BW312 Hordeum vulgare semi-dwarf mutant exhibits a shifted metabolic profile towards pathogen resistance.
Fusarium graminearum
Hordeum vulgare
Pyrenophora teres
Non-targeted metabolomics
Pathogen resistance
Journal
Metabolomics : Official journal of the Metabolomic Society
ISSN: 1573-3890
Titre abrégé: Metabolomics
Pays: United States
ID NLM: 101274889
Informations de publication
Date de publication:
22 Oct 2024
22 Oct 2024
Historique:
received:
18
10
2023
accepted:
19
09
2024
medline:
23
10
2024
pubmed:
23
10
2024
entrez:
22
10
2024
Statut:
epublish
Résumé
Plant hormonal mutants, which do not produce or are insensitive to hormones, are often affected in their growth and development, but other metabolic rearrangements might be involved. A trade-off between growth and stress response is necessary for the plant survival. Here, we explore the metabolic profile and the pathogen resistance of a brassinosteroid-insensitive Hordeum vulgare L. semi-dwarf mutant, BW312. We investigate BW312 metabolism through a chemical enrichment analysis, confirming a shifted metabolic profile towards pathogen resistance. The effective pathogen resistance of the mutant was tested in presence of Pyrenophora teres and Fusarium graminearum. Four compound families were increased in the mutant (pyrrolidines, basic amino acids, alkaloids, monounsaturated fatty acids), while two compound families were decreased (pyrrolidinones, anthocyanins). Dipeptides were also altered (increased and decreased). BW312 displayed a better resistance to Pyrenophora teres in the earliest stage of infection with a 21.5% decrease of the lesion length 10 days after infection. BW312 also exhibited a reduced lesion length (43.3%) and a reduced browning of the lesions (55.5%) when exposed to Fusarium graminearum at the seedling stage. The observed metabolomic shift strongly suggests that the BW312 semi-dwarf mutant is in a primed state, resulting in a standby state of alertness to pathogens.
Identifiants
pubmed: 39438353
doi: 10.1007/s11306-024-02174-3
pii: 10.1007/s11306-024-02174-3
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
119Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Ali, S. S., Kumar, G. B. S., Khan, M., & Doohan, F. M. (2013). Brassinosteroid enhances resistance to fusarium diseases of barley. Phytopathology, 103(12), 1260–1267. https://doi.org/10.1094/PHYTO-05-13-0111-R
doi: 10.1094/PHYTO-05-13-0111-R
pubmed: 23777406
Ali, S. S., Gunupuru, L. R., Kumar, G. B. S., Khan, M., Scofield, S., Nicholson, P., & Doohan, F. M. (2014). Plant disease resistance is augmented in uzu barley lines modified in the brassinosteroid receptor BRI1. BMC Plant Biology, 14(1), 227. https://doi.org/10.1186/s12870-014-0227-1
doi: 10.1186/s12870-014-0227-1
pubmed: 25135116
pmcid: 4158134
Barupal, D. K., & Fiehn, O. (2017). Chemical Similarity Enrichment Analysis (ChemRICH) as alternative to biochemical pathway mapping for metabolomic datasets. Scientific Reports, 7(1), 1–11. https://doi.org/10.1038/s41598-017-15231-w
doi: 10.1038/s41598-017-15231-w
Bhat, A. A., Singh, I., Tandon, N., & Tandon, R. (2023). Structure activity relationship (SAR) and anticancer activity of pyrrolidine derivatives: Recent developments and future prospects (A review). European Journal of Medicinal Chemistry. https://doi.org/10.1016/j.ejmech.2022.114954
doi: 10.1016/j.ejmech.2022.114954
pubmed: 36481599
Cai, J., & Aharoni, A. (2022). Amino acids and their derivatives mediating defense priming and growth tradeoff. Current Opinion in Plant Biology, 69, 102288. https://doi.org/10.1016/j.pbi.2022.102288
doi: 10.1016/j.pbi.2022.102288
pubmed: 35987012
