The Role of a Cytokinin Antagonist in the Progression of Clubroot Disease

. 2023 Feb 05 ; 13 (2) : . [epub] 20230205

Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid36830668

Plasmodiophora brassicae is an obligate biotrophic pathogen causing clubroot disease in cruciferous plants. Infected plant organs are subject to profound morphological changes, the roots form characteristic galls, and the leaves are chlorotic and abscise. The process of gall formation is governed by timely changes in the levels of endogenous plant hormones that occur throughout the entire life cycle of the clubroot pathogen. The homeostasis of two plant hormones, cytokinin and auxin, appears to be crucial for club development. To investigate the role of cytokinin and auxin in gall formation, we used metabolomic and transcriptomic profiling of Arabidopsis thaliana infected with clubroot, focusing on the late stages of the disease, where symptoms were more pronounced. Loss-of-function mutants of three cytokinin receptors, AHK2, AHK3, and CRE1/AHK4, were employed to further study the homeostasis of cytokinin in response to disease progression; ahk double mutants developed characteristic symptoms of the disease, albeit with varying intensity. The most susceptible to clubroot disease was the ahk3 ahk4 double mutant, as revealed by measuring its photosynthetic performance. Quantification of phytohormone levels and pharmacological treatment with the cytokinin antagonist PI-55 showed significant changes in the levels of endogenous cytokinin and auxin, which was manifested by both enhanced and reduced development of disease symptoms in different genotypes.

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Dixon G.R. The Occurrence and Economic Impact of Plasmodiophora brassicae and Clubroot Disease. J. Plant Growth Regul. 2009;28:194–202. doi: 10.1007/s00344-009-9090-y. DOI

Ciaghi S., Schwelm A., Neuhauser S. Transcriptomic response in symptomless roots of clubroot infected kohlrabi (Brassica oleracea var. gongylodes) mirrors resistant plants. BMC Plant Biol. 2019;19:288. doi: 10.1186/s12870-019-1902-z. PubMed DOI PMC

Irani S., Trost B., Waldner M., Nayidu N., Tu J., Kusalik A.J., Todd C.D., Wei Y., Bonham-Smith P.C. Transcriptome analysis of response to Plasmodiophora brassicae infection in the Arabidopsis shoot and root. BMC Genom. 2018;19:23. doi: 10.1186/s12864-017-4426-7. PubMed DOI PMC

Rolfe S.A., Strelkov S.E., Links M.G., Clarke W.E., Robinson S.J., Djavaheri M., Malinowski R., Haddadi P., Kagale S., Parkin I.A.P., et al. The compact genome of the plant pathogen Plasmodiophora brassicae is adapted to intracellular interactions with host Brassica spp. BMC Genom. 2016;17:272. doi: 10.1186/s12864-016-2597-2. PubMed DOI PMC

Schwelm A., Fogelqvist J., Knaust A., Jülke S., Lilja T., Rosso G.B., Karlsson M., Shevchenko A., Dhandapani V., Choi S.R., et al. The Plasmodiophora brassicae genome reveals insights in its life cycle and ancestry of chitin synthases. Sci. Rep. 2015;5:11153. doi: 10.1038/srep11153. PubMed DOI PMC

Javed M.A., Schwelm A., Zamani-Noor N., Salih R., Vañó M.S., Wu J., García M.G., Heick T.M., Luo C., Prakash P., et al. The clubroot pathogen Plasmodiophora brassicae: A profile update. Mol. Plant Pathol. 2022;24:89–106. doi: 10.1111/mpp.13283. PubMed DOI PMC

Ludwig-Müller J., Jülke S., Geiß K., Richter F., Mithöfer A., Šola I., Rusak G., Keenan S., Bulman S. A novel methyltransferase from the intracellular pathogen Plasmodiophora brassicae methylates salicylic acid. Mol. Plant Pathol. 2015;16:349–364. doi: 10.1111/mpp.12185. PubMed DOI PMC

Kageyama K., Asano T. Life Cycle of Plasmodiophora brassicae. J. Plant Growth Regul. 2009;28:203–211. doi: 10.1007/s00344-009-9101-z. DOI

Aist J.R., Williams P.H. The cytology and kinetics of cabbage root hair penetration by Plasmodiophora brassicae. Can. J. Bot. 1971;49:2023–2034. doi: 10.1139/b71-284. DOI

Malinowski R., Truman W., Blicharz S. Genius Architect or Clever Thief—How Plasmodiophora brassicae Reprograms Host Development to Establish a Pathogen-Oriented Physiological Sink. Mol. Plant Microbe Interact. 2019;32:1259–1266. doi: 10.1094/MPMI-03-19-0069-CR. PubMed DOI

