The Cytokinin Complex Associated With Rhodococcus fascians: Which Compounds Are Critical for Virulence?

. 2019 ; 10 () : 674. [epub] 20190522

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid31191583

Virulent strains of Rhodococcus fascians cause a range of disease symptoms, many of which can be mimicked by application of cytokinin. Both virulent and avirulent strains produce a complex of cytokinins, most of which can be derived from tRNA degradation. To test the three current hypotheses regarding the involvement of cytokinins as virulence determinants, we used PCR to detect specific genes, previously associated with a linear virulence plasmid, including two methyl transferase genes (mt1 and mt2) and fas4 (dimethyl transferase), of multiple strains of R. fascians. We inoculated Pisum sativum (pea) seeds with virulent and avirulent strains of R. fascians, monitored the plants over time and compared these to mock-inoculated controls. We used RT-qPCR to monitor the expression of mt1, mt2, and fas4 in inoculated tissues and LC-MS/MS to obtain a comprehensive picture of the cytokinin complement of inoculated cotyledons, roots and shoots over time. The presence and expression of mt1 and mt2 was associated with those strains of R. fascians classed as virulent, and not those classed as avirulent. Expression of mt1, mt2, and fas4 peaked at 9 days post-inoculation (dpi) in cotyledons and at 15 dpi in shoots and roots developed from seeds inoculated with virulent strain 602. Pea plants inoculated with virulent and avirulent strains of R. fascians both contained cytokinins likely to have been derived from tRNA turnover including the 2-methylthio cytokinins and cis-zeatin-derivatives. Along with the isopentenyladenine-type cytokinins, the levels of these compounds did not correlate with virulence. Only the novel 1- and 2-methylated isopentenyladenine cytokinins were uniquely associated with infection by the virulent strains and are, therefore, the likely causative factors of the disease symptoms.

Zobrazit více v PubMed

Armstrong D. J., Scarbrough E., Skoog F. (1976). Cytokinins in Corynebacterium fascians cultures: isolation and identification of 6-(4-Hydroxy-3-methyl-cis-2-butenylamino)-2-methylthiopurine. Plant Physiol. 58, 749–752. 10.1104/pp.58.6.749 PubMed DOI PMC

Bai Y., Müller D. B., Srinivas G., Garrido-Oter R., Potthoff E., Rott M., et al. (2015). Functional overlap and specialization of the Arabidopsis leaf and root microbiotas. Nature 528:364–369. 10.1038/nature16192 PubMed DOI

Bustin S. A., Benes V., Garson J. A., Hellemans J., Huggett J., Kubista M., et al. . (2009). The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55, 611–622. 10.1373/clinchem.2008.112797 PubMed DOI

Creason A. L., Vandeputte O. M., Savory E. A., Davis E. W. I. I., Putnam M. L., Hu E., et al. . (2014). Analysis of genome sequences from plant pathogenic Rhodococcus reveals genetic novelties in virulence loci. PLoS ONE 9:e101996. 10.1371/journal.pone.0101996 PubMed DOI PMC

Crespi M., Messens E., Caplan A. B., Van Montagu M., Desomer J. (1992). Fasciation induction by the phytopathogen Rhodococcus fascians depends upon a linear plasmid encoding a cytokinin synthase gene. EMBO J. 11, 795–804. 10.1002/j.1460-2075.1992.tb05116.x PubMed DOI PMC

de O Manes C. L., Van Montagu M., Prinsen E., Goethals K., Holsters M. (2001). De novo cortical cell division triggered by the phytopathogen Rhodococcus fascians in tobacco. Mol. Plant Microbe Interact. 14, 189–195. 10.1094/MPMI.2001.14.2.189 PubMed DOI

Depuydt S., Doležal K., Van Lijsebettens M., Moritz T., Holsters M., Vereecke D. (2008). Modulation of the hormone setting by Rhodococcus fascians results in ectopic KNOX activation in Arabidopsis. Plant Physiol. 146, 1267–1281. 10.1104/pp.107.113969 PubMed DOI PMC

