Powdery mildew is a common disease affecting the commercial production of gerbera flowers (Gerbera hybrida, Asteraceae). Some varieties show a certain degree of resistance to it. Our objective was to identify biomarkers of resistance to powdery mildew using an 1H nuclear magnetic resonance spectroscopy and chemometrics approach in a complex, fully factorial experiment to suggest a target for selection and breeding. Resistant varieties were found to differ from those that were susceptible in the metabolites of the polyketide pathway, such as gerberin, parasorboside, and gerberinside. A new compound probably involved in resistance, 5-hydroxyhexanoic acid 3-O-β-D-glucoside, was described for the first time. A decision tree model was built to distinguish resistant varieties, with an accuracy of 57.7%, sensitivity of 72%, and specificity of 44.44% in an independent test. Our results suggest the mechanism of resistance to powdery mildew in gerbera and provide a potential tool for resistance screening in breeding programs.

Business Unit Greenhouse Horticulture Wageningen University and Research Bleiswijk Netherlands

Department of Food Science Faculty of Agrobiology Food and Natural Resources Czech University of Life Sciences Prague Prague Czechia

Department of Natural Drugs Faculty of Pharmacy Masaryk University Brno Czechia

Zobrazit více v PubMed

Allwood J. W., Ellis D. I., Goodacre R. (2008). Metabolomic technologies and their application to the study of plants and plant-host interactions. Physiol. Plant. 132, 117–135. doi: 10.1111/j.1399-3054.2007.01001.x, PMID: PubMed DOI

Bashandy H., Pietiäinen M., Carvalho E., Lim K. J., Elomaa P., Martens S., et al. . (2015). Anthocyanin biosynthesis in gerbera cultivar ‘Estelle’ and its acyanic sport ‘Ivory’. Planta 242, 601–611. doi: 10.1007/s00425-015-2349-6, PMID: PubMed DOI

Bhattarai K., Conesa A., Xiao S., Peres N. A., Clark D. G., Parajuli S., et al. . (2020). Sequencing and analysis of gerbera daisy leaf transcriptomes reveal disease resistance and susceptibility genes differentially expressed and associated with powdery mildew resistance. BMC Plant Biol. 20:539. doi: 10.1186/s12870-020-02742-4, PMID: PubMed DOI PMC

Bohlmann F., Zdero C., Heinrich F. (1973). Uber die Inhaltsstoffe der Gattung Gerbera. Chem. Ber. 106, 382–387. doi: 10.1017/CBO9781107415324.004 PubMed DOI

Bourgaud F., Hehn A., Larbat R., Doerper S., Gontier E., Kellner S., et al. . (2006). Biosynthesis of coumarins in plants: a major pathway still to be unravelled for cytochrome P450 enzymes. Phytochem. Rev. 5, 293–308. doi: 10.1007/s11101-006-9040-2 DOI

Broholm S. K., Pöllänen E., Ruokolainen S., Tähtiharju S., Kotilainen M., Albert V. A., et al. . (2010). Functional characterization of B class MADS-box transcription factors in Gerbera hybrida. J. Exp. Bot. 61, 75–85. doi: 10.1093/jxb/erp279, PMID: PubMed DOI PMC

Deng Z., Harbaugh B. K. (2010). UFGE 4141, UFGE 7014, UFGE 7015, UFGE 7023, UFGE 7032, and UFGE 7034: six new gerbera cultivars for marketing flowering plants in large containers. HortScience 45, 971–974. doi: 10.21273/HORTSCI.45.6.971 DOI

Eckermann S., Schröder G., Schmidt J., Streck D., Edrada R. A., Helariutta Y., et al. . (1998). New pathway to polyketides in plants. Nature 396, 387–390. doi: 10.1038/24652, PMID: PubMed DOI

Gachon C. M. M., Langlois-Meurinne M., Saindrenan P. (2005). Plant secondary metabolism glycosyltransferases: the emerging functional analysis. Trends Plant Sci. 10, 542–549. doi: 10.1016/j.tplants.2005.09.007, PMID: PubMed DOI

