Infection by Rhodococcus fascians maintains cotyledons as a sink tissue for the pathogen
Jazyk angličtina Země Anglie, Velká Británie Médium print
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
27864224
PubMed Central
PMC5378184
DOI
10.1093/aob/mcw202
PII: mcw202
Knihovny.cz E-zdroje
- Klíčová slova
- Apical dominance, Pisum sativum L., Rhodococcus fascians, SWEET, amino acid transporter, cell wall invertase, cytokinin, cytokinin oxidase/dehydrogenase, pea, seed, sink and source, sucrose transporter,
- MeSH
- cytokininy metabolismus MeSH
- hrách setý genetika mikrobiologie MeSH
- interakce hostitele a patogenu MeSH
- klíčení MeSH
- kotyledon růst a vývoj mikrobiologie MeSH
- nemoci rostlin mikrobiologie MeSH
- polymerázová řetězová reakce MeSH
- Rhodococcus fyziologie MeSH
- semena rostlinná mikrobiologie MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- cytokininy MeSH
BACKGROUND AND AIMS: Pisum sativum L. (pea) seed is a source of carbohydrate and protein for the developing plant. By studying pea seeds inoculated by the cytokinin-producing bacterium, Rhodococcus fascians , we sought to determine the impact of both an epiphytic (avirulent) strain and a pathogenic strain on source-sink activity within the cotyledons during and following germination. METHODS: Bacterial spread was monitored microscopically, and real-time reverse transcription-quantitative PCR was used to determine the expression of cytokinin biosynthesis, degradation and response regulator gene family members, along with expression of family members of SWEET , SUT , CWINV and AAP genes - gene families identified initially in pea by transcriptomic analysis. The endogenous cytokinin content was also determined. KEY RESULTS: The cotyledons infected by the virulent strain remained intact and turned green, while multiple shoots were formed and root growth was reduced. The epiphytic strain had no such marked impact. Isopentenyl adenine was elevated in the cotyledons infected by the virulent strain. Strong expression of RfIPT , RfLOG and RfCKX was detected in the cotyledons infected by the virulent strain throughout the experiment, with elevated expression also observed for PsSWEET , PsSUT and PsINV gene family members. The epiphytic strain had some impact on the expression of these genes, especially at the later stages of reserve mobilization from the cotyledons. CONCLUSIONS: The pathogenic strain retained the cotyledons as a sink tissue for the pathogen rather than the cotyledon converting completely to a source tissue for the germinating plant. We suggest that the interaction of cytokinins, CWINVs and SWEETs may lead to the loss of apical dominance and the appearance of multiple shoots.
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Ando S, Asano T, Tsushima S, Kamachi S, Hagio T, Tabei Y.. 2005. Changes in gene expression of putative isopentenyltransferase during clubroot development in Chinese cabbage (Brassica rapa L.). Physiological and Molecular Plant Pathology 67: 59–67.
Antoniadi I, Plačková L, Simonovik B, et al. 2015. Cell-type specific cytokinin distribution within the Arabidopsis primary root apex. The Plant Cell 27: 1955–1967. PubMed PMC
Albacete A, Cantero-Navarro E, Großkinsky DK, et al. 2015. Ectopic overexpression of the cell wall invertase gene CIN1 leads to dehydration avoidance in tomato. Journal of Experimental Botany 66: 863–878. PubMed PMC
Balibrea Lara ME, Gonzalez Garcia M-C, Fatima T, et al. 2004. Extracellular invertase is an essential component of cytokinin-mediated delay of senescence. The Plant Cell 16: 1276–1287. PubMed PMC
Barau J, Grandis A, Carvalho VMdA, et al. 2015. Apoplastic and intracellular plant sugars regulate developmental transitions in witches’ broom disease of cacao. Journal of Experimental Botany 66: 1325–1337. PubMed PMC
Barbier FF, Lunn JE, Beveridge CA.. 2015. Ready, steady, go! A sugar hit starts the race to shoot branching. Current Opinion in Plant Biology 25: 39–45. PubMed
Berger S, Sinha AK, Roitsch T.. 2007. Plant physiology meets phytopathology: plant primary metabolism and plant–pathogen interactions. Journal of Experimental Botany 58: 4019–4026. PubMed
Bustin SA, Benes V, Garson JA, et al. 2009. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 55: 611–622. PubMed
Carletom HM, Druvy RAB.. 1957. Histological technique for normal pathological tissues and the identification of parasites, 3rd edn.London: Oxford University Press.
