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.

Group of Genetics Breeding and Biochemistry of Brassicas Mision Biologica de Galicia Pontevedra Spain

Institute for Multidisciplinary Research in Applied Biology Universidad Pública de Navarra Pamplona Spain

Laboratory of Fungal Genetics and Metabolism Institute of Microbiology of the Czech Academy of Sciences Prague Czechia

Microbiology and Genetics Department and Institute for Agribiotechnology Research University of Salamanca Salamanca Spain

Zobrazit více v PubMed

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 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 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 PubMed DOI

Berbee M. L., Pirseyedi M., Hubbard S. (1999). DOI

Card S. D., Hume D. E., Roodi D., McGill C. R., Millner J. P., Johnson R. D. (2015). Beneficial endophytic microorganisms of DOI

Chen J., Ullah C., Reichelt M., Beran F., Yang Z. L., Gershenzon J., et al. (2020). The phytopathogenic fungus 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 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 ( DOI

Francisco M., Tortosa M., Martínez-Ballesta M. D. C., Velasco P., García-Viguera C., Moreno D. A. (2017). Nutritional and phytochemical value of DOI

Garcia-Fraile P., Rivas R., Willems A., Peix A., Martens M., Martinez-Molina E., et al. (2007). PubMed DOI

Hou L., Yu J., Zhao L., He X. (2019). Dark septate endophytes improve the growth and tolerance of 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 PubMed DOI PMC

Ismail I. A., Godfrey D., Able A. J. (2014). Proteomic analysis reveals the potential involvement of xylanase from 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 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 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 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 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 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 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 PubMed DOI PMC

Maximiano M. R., de Jesus Miranda V., de Barros E. G., Dias S. C. (2020). Validation of an PubMed DOI

Mehmood A., Irshad M., Husna A. A., Hussain A. (2018).

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

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 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 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 ( 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 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: PubMed DOI PMC

Poveda J., Baptista P. (2021). Filamentous fungi as biocontrol agents in olive ( 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 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 ( PubMed DOI PMC

Poveda J., Zabalgogeazcoa I., Soengas P., Rodríguez V. M., Cartea M. E., Abilleira R., et al. (2020a). 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 PubMed DOI PMC

Šamec D., Urlić B., Salopek-Sondi B. (2020). Kale ( PubMed DOI

Sotelo T., Velasco P., Soengas P., Rodríguez V. M., Cartea M. E. (2016). Modification of leaf glucosinolate contents in 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 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 ( 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 PubMed DOI

Vela-Corcía D., Srivastava D. A., Dafa-Berger A., Rotem N., Barda O., Levy M. (2019). MFS transporter from PubMed DOI PMC

Velasco P., Rodríguez V. M., Soengas P., Poveda J. (2021). 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 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). PubMed DOI PMC

Wu X., Huang H., Childs H., Wu Y., Yu L., Pehrsson P. R. (2021). Glucosinolates in PubMed DOI

Yang Y., Zuzak K., Harding M., Neilson E., Feindel D., Feng J. (2017). First report of pink root rot caused by DOI

Transcriptome-guided discovery of novel plant-associated genes in a rhizosphere Pseudomonas

Speciation Features of Ferdinandcohnia quinoae sp. nov to Adapt to the Plant Host