Wei X., Zhang Y., Zhao Y., Xie Z., Hossain M.R., Yang S., Shi G., Lv Y., Wang Z., Tian B., et al. Root Transcriptome and Metabolome Profiling Reveal Key Phytohormone-Related Genes and Pathways Involved Clubroot Resistance in Brassica rapa L. Front. Plant Sci. 2021;12:759623. doi: 10.3389/fpls.2021.759623. PubMed DOI PMC

Devos S., Laukens K., Deckers P., Van Der Straeten D., Beeckman T., Inzé D., Van Onckelen H., Witters E., Prinsen E. A Hormone and Proteome Approach to Picturing the Initial Metabolic Events During Plasmodiophora brassicae Infection on Arabidopsis. Mol. Plant Microbe Interact. 2006;19:1431–1443. doi: 10.1094/MPMI-19-1431. PubMed DOI

Siemens J., Keller I., Sarx J., Kunz S., Schuller A., Nagel W., Schmülling T., Parniske M., Ludwig-Müller J. Transcriptome Analysis of Arabidopsis Clubroots Indicate a Key Role for Cytokinins in Disease Development. Mol. Plant Microbe Interact. 2006;19:480–494. doi: 10.1094/MPMI-19-0480. PubMed DOI

Boivin S., Fonouni-Farde C., Frugier F. How Auxin and Cytokinin Phytohormones Modulate Root Microbe Interactions. Front. Plant Sci. 2016;7:1240. doi: 10.3389/fpls.2016.01240. PubMed DOI PMC

Malinowski R., Smith J.A., Fleming A.J., Scholes J.D., Rolfe S.A. Gall formation in clubroot-infected Arabidopsis results from an increase in existing meristematic activities of the host but is not essential for the completion of the pathogen life cycle. Plant J. 2012;71:226–238. doi: 10.1111/j.1365-313X.2012.04983.x. PubMed DOI

Malinowski R., Novak O., Borhan M.H., Spíchal L., Strnad M., Rolfe S.A. The role of cytokinins in clubroot disease. Eur. J. Plant Pathol. 2016;145:543–557. doi: 10.1007/s10658-015-0845-y. DOI

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

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

Bryksová M., Dabravolski S., Kučerová Z., Kokáš F.Z., Špundová M., Plíhalová L., Takáč T., Grúz J., Hudeček M., Hloušková V., et al. Aromatic Cytokinin Arabinosides Promote PAMP-like Responses and Positively Regulate Leaf Longevity. ACS Chem. Biol. 2020;15:1949–1963. doi: 10.1021/acschembio.0c00306. PubMed DOI

Mok D.W., Mok M.C. Cytokinin metabolism and action. Annu. Rev. Plant Biol. 2001;52:89–118. doi: 10.1146/annurev.arplant.52.1.89. PubMed DOI

Kudo T., Kiba T., Sakakibara H. Metabolism and Long-distance Translocation of Cytokinins. J. Integr. Plant Biol. 2010;52:53–60. doi: 10.1111/j.1744-7909.2010.00898.x. PubMed DOI

Chatfield J.M., Armstrong D.J. Regulation of Cytokinin Oxidase Activity in Callus Tissues of Phaseolus vulgaris L. cv Great Northern. Plant Physiol. 1986;80:493–499. doi: 10.1104/pp.80.2.493. PubMed DOI PMC

Kakimoto T. Identification of Plant Cytokinin Biosynthetic Enzymes as Dimethylallyl Diphosphate:ATP/ADP Isopentenyltransferases. Plant Cell Physiol. 2001;42:677–685. doi: 10.1093/pcp/pce112. PubMed DOI

Inoue T., Higuchi M., Hashimoto Y., Seki M., Kobayashi M., Kato T., Tabata S., Shinozaki K., Kakimoto T. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature. 2001;409:1060–1063. doi: 10.1038/35059117. PubMed DOI

Ueguchi C., Sato S., Kato T., Tabata S. The AHK4 Gene Involved in the Cytokinin-Signaling Pathway as a Direct Receptor Molecule in Arabidopsis thaliana. Plant Cell Physiol. 2001;42:751–755. doi: 10.1093/pcp/pce094. PubMed DOI

Ueguchi C., Koizumi H., Suzuki T., Mizuno T. Novel family of sensor histidine kinase genes in Arabidopsis thaliana. Plant Cell Physiol. 2001;42:231–235. doi: 10.1093/pcp/pce015. PubMed DOI