Chandran D. 2015. Co-option of developmentally regulated plant SWEET transporters for pathogen nutrition and abiotic stress tolerance. IUBMB Life 67: 461–71. PubMed
Chandran D, Inada N, Hather G, Kleindt CK, Wildermuth MC.. 2010. Laser microdissection of Arabidopsis cells at the powdery mildew infection site reveals site-specific processes and regulators. Proceedings of the National Academy of Sciences, USA 107: 460–465. PubMed PMC
Chen H-Y, Huh J-H, Yu Y-C, et al. 2015. The Arabidopsis vacuolar sugar transporter SWEET2 limits carbon sequestration from roots and restricts Pythium infection. The Plant Journal 83: 1046–1058. PubMed
Chen L-Q, Hou B-H, Lalonde S, et al. 2010. Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468: 527–532. PubMed PMC
Chen L-Q, Qu XQ, Hou B-H, et al. 2012. Sucrose efflux mediated by SWEET proteins as a key step for phloem transport. Science 335: 207–211. PubMed
Cornelis K, Ritsema T, Nijsse J, Holsters M, Goethals K, Jaziri M.. 2001. The plant pathogen Rhodococcus fascians colonizes the exterior and interior of the aerial parts of plants. Molecular Plant-Microbe Interactions 14: 599–608. PubMed
Creason AL, Vandeputte OM, Savory EA, et al. 2014. Analysis of genome sequences from plant pathogenic Rhodococcus reveals genetic novelties in virulence loci. PLoS One 9: e101996. PubMed PMC
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 Physiology 146: 1267–1281. PubMed PMC
Depuydt S, Tenkamp S, Fernie AR, et al. 2009. An integrated genomics approach to define niche establishment by Rhodococcus fascians. Plant Physiology 149: 1366–1386. PubMed PMC
Derveaux S, Vandesompele J, Hellemans J.. 2010. How to do successful gene expression analysis using real-time PCR. Methods 50: 227–230. PubMed
Dhandapani P. 2014. Rhodococcus fascians–plant interactions: microbiological and molecular aspects. PhD Thesis, University of Canterbury, New Zealand.
Dobrev PI, Kamínek M.. 2002. Fast and efficient separation of cytokinins from auxin and abscisic acid and their purification using mixed-mode solid-phase extraction. Journal of Chromatography A 950: 21–29. PubMed
Eason JR, Jameson PE, Bannister P.. 1995. Virulence assessment of Rhodococcus fascians strains on pea cultivars. Plant Pathology 44: 141–147.
Eason JR, Morris RO, Jameson PE.. 1996. The relationship between virulence and cytokinin production by Rhodococcus fascians (Tilford 1936) Goodfellow 1984. Plant Pathology 45: 323–331.
Ehness R, Ecker M, Godt DE, Roitsch T.. 1997. Glucose and stress independently regulate source and sink metabolism and defense mechanisms via signal transduction pathways involving protein phosphorylation. The Plant Cell 9: 1825–1841. PubMed PMC
Ehneß R, Roitsch T.. 1997. Co-ordinated induction of mRNAs for extracellular invertase and a glucose transporter in Chenopodium rubrum by cytokinins. The Plant Journal 11: 539–548. PubMed
Eom JS, Chen LQ, Sosso D, et al. 2015. SWEETs, transporters for intracellular and intercellular sugar translocation. Current Opinion in Plant Biology 25: 53–62. PubMed
Evans T, Song J, Jameson PE.. 2012. Micro-scale chlorophyll analysis and developmental expression of a cytokinin oxidase/dehydrogenase gene during leaf development and senescence. Plant Growth Regulation 66: 95–99.
Fagard M, Launay A, Clément G, et al. 2014. Nitrogen metabolism meets phytopathology. Journal of Experimental Botany 65: 5643–5656. PubMed
Francis IM, 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 Biotechnology (in press). PubMed
Galis I, Bilyeu K, Wood G, Jameson PE.. 2005. Rhodococcus fascians: shoot proliferation without elevated cytokinins? Plant Growth Regulation 46: 109–115.
