Interactions of Bunias orientalis plant chemotypes and fungal pathogens with different host specificity in vivo and in vitro

Bennett, R. N. & Wallsgrove, R. M. Secondary metabolites in plant defense-mechanisms. New Phytol. 127, 617–633. https://doi.org/10.1111/j.1469-8137.1994.tb02968.x (1994).

CAS  Article  Google Scholar 

Giamoustaris, A. & Mithen, R. Glucosinolates and disease resistance in oilseed rape (Brassica napus ssp. oleifera). Plant Pathol. 46, 271–275. https://doi.org/10.1046/j.1365-3059.1997.d01-222.x (1997).

CAS  Article  Google Scholar 

Schoonhoven, L. M., Van Loon, J. J. A. & Dicke, M. Insect-plant biology 2nd edn. (Oxford University Press, Oxford, 2005).

Google Scholar 

van der Meijden, E. Plant defence, an evolutionary dilemma: Contrasting effects of (specialist and generalist) herbivores and natural enemies. Entomol. Exp. Appl. 80, 307–310. https://doi.org/10.1111/j.1570-7458.1996.tb00941.x (1996).

Article  Google Scholar 

Maor, R. & Shirasu, K. The arms race continues: Battle strategies between plants and fungal pathogens. Curr. Opin. Microbiol. 8, 399–404. https://doi.org/10.1016/j.mib.2005.06.008 (2005).

CAS  Article  PubMed  Google Scholar 

Bednarek, P. & Osbourn, A. Plant-microbe interactions: Chemical diversity in plant defense. Science 324, 746–748. https://doi.org/10.1126/science.1171661 (2009).

ADS  CAS  Article  PubMed  Google Scholar 

Macel, M. & Klinkhamer, P. G. L. Chemotype of Senecio jacobaea affects damage by pathogens and insect herbivores in the field. Evol. Ecol. 24, 237–250. https://doi.org/10.1007/s10682-009-9303-7 (2010).

Article  Google Scholar 

Kleine, S. & Müller, C. Intraspecific plant chemical diversity and its effects on herbivores. Oecologia 166, 175–186. https://doi.org/10.1007/s00442-010-1827-6 (2011).

ADS  Article  PubMed  Google Scholar 

Züst, T. et al. Natural enemies drive geographic variation in plant defenses. Science 338, 116–119. https://doi.org/10.1126/science.1226397 (2012).

ADS  CAS  Article  PubMed  Google Scholar 

Christensen, S. et al. Different geographical distributions of two chemotypes of Barbarea vulgaris that differ in resistance to insects and a pathogen. J. Chem. Ecol. 40, 491–501. https://doi.org/10.1007/s10886-014-0430-4 (2014).

CAS  Article  PubMed  Google Scholar 

Poelman, E. H., van Dam, N. M., van Loon, J. J. A., Vet, L. E. M. & Dicke, M. Chemical diversity in Brassica oleracea affects biodiversity of insect herbivores. Ecology 90, 1863–1877. https://doi.org/10.1890/08-0977.1 (2009).

Article  PubMed  Google Scholar 

Richards, L. A. et al. Phytochemical diversity drives plant–insect community diversity. Proc. Natl. Acad. Sci. USA 112, 10973–10978. https://doi.org/10.1073/pnas.1504977112 (2015).

ADS  CAS  Article  PubMed  Google Scholar 

Arany, A. M. et al. Glucosinolates and other metabolites in the leaves of Arabidopsis thaliana from natural populations and their effects on a generalist and a specialist herbivore. Chemoecology 18, 65–71. https://doi.org/10.1007/s00049-007-0394-8 (2008).

ADS  CAS  Article  Google Scholar 

Bidart-Bouzat, M. G. & Kliebenstein, D. J. Differential levels of insect herbivory in the field associated with genotypic variation in glucosinolates in Arabidopsis thaliana. J. Chem. Ecol. 34, 1026–1037. https://doi.org/10.1007/s10886-008-9498-z (2008).

CAS  Article  PubMed  Google Scholar 

van Leur, H., Vet, L. E. M., Van der Putten, W. H. & van Dam, N. M. Barbarea vulgaris glucosinolate phenotypes differentially affect performance and preference of two different species of lepidopteran herbivores. J. Chem. Ecol. 34, 121–131. https://doi.org/10.1007/s10886-007-9424-9 (2008).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Gols, R. et al. Genetic variation in defense chemistry in wild cabbages affects herbivores and their endoparasitoids. Ecology 89, 1616–1626. https://doi.org/10.1890/07-0873.1 (2008).

Article  PubMed  Google Scholar 

Harvey, J. A., van Dam, N. M., Raaijmakers, C. E., Bullock, J. M. & Gols, R. Tri-trophic effects of inter- and intra-population variation in defence chemistry of wild cabbage (Brassica oleracea). Oecologia 166, 421–431. https://doi.org/10.1007/s00442-010-1861-4 (2011).

ADS  Article  PubMed  Google Scholar 

van Mölken, T. et al. Consequences of combined herbivore feeding and pathogen infection for fitness of Barbarea vulgaris plants. Oecologia 175, 589–600. https://doi.org/10.1007/s00442-014-2928-4 (2014).

ADS  Article  PubMed  Google Scholar 

Agerbirk, N. & Olsen, C. E. Glucosinolate structures in evolution. Phytochemistry 77, 16–45. https://doi.org/10.1016/j.phytochem.2012.02.005 (2012).

CAS  Article  PubMed  Google Scholar 

Hopkins, R. J., van Dam, N. M. & van Loon, J. J. A. Role of glucosinolates in insect–plant relationships and multitrophic interactions. Annu. Rev. Entomol. 54, 57–83. https://doi.org/10.1146/annurev.ento.54.110807.090623 (2009).