Dhandapani P., Song J., Novák O., Jameson P. E. (2017). Infection by Rhodococcus fascians maintains cotyledons as a sink tissue for the pathogen. Ann. Bot. 119, 841–852. 10.1093/aob/mcw202 PubMed DOI PMC

Dhandapani P., Song J., Novák O., Jameson P. E. (2018). Both epiphytic and endophytic strains of Rhodococcus fascians influence transporter gene expression and cytokinins in infected Pisum sativum L. seedlings. Plant Growth Regul. 85, 231–242. 10.1007/s10725-018-0387-3 DOI

Dobrev P. I., Kamínek M. (2002). Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction. J. Chromatogr. A 950, 21–29. 10.1016/S0021-9673(02)00024-9 PubMed DOI

Dolzblasz A., Banasiak A. H., Vereecke D. (2018) Neovascularization during leafy gall formation on Arabidopsis thaliana upon Rhodococcus fascians infection. Planta 247, 215–228. 10.1007/s00425-017-2778-5 PubMed DOI

Dulla G., Lindow S. E. (2008). Quorum size of Pseudomonas syringae is small and dictated by water availability on the leaf surface. Proc. Natl. Acad. Sci. U.S.A. 105, 3082–3087. 10.1073/pnas.0711723105 PubMed DOI PMC

Eason J. R., Jameson E. P., Bannister P. (1995). Virulence assessment of Rhodococcus fascians strains on pea cultivars. Plant Pathol. 44, 141–147.

Eason J. R., Morris R. O., Jameson E. P. (1996). The relationship between virulence and cytokinin production by Rhodococcus fascians (Tilford 1936) Goodfellow 1984. Plant Pathol. 45, 323–331. 10.1046/j.1365-3059.1996.d01-130.x DOI

Evidente A., Fujii T., Iacobellis N. S., Riva S., Sisto A., Surico G. (1991). Structure-activity relationships of zeatin cytokinins produced by plant pathogenic Pseudomonades. Phytochem 30, 3505–3510. 10.1016/0031-9422(91)80055-6 DOI

Evidente A., Suricot G., Iacobellis N. S., Randazzo G. (1986). 1′-methyl-zeatin, an additional cytokinin from Pseudomonas syringae pv. savastanoi. Phytochem 25, 525–526. 10.1016/S0031-9422(00)85515-6 DOI

Francis I., De Keyser A., De Backer P., Simon-Mateo C., Kalkus J., Pertry I., et al. . (2012). pFiD188, the linear virulence plasmid of Rhodococcus fascians D188. Mol. Plant Mic. Int. 25, 637–647. 10.1094/MPMI-08-11-0215 PubMed DOI

Francis I. M., Stes E., Zhang Y., Rangel D., Audenaert K., Vereecke D. (2016). Mining the genome of Rhodococcus fascians, a plant growth-promoting bacterium gone astray. New Biotechnol. 33, 706–717. 10.1016/j.nbt.2016.01.009 PubMed DOI

Francis I. M., Vereecke D. (2019) Plant-associated Rhodococcus species, for better for worse, in Biology of Rhodococcus, Vol. 16, ed Alvarez H. Microbiology Monographs (Cham: Springer; ), 359–377. 10.1007/978-3-030-11461-9_13 DOI

Gajdošová S., Spíchal L., Kamínek M., Hoyerová K., Novák O., Dobrev P. I., et al. . (2011). Distribution, biological activities, metabolism, and the conceivable function of cis-zeatin-type cytokinins in plants. J. Exp. Bot. 62, 2827–2840. 10.1093/jxb/erq457 PubMed DOI

Gális I., Bilyeu K., Wood G., Jameson P. E. (2005). Rhodococcus fascians: shoot proliferation without elevated cytokinins? Plant Growth Regul. 46, 109–115. 10.1007/s10725-005-7752-8 DOI

Goethals K., Vereecke D., Jaziri M., Van Montagu M., Holsters M. (2001). Leafy gall formation by Rhodococcus fascians. Annu. Rev. Phytopathol. 3, 27–52. 10.1146/annurev.phyto.39.1.27 PubMed DOI

