Endophytic fungi from kale (Brassica oleracea var. acephala) modify roots-glucosinolate profile and promote plant growth in cultivated Brassica species. First description of Pyrenophora gallaeciana
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
36274741
PubMed Central
PMC9580329
DOI
10.3389/fmicb.2022.981507
Knihovny.cz E-zdroje
- Klíčová slova
- Acrocalymma vagum, Brassica U’s triangle, Fusarium oxysporum, Setophoma terrestris, glucosinolates, indoleacetic acid, sinigrin,
- Publikační typ
- časopisecké články MeSH
Endophytic fungi of crops can promote plant growth through various mechanisms of action (i.e., improve nutrient uptake and nutrient use efficiency, and produce and modulate plant hormones). The genus Brassica includes important horticultural crops, which have been little studied in their interaction with endophytic fungi. Previously, four endophytic fungi were isolated from kale roots (Brassica oleracea var. acephala), with different benefits for their host, including plant growth promotion, cold tolerance, and induction of resistance to pathogens (Xanthomonas campestris) and pests (Mamestra brassicae). In the present work, the molecular and morphological identification of the four different isolates were carried out, describing them as the species Acrocalymma vagum, Setophoma terrestris, Fusarium oxysporum, and the new species Pyrenophora gallaeciana. In addition, using a representative crop of each Brassica U's triangle species and various in vitro biochemical tests, the ability of these fungi to promote plant growth was described. In this sense, the four fungi used promoted the growth of B. rapa, B. napus, B. nigra, B. juncea, and B. carinata, possibly due to the production of auxins, siderophores, P solubilization or cellulase, xylanase or amylase activity. Finally, the differences in root colonization between the four endophytic fungi and two pathogens (Leptosphaeria maculans and Sclerotinia sclerotiorum) and the root glucosinolate profile were studied, at different times. In this way, how the presence of progoitrin in the roots reduces their colonization by endophytic and pathogenic fungi was determined, while the possible hydrolysis of sinigrin to fungicidal products controls the colonization of endophytic fungi, but not of pathogens.
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Abdel-Farid I. B., Jahangir M., Mustafa N. R., Van Dam N. M., Van den Hondel C. A., Kim H. K., et al. . (2010). Glucosinolate profiling of Brassica rapa cultivars after infection by Leptosphaeria maculans and fusarium oxysporum. Biochem. System. Ecol. 38, 612–620. doi: 10.1016/j.bse.2010.07.008 DOI
Al-Ani L. K. T. (2019). “Recent patents on endophytic fungi and their international market” in Intellectual Property Issues in Microbiology. eds. Singh H. B., Keswani C., Singh S. P. (Berlin, Germany: Springer). 271–284.
Amaike S., Ozga J. A., Basu U., Strelkov S. E. (2008). Quantification of ToxB gene expression and formation of appressoria by isolates of Pyrenophora tritici-repentis differing in pathogenicity. Plant Pathol. 57, 623–633. doi: 10.1111/j.1365-3059.2007.01821.x DOI
Anthony M. A., Celenza J. L., Armstrong A., Frey S. D. (2020). Indolic glucosinolate pathway provides resistance to mycorrhizal fungal colonization in a non-host Brassicaceae. Ecosphere 11:e03100. doi: 10.1002/ecs2.3100 DOI
Bakri Y., Arabi M. I. E., Jawhar M. (2011). Heterogeneity in the ITS of the ribosomal DNA of Pyrenophora graminea isolates differing in xylanase and amylase production. Microbiology 80, 492–495. doi: 10.1134/S0026261711040023 PubMed DOI
