Skip to main content
SpringerLink
Log in

Phenolic profiles of two Melampyrum species differing in susceptibility to Cronartium rust

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Cronartium flaccidum is an important pathogen in boreal forestry where it causes pine stem rust. The hemiparasite Melampyrum sylvaticum serves as a telial host for this heteroecious fungus while the congeneric M. pratense is highly resistant. We hypothesized that the variation in susceptibility is due to differences in the composition of secondary phenolic compounds in host plant tissues. To test this hypothesis, phenolic compounds of leaf extracts taken from both species of Melampyrum were analyzed with HPLC. Principal component analysis (PCA) and hierarchical cluster analysis (HCA) were used for data processing. PCA indicated difference between the species, with the first two components explaining more than 70 % of the total variance of data that was separated into two distinct groups in a scatter plot. Two clusters, formed by the two species, were also suggested by HCA. Phenolic acids (such as chlorogenic acid), flavanones and apigenin flavonoids dominated the profiles of rust-resistant M. pratense, while kaempferol and luteolin flavonoids occurred in high relative concentrations in rust-susceptible M. sylvaticum. Our results suggest that phenolics may contribute to resistance or susceptibility of Melampyrum to Cronartium rusts as one factor. Future studies on the mode of action of phenolics in this interaction are thus warranted.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Boyer, M. G. (1964). Studies on white pine phenols in relation to blister rust. Canadian Journal of Botany, 42, 979–987.

    Article  CAS  Google Scholar 

  • Burda, S., & Oleszek, W. (2001). Antioxidant and antiradical activities of flavonoids. Journal of Agricultural Food Chemistry, 49, 2774–2779.

    Article  CAS  PubMed  Google Scholar 

  • Caetano-Anollés, G., Crist-Estes, D. K., & Bauer, W. D. (1988). Chemotaxis of Rhizobium meliloti to the plant flavone luteolin requires functional nodulation genes. Journal of Bacteriology, 170(7), 3164–3169.

    PubMed Central  PubMed  Google Scholar 

  • Cushnie, T. P. T., & Lamb, A. J. (2005). Antimicrobial activity of flavonoids. International Journal of Antimicrobial Agents, 26, 343–356.

    Article  CAS  PubMed  Google Scholar 

  • Fokom, R., Nana Wakam, L., Tchameni, S., & Nwaga, D. (2010). Arbuscular Mycorrhizal Fungi (AMF) colonisation and Rhizobia nodulation of cowpea as affected by flavonoid application. Research Journal of Agriculture & Biological Sciences, 6(6), 1015–1021.

    CAS  Google Scholar 

  • Gäumann, E. (1959). Die Rostpilze Mitteleuropas. Beiträge zur Kryptogamenflora der Schweiz, 12, 85–93.

    Google Scholar 

  • Golowska, S., Lukasik, I., Kapusta, I., & Janda, B. (2012). Do the contents of luteolin, tricin and chryseriol glycosides in alfalfa (Medigo sativa L.) affect the behavior of pea aphid (Acyrthosiphon pisum)? Polish Journal of Environmental Studies, 21, 1613–1619.

    Google Scholar 

  • Hakulinen, J. (1998). Nitrogen-induced reduction in leaf phenolic level is not accompanied by increased rust frequency in a compatible willow (Salix myrsinifolia)—Melampsora rust interaction. Physiologia Plantarum, 102, 101–110.

    Article  CAS  Google Scholar 

  • Hakulinen, J., Sorjonen, S., & Julkunen-Tiitto, R. (1999). Leaf phenolics of willow clones differing in resistance to Melampsora rust. Physiologia Plantarum, 105, 662–669.

    Article  CAS  Google Scholar 

  • Hämet-Ahti, L., Suominen, J., Ulvinen, T., & Uotila, P. (1998). Retkeilykasvio. Helsinki: Suomen Luonnontieteellinen keskusmuseo, Kasvimuseo.

    Google Scholar 

  • Hanover, J. W., & Hoff, R. J. (1966). A Comparison of phenolic constituents of Pinus monticola resistant and susceptible to Cronartium ribicola. Physiologia Plantarum, 19, 554–562.

    Article  CAS  Google Scholar 

  • Hudgins, J. W., McDonald, G. I., Zambino, P. J., Klopfenstein, N. B., & Franceschi, V. R. (2005). Anatomical and cellular responses of Pinus monticola stem tissues to invasion by Cronartium ribicola. Forest Pathology, 35(6), 423–443.

    Article  Google Scholar 

  • Hylander, N., Jørstad, I., & Nannfeldt, J. A. (1953). Enumeratio Uredinearum Scandinavicarum. Opera Botanica, 1, 12–13.

    Google Scholar 

  • Kaitera, J. (1999). Cronartium flaccidum fruitbody production on Melampyrum spp. and some important alternate hosts to pine. European Journal of Forest Pathology, 29, 391–398.

    Article  Google Scholar 

  • Kaitera, J. (2000). Analysis of Cronartium flaccidum lesion development on pole-stage Scots pines. Silva Fennica, 34, 21–27.

    Article  Google Scholar 

  • Kaitera, J., & Hantula, J. (1998). Melampyrum sylvaticum, a new alternate host for pine stem rust Cronartium flaccidum. Mycologia, 90, 1028–1030.

    Article  Google Scholar 

  • Kaitera, J., & Hiltunen, R. (2011). Susceptibility of Pedicularis spp. to Cronartium ribicola and C. flaccidum in Finland. Forest Pathology, 41, 237–242.

    Article  Google Scholar 

  • Kaitera, J., & Hiltunen, R. (2012). New alternate hosts for the rusts Cronartium ribicola and Cronartium flaccidum in Finland. Canadian Journal of Forest Research, 42, 1661–1668.

    Article  Google Scholar 

  • Kaitera, J., & Nuorteva, H. (2003a). Cronartium flaccidum produces uredinia and telia on Melampyrum nemorosum and on Finnish Vincetoxicum hirundinaria. Forest Pathology, 33, 205–213.

    Article  Google Scholar 

  • Kaitera, J., & Nuorteva, H. (2003b). Relative susceptibility of four Melampyrum species to Cronartium flaccidum. Scandinavian Journal of Forest Research, 18, 499–504.

    Article  Google Scholar 

  • Kaitera, J., Aalto, T., & Jalkanen, R. (1994). Effect of resin-top disease caused by Peridermium pini on the volume and value of Pinus sylvestris saw timber and pulpwood. Scandinavian Journal of Forest Research, 9, 376–381.

    Article  Google Scholar 

  • Kaitera, J., Seitamäki, L., Hantula, J., Jalkanen, R., & Kurkela, T. (1999). Inoculation of known and potential alternate hosts with Peridermium pini and Cronartium flaccidum aeciospores. Mycological Research, 103, 235–241.

    Article  Google Scholar 

  • Kaitera, J., Nuorteva, H., & Hantula, J. (2005). Distribution and frequency of Cronartium flaccidum on Melampyrum spp. in Finland. Canadian Journal of Forest Research, 35, 229–234.

    Article  Google Scholar 

  • Kaitera, J., Hantula, J., & Nevalainen, S. (2011). Distribution and frequency of Cronartium flaccidum on Melampyrum spp. in permanent sample plots in Finland. Scandinavian Journal of Forest Research, 26, 413–420.

    Article  Google Scholar 

  • Kaitera, J., Hiltunen, R., & Samils, B. (2012). Alternate host ranges of Cronartium flaccidum and Cronartium ribicola in northern Europe. Botany, 90, 694–703.

    Article  Google Scholar 

  • Kaitera, J., Hiltunen, R., & Hantula, J. (2015). Cronartium rusts sporulation on hemiparasitic plants. Plant Pathology, 64(3), 738–747.

    Article  Google Scholar 

  • Keinänen, M., & Julkunen-Tiitto, R. (1996). Effect of sample preparation method on birch (Betula pendula Roth) leaf phenolics. Journal of Agricultural and Food Chemistry, 44, 2724–2727.

    Article  Google Scholar 

  • 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 Physiology, 150, 1567–1575.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lizzi, Y., Rogger, J. P., & Coulomb, P. J. (1995). Behavior of the phenolic compounds on Capsicum annuum leaves infected with Phytophthora capsici. Journal of Phytopathology, 143, 619–627.

    Article  CAS  Google Scholar 

  • Marinova, K., Kleinschmidt, K., Weissenböck, G., & Klein, M. (2007). Flavonoid biosynthesis in barley primary leaves requires the presence of the vacuole and controls the activity of vacuolar flavonoid transport. Plant Physiology, 144(1), 432–444.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Martinsson, O., & Nilsson, B. (1987). The impact of Cronartium flaccidum on the growth of Pinus sylvestris. Scandinavian Journal of Forest Research, 2, 349–357.

    Article  Google Scholar 

  • Melo, G. A., Shimizu, M. M., & Mazzafera, P. (2006). Polyphenoloxidase activity in coffee leaves and its role in resistance against the coffee leaf miner and coffee leaf rust. Phytochemistry, 67(3), 277–285.

    Article  CAS  PubMed  Google Scholar 

  • Moricca, S., & Ragazzi, A. (1996). Culture characteristics and variation of Cronartium flaccidum isolates. Canadian Journal of Botany, 74(6), 924–933.

    Article  Google Scholar 

  • Nagle, A. M., Mcpherson, B. A., Wood, D. L., Garbelotto, M., & Bonello, P. (2011). Relationship between field resistance to Phytophthora ramorum and constitutive phenolic chemistry of coast live oak. Forest Pathology, 41, 464–469.

    Article  Google Scholar 

  • Naumov, P., Kuzmanovski, I., & Stefova, M. (1998). Flavonoids of Verbascum scardicolum and Melampyrum scardicum. Bulletin of the Chemists and Technologists of Macedonia, 17(1), 41–44.

    CAS  Google Scholar 

  • Pietta, P. G. (2000). Flavonoids as antioxidants. Journal of Natural Products, 63, 1035–1042.

    Article  CAS  PubMed  Google Scholar 

  • Samils, B., Ihrmark, K., Kaitera, J., Hansson, P., & Barklund, P. (2010). Genetic structure of Scots pine blister rust (Cronartium flaccidum and Peridermium pini). Phytopathologia Mediterranea, 49, 428.

    Google Scholar 

  • Scervino, J. M., Ponce, M. A., Erra-Bassells, R., Vierheilig, H., Ocampo, J. A., & Godeas, A. (2005a). Arbuscular mycorrhizal colonization of tomato by Gigaspora and Glomerus species in the presence of root flavonoids. Journal of Plant Physiology, 162, 625–633.

    Article  CAS  PubMed  Google Scholar 

  • Scervino, J. M., Ponce, M. A., Erra-Bassells, R., Vierheilig, H., Ocampo, J. A., & Godeas, A. (2005b). Flavonoids exhibit fungal species and genus specific effects on the presymbiotic growth of Gigaspora and Glomus. Mycological Research, 109(7), 789–794.

    Article  CAS  PubMed  Google Scholar 

  • Sniezko, R. A., Smith, J., Liu, J.-J., & Hamelin, R. C. (2014). Genetic resistance to fusiform rust in southern pines and white pine blister rust in white pines—a contrasting tale of two rust pathosystems—current status and future prospects. Forests, 5(9), 2050–2083.

    Article  Google Scholar 

  • Witzell, J., & Martín, J. A. (2008). Phenolic metabolites in pathogen resistance of northern forest trees—past experiences and future prospects. Canadian Journal of Forest Research, 38, 2711–2727.

    Article  Google Scholar 

  • Zampino, P. J. (2010). Biology and pathology of Ribes and their implications for management of white pine blister rust. Forest Pathology, 40, 264–291.

    Article  Google Scholar 

  • Zielinski, A. A. F., Haminiuk, C. W. I., Alberti, A., Nogueira, A., Demiate, I. M., & Granato, D. (2014). A comparative study of the phenolic compounds and the in vitro antioxidant activity of different Brazilian teas using multivariate statistical techniques. Food Research International, 60, 246–254.

    Article  CAS  Google Scholar 

  • Ziller, W. G. (1974). The tree rusts of western Canada. Canadian Forest Service Publications, 1329, 1–272.

    Google Scholar 

Download references

Acknowledgments

We thank Dr. Michael Hardman for checking the language and Ms. Iryna Semashko for assistance with laboratory analyses.

Author information

Authors and Affiliations

  1. Natural Resources Institute Finland, University of Oulu, P. O. Box 413, FI-90014, Oulu, Finland

    Juha Kaitera

  2. Faculty of Science and Forestry, University of Eastern Finland, P.O. Box 111, FI-80101, Joensuu, Finland

    Johanna Witzell

  3. Institut för Sydsvensk Skogsvetenskap, P. O. Box 49, SE-23053, Alnarp, Sweden

    Johanna Witzell

Authors
  1. Juha Kaitera
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Johanna Witzell
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Juha Kaitera.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kaitera, J., Witzell, J. Phenolic profiles of two Melampyrum species differing in susceptibility to Cronartium rust. Eur J Plant Pathol 144, 133–140 (2016). https://doi.org/10.1007/s10658-015-0757-x

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-015-0757-x

Keywords

Search

Navigation