Sci. 2022;23:5946. doi: 10.3390/ijms23115946. PubMed DOI PMC
Choi J., Huh S.U., Kojima M., Sakakibara H., Paek K.-H., Hwang I. The Cytokinin-Activated Transcription Factor ARR2 Promotes Plant Immunity via TGA3/NPR1-Dependent Salicylic Acid Signaling in Arabidopsis. Dev. Cell. 2010;19:284–295. doi: 10.1016/j.devcel.2010.07.011. PubMed DOI
Arnaud D., Lee S., Takebayashi Y., Choi D., Choi J., Sakakibara H., Hwang I. Cytokinin-Mediated Regulation of Reactive Oxygen Species Homeostasis Modulates Stomatal Immunity in Arabidopsis. Plant Cell. 2017;29:543. doi: 10.1105/tpc.16.00583. PubMed DOI PMC
Gupta R., Elkabetz D., Leibman-Markus M., Sayas T., Schneider A., Jami E., Kleiman M., Bar M. Cytokinin drives assembly of the phyllosphere microbiome and promotes disease resistance through structural and chemical cues. ISME J. 2022;16:122–137. doi: 10.1038/s41396-021-01060-3. PubMed DOI PMC
Gómez-Gómez L., Boller T. FLS2: An LRR Receptor–like Kinase Involved in the Perception of the Bacterial Elicitor Flagellin in Arabidopsis. Mol. Cell. 2000;5:1003–1011. doi: 10.1016/S1097-2765(00)80265-8. PubMed DOI
Yi S.Y., Shirasu K., Moon J.S., Lee S.-G., Kwon S.-Y. The Activated SA and JA Signaling Pathways Have an Influence on flg22-Triggered Oxidative Burst and Callose Deposition. PLoS ONE. 2014;9:e88951. doi: 10.1371/journal.pone.0088951. PubMed DOI PMC
Pizarro L., Munoz D., Marash I., Gupta R., Anand G., Leibman-Markus M., Bar M. Cytokinin Modulates Cellular Trafficking and the Cytoskeleton, Enhancing Defense Responses. Cells. 2021;10:1634. doi: 10.3390/cells10071634. PubMed DOI PMC
Gigli-Bisceglia N., Engelsdorf T., Strnad M., Vaahtera L., Khan G.A., Yamoune A., Alipanah L., Novák O., Persson S., Hejatko J., et al. Cell wall integrity modulates Arabidopsis thaliana cell cycle gene expression in a cytokinin- and nitrate reductase-dependent manner. Development. 2018;145:dev166678. doi: 10.1242/dev.166678. PubMed DOI
Ha S., Vankova R., Yamaguchi-Shinozaki K., Shinozaki K., Tran L.-S.P. Cytokinins: Metabolism and function in plant adaptation to environmental stresses. Trends Plant Sci. 2012;17:172–179. doi: 10.1016/j.tplants.2011.12.005. PubMed DOI
Schippers J.H., Jing H.-C., Hille J., Dijkwel P.P. Senescence Process in Plants. Volume 26. Wiley-Blackwell; Hoboken, NJ, USA: 2007. Developmental and hormonal control of leaf senescence; pp. 145–170.