Goodfellow M. (1984). Reclassification of Corynebacterium fascians (Tilford) Dawson in the genus Rhodococcus as Rhodococcus fascians comb. Nov. Syst. Appl. Microbiol. 5, 225–229. 10.1016/S0723-2020(84)80023-5 DOI

Hoyerová K., Gaudinová A., Malbeck J., Dobrev P. I., Kocábek T., Šolcová B., et al. . (2006). Efficiency of different methods of extraction and purification of cytokinins. Phytochemistry 67, 1151–1159. 10.1016/j.phytochem.2006.03.010 PubMed DOI

Jameson P. E. (1994). Cytokinin metabolism and compartmentation, in Cytokinins—Chemistry, Activity, and Function, eds Mok D. W. S., Mok M. C. (Boca Raton, FL, CRC Press; ), 113–128.

Jameson P. E. (2000). Cytokinins and auxins in plant-pathogen interactions – an overview. Plant Growth Regul. 32, 369–380. 10.1023/A:1010733617543 DOI

Kado C. I., Heskett M. G. (1970). Selective media for isolation of Agrobacterium, Corynebacterium, Erwinia, Pseudomonas and Xanthomonas. Phytopathol. 60, 969–976. 10.1094/Phyto-60-969 PubMed DOI

Keikha M. (2018). Williamsia spp. are emerging opportunistic bacteria. N. Microbes N. Infect. 21, 88–89. 10.1016/j.nmni.2017.11.002 PubMed DOI PMC

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

Klämbt D., Thies G., Skoog F. (1966). Isolation of cytokinins from Corynebacterium fascians. Proc. Natl. Acad. Sci. U.S.A. 56, 52–59. 10.1073/pnas.56.1.52 PubMed DOI PMC

Kuroha T., Tokunaga H., Kojima M., Ueda N., Ishida T., Nagawa S., et al. . (2009). Functional analyses of LONELY GUY cytokinin-activating enzymes reveal the importance of the direct activation pathway in Arabidopsis. Plant Cell 21, 3152–3169. 10.1105/tpc.109.068676 PubMed DOI PMC

Lacey M. S. (1936). Studies in bacteriosis. XXII. 1. Isolation of a bacterium associated with “fasciaton” of sweet peas, “cauliflower” strawberry plants and “leafy gall” of various plants. Ann. Applied Biol. 23, 302–310. 10.1111/j.1744-7348.1936.tb05569.x DOI

Lacey M. S. (1939). Studies in bacteriosis. XXIV. studies on bacterium associated with leafy galls, fasciaton and “cauliflower” disease of various plants. Part III. Further isolation, inoculation experiments and cultural studies. Ann. Appl. Biol. 26, 262–278. 10.1111/j.1744-7348.1939.tb06970.x DOI

Lawson E., Gantotti B., Starr M. (1982). A 78-megadalton plasmid occurs in avirulent strains as well as virulent strains of Corynebacterium fascians. Curr. Microbiol. 7, 327–332. 10.1007/BF01572598 DOI

Lomin S. N., Krivosheev D. M., Steklov M. Y., Arkhipov D. V., Osolodkin D. I., Schmülling T., et al. . (2015). Plant membrane assays with cytokinin receptors underpin the unique role of free cytokinin bases as biologically active ligands. J. Exp. Bot. 66, 1851–1863. 10.1093/jxb/eru522 PubMed DOI PMC

MacDonald E. M., Powell G. K., Regier D. A., Glass N. L., Roberto F., Kosuge T., et al. . (1986). Secretion of zeatin, ribosylzeatin, and ribosyl-1″-methylzeatin by Pseudomonas savastanoi: plasmid-coded cytokinin biosynthesis. Plant Physiol. 82, 742–747. 10.1104/pp.82.3.742 PubMed DOI PMC

McKenzie M. J., Mett V., Reynolds P. H. S., Jameson P. E. (1998). Controlled cytokinin production in transgenic tobacco using a copper-inducible promoter. Plant Physiol. 116, 969–977. 10.1104/pp.116.3.969 PubMed DOI PMC