Berbee M. L., Pirseyedi M., Hubbard S. (1999). Cochliobolus phylogenetics and the origin of known, highly virulent pathogens, inferred from ITS and glyceraldehyde-3-phosphate dehydrogenase gene sequences. Mycologia 91, 964–977. doi: 10.1080/00275514.1999.12061106 DOI
Card S. D., Hume D. E., Roodi D., McGill C. R., Millner J. P., Johnson R. D. (2015). Beneficial endophytic microorganisms of brassica–a review. Biol. Control 90, 102–112. doi: 10.1016/j.biocontrol.2015.06.001 DOI
Chen J., Ullah C., Reichelt M., Beran F., Yang Z. L., Gershenzon J., et al. . (2020). The phytopathogenic fungus Sclerotinia sclerotiorum detoxifies plant glucosinolate hydrolysis products via an isothiocyanate hydrolase. Nat. Commun. 11, 3090–3012. doi: 10.1038/s41467-020-16921-2, PMID: PubMed DOI PMC
Ellwood S. R., Liu Z., Syme R. A., Lai Z., Hane J. K., Keiper F., et al. . (2010). A first genome assembly of the barley fungal pathogen Pyrenophora teres f. teres. Genome Biol. 11, R109–R114. doi: 10.1186/gb-2010-11-11-r109, PMID: PubMed DOI PMC
Eugui D., Escobar C., Velasco P., Poveda J. (2022). Glucosinolates as an effective tool in plant-parasitic nematodes control: exploiting natural plant defenses. Appl. Soil Ecol. 176:104497. doi: 10.1016/j.apsoil.2022.104497 DOI
Farouk H. M., Attia E. Z., El-Katatny M. M. H. (2020). Hydrolytic enzyme production of endophytic fungi isolated from soybean (Glycine max). J. Mod. Res. 2, 1–7. doi: 10.21608/jmr.2019.15748.1008 DOI
Francisco M., Tortosa M., Martínez-Ballesta M. D. C., Velasco P., García-Viguera C., Moreno D. A. (2017). Nutritional and phytochemical value of brassica crops from the Agri-food perspective. Ann. Appl. Biol. 170, 273–285. doi: 10.1111/aab.12318 DOI
Garcia-Fraile P., Rivas R., Willems A., Peix A., Martens M., Martinez-Molina E., et al. . (2007). Rhizobium cellulosilyticum sp. nov., isolated from sawdust of Populus alba. Int. J. Syst. Evol. Microbiol. 57, 844–848. doi: 10.1099/ijs.0.64680-0, PMID: PubMed DOI
Hou L., Yu J., Zhao L., He X. (2019). Dark septate endophytes improve the growth and tolerance of Medicago sativa and Ammopiptanthus mongolicus under cadmium stress. Front. Microbiol. 10:3061. doi: 10.3389/fmicb.2019.03061, PMID: PubMed DOI PMC
Hu X., Chen J., Guo J. (2006). Two phosphate-and potassium-solubilizing bacteria isolated from Tianmu Mountain, Zhejiang, China. World J. Microbiol. Biotechnol. 22, 983–990. doi: 10.1007/s11274-006-9144-2 DOI
Hu Z., Parekh U., Maruta N., Trusov Y., Botella J. R. (2015). Down-regulation of fusarium oxysporum endogenous genes by host-delivered RNA interference enhances disease resistance. Front. Chem. 3:1. doi: 10.3389/fchem.2015.00001, PMID: PubMed DOI PMC
Ismail I. A., Godfrey D., Able A. J. (2014). Proteomic analysis reveals the potential involvement of xylanase from Pyrenophora teres f. teres in net form net blotch disease of barley. Australas. Plant Pathol. 43, 715–726. doi: 10.1007/s13313-014-0314-7 DOI
Jiménez-Gómez A., Saati-Santamaría Z., Igual J. M., Rivas R., Mateos P. F., García-Fraile P. (2019). Genome insights into the novel species microvirga brassicacearum, a rapeseed endophyte with biotechnological potential. Microorganisms 7:354. doi: 10.3390/microorganisms7090354, PMID: PubMed DOI PMC
Jiménez-Gómez A., Saati-Santamaría Z., Kostovcik M., Rivas R., Velázquez E., Mateos P. F., et al. . (2020). Selection of the root endophyte pseudomonas brassicacearum CDVBN10 as plant growth promoter for Brassica napus L. crops. Agronomy 10:1788. doi: 10.3390/agronomy10111788 DOI