Eisele J.F., Fäßler F., Bürgel P.F., Chaban C. A Rapid and Simple Method for Microscopy-Based Stomata Analyses. PLoS ONE. 2016;11:e0164576. doi: 10.1371/journal.pone.0164576. PubMed DOI PMC
Berka M., Luklová M., Dufková H., Berková V., Novák J., Saiz-Fernández I., Rashotte A.M., Brzobohatý B., Černý M. Barley Root Proteome and Metabolome in Response to Cytokinin and Abiotic Stimuli. Front. Plant Sci. 2020;11:590337. doi: 10.3389/fpls.2020.590337. PubMed DOI PMC
Love M.I., Huber W., Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550. doi: 10.1186/s13059-014-0550-8. PubMed DOI PMC
Mach J.M., Castillo A.R., Hoogstraten R., Greenberg J.T. The Arabidopsis-accelerated cell death gene ACD encodes red chlorophyll catabolite reductase and suppresses the spread of disease symptoms. Proc. Natl. Acad. Sci. USA. 2001;98:771. doi: 10.1073/pnas.98.2.771. PubMed DOI PMC
Zurbriggen M.D., Carrillo N., Hajirezaei M.-R. ROS signaling in the hypersensitive response. Plant Signal. Behav. 2010;5:393–396. doi: 10.4161/psb.5.4.10793. PubMed DOI PMC
Muñoz-Espinoza V.A., López-Climent M.F., Casaretto J.A., Gómez-Cadenas A. Water Stress Responses of Tomato Mutants Impaired in Hormone Biosynthesis Reveal Abscisic Acid, Jasmonic Acid and Salicylic Acid Interactions. Front. Plant Sci. 2015;6:997. doi: 10.3389/fpls.2015.00997. PubMed DOI PMC
Brouwer S.M., Odilbekov F., Burra D.D., Lenman M., Hedley P.E., Grenville-Briggs L., Alexandersson E., Liljeroth E., Andreasson E. Intact salicylic acid signalling is required for potato defence against the necrotrophic fungus Alternaria solani. Plant Mol. Biol. 2020;104:1–19. doi: 10.1007/s11103-020-01019-6. PubMed DOI PMC
Abreu M.E., Munné-Bosch S. Salicylic acid deficiency in NahG transgenic lines and sid2 mutants increases seed yield in the annual plant Arabidopsis thaliana. J. Exp. Bot. 2009;60:1261–1271. doi: 10.1093/jxb/ern363. PubMed DOI PMC
Howlader P., Bose S.K., Jia X., Zhang C., Wang W., Yin H. Oligogalacturonides induce resistance in Arabidopsis thaliana by triggering salicylic acid and jasmonic acid pathways against Pst DC3000. Int. J. Biol. Macromol. 2020;164:4054–4064. doi: 10.1016/j.ijbiomac.2020.09.026. PubMed DOI
Dewdney J., Reuber T.L., Wildermuth M.C., Devoto A., Cui J., Stutius L.M., Drummond E.P., Ausubel F.M. Three unique mutants of Arabidopsis identify eds loci required for limiting growth of a biotrophic fungal pathogen. Plant J. 2000;24:205–218. doi: 10.1046/j.1365-313x.2000.00870.x. PubMed DOI
Foyer C.H., Noctor G. Redox Homeostasis and Antioxidant Signaling: A Metabolic Interface between Stress Perception and Physiological Responses. Plant Cell. 2005;17:1866–1875. doi: 10.1105/tpc.105.033589. PubMed DOI PMC
Bela K., Horváth E., Gallé Á., Szabados L., Tari I., Csiszár J. Plant glutathione peroxidases: Emerging role of the antioxidant enzymes in plant development and stress responses. J. Plant Physiol. 2015;176:192–201. doi: 10.1016/j.jplph.2014.12.014. PubMed DOI
Xu N., Chen G., Liu H. Antioxidative Categorization of Twenty Amino Acids Based on Experimental Evaluation. Molecules. 2017;22:2066. doi: 10.3390/molecules22122066. PubMed DOI PMC
Filiz E., Ozyigit I.I., Saracoglu I.A., Uras M.E., Sen U., Yalcin B. Abiotic stress-induced regulation of antioxidant genes in different Arabidopsis ecotypes: Microarray data evaluation. Biotechnol. Biotechnol. Equip. 2019;33:128–143. doi: 10.1080/13102818.2018.1556120. DOI
Hématy K., Cherk C., Somerville S. Host–pathogen warfare at the plant cell wall. Curr. Opin. Plant Biol. 2009;12:406–413. doi: 10.1016/j.pbi.2009.06.007. PubMed DOI