Miller H. J., Janse J. D., Kamerman W., Muller P. J. (1980). Recent observations on leafy gall in Liliaceae and some other families. Netherlands J Plant Pathol. 86, 55–68. 10.1007/BF01974335 DOI

Miyawaki K., Tarkowski P., Matsumoto-Kitano M., Kato T., Sato S., Tarkowska D., et al. . (2006). Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 103, 16598–16603. 10.1073/pnas.0603522103 PubMed DOI PMC

Morris R. O. (1987). Molecular aspects of hormone synthesis and action genes specifying auxin and cytokinin biosynthesis in prokaryotes, in Plant Hormones, ed. Davies P. J. (Dordrecht: Kluwer Academic Publishers; ), 318–339.

Murai N., Skoog F., Doyle M. E., Hanson R. S. (1980). Relationships between cytokinin production, presence of plasmids, and fasciation caused by strains of Corynebacterium fascians. Proc. Natl. Acad. Sci. U.S.A. 77, 619–623. 10.1073/pnas.77.1.619 PubMed DOI PMC

Ninan A. S., Grant J., Song J., Jameson P. E. (2019). Expression of genes related to sugar and amino acid transport and cytokinin metabolism during leaf development and senescence in Pisum sativum L. Plants 8:76. 10.3390/plants8030076 PubMed DOI PMC

Oduro K. A., Munnecke D. E. (1975). Persistence of pea cotyledons induced by Corynebacterium fascians. Phytopathol 65, 1114–1116. 10.1094/Phyto-65-1114 DOI

Perrson B. C., Esberg B., Olafsson O., Bjork G. R. (1994). Synthesis and fuction of isopentyl adenosine derivatives in tRNA. Biochimie 76, 1152–1160. 10.1016/0300-9084(94)90044-2 PubMed DOI

Pertry I. (2009). How the Fas Locus Contributes to Rhodococcus fascians Cytokinin Production: an in-depth Molecular and Biochemical Analysis. Gent: Ghent University; Available online at: http://hdl.handle.net/1854/LU-529624

Pertry I., Václavíková K., Depuydt S., Galuszka P., Spíchal L., Temmerman W., et al. . (2009). Identification of Rhodococcus fascians cytokinins and their modus operandi to reshape the plant. Proc. Natl. Acad. Sci. U.S.A. 106, 929–934. 10.1073/pnas.0811683106 PubMed DOI PMC

Pertry I., Václavíková K., Gemrotová M., Spíchal L., Galuszka P., Depuydt S., et al. . (2010). Rhodococcus fascians impacts plant development through the dynamic fas-mediated production of a cytokinin mix. Mol. Plant Mic. Interact. 23, 1164–1174. 10.1094/MPMI-23-9-1164 PubMed DOI

Powell G. K., Hommes N. G., Kuo J., Castle L. A., Morris R. O. (1988). Inducible expression of cytokinin biosynthesis in Agrobacterium tumefaciens by plant phenolics. Mol. Plant Mic. Interact. 1, 235–242. 10.1094/MPMI-1-235 PubMed DOI

Radhika V., Ueda N., Tsuboi Y., Kojima M., Kikuchi J., Kudo K., et al. . (2015). Methylated cytokinins from the phytopathogen Rhodococcus fascians mimic plant hormone activity. Plant Physiol. 169, 1118–1126. 10.1104/pp.15.00787 PubMed DOI PMC

Rittenberg D., Foster L. (1940). A new procedure for quantitative analysis by isotope dilution, with application to the determination of amino acids and fatty acids. J. Biol. Chem. 133, 727–744.