Green TR, Baisted DJ.. 1972. Development of the activities of enzymes of the isoprenoid pathway during early stages of pea-seed germination. Biochemical Journal 130: 983–995. PubMed PMC
Großkinsky DK, Naseem M, Abdelmohsen UR, et al. 2011. Cytokinins mediate resistance against Pseudomonas syringae in tobacco through increased antimicrobial phytoalexin synthesis independent of salicylic acid signaling. Plant Physiology 157: 815–830. PubMed PMC
Guo WJ, Nagy R, Chen HY, et al. 2014. SWEET17, a facilitative transporter, mediates fructose transport across the tonoplast of Arabidopsis roots and leaves. Plant Physiology 164: 777–789. PubMed PMC
Gutierrez L, Mauriat M, Pelloux J, Bellini C, Van Wuytswinkel O.. 2008. Towards a systematic validation of references in real-time RT–PCR. The Plant Cell 20: 1734–1735. PubMed PMC
Hwang I, Sheen J, Muller B.. 2012. Cytokinin signaling networks. Annual Review of Plant Biology 63: 353–380. PubMed
Jameson PE. 2000. Cytokinins and auxins in plant–pathogen interactions – an overview. Plant Growth Regulation 32: 369–380.
Jameson PE. 2017. Cytokinins In: Thomas B, Murray B, Murphy DJ, eds. Encyclopedia of applied plant sciences, Vol 1 Waltham, MA: Academic Press, pp. 391-402.
Jameson PE, Song J.. 2016. Cytokinin: a key driver of seed yield. Journal of Experimental Botany 67: 593–606. PubMed
Kado CI, Heskett MG.. 1970. Selective media for isolation of Agrobacterium, Corynebacterium, Erwinia, Pseudomonas and Xanthomonas. Phytopatholoy 60: 969–976. PubMed
Kitin P, Iliev I, Scaltsoyiannes A, Nellas C, Rubos A, Funada R.. 2005. A comparative histological study between normal and fasciated shoots of Prunus avium generated in vitro. Plant Cell, Tissue and Organ Culture 82: 141–150.
Lacey MS. 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. Annals of Applied Biology 23: 302–310.
Lawson E, Gantotti B, Starr M.. 1982. A 78-megadalton plasmid occurs in avirulent strains as well as virulent strains of Corynebacterium fascians. Current Microbiology 7: 327–332.
Li T, Huang S, Zhou J, Yang B.. 2013. Designer TAL effectors induce disease susceptibility and resistance to Xanthomonas oryzae pv. oryzae in rice. Molecular Plant 6: 781–789. PubMed
Lomin SN, Krivosheev DM, Steklov MY, et al. 2015. Plant membrane assays with cytokinin receptors underpin the unique role of free cytokinin bases as biologically active ligands. Journal of Experimental Botany 66: 1851–1863. PubMed PMC
Mothes K, Engelbrecht L.. 1963. On the activity of a kinetin-like root factor. Life Sciences 2: 852–857.
Nandi S, Palni L.. 1989. Transport and metabolism of dihydrozeatin riboside in germinating lupin seeds. Journal of Experimental Botany 40: 615–621.
Nandi S, Palni L, Letham D, Knypl J.. 1988. The biosynthesis of cytokinins in germinating lupin seeds. Journal of Experimental Botany 39: 1649–1665.
Nawa Y, Asahi T.. 1971. Rapid development of mitichondria in pea cotyledons during early stage of germination. Plant Physiology 48: 671–674. PubMed PMC
Patil G, Valliyodan B, Deshmukh R, et al. 2015. Soybean (Glycine max) SWEET gene family: insights through comparative genomics, transcriptome profiling and whole genome re-sequence analysis. BMC Genomics 16: 520. PubMed PMC
Pertry I, Václavíková K, Depuydt S, et al. 2009. Identification of Rhodococcus fascians cytokinins and their modus operandi to reshape the plant. Proceedings of the National Academy of Sciences, USA 106: 929–934. PubMed PMC
Pertry I, Václavíková K, Gemrotová M, et al. 2010. Rhodococcus fascians impacts plant development through the dynamic fas-mediated production of a cytokinin mix. Molecular Plant-Microbe Interactions 23: 1164–1174. PubMed
Pfaffl M, Hageleit M.. 2001. Validities of mRNA quantification using recombinant RNA and recombinant DNA external calibration curves in real-time RT–PCR. Biotechnology Letters 23: 275–282.