Katoh K., Standley D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780. doi: 10.1093/molbev/mst010, PMID: PubMed DOI PMC
Khalid A., Arshad M., Zahir Z. A. (2004). Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. J. Appl. Microbiol. 96, 473–480. doi: 10.1046/j.1365-2672.2003.02161.x, PMID: PubMed DOI
Khan A. L., Hussain J., Al-Harrasi A., Al-Rawahi A., Lee I. J. (2015). Endophytic fungi: resource for gibberellins and crop abiotic stress resistance. Crit. Rev. Biotechnol. 35, 62–74. doi: 10.3109/07388551.2013.800018, PMID: PubMed DOI
Kim C. K., Seol Y. J., Perumal S., Lee J., Waminal N. E., Jayakodi M., et al. . (2018). Re-exploration of U’s triangle brassica species based on chloroplast genomes and 45S nrDNA sequences. Sci. Rep. 8, 1–11. doi: 10.1038/s41598-018-25585-4, PMID: PubMed DOI PMC
Kliebenstein D. J., Kroymann J., Brown P., Figuth A., Pedersen D., Gershenzon J., et al. . (2001). Genetic control of natural variation in Arabidopsis glucosinolate accumulation. Plant Physiol. 126, 811–825. doi: 10.1104/pp.126.2.811, PMID: PubMed DOI PMC
Kubatko L. S., Degnan J. H. (2007). Inconsistency of phylogenetic estimates from concatenated data under coalescence. Syst. Biol. 56, 17–24. doi: 10.1080/10635150601146041, PMID: PubMed DOI
Larsson A. (2014). AliView: a fast and lightweight alignment viewer and editor for large data sets. Bioinformatics 30, 3276–3278. doi: 10.1093/bioinformatics/btu531, PMID: PubMed DOI PMC
Letunic I., Bork P. (2021). Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 49, W293–W296. doi: 10.1093/nar/gkab301, PMID: PubMed DOI PMC
Liu Y., Wei X. (2019). Dark septate endophyte improves drought tolerance of Ormosia hosiei Hemsley & EH Wilson by modulating root morphology, ultrastructure, and the ratio of root hormones. Forests 10:830. doi: 10.3390/f10100830 DOI
Liu Y. J., Whelen S., Hall B. D. (1999). Phylogenetic relationships among ascomycetes: evidence from an RNA polymerse II subunit. Mol. Biol. Evol. 16, 1799–1808. doi: 10.1093/oxfordjournals.molbev.a026092, PMID: PubMed DOI
Madloo P., Lema M., Francisco M., Soengas P. (2019). Role of major glucosinolates in the defense of kale against Sclerotinia sclerotiorum and Xanthomonas campestris pv. Campestris. Phytopathology 109, 1246–1256. doi: 10.1094/PHYTO-09-18-0340-R, PMID: PubMed DOI
Mateos P. F., Jimenez-Zurdo J. I., Chen J., Squartini A. S., Haack S. K., Martinez-Molina E., et al. . (1992). Cell-associated pectinolytic and cellulolytic enzymes in rhizobium leguminosarum biovar trifolii. Appl. Environ. Microbiol. 58, 1816–1822. doi: 10.1128/aem.58.6.1816-1822.1992, PMID: PubMed DOI PMC
Maximiano M. R., de Jesus Miranda V., de Barros E. G., Dias S. C. (2020). Validation of an in vitro system to trigger changes in the gene expression of effectors of Sclerotinia sclerotiorum. J. Appl. Microbiol. 131, 885–897. doi: 10.1111/jam.14973 PubMed DOI
Mehmood A., Irshad M., Husna A. A., Hussain A. (2018). In vitro maize growth promotion by endophytic fusarium oxysporum WLW. J. Appl. Environ. Biol. Sci. 8, 30–35.
Minh B. Q., Schmidt H. A., Chernomor O., Schrempf D., Woodhams M. D., von Haeseler A., et al. . (2020). IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530–1534. doi: 10.1093/molbev/msaa015, PMID: PubMed DOI PMC
Murphy B. R., Doohan F. M., Hodkinson T. R. (2018). From concept to commerce: developing a successful fungal endophyte inoculant for agricultural crops. J. Fungi 4:24. doi: 10.3390/jof4010024, PMID: PubMed DOI PMC
Nagaharu U., Nagaharu N. (1935). Genome analysis in brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Jpn. J. Bot. 7, 389–452.