Suzuki T., Miwa K., Ishikawa K., Yamada H., Aiba H., Mizuno T. The Arabidopsis Sensor His-kinase, AHK4, Can Respond to Cytokinins. Plant Cell Physiol. 2001;42:107–113. doi: 10.1093/pcp/pce037. PubMed DOI

Yamada H., Suzuki T., Terada K., Takei K., Ishikawa K., Miwa K., Yamashino T., Mizuno T. The Arabidopsis AHK4 Histidine Kinase is a Cytokinin-Binding Receptor that Transduces Cytokinin Signals Across the Membrane. Plant Cell Physiol. 2001;42:1017–1023. doi: 10.1093/pcp/pce127. PubMed DOI

Riefler M., Novak O., Strnad M., Schmülling T. ArabidopsisCytokinin Receptor Mutants Reveal Functions in Shoot Growth, Leaf Senescence, Seed Size, Germination, Root Development, and Cytokinin Metabolism. Plant Cell. 2006;18:40–54. doi: 10.1105/tpc.105.037796. PubMed DOI PMC

Spíchal L., Werner T., Popa I., Riefler M., Schmülling T., Strnad M. The purine derivative PI-55 blocks cytokinin action via receptor inhibition. FEBS J. 2009;276:244–253. doi: 10.1111/j.1742-4658.2008.06777.x. PubMed DOI

Hoyerova K., Gaudinova A., Malbeck J., Dobrev P., Kocabek T., Solcova B., Trávníčková A., Kaminek M. Efficiency of different methods of extraction and purification of cytokinins. Phytochemistry. 2006;67:1151–1159. doi: 10.1016/j.phytochem.2006.03.010. PubMed DOI

Svačinová J., Novák O., Plačková L., Lenobel R., Holík J., Strnad M., Doležal K. A new approach for cytokinin isolation from Arabidopsis tissues using miniaturized purification: Pipette tip solid-phase extraction. Plant Methods. 2012;8:17. doi: 10.1186/1746-4811-8-17. PubMed DOI PMC

Novák O., Hauserová E., Amakorová P., Doležal K., Strnad M. Cytokinin profiling in plant tissues using ultra-performance liquid chromatography–electrospray tandem mass spectrometry. Phytochemistry. 2008;69:2214–2224. doi: 10.1016/j.phytochem.2008.04.022. PubMed DOI

Pěnčík A., Rolčík J., Novák O., Magnus V., Barták P., Buchtík R., Salopek-Sondi B., Strnad M. Isolation of novel indole-3-acetic acid conjugates by immunoaffinity extraction. Talanta. 2009;80:651–655. doi: 10.1016/j.talanta.2009.07.043. PubMed DOI

Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT Method. Methods. 2001;25:402–408. doi: 10.1006/meth.2001.1262. PubMed DOI

Grsic-Rausch S., Kobelt P., Siemens J.M., Bischoff M., Ludwig-Müller J. Expression and Localization of Nitrilase during Symptom Development of the Clubroot Disease in Arabidopsis. Plant Physiol. 2000;122:369–378. doi: 10.1104/pp.122.2.369. PubMed DOI PMC

Devos S., Vissenberg K., Verbelen J., Prinsen E. Infection of Chinese cabbage by Plasmodiophora brassicae leads to a stimulation of plant growth: Impacts on cell wall metabolism and hormone balance. New Phytol. 2005;166:241–250. doi: 10.1111/j.1469-8137.2004.01304.x. PubMed DOI

Miyawaki K., Tarkowski P., Matsumoto-Kitano M., Kato T., Sato S., Tarkowska D., Tabata S., Sandberg G., Kakimoto T. Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proc. Natl. Acad. Sci. USA. 2006;103:16598–16603. doi: 10.1073/pnas.0603522103. PubMed DOI PMC

Bielach A., Podlešáková K., Marhavý P., Duclercq J., Cuesta C., Müller B., Grunewald W., Tarkowski P., Benková E. Spatiotemporal Regulation of Lateral Root Organogenesis in Arabidopsis by Cytokinin. Plant Cell. 2012;24:3967–3981. doi: 10.1105/tpc.112.103044. PubMed DOI PMC

Ando S., Asano T., Tsushima S., Kamachi S., Hagio T., Tabei Y. Changes in gene expression of putative isopentenyltransferase during clubroot development in Chinese cabbage (Brassica rapa L.) Physiol. Mol. Plant Pathol. 2005;67:59–67. doi: 10.1016/j.pmpp.2005.09.005. DOI

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