• This record comes from PubMed

Novel Insights into the Effect of Pythium Strains on Rapeseed Metabolism

. 2020 Sep 25 ; 8 (10) : . [epub] 20200925

Status PubMed-not-MEDLINE Language English Country Switzerland Media electronic

Document type Journal Article

Grant support
TJ01000451 Technology Agency of the Czech Republic
1304119 Grantová Agentura, Univerzita Karlova
SVV260427/2020 Grantová Agentura, Univerzita Karlova

Links

PubMed 32992822
PubMed Central PMC7650609
DOI 10.3390/microorganisms8101472
PII: microorganisms8101472
Knihovny.cz E-resources

Pythium oligandrum is a unique biological control agent. This soil oomycete not only acts as a mycoparasite, but also interacts with plant roots and stimulates plant defense response via specific elicitors. In addition, P. oligandrum can synthetize auxin precursors and stimulate plant growth. We analyzed the secretomes and biochemical properties of eleven Pythium isolates to find a novel and effective strain with advantageous features for plants. Our results showed that even closely related P. oligandrum isolates significantly differ in the content of compounds secreted into the medium, and that all strains secrete proteins, amino acids, tryptamine, phenolics, and hydrolytic enzymes capable of degrading cell walls (endo-β-1,3-glucanase, chitinase, and cellulase), exoglycosidases (especially β-glucosidase), proteases, and phosphatases. The most different strain was identified as a not yet described Pythium species. The changes in metabolism of Brassica napus plants grown from seeds coated with the tested Pythium spp. were characterized. Enhanced levels of jasmonates, ethylene precursor, and salicylic acid may indicate better resistance to a wide variety of pathogens. Glucosinolates, as defense compounds against insects and herbivores, were enhanced in young plants. Altogether, P. oligandrum strains varied in their life strategies, and either they could perform equally as plant growth promoters and mycoparasites or they had developed one of these strategies better.

See more in PubMed

Gerbore J., Benhamou N., Vallance J., Le Floch G., Grizard D., Regnault-Roger C., Rey P. Biological control of plant pathogens: Advantages and limitations seen through the case study of Pythium oligandrum. Environ. Sci. Pollut. Res. Int. 2014;21:4847–4860. doi: 10.1007/s11356-013-1807-6. PubMed DOI

Sivan A., Elad Y., Chet I. Biological control effects of a new isolate of Trichoderma harzianum on Pythium aphanidermatum. Phytopathology. 1984;74:498–501. doi: 10.1094/Phyto-74-498. DOI

Benhamou N., le Floch G., Vallance J., Gerbore J., Grizard D., Rey P. Pythium oligandrum: An example of opportunistic success. Microbiology. 2012;158:2679–2694. doi: 10.1099/mic.0.061457-0. PubMed DOI

Gabrielova A., Mencl K., Suchanek M., Klimes R., Hubka V., Kolarik M. The oomycete Pythium oligandrum can suppress and kill the causative agents of dermatophytoses. Mycopathologia. 2018;183:751–764. doi: 10.1007/s11046-018-0277-2. PubMed DOI PMC

Kushwaha S.K., Vetukuri R.R., Grenville-Briggs L.J. Draft genome sequence of the mycoparasitic oomycete Pythium periplocum strain CBS 532.74. Genome Announc. 2017;5:e00057–17. doi: 10.1128/genomeA.00057-17. PubMed DOI PMC

Ponchet M., Panabieres F., Milat M.L., Mikes V., Montillet J.L., Suty L., Triantaphylides C., Tirilly Y., Blein J.P. Are elicitins cryptograms in plant-Oomycete communications? Cell Mol. Life Sci. 1999;56:1020–1047. doi: 10.1007/s000180050491. PubMed DOI PMC

Masunaka A., Sekiguchi H., Takahashi H., Takenaka S. Distribution and expression of elicitin-like protein genes of the biocontrol agent Pythium oligandrum. J. Phytopathol. 2010;158:417–426. doi: 10.1111/j.1439-0434.2009.01641.x. DOI

Le Floch G., Rey P., Benizri E., Benhamou N., Tirilly Y. Impact of auxin-compounds produced by the antagonistic fungus Pythium oligandrum or the minor pathogen Pythium group F on plant growth. Plant Soil. 2003;257:459–470. doi: 10.1023/A:1027330024834. DOI

Whipps J.M. Effect of media on growth and interactions between a range of soil-born glasshouse pathogens and antagonistic fungi. New Phytol. 1987;107:127–142. doi: 10.1111/j.1469-8137.1987.tb04887.x. DOI

Vesely D. Studies of the mycoparasitism in rhizosphere of emerging sugar-beet. Zentralbl. Bakteriol. Naturwiss. 1978;133:195–200. doi: 10.1016/S0323-6056(78)80001-9. PubMed DOI