Newton A. C., Fitt B. D., Atkins S. D., Walters D. R., Daniell T. J. (2010). Pathogenesis, parasitism and mutualism in the trophic space of microbe–plant interactions. Trends Microbiol. 18, 365–373. doi: 10.1016/j.tim.2010.06.002, PMID: PubMed DOI
Onofre S. B., Mattiello S. P., da Silva G. C., Groth D., Malagi I. (2013). Production of cellulases by the endophytic fungus fusarium oxysporum. J. Microbiol. Res. 3, 131–134. doi: 10.5923/j.microbiology.20130304.01 DOI
Ortega H. E., Torres-Mendoza D., Cubilla-Rios L. (2020). Patents on endophytic fungi for agriculture and bio-and phytoremediation applications. Microorganisms 8:1237. doi: 10.3390/microorganisms8081237, PMID: PubMed DOI PMC
Petit-Houdenot Y., Degrave A., Meyer M., Blaise F., Ollivier B., Marais C. L., et al. . (2019). A two genes–for–one gene interaction between Leptosphaeria maculans and Brassica napus. New Phytol. 223, 397–411. doi: 10.1111/nph.15762, PMID: PubMed DOI
Petzel J. P., Hartman P. A. (1986). A note on starch hydrolysis and β-glucuronidase activity among flavobacteria. J. Appl. Microbiol. 61, 421–426. doi: 10.1111/j.1365-2672.1986.tb04306.x, PMID: PubMed DOI
Plaszkó T., Szűcs Z., Cziáky Z., Ács-Szabó L., Csoma H., Géczi L., et al. . (2022). Correlations between the metabolome and the endophytic fungal metagenome suggests importance of various metabolite classes in community assembly in horseradish (Armoracia rusticana, Brassicaceae) roots. Front. Plant Sci. 13:921008. doi: 10.3389/fpls.2022.921008, PMID: PubMed DOI PMC
Posada D. (2008). jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25, 1253–1256. doi: 10.1093/molbev/msn083, PMID: PubMed DOI
Poveda J. (2021). Glucosinolates profile of Arabidopsis thaliana modified root colonization of Trichoderma species. Biol. Control 155:104522. doi: 10.1016/j.biocontrol.2020.104522 DOI
Poveda J. (2022). Effect of volatile and non-volatile metabolites from Leptosphaeria maculans on tomato calli under abiotic stresses. Plant Stress 3:100054. doi: 10.1016/j.stress.2021.100054 DOI
Poveda J., Abril-Urias P., Escobar C. (2020c). Biological control of plant-parasitic nematodes by filamentous fungi inducers of resistance: Trichoderma, mycorrhizal and endophytic fungi. Front. Microbiol. 11:992. doi: 10.3389/fmicb.2020.00992, PMID: PubMed DOI PMC
Poveda J., Baptista P. (2021). Filamentous fungi as biocontrol agents in olive (Olea europaea L.) diseases: mycorrhizal and endophytic fungi. Crop Prot. 146:105672. doi: 10.1016/j.cropro.2021.105672 DOI
Poveda J., Díaz-González S., Díaz-Urbano M., Velasco P., Sacristán S. (2022). Fungal endophytes of Brassicaceae: molecular interactions and crop benefits. Front. Plant Sci. 13:932288. doi: 10.3389/fpls.2022.932288, PMID: PubMed DOI PMC
Poveda J., Eugui D., Abril-Urías P., Velasco P. (2021a). Endophytic fungi as direct plant growth promoters for sustainable agricultural production. Symbiosis 85, 1–19. doi: 10.1007/s13199-021-00789-x DOI
Poveda J., Eugui D., Velasco P. (2020b). Natural control of plant pathogens through glucosinolates: an effective strategy against fungi and oomycetes. Phytochem. Rev. 19, 1045–1059. doi: 10.1007/s11101-020-09699-0 DOI
Poveda J., Hermosa R., Monte E., Nicolás C. (2019). The Trichoderma harzianum Kelch protein ThKEL1 plays a key role in root colonization and the induction of systemic defense in Brassicaceae plants. Front. Plant Sci. 10:1478. doi: 10.3389/fpls.2019.01478, PMID: PubMed DOI PMC
Poveda J., Velasco P., de Haro A., Johansen T. J., McAlvay A. C., Möllers C., et al. . (2021b). Agronomic and metabolomic side-effects of a divergent selection for indol-3-ylmethylglucosinolate content in kale (Brassica oleracea var. acephala). Meta 11:384. doi: 10.3390/metabo11060384, PMID: PubMed DOI PMC
Poveda J., Zabalgogeazcoa I., Soengas P., Rodríguez V. M., Cartea M. E., Abilleira R., et al. . (2020a). Brassica oleracea var. acephala (kale) improvement by biological activity of root endophytic fungi. Sci. Rep. 10, 20224–20212. doi: 10.1038/s41598-020-77215-7, PMID: PubMed DOI PMC
Rana K. L., Kour D., Sheikh I., Yadav N., Yadav A. N., Kumar V., et al. . (2019). “Biodiversity of endophytic fungi from diverse niches and their biotechnological applications” in Advances in Endophytic Fungal Research. ed. Singh B. P. (Berlin: Springer; ), 105–144.