Ghani M., Sharma S. K. (2019). Induction of powdery mildew resistance in gerbera (Gerbera jamesonii) through gamma irradiation. Physiol. Mol. Biol. Plants 25, 159–166. doi: 10.1007/s12298-018-0613-5, PMID: PubMed DOI PMC

He F., Wang M., Gao M., Zhao M., Bai Y., Zhao C. (2014). Chemical composition and biological activities of Gerbera anandria. Molecules 19, 4046–4057. doi: 10.3390/molecules19044046, PMID: PubMed DOI PMC

Helariutta Y., Kotilainen M., Elomaa P., Kalkkinen N., Bremer K., Teeri T. H., et al. . (1996). Duplication and functional divergence in the chalcone synthase gene family of Asteraceae: evolution with substrate change and catalytic simplification. Proc. Natl. Acad. Sci. U. S. A. 93, 9033–9038. doi: 10.1073/pnas.93.17.9033, PMID: PubMed DOI PMC

Hothorn T., Hornik K., Zeileis A. (2006). Unbiased recursive partitioning: a conditional inference framework. J. Comput. Graph. Stat. 15, 651–674. doi: 10.1198/106186006X133933, PMID: PubMed DOI

Inoue T., Toyonaga T., Nagumo S., Nagai M. (1989). Biosynthesis of 4-hydroxy-5-methylcoumarin in a Gerbera jamesonii hybrid. Phytochemistry 28, 2329–2330. doi: 10.1016/S0031-9422(00)97977-9 DOI

Jones P., Vogt T. (2001). Glycosyltransferases in secondary plant metabolism: tranquilizers and stimulant controllers. Planta 213, 164–174. doi: 10.1007/s004250000492, PMID: PubMed DOI

Kashif A., Federica M., Eva Z., Martina R., Young H. C., Robert V. (2009). NMR metabolic fingerprinting based identification of grapevine metabolites associated with downy mildew resistance. J. Agric. Food Chem. 57, 9599–9606. doi: 10.1021/jf902069f, PMID: PubMed DOI

Kim H. K., Choi Y. H., Verpoorte R. (2010). NMR-based metabolomic analysis of plants. Nat. Protoc. 5, 536–549. doi: 10.1038/nprot.2009.237, PMID: PubMed DOI

Kloos W. E., George C. G., Sorge L. K. (2005a). Dark disk color in the flower of Gerbera hybrida is determined by a dominant gene, Dc. HortScience 40, 1992–1994. doi: 10.21273/hortsci.40.7.1992 DOI

Kloos W. E., George C. G., Sorge L. K. (2005b). Inheritance of powdery mildew resistance and leaf macrohair density in Gerbera hybrida. HortScience 40, 1246–1251. doi: 10.21273/hortsci.40.5.1246 DOI

Koskela S., Elomaa P., Helariutta Y., Kilpeläinen I., Harjunpää T., Teeri T. H., et al. . (2001). Two bioactive compounds and a novel chalcone synthaselike enzyme identified in Gerbera hybrida. Acta Hortic. 560, 271–274. doi: 10.17660/ActaHortic.2001.560.52 DOI

Koskela S., Söderholm P. P., Ainasoja M., Wennberg T., Klika K. D., Ovcharenko V. V., et al. . (2011). Polyketide derivatives active against Botrytis cinerea in Gerbera hybrida. Planta 233, 37–48. doi: 10.1007/s00425-010-1277-8, PMID: PubMed DOI

Kotsiantis S. B. (2013). Decision trees: a recent overview. Artif. Intell. Rev. 39, 261–283. doi: 10.1007/s10462-011-9272-4, PMID: PubMed DOI

Leiss K. A., Choi Y. H., Verpoorte R., Klinkhamer P. G. L. (2011). An overview of NMR-based metabolomics to identify secondary plant compounds involved in host plant resistance. Phytochem. Rev. 10, 205–216. doi: 10.1007/s11101-010-9175-z, PMID: PubMed DOI PMC