Pratelli R, Pilot G.. 2014. Regulation of amino acid metabolic enzymes and transporters in plants. Journal of Experimental Botany 65: 5535–5556. PubMed
Radhika V, Ueda N, Tsuboi Y, et al. 2015. Methylated cytokinins from the phytopathogen Rhodococcus fascians mimic plant hormone activity. Plant Physiology 169: 1118–1126. PubMed PMC
Roitsch T, Gonzalez MC.. 2004. Function and regulation of plant invertases: sweet sensations. Trends in Plant Science 9: 606–613. PubMed
Siemens J, Gonzalez MC, Wolf S, et al. 2011. Extracellular invertase is involved in the regulation of clubroot disease in Arabidopsis thaliana. Molecular Plant Pathology 12: 247–262. PubMed PMC
Song J, Jiang L, Jameson PE.. 2012. Co-ordinate regulation of cytokinin gene family members during flag leaf and reproductive development in wheat. BMC Plant Biology 12: 78. PubMed PMC
Spichal L. 2012. Cytokinins – recent news and views of evolutionally old molecules. Functional Plant Biology 39: 267–284. PubMed
Stange RR, Jr, Jeffares D, Young C, Scott DB, Eason JR, Jameson PE.. 1996. PCR amplification of the fas-1 gene for the detection of virulent strains of Rhodococcus fascians. Plant Pathology 45: 407–417.
Stes E, Vandeputte OM, El Jazziri M, Holsters M, Vereecke D.. 2011. A successful bacterial coup d’état: how Rhodococcus fascians redirects plant development. Annual Review of Phytopathology 49: 69–86. PubMed
Streubel J, Pesce C, Hutin M, Koebnik R, Boch J, Szurek B.. 2013. Five phylogenetically close rice SWEET genes confer TAL effector-mediated susceptibility to Xanthomonas oryzae pv. oryzae. New Phytologist 200: 808–819. PubMed
Svačinová J, Novák O, Plačková L, et al. 2012. A new approach for cytokinin isolation from Arabidopsis tissues using miniaturized purification: pipette tip solid-phase extraction. Plant Methods 8: 17. PubMed PMC
Tamura K, Dudley J, Nei Ma, Kumar S.. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596–1599. PubMed
Tegeder M. 2012. Transporters for amino acids in plant cells: some functions and many unknowns. Current Opinion in Plant Biology 15: 315–21. PubMed
Tegeder M, Ward JM.. 2012. Molecular evolution of plant AAP and LHT amino acid transporters. Frontiers in Plant Science 3: 21. PubMed PMC
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG.. 1997. The CLUSTALX windows interface: flexible strategies for multiple sequence alignment aided by quality tools. Nucleic Acids Research 25: 4876–4882. PubMed PMC
Vandesompele J, De Preter K, Pattyn F, et al. 2002. Accurate normalization of real-time quantitative RT–PCR data by geometric averaging of multiple internal control genes. Genome Biology 3: research0034.1–research0034.1. PubMed PMC
Weitbrecht K, Muller K, Leubner-Metzger G.. 2011. First off the mark: early seed germination. Journal of Experimental Botany 62: 3289–3309. PubMed
Wellburn AR. 1994. The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. Journal of Plant Physiology 144: 307–313.
Werner T, Schmülling T.. 2009. Cytokinin action in plant development. Current Opinion in Plant Biology 12: 527–538. PubMed
Zhou J, Peng Z, Long J, et al. 2015. Gene targeting by the TAL effector PthXo2 reveals cryptic resistance gene for bacterial blight of rice. The Plant Journal 82: 632–43. PubMed
Cytokinins and Expression of SWEET, SUT, CWINV and AAP Genes Increase as Pea Seeds Germinate