Camejo, D., Guzmán-Cedeño, Á., & Moreno, A. (2016). Reactive oxygen species, essential molecules, during plant-pathogen interactions. Plant Physiology and Biochemistry, 103, 10–23. https://doi.org/10.1016/j.plaphy.2016.02.035
doi: 10.1016/j.plaphy.2016.02.035
pubmed: 26950921
Campos, L., Lisón, P., López-Gresa, M. P., Rodrigo, I., Zacarés, L., Conejero, V., & Bellés, J. M. (2014). Transgenic tomato plants overexpressing tyramine N-hydroxycinnamoyltransferase exhibit elevated hydroxycinnamic acid amide levels and enhanced resistance to Pseudomonas syringae. Molecular Plant-Microbe Interactions, 27(10), 1159–1169. https://doi.org/10.1094/MPMI-04-14-0104-R
doi: 10.1094/MPMI-04-14-0104-R
pubmed: 25014592
Cecchini, N. M., Steffes, K., Schlappi, M. R., Gifford, A. N., & Greenberg, J. T. (2015). Arabidopsis AZI1 family proteins mediate signal mobilization for systemic defence priming. Nature Communications. https://doi.org/10.1038/ncomms8658
doi: 10.1038/ncomms8658
pubmed: 26203923
Chen, H., McCaig, B. C., Melotto, M., He, S. Y., & Howe, G. A. (2004). Regulation of plant arginase by wounding, jasmonate, and the phytotoxin coronatine. Journal of Biological Chemistry, 279(44), 45998–46007. https://doi.org/10.1074/jbc.M407151200
doi: 10.1074/jbc.M407151200
pubmed: 15322128
Chono, M., Honda, I., Zeniya, H., Yoneyama, K., Saisho, D., Takeda, K., et al. (2003). A semidwarf phenotype of Barley uzu results from a nucleotide substitution in the gene encoding a putative brassinosteroid receptor. Plant Physiology, 133, 1209–1219. https://doi.org/10.1104/pp.103.026195
doi: 10.1104/pp.103.026195
pubmed: 14551335
pmcid: 281616
Dockter, C., & Hansson, M. (2015). Improving barley culm robustness for secured crop yield in a changing climate. Journal of Experimental Botany, 66(12), 3499–3509. https://doi.org/10.1093/jxb/eru521
doi: 10.1093/jxb/eru521
pubmed: 25614659
Dockter, C., Gruszka, D., Braumann, I., Druka, A., Druka, I., Franckowiak, J., et al. (2014). Induced variations in brassinosteroid genes define barley height and sturdiness, and expand the green revolution genetic toolkit. Plant Physiology, 166(4), 1912–1927. https://doi.org/10.1104/pp.114.250738
doi: 10.1104/pp.114.250738
pubmed: 25332507
pmcid: 4256852
Druka, A., Franckowiak, J., Lundqvist, U., Bonar, N., Alexander, J., Houston, K., et al. (2011). Genetic dissection of barley morphology and development. Plant Physiology, 155(2), 617–627. https://doi.org/10.1104/pp.110.166249
doi: 10.1104/pp.110.166249
pubmed: 21088227
Gauthier, L., Atanasova-Penichon, V., Chéreau, S., & Richard-Forget, F. (2015). Metabolomics to decipher the chemical defense of cereals against Fusarium graminearum and deoxynivalenol accumulation. International Journal of Molecular Sciences. https://doi.org/10.3390/ijms161024839
doi: 10.3390/ijms161024839
pubmed: 26492237
pmcid: 4632779
Goddard, R., Peraldi, A., Ridout, C., & Nicholson, P. (2014). Enhanced disease resistance caused by BRI1 mutation is conserved between Brachypodium distachyon and barley (Hordeum vulgare). Molecular Plant-Microbe Interactions, 27(10), 1095–1106. https://doi.org/10.1094/MPMI-03-14-0069-R
doi: 10.1094/MPMI-03-14-0069-R
pubmed: 24964059
Gruszka, D., Szarejko, I., & Maluszynski, M. (2011a). New allele of HvBRI1 gene encoding brassinosteroid receptor in barley. Journal of Applied Genetics, 52(3), 257–268. https://doi.org/10.1007/s13353-011-0031-7
doi: 10.1007/s13353-011-0031-7
pubmed: 21302020
pmcid: 3132423
Gruszka, D., Szarejko, I., & Maluszynski, M. (2011b). Identification of barley DWARF gene involved in brassinosteroid synthesis. Plant Growth Regulation, 65(2), 343–358. https://doi.org/10.1007/s10725-011-9607-9