Sakakibara H. (2006). Cytokinins: activity, biosynthesis, and translocation. Ann. Rev. Plant Biol. 57, 431–449. 10.1146/annurev.arplant.57.032905.105231 PubMed DOI

Savory E. A., Fuller S. L., Weisberg A. J., Thomas W. J., Gordon M. I., Stevens D. M., et al. . (2017). Evolutionary transitions between beneficial and phytopathogenic Rhodococcus challenge disease management. eLife 6:e30925. 10.7554/eLife.30925 PubMed DOI PMC

Scarbrough E., Armstrong D. J., Skoog F., Frihart C. R., Leonard N. J. (1973). Isolation of cis-zeatin from Corynebacterium fascians cultures. Proc. National Acad. Sci. U.S.A. 70, 3825–3829. 10.1073/pnas.70.12.3825 PubMed DOI PMC

Schäfer M., Brütting C., Meza-Canales I. D., Großkinsky D. K., Vankova R., Baldwin I. T., et al. . (2015). The role of cis-zeatin-type cytokinins in plant growth regulation and mediating responses to environmental interactions. J. Exp. Bot. 66, 4873–4884. 10.1093/jxb/erv214 PubMed DOI PMC

Skoog F., Miller C. O. (1957). Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp. Soc. Exp. Biol. 11, 118–130. PubMed

Song J., Jiang L., Jameson P. E. (2012). Co-ordinate regulation of cytokinin gene family members during flag leaf and reproductive development in wheat. BMC Plant Biol. 12:78. 10.1186/1471-2229-12-78 PubMed DOI PMC

Stange R. R., Jeffares D., Young C., Scott D. B., Eason J. R., Jameson P. E. (1996). PCR amplification of the fas-1 gene for the detection of virulent strains of Rhodococcus fascians. Plant Pathol. 45, 407–417. 10.1046/j.1365-3059.1996.d01-154.x DOI

Stes E., Francis I., Pertry I., Dolzblasz A., Depuydt S., Vereecke D. (2013). The leafy gall syndrome induced by Rhodococcus fascians. FEMS Microbiol Lett. 342, 187–194. 10.1111/1574-6968.12119 PubMed DOI

Stes E., Vandeputte O. M., Jaziri M. E., Holsters M., Vereecke D. (2011). A successful bacterial coup d'état: how Rhodococcus fascians redirects plant development. Annu. Rev. Phytopathol. 49, 69–86. 10.1146/annurev-phyto-072910-095217 PubMed DOI

Suzuki R., Shimodaira H. (2006). Pvclust: An R Package for Assessing the Uncertainty in Hierarchical Clustering. Bioinformatics 22, 1540–1542. 10.1093/bioinformatics/btl117 PubMed DOI

Svačinová J., Novák O., Plačková L., Lenobel R., Holík J., Strnad M., et al. (2012). A new approach for cytokinin isolation from Arabidopsis tissues using miniaturized purification: pipette tip solid-phase extraction. Plant Methods 18:17 10.1186/1746-4811-8-17 PubMed DOI PMC

Taller B. J. (1994). Distribution, biosynthesis, and function of cytokinins in tRNA, in Cytokinins: Chemistry, Activity, and Function, eds. Mok D.W.S., Mok M. C. (CRC Press, Boca Raton, FL: ), 101–112.

Tarkowski P., Václavíkova K., Novák O., Pertry I., Hanuš J., Whenham R., et al. . (2010). Analysis of 2-methylthio-derivatives of isoprenoid cytokinins by liquid chromatography-tandem mass spectrometry. Anal. Chim. Acta 680, 86–91. 10.1016/j.aca.2010.09.020 PubMed DOI

Thimann K. V., Sachs T. (1966). The role of cytokinins in the “fasciation” disease caused by Corynebacterium fascians. American J. Bot. 53, 731–739. 10.1002/j.1537-2197.1966.tb14030.x DOI

Tilford P. E. (1936). Fasciation of sweet peas caused by Phytomonas fascians. J. Agri. Res. 53, 383–394.

Vereecke D., Burssens S., Simón-Mateo C., Inze D., Van Montagu M., Goethals K., et al. . (2000). The Rhodococcus fascians-plant interaction: morphological traits and biotechnological applications. Planta 210, 241–251. 10.1007/PL00008131 PubMed DOI

Zürcher E., Müller B. (2016). Cytokinin synthesis, signaling, and function—advances and new insights. Int. Rev. Cell Mol. Biol. 324, 1–38. 10.1016/bs.ircmb.2016.01.001 PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...