Leiss K. A., Cristofori G., Van Steenis R., Verpoorte R., Klinkhamer P. G. L. (2013). An eco-metabolomic study of host plant resistance to Western flower thrips in cultivated, biofortified and wild carrots. Phytochemistry 93, 63–70. doi: 10.1016/j.phytochem.2013.03.011, PMID: PubMed DOI

Leiss K. A., Maltese F., Choi Y. H., Verpoorte R., Klinkhamer P. G. L. (2009). Identification of chlorogenic acid as a resistance factor for thrips in chrysanthemum. Plant Physiol. 150, 1567–1575. doi: 10.1104/pp.109.138131, PMID: PubMed DOI PMC

Mascellani A., Natali L., Cavallini A., Mascagni F., Caruso G., Gucci R., et al. . (2021). Moderate salinity stress affects expression of main sugar metabolism and transport genes and soluble carbohydrate content in ripe fig fruits (Ficus carica l. cv. dottato). Plan. Theory 10:1861. doi: 10.3390/plants10091861, PMID: PubMed DOI PMC

Minic Z. (2008). Physiological roles of plant glycoside hydrolases. Planta 227, 723–740. doi: 10.1007/s00425-007-0668-y, PMID: PubMed DOI

Murphy C., Powlowski J., Wu M., Butler G., Tsang A. (2011). Curation of characterized glycoside hydrolases of fungal origin. Database 2011:bar020. doi: 10.1093/database/bar020, PMID: PubMed DOI PMC

Nagumo S., Toyonaga T., Inoue T., Masahiro N. (1989). New glucosides of a 4-hydroxy-5-methylcoumarin and a dihydro-α-pyrone from Gerbera jamesonii hybrida. Chem. Pharm. Bull. 37, 2621–2623. doi: 10.1248/cpb.37.2621 DOI

Numata A., Takahashi C., Fujiki R., Kitano E., Kitajima A., Takemura T. (1990). Plant constitutents biologically active to insects. VI. Antifeedants for larvae of the yellow butterfly Eurema hecabe mandarina in Osmunda japonica. Chem. Pharm. Bull. 38, 2862–2865. doi: 10.1248/cpb.38.2862, PMID: PubMed DOI

Osbourn A. E. (1996). Preformed antimicrobial compounds and plant defense against fungal attack. Plant Cell 8, 1821–1831. doi: 10.2307/3870232, PMID: PubMed DOI PMC

Paknikar S. K., Pai Fondekar K. P., Kirtany J. K., Natori S. (1996). 4-hydroxy-5-methylcoumarin derivatives from Diospyros kaki thunb and D. kaki var. sylvestris makino; structure and synthesis of 11-methylgerberinol. Phytochemistry 41, 931–933. doi: 10.1016/0031-9422(95)00698-2 DOI

Pang Z., Chong J., Li S., Xia J. (2020). Metaboanalystr 3.0: toward an optimized workflow for global metabolomics. Meta 10:186. doi: 10.3390/metabo10050186, PMID: PubMed DOI PMC

Pichersky E., Gang D. R. (2000). Genetics and biochemistry of secondary metabolites in plants: an evolutionary perspective. Trends Plant Sci. 5, 439–445. doi: 10.1016/S1360-1385(00)01741-6, PMID: PubMed DOI

Pietiäinen M., Kontturi J., Paasela T., Deng X., Ainasoja M., Nyberg P., et al. . (2016). Two polyketide synthases are necessary for 4-hydroxy-5-methylcoumarin biosynthesis in Gerbera hybrida. Plant J. 87, 548–558. doi: 10.1111/tpj.13216, PMID: PubMed DOI

R Core Team (2020). R: a language and environment for statistical computing. Available at: https://www.r-project.org/ (Accessed May 31, 2010).