Hyde K.D., Nilsson R.H., Alias S.A., Ariyawansa H.A., Blair J.E., Cai L., de Cock A.W., Dissanayake A.J., Glockling S.L., Goonasekara I.D. One stop shop: Backbones trees for important phytopathogenic genera: I. Fungal Divers. 2014;67:21–125. doi: 10.1007/s13225-014-0298-1. DOI

Robideau G.P., De Cock A.W., Coffey M.D., Voglmayr H., Brouwer H., Bala K., Chitty D.W., Desaulniers N., Eggertson Q.A., Gachon C.M., et al. DNA barcoding of oomycetes with cytochrome c oxidase subunit I and internal transcribed spacer. Mol. Ecol. Resour. 2011;11:1002–1011. doi: 10.1111/j.1755-0998.2011.03041.x. PubMed DOI PMC

White T.J., Bruns T., Lee S., Taylor J.W. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M.A., Gelfand D.H., Sninsky J.J., White T.J., editors. PCR Protocols: A Guide to Methods and Applications. Academic Press, Inc.; New York, NY, USA: 1990. pp. 315–322.

Chen J., Lü L., Ye W., Wang Y.-C., Zheng X.-B. Pythium cedri sp. nov. (Pythiaceae, Pythiales) from southern China based on morphological and molecular characters. Phytotaxa. 2017;309:135–142. doi: 10.11646/phytotaxa.309.2.4. DOI

Faure C., Veyssiere M., Boelle B., San Clemente H., Bouchez O., Lopez-Roques C., Chaubet A., Martinez Y., Bezouska K., Suchanek M., et al. Long-read genome sequence of the sugar beet rhizosphere mycoparasite Pythium oligandrum. G3 Genes Genom. Genet. 2020;10:431–436. doi: 10.1534/g3.119.400746. PubMed DOI PMC

Berger H., Yacoub A., Gerbore J., Grizard D., Rey P., Sessitsch A., Compant S. Draft genome sequence of biocontrol agent Pythium oligandrum strain Po37, an Oomycota. Genome Announc. 2016;4:e00215–00216. doi: 10.1128/genomeA.00215-16. PubMed DOI PMC

Katoh K., Standley D.M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 2013;30:772–780. doi: 10.1093/molbev/mst010. PubMed DOI PMC

Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W., Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: Assessing the performance of PhyML 3.0. Syst. Biol. 2010;59:307–321. doi: 10.1093/sysbio/syq010. PubMed DOI

Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976;72:248–254. doi: 10.1016/0003-2697(76)90527-3. PubMed DOI

Schagger H. Tricine-SDS-PAGE. Nat. Protoc. 2006;1:16–22. doi: 10.1038/nprot.2006.4. PubMed DOI

Laemmli U.K. Cleavage of structural proteins during assembly of head of bacteriophage-T4. Nature. 1970;227:680–685. doi: 10.1038/227680a0. PubMed DOI

Hodek O., Krizek T., Coufal P., Ryslava H. Design of experiments for amino acid extraction from tobacco leaves and their subsequent determination by capillary zone electrophoresis. Anal. Bional. Chem. 2017;409:2383–2391. doi: 10.1007/s00216-017-0184-2. PubMed DOI

Dudonne S., Vitrac X., Coutiere P., Woillez M., Merillon J.M. Comparative study of antioxidant properties and total phenolic content of 30 plant extracts of industrial interest using DPPH, ABTS, FRAP, SOD, and ORAC assays. J. Agric. Food Chem. 2009;57:1768–1774. doi: 10.1021/jf803011r. PubMed DOI

Tupec M., Hyskova V., Belonoznikova K., Hranicek J., Cerveny V., Ryslava H. Characterization of some potential medicinal plants from Central Europe by their antioxidant capacity and the presence of metal elements. Food Biosci. 2017;20:43–50. doi: 10.1016/j.fbio.2017.08.001. DOI

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

Dobrev P.I., Vankova R. Quantification of abscisic acid, cytokinin, and auxin content in salt-stressed plant tissues. Methods Mol. Biol. 2012;913:251–261. doi: 10.1007/978-1-61779-986-0_17. PubMed DOI

Prerostova S., Dobrev P.I., Konradyova V., Knirsch V., Gaudinova A., Kramna B., Kazda J., Ludwig-Muller J., Vankova R. Hormonal responses to Plasmodiophora brassicae infection in Brassica napus cultivars differing in their pathogen resistance. Int. J. Mol. Sci. 2018;19:4024. doi: 10.3390/ijms19124024. PubMed DOI PMC

Lechtenberg M., Hensel A. Determination of glucosinolates in broccoli-based dietary supplements by cyclodextrin-mediated capillary zone electrophoresis. J. Food Compos. Anal. 2019;78:138–149. doi: 10.1016/j.jfca.2019.02.007. DOI