doi: 10.1007/s10725-011-9607-9
Gruszka, D., Janeczko, A., Dziurka, M., Pociecha, E., Oklestkova, J., & Szarejko, I. (2016). Barley brassinosteroid mutants provide an insight into phytohormonal homeostasis in plant reaction to drought stress. Frontiers in Plant Science, 7, 1–14. https://doi.org/10.3389/fpls.2016.01824
doi: 10.3389/fpls.2016.01824
Hameed, A., Poznanski, P., Noman, M., Ahmed, T., Iqbal, A., Nadolska-Orczyk, A., & Orczyk, W. (2022). Barley resistance to Fusarium graminearum infections: from transcriptomics to field with food safety concerns. Journal of Agricultural and Food Chemistry. https://doi.org/10.1021/acs.jafc.2c05488
doi: 10.1021/acs.jafc.2c05488
pubmed: 36350344
Honda, I., Zeniya, H., Yoneyama, K., Chono, M., Kaneko, S., & Watanabe, Y. (2003). Uzu mutation in barley (Hordeum vulgare L.) reduces the leaf unrolling response to brassinolide. Bioscience, Biotechnology, and Biochemistry., 67(5), 1194–1197.
doi: 10.1271/bbb.67.1194
pubmed: 12834311
Karasov, T. L., Chae, E., Herman, J. J., & Bergelson, J. (2017). Mechanisms to mitigate the trade-off between growth and defense. The Plant Cell, 29(4), 666–680. https://doi.org/10.1105/tpc.16.00931
doi: 10.1105/tpc.16.00931
pubmed: 28320784
pmcid: 5435432
Lenk, M., Wenig, M., Mengel, F., Häubler, F., & Corina Vlot, A. (2018). Arabidopsis thaliana immunity-related compounds modulate disease susceptibility in barley. Agronomy. https://doi.org/10.3390/agronomy8080142
doi: 10.3390/agronomy8080142
Liu, Z., Ellwood, S. R., Oliver, R. P., & Friesen, T. L. (2011). Pyrenophora teres: Profile of an increasingly damaging barley pathogen. Molecular Plant Pathology, 12(1), 1–19. https://doi.org/10.1111/j.1364-3703.2010.00649.x
doi: 10.1111/j.1364-3703.2010.00649.x
pubmed: 21118345
Maurer, L., Zumsteg, J., Lutz, C., Ottermatte, M. P., Wanko, A., Heintz, D., & Villette, C. (2021). Towards a model for road runoff infiltration management. Npj Clean Water. https://doi.org/10.1038/s41545-021-00136-z
doi: 10.1038/s41545-021-00136-z
Morrell, P. L., & Clegg, M. T. (2007). Genetic evidence for a second domestication of barley (Hordeum vulgare) east of the Fertile Crescent. Proceedings of the National Academy of Sciences of the United States of America, 104(9), 3289–3294. https://doi.org/10.1073/pnas.0611377104
doi: 10.1073/pnas.0611377104
pubmed: 17360640
pmcid: 1805597
Návarová, H., Bernsdorff, F., Döring, A. C., & Zeier, J. (2013). Pipecolic acid, an endogenous mediator of defense amplification and priming, is a critical regulator of inducible plant immunity. The Plant Cell, 24(12), 5123–5141. https://doi.org/10.1105/tpc.112.103564
doi: 10.1105/tpc.112.103564
Newman, M. A., Von Roepenack-Lahaye, E., Parr, A., Daniels, M. J., & Dow, J. M. (2001). Induction of hydroxycinnamoyl-tyramine conjugates in pepper by Xanthomonas campestris, a plant defense response activated by hrp gene-dependent and hrp gene-independent mechanisms. Molecular Plant-Microbe Interactions, 14(6), 785–792. https://doi.org/10.1094/MPMI.2001.14.6.785
doi: 10.1094/MPMI.2001.14.6.785
pubmed: 11386374
Schymanski, E. L., Jeon, J., Gulde, R., Fenner, K., Ruff, M., Singer, H. P., & Hollender, J. (2014). Identifying small molecules via high resolution mass spectrometry: communicating confidence. Environmental Science and Technology, 48(4), 2097–2098. https://doi.org/10.1021/es5002105
doi: 10.1021/es5002105
pubmed: 24476540
Sun, G., Strebl, M., Merz, M., Blamberg, R., Huang, F.-C., McGraphery, K., et al. (2019). Glucosylation of the phytoalexin N-feruloyl tyramine modulates the levels of pathogen-responsive metabolites in Nicotiana benthamiana. The Plant Journal, 100, 20–37.