Rigobelo E. C., Baron N. C. (2021). Endophytic fungi: a tool for plant growth promotion and sustainable agriculture. Mycology 13, 39–55. doi: 10.1080/21501203.2021.1945699, PMID: PubMed DOI PMC
Rybak K., See P. T., Phan H. T., Syme R. A., Moffat C. S., Oliver R. P., et al. . (2017). A functionally conserved Zn2Cys6 binuclear cluster transcription factor class regulates necrotrophic effector gene expression and host-specific virulence of two major Pleosporales fungal pathogens of wheat. Mol. Plant Pathol. 18, 420–434. doi: 10.1111/mpp.12511, PMID: PubMed DOI PMC
Šamec D., Urlić B., Salopek-Sondi B. (2020). Kale (Brassica oleracea var. acephala) as a superfood: review of the scientific evidence behind the statement. Crit. Rev. Food Sci. Nutr. 59, 2411–2422. doi: 10.1080/10408398.2018.1454400, PMID: PubMed DOI
Sotelo T., Velasco P., Soengas P., Rodríguez V. M., Cartea M. E. (2016). Modification of leaf glucosinolate contents in Brassica oleracea by divergent selection and effect on expression of genes controlling glucosinolate pathway. Front. Plant Sci. 7:1012. doi: 10.3389/fpls.2016.01012, PMID: PubMed DOI PMC
Stotz H. U., Sawada Y., Shimada Y., Hirai M. Y., Sasaki E., Krischke M., et al. . (2011). Role of camalexin, indole glucosinolates, and side chain modification of glucosinolate-derived isothiocyanates in defense of Arabidopsis against Sclerotinia sclerotiorum. Plant J. 67, 81–93. doi: 10.1111/j.1365-313X.2011.04578.x, PMID: PubMed DOI
Szűcs Z., Plaszkó T., Cziáky Z., Kiss-Szikszai A., Emri T., Bertóti R., et al. . (2018). Endophytic fungi from the roots of horseradish (Armoracia rusticana) and their interactions with the defensive metabolites of the glucosinolate-myrosinase-isothiocyanate system. BMC Plant Biol. 18, 1–15. doi: 10.1186/s12870-018-1295-4, PMID: PubMed DOI PMC
Vandicke J., De Visschere K., Deconinck S., Leenknecht D., Vermeir P., Audenaert K., et al. . (2020). Uncovering the biofumigant capacity of allyl isothiocyanate from several Brassicaceae crops against fusarium pathogens in maize. J. Sci. Food Agric. 100, 5476–5486. doi: 10.1002/jsfa.10599, PMID: PubMed DOI
Vela-Corcía D., Srivastava D. A., Dafa-Berger A., Rotem N., Barda O., Levy M. (2019). MFS transporter from Botrytis cinerea provides tolerance to glucosinolate-breakdown products and is required for pathogenicity. Nat. Commun. 10, 2886–2811. doi: 10.1038/s41467-019-10860-3, PMID: PubMed DOI PMC
Velasco P., Rodríguez V. M., Soengas P., Poveda J. (2021). Trichoderma hamatum increases productivity, glucosinolate content and antioxidant potential of different leafy brassica vegetables. Plan. Theory 10:2449. doi: 10.3390/plants10112449, PMID: PubMed DOI PMC
Vierheilig H., Bennett R., Kiddle G., Kaldorf M., Ludwig-Müller J. (2000). Differences in glucosinolate patterns and arbuscular mycorrhizal status of glucosinolate-containing plant species. New Phytol. 146, 343–352. doi: 10.1046/j.1469-8137.2000.00642.x, PMID: PubMed DOI
Vilgalys R., Hester M. (1990). Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J. Bacteriol. 172, 4238–4246. doi: 10.1128/jb.172.8.4238-4246.1990, PMID: PubMed DOI PMC
White T. J., Bruns T., Lee S. J. W. T., Taylor J. (1990). “Amplifcation and direct sequencing of fungal ribosomal rna genes for phylogenetics” in PCR Protocols: A Guide to Methods and Applications. eds. Innis M. A., Garfield D. H., Sninsky J. J., White T. J. (Cambridge: Academic Press; ), 315–322.
Witzel K., Hanschen F. S., Klopsch R., Ruppel S., Schreiner M., Grosch R. (2015). Verticillium longisporum infection induces organ-specific glucosinolate degradation in Arabidopsis thaliana. Front. Plant Sci. 6:508. doi: 10.3389/fpls.2015.00508, PMID: PubMed DOI PMC
Wu X., Huang H., Childs H., Wu Y., Yu L., Pehrsson P. R. (2021). Glucosinolates in brassica vegetables: characterization and factors that influence distribution, content, and intake. Ann. Rev. Food Sci. Tech. 12, 485–511. doi: 10.1146/annurev-food-070620-025744, PMID: PubMed DOI
Yang Y., Zuzak K., Harding M., Neilson E., Feindel D., Feng J. (2017). First report of pink root rot caused by Setophoma (Pyrenochaeta) terrestris on canola. Can. J. Plant Pathol. 39, 354–360. doi: 10.1080/07060661.2017.1355849 DOI
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