Vojta P., Kokáš F., Husičková A., Grúz J., Bergougnoux V., Marchetti C.F., Jiskrová E., Ježilová E., Mik V., Ikeda Y., et al. 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
Sun L., Ren H., Liu R., Li B., Wu T., Sun F., Liu H., Wang X., Dong H. An h-type thioredoxin functions in tobacco defense responses to two species of viruses and an abiotic oxidative stress. Mol. Plant Microbe Interact. 2010;23:1470–1485. doi: 10.1094/MPMI-01-10-0029. PubMed DOI
Luna E., Pastor V., Robert J., Flors V., Mauch-Mani B., Ton J. Callose deposition: A multifaceted plant defense response. Mol. Plant Microbe Interact. 2011;24:183–193. doi: 10.1094/MPMI-07-10-0149. PubMed DOI
Abou-Saleh R.H., Hernandez-Gomez M.C., Amsbury S., Paniagua C., Bourdon M., Miyashima S., Helariutta Y., Fuller M., Budtova T., Connell S.D., et al. Interactions between callose and cellulose revealed through the analysis of biopolymer mixtures. Nat. Commun. 2018;9:4538. doi: 10.1038/s41467-018-06820-y. PubMed DOI PMC
Schenke D., Böttcher C., Scheel D. Crosstalk between abiotic ultraviolet-B stress and biotic (flg22) stress signalling in Arabidopsis prevents flavonol accumulation in favor of pathogen defence compound production. Plant Cell Environ. 2011;34:1849–1864. doi: 10.1111/j.1365-3040.2011.02381.x. PubMed DOI
Samalova M., Elsayad K., Melnikava A., Peaucelle A., Gahurova E., Gumulec J., Spyroglou I., Zemlyanskaya E.V., Ubogoeva E.V., Hejatko J. Expansin-controlled cell wall stiffness regulates root growth in Arabidopsis. BioRxiv. 2020:170969. doi: 10.1101/2020.06.25.170969. DOI
Dumez S., Wattebled F., Dauvillee D., Delvalle D., Planchot V.r., Ball S.G., D’Hulst C. Mutants of Arabidopsis Lacking Starch Branching Enzyme II Substitute Plastidial Starch Synthesis by Cytoplasmic Maltose Accumulation. Plant Cell. 2006;18:2694–2709. doi: 10.1105/tpc.105.037671. PubMed DOI PMC
Tang X.-J., Peng C., Zhang J., Cai Y., You X.-M., Kong F., Yan H.-G., Wang G.-X., Wang L., Jin J., et al. ADP-glucose pyrophosphorylase large subunit 2 is essential for storage substance accumulation and subunit interactions in rice endosperm. Plant Sci. 2016;249:70–83. doi: 10.1016/j.plantsci.2016.05.010. PubMed DOI
Miyazawa Y., Sakai A., Miyagishima S.-y., Takano H., Kawano S., Kuroiwa T.J.P.P. Auxin and cytokinin have opposite effects on amyloplast development and the expression of starch synthesis genes in cultured bright yellow-2 tobacco cells. Plant Physiol. 1999;121:461–470. doi: 10.1104/pp.121.2.461. PubMed DOI PMC
Peterhansel C., Horst I., Niessen M., Blume C., Kebeish R., Kürkcüoglu S., Kreuzaler F. Photorespiration. Arab. Book. 2010;8:e0130. doi: 10.1199/tab.0130. PubMed DOI PMC
Dellero Y., Jossier M., Glab N., Oury C., Tcherkez G., Hodges M. Decreased glycolate oxidase activity leads to altered carbon allocation and leaf senescence after a transfer from high CO2 to ambient air in Arabidopsis thaliana. J. Exp. Bot. 2016;67:3149–3163. doi: 10.1093/jxb/erw054. PubMed DOI
Ritchie G.A.J.P.R. Chlorophyll Fluorescence: What Is It and. Proceedings RMRS. 1998;2:34.
Ruban A.V. Nonphotochemical Chlorophyll Fluorescence Quenching: Mechanism and Effectiveness in Protecting Plants from Photodamage. Plant Physiol. 2016;170:1903–1916. doi: 10.1104/pp.15.01935. PubMed DOI PMC
Göhre V., Jones A.M.E., Sklenář J., Robatzek S., Weber A.P.M. Molecular Crosstalk Between PAMP-Triggered Immunity and Photosynthesis. Mol. Plant Microbe Interact. 2012;25:1083–1092. doi: 10.1094/MPMI-11-11-0301. PubMed DOI
Xylem Sap Proteome Analysis Provides Insight into Root-Shoot Communication in Response to flg22