doi: 10.1111/tpj.14420
pubmed: 31124249
Tits, M., Desaive, C., Marnette, J. M., Bassleer, B., & Angenot, L. (1984). Antemitotic activity of strychnopentamine, a bisindolic alkaloid. Journal of Ethnopharmacology, 12(3), 287–292. https://doi.org/10.1016/0378-8741(84)90058-8
doi: 10.1016/0378-8741(84)90058-8
pubmed: 6533414
Tugizimana, F., Mhlongo, M. I., Piater, L. A., & Dubery, I. A. (2018). Metabolomics in plant priming research: The way forward? International Journal of Molecular Sciences. https://doi.org/10.3390/ijms19061759
doi: 10.3390/ijms19061759
pubmed: 30158424
pmcid: 6163672
Tünnermann, L., Colou, J., Näsholm, T., & Gratz, R. (2022). To have or not to have: Expression of amino acid transporters during pathogen infection. Plant Molecular Biology, 109(4–5), 413–425. https://doi.org/10.1007/s11103-022-01244-1
doi: 10.1007/s11103-022-01244-1
pubmed: 35103913
pmcid: 9213295
Villette, C., Zumsteg, J., Schaller, H., & Heintz, D. (2018). Non-targeted metabolic profiling of BW312 Hordeum vulgare semi dwarf mutant using UHPLC coupled to QTOF high resolution mass spectrometry. Scientific Reports. https://doi.org/10.1038/s41598-018-31593-1
doi: 10.1038/s41598-018-31593-1
pubmed: 30397227
pmcid: 6218535
Villette, C., Maurer, L., Delecolle, J., Zumsteg, J., Erhardt, M., & Heintz, D. (2019a). In situ localization of micropollutants and associated stress response in Populus nigra leaves. Environment International, 126, 523–532. https://doi.org/10.1016/j.envint.2019.02.066
doi: 10.1016/j.envint.2019.02.066
pubmed: 30851483
Villette, C., Maurer, L., Wanko, A., & Heintz, D. (2019b). Xenobiotics metabolization in Salix alba leaves uncovered by mass spectrometry imaging. Metabolomics. https://doi.org/10.1007/s11306-019-1572-8
doi: 10.1007/s11306-019-1572-8
pubmed: 31471668
Winter, G., Todd, C. D., Trovato, M., Forlani, G., & Funck, D. (2015). Physiological implications of arginine metabolism in plants. Frontiers in Plant Science, 6, 1–14. https://doi.org/10.3389/fpls.2015.00534
doi: 10.3389/fpls.2015.00534
Zeier, J. (2013). New insights into the regulation of plant immunity by amino acid metabolic pathways. Plant, Cell and Environment, 36(12), 2085–2103. https://doi.org/10.1111/pce.12122
doi: 10.1111/pce.12122
pubmed: 23611692