Ruokolainen S., Ng Y. P., Broholm S. K., Albert V. A., Elomaa P., Teeri T. H. (2010). Characterization of SQUAMOSA-like genes in Gerbera hybrida, including one involved in reproductive transition. BMC Plant Biol. 10:128. doi: 10.1186/1471-2229-10-128, PMID: PubMed DOI PMC

Sardari S., Nishibe S., Daneshtalab M. (2000). Coumarins, the bioactive structures with antifungal property. Stud. Nat. Prod. Chem. 23, 335–393. doi: 10.1016/S1572-5995(00)80133-7 DOI

Sirikantaramas S., Yamazaki M., Saito K. (2008). Mechanisms of resistance to self-produced toxic secondary metabolites in plants. Phytochem. Rev. 7, 467–477. doi: 10.1007/s11101-007-9080-2 DOI

Song X., Deng Z. (2013). Powdery mildew resistance in gerbera: mode of inheritance, quantitative trait locus identification, and resistance responses. J. Am. Soc. Hortic. Sci. 138, 470–478. doi: 10.21273/jashs.138.6.470 DOI

Song X., Deng Z., Gong L., Hu J., Ma Q. (2012). Cloning and characterization of resistance gene candidate sequences and molecular marker development in gerbera (Gerbera hybrida). Sci. Hortic. 145, 68–75. doi: 10.1016/j.scienta.2012.07.027 DOI

Teeri T. H., Elomaa P., Kotilainen M., Albert V. A. (2006). Mining plant diversity: gerbera as a model system for plant developmental and biosynthetic research. BioEssays 28, 756–767. doi: 10.1002/bies.20439, PMID: PubMed DOI

Tschesche R., Hoppe H., Snatzke G., Walff G., Fehlhaber H.-W. (1971). Über Glykoside mit lacton-bildendem Aglykon, III. Über Parasorbosid, den glykosidischen Vorläufer der Parasorbinsäure, aus Vogelbeeren. Chem. Ber. 104, 1420–1428. doi: 10.1002/cber.19711040510 DOI

USDA (2019). Floriculture crops 2018 summary. National Agricultural Statistics Service.

Verpoorte R., Choi Y. H., Kim H. K. (2007). NMR-based metabolomics at work in phytochemistry. Phytochem. Rev. 6, 3–14. doi: 10.1007/s11101-006-9031-3, PMID: PubMed DOI

Verpoorte R., Choi Y. H., Mustafa N. R., Kim H. K. (2008). Metabolomics: back to basics. Phytochem. Rev. 7, 525–537. doi: 10.1007/s11101-008-9091-7, PMID: PubMed DOI

Wickham H. (2016). ggplot2: Elegant Graphics for Data Analysis. New York: Springer Verlag.

Winning H., Larsen F. H., Bro R., Engelsen S. B. (2008). Quantitative analysis of NMR spectra with chemometrics. J. Magn. Reson. 190, 26–32. doi: 10.1016/j.jmr.2007.10.005, PMID: PubMed DOI

Wolfender J. L., Ndjoko K., Hostettmann K. (2003). Liquid chromatography with ultraviolet absorbance-mass spectrometric detection and with nuclear magnetic resonance spectroscopy: a powerful combination for the on-line structural investigation of plant metabolites. J. Chromatogr. A 1000, 437–455. doi: 10.1016/S0021-9673(03)00303-0, PMID: PubMed DOI

Yrjönen T., Vuorela P., Klika K. D., Pihlaja K., Teeri T. H., Vuorela H. (2002). Application of centrifugal force to the extraction and separation of parasorboside and gerberin from Gerbera hybrida. Phytochem. Anal. 13, 349–353. doi: 10.1002/pca.665, PMID: PubMed DOI

Zdero C., Bohlmann F., Solomon J. (1988). Further 5-methylcoumarin derivatives from Mutisia orbignyana. Phytochemistry 27, 891–897. doi: 10.1016/0031-9422(88)84114-1 DOI

Phytochemical S-methyl-L-cysteine sulfoxide from Brassicaceae: a key to health or a poison for bees?