Hyskova V., Pliskova V., Cerveny V., Ryslava H. NADP-dependent enzymes are involved in response to salt and hypoosmotic stress in cucumber plants. Gen. Physiol. Biophys. 2017;36:247–258. doi: 10.4149/gpb_2016053. PubMed DOI

Yannarelli G.G., Fernandez-Alvarez A.J., Santa-Cruz D.M., Tomaro M.L. Glutathione reductase activity and isoforms in leaves and roots of wheat plants subjected to cadmium stress. Phytochemistry. 2007;68:505–512. doi: 10.1016/j.phytochem.2006.11.016. PubMed DOI

Coelho D.F., Saturnino T.P., Fernandes F.F., Mazzola P.G., Silveira E., Tambourgi E.B. Azocasein substrate for determination of proteolytic activity: Reexamining a traditional method using bromelain samples. BioMed Res. Int. 2016;2016:ID8409183. doi: 10.1155/2016/8409183. PubMed DOI PMC

Nakata H., Ishii S. Substrate activation of trypsin and acetyltrypsin caused by -N-benzoyl-L-arginine p-nitroanilide. J. Biochem. 1972;72:281–290. doi: 10.1093/oxfordjournals.jbchem.a129907. PubMed DOI

Anthon G.E., Barrett D.M. Determination of reducing sugars with 3-methyl-2-benzothiazolinonehydrazone. Anal. Biochem. 2002;305:287–289. doi: 10.1006/abio.2002.5644. PubMed DOI

Maseko S.T., Dakora F.D. Rhizosphere acid and alkaline phosphatase activity as a marker of P nutrition in nodulated Cyclopia and Aspalathus species in the Cape fynbos of South Africa. S. Afr. J. Bot. 2013;89:289–295. doi: 10.1016/j.sajb.2013.06.023. DOI

Beauchamp C., Fridovich I. Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. Anal. Biochem. 1971;44:276–287. doi: 10.1016/0003-2697(71)90370-8. PubMed DOI

Synkova H., Semoradova S., Schnablova R., Muller K., Pospisilova J., Ryslava H., Malbeck J., Cerovska N. Effects of biotic stress caused by Potato virus Y on photosynthesis in ipt transgenic and control Nicotiana tabacum L. Plant Sci. 2006;171:607–616. doi: 10.1016/j.plantsci.2006.06.002. DOI

Spoustova P., Hyskova V., Muller K., Schnablova R., Ryslava H., Cerovska N., Malbeck J., Cvikrova M., Synkova H. Tobacco susceptibility to Potato virus Y-NTN infection is affected by grafting and endogenous cytokinin content. Plant Sci. 2015;235:25–36. doi: 10.1016/j.plantsci.2015.02.017. PubMed DOI

Plaats-Niterink A.J.v.d. Monograph of the genus Pythium. Stud. Mycol. 1981;21:1–244.

McGowan J., Fitzpatrick D.A. Genomic, network, and phylogenetic analysis of the oomycete effector arsenal. MSphere. 2017;2:e00408–17. doi: 10.1128/mSphere.00408-17. PubMed DOI PMC

Judelson H.S. Metabolic diversity and novelties in the oomycetes. Annu. Rev. Microbiol. 2017;71:21–39. doi: 10.1146/annurev-micro-090816-093609. PubMed DOI

Brunner F., Wirtz W., Rose J.K., Darvill A.G., Govers F., Scheel D., Nurnberger T. A beta-glucosidase/xylosidase from the phytopathogenic oomycete, Phytophthora infestans. Phytochemistry. 2002;59:689–696. doi: 10.1016/S0031-9422(02)00045-6. PubMed DOI

Bowyer P., Clarke B.R., Lunness P., Daniels M.J., Osbourn A.E. Host range of a plant pathogenic fungus determined by a saponin detoxifying enzyme. Science. 1995;267:371–374. doi: 10.1126/science.7824933. PubMed DOI

Crombie W.M.L., Crombie L., Green J.B., Lucas J.A. Pathogenicity of ‘take-all’ fungus to oats: Its relationship to the concentration and detoxification of the four avenacins. Phytochemistry. 1986;25:2075–2083. doi: 10.1016/0031-9422(86)80069-3. DOI

Ivanov D.A., Bernards M.A. Ginsenosidases and the pathogenicity of Pythium irregulare. Phytochemistry. 2012;78:44–53. doi: 10.1016/j.phytochem.2012.02.024. PubMed DOI

Brzobohaty B., Moore I., Kristoffersen P., Bako L., Campos N., Schell J., Palme K. Release of active cytokinin by a beta-glucosidase localized to the maize root meristem. Science. 1993;262:1051–1054. doi: 10.1126/science.8235622. PubMed DOI

Le Roy J., Huss B., Creach A., Hawkins S., Neutelings G. Glycosylation is a major regulator of phenylpropanoid availability and biological activity in plants. Front. Plant Sci. 2016;7:735. doi: 10.3389/fpls.2016.00735. PubMed DOI PMC

Ma Y. Seed coating with beneficial microorganisms for precision agriculture. Biotechnol. Adv. 2019;37:1–11. doi: 10.1016/j.biotechadv.2019.107423. PubMed DOI

Tsuda K. Division of Tasks: Defense by the Spatial Separation of Antagonistic Hormone Activities. Plant Cell Physiol. 2017;54:3–4. doi: 10.1093/pcp/pcx208. PubMed DOI

Pieterse C.M., Van der Does D., Zamioudis C., Leon-Reyes A., Van Wees S.C. Hormonal modulation of plant immunity. Annu. Rev. Cell Dev. Biol. 2012;28:489–521. doi: 10.1146/annurev-cellbio-092910-154055. PubMed DOI

Kawamura Y., Takenaka S., Hase S., Kubota M., Ichinose Y., Kanayama Y., Nakaho K., Klessig D.F., Takahashi H. Enhanced defense responses in Arabidopsis induced by the cell wall protein fractions from Pythium oligandrum require SGT1, RAR1, NPR1 and JAR1. Plant Cell Physiol. 2009;50:924–934. doi: 10.1093/pcp/pcp044. PubMed DOI

Takenaka S., Yamaguchi K., Masunaka A., Hase S., Inoue T., Takahashi H. Implications of oligomeric forms of POD-1 and POD-2 proteins isolated from cell walls of the biocontrol agent Pythium oligandrum in relation to their ability to induce defense reactions in tomato. J. Plant Physiol. 2011;168:1972–1979. doi: 10.1016/j.jplph.2011.05.011. PubMed DOI

Bjorkman M., Klingen I., Birch A.N., Bones A.M., Bruce T.J., Johansen T.J., Meadow R., Molmann J., Seljasen R., Smart L.E., et al. Phytochemicals of Brassicaceae in plant protection and human health-influences of climate, environment and agronomic practice. Phytochemistry. 2011;72:538–556. doi: 10.1016/j.phytochem.2011.01.014. PubMed DOI

Ishikawa S., Maruyama A., Yamamoto Y., Hara S. Extraction and characterization of glucosinolates and isothiocyanates from rape seed meal. J. Oleo Sci. 2014;63:303–308. doi: 10.5650/jos.ess13170. PubMed DOI

Schaefer H.L., Brandes H., Ulber B., Becker H.C., Vidal S. Evaluation of nine genotypes of oilseed rape (Brassica napus L.) for larval infestation and performance of rape stem weevil (Ceutorhynchus napi Gyll.) PLoS ONE. 2017;12:e0180807. doi: 10.1371/journal.pone.0180807. PubMed DOI PMC

Angelino D., Dosz E.B., Sun J., Hoeflinger J.L., Van Tassell M.L., Chen P., Harnly J.M., Miller M.J., Jeffery E.H. Myrosinase-dependent and -independent formation and control of isothiocyanate products of glucosinolate hydrolysis. Front. Plant Sci. 2015;6:831. doi: 10.3389/fpls.2015.00831. PubMed DOI PMC

Halkier B.A., Gershenzon J. Biology and biochemistry of glucosinolates. Annu. Rev. Plant Biol. 2006;57:303–333. doi: 10.1146/annurev.arplant.57.032905.105228. PubMed DOI

Wittstock U., Kliebenstein D.J., Lambrix V., Reichelt M., Gershenzon J. Chapter five Glucosinolate hydrolysis and its impact on generalist and specialist insect herbivores. Recent Adv. Phytochem. 2003;37:101–125. doi: 10.1016/S0079-9920(03)80020-5. DOI

Brader G., Mikkelsen M.D., Halkier B.A., Tapio Palva E. Altering glucosinolate profiles modulates disease resistance in plants. Plant J. 2006;46:758–767. doi: 10.1111/j.1365-313X.2006.02743.x. PubMed DOI

Giamoustaris A., Mithen R. Glucosinolates and disease resistance in oilseed rape (Brassica napus ssp. oleifera) Plant Pathol. 1997;46:271–275. doi: 10.1046/j.1365-3059.1997.d01-222.x. DOI

Schlaeppi K., Abou-Mansour E., Buchala A., Mauch F. Disease resistance of Arabidopsis to Phytophthora brassicae is established by the sequential action of indole glucosinolates and camalexin. Plant J. 2010;62:840–851. doi: 10.1111/j.1365-313X.2010.04197.x. PubMed DOI

Find record

Citation metrics

Loading data ...

Archiving options

Loading data ...