CAS  Article  PubMed  Google Scholar 

Renwick, J. A. A. The chemical world of crucivores: lures, treats and traps. Entomol. Exp. Appl. 104, 35–42. https://doi.org/10.1046/j.1570-7458.2002.00988.x (2002).

CAS  Article  Google Scholar 

Poelman, E. H., Galiart, R., Raaijmakers, C. E., van Loon, J. J. A. & van Dam, N. M. Performance of specialist and generalist herbivores feeding on cabbage cultivars is not explained by glucosinolate profiles. Entomol. Exp. Appl. 127, 218–228. https://doi.org/10.1111/j.1570-7458.2008.00700.x (2008).

Article  Google Scholar 

Tewes, L. J., Michling, F., Koch, M. A. & Müller, C. Intracontinental plant invader shows matching genetic and chemical profiles and might benefit from high defence variation within populations. J. Ecol. 106, 714–726. https://doi.org/10.1111/1365-2745.12869 (2018).

CAS  Article  Google Scholar 

Fortuna, T. M. et al. Variation in plant defences among populations of a range-expanding plant: Consequences for trophic interactions. New Phytol. 204, 989–999. https://doi.org/10.1111/nph.12983 (2014).

Article  PubMed  Google Scholar 

Tewes, L. J. & Müller, C. Syndromes in suites of correlated traits suggest multiple mechanisms facilitating invasion in a plant range-expander. NeoBiota 37, 1–22. https://doi.org/10.3897/neobiota.37.21470 (2018).

Article  Google Scholar 

Koch, M. A. et al. Early-Mid Pleistocene genetic differentiation and range expansions as exemplified by invasive Eurasian Bunias orientalis (Brassicaceae) indicates the Caucasus as key region. Sci. Rep. 7, 1–13. https://doi.org/10.1038/s41598-017-17085-8 (2017).

CAS  Article  Google Scholar 

Möbius, N. & Hertweck, C. Fungal phytotoxins as mediators of virulence. Curr. Opin. Plant Biol. 12, 390–398. https://doi.org/10.1016/j.pbi.2009.06.004 (2009).

CAS  Article  PubMed  Google Scholar 

Thomma, B. P. H. J. Alternaria spp.: From general saprophyte to specific parasite. Mol. Plant Pathol. 4, 225–236. https://doi.org/10.1046/j.1364-3703.2003.00173.x (2003).

CAS  Article  PubMed  Google Scholar 

Farr, D. F. & Rossman, A. Y. Fungal Databases, U.S. National Fungus Collections, ARS, USDA. Accessed 8 June 2019 https://nt.ars-grin.gov/fungaldatabases/ (2019).

Williamson, B., Tudzynsk, B., Tudzynski, P. & van Kan, J. A. L. Botrytis cinerea: the cause of grey mould disease. Mol. Plant Pathol. 8, 561–580. https://doi.org/10.1111/j.1364-3703.2007.00417.x (2007).

CAS  Article  PubMed  Google Scholar 

Ahuja, I., Kissen, R. & Bones, A. M. Phytoalexins in defense against pathogens. Trends Plant Sci. 17, 73–90. https://doi.org/10.1016/j.tplants.2011.11.002 (2012).

CAS  Article  PubMed  Google Scholar 

Ribera, A. E. & Zuñiga, G. Induced plant secondary metabolites for phytopatogenic fungi control: A review. J. Soil Sci. Plant Nutr. 12, 893–911. https://doi.org/10.4067/s0718-95162013005000029 (2012).

Article  Google Scholar 

Pedras, M. S. C., Yaya, E. E. & Glawischnig, E. The phytoalexins from cultivated and wild crucifers: Chemistry and biology. Nat. Prod. Rep. 28, 1381–1405. https://doi.org/10.1039/c1np00020a (2011).

CAS  Article  PubMed  Google Scholar 

Conn, K. L., Tewari, J. P. & Dahiya, J. S. Resistance to Alternaria brassicae and phytoalexin-elicitation in rapeseed and other crucifers. Plant Sci. 56, 21–25. https://doi.org/10.1016/0168-9452(88)90180-x (1988).

CAS  Article  Google Scholar 

Sellam, A., Iacomi-Vasilescu, B., Hudhomme, P. & Simoneau, P. In vitro antifungal activity of brassinin, camalexin and two isothiocyanates against the crucifer pathogens Alternaria brassicicola and Alternaria brassicae. Plant Pathol. 56, 296–301. https://doi.org/10.1111/j.1365-3059.2006.01497.x (2007).

CAS  Article  Google Scholar 

Elad, Y. & Evensen, K. Physiological aspects of resistance to Botrytis cinerea. Phytopathology 85, 637–643. https://doi.org/10.1094/Phyto-85-637 (1995).

Article  Google Scholar 

Kliebenstein, D. J., Rowe, H. C. & Denby, K. J. Secondary metabolites influence Arabidopsis/Botrytis interactions: Variation in host production and pathogen sensitivity. Plant J. 44, 25–36. https://doi.org/10.1111/j.1365-313X.2005.02508.x (2005).

CAS  Article  PubMed  Google Scholar 

Ayer, W. A. & Pena-Rodriguez, L. M. Metabolites produced by Alternaria brassicae, the black spot pathogen of canola. Part 1, the phytotoxic components. J. Nat. Prod. 50, 400–407. https://doi.org/10.1021/np50051a010 (1987).

CAS  Article  Google Scholar 

Bains, P. S. & Tewari, J. P. Purification, chemical characterization and host-specificity of the toxin produced by Alternaria brassicae. Physiol. Mol. Plant Pathol. 30, 259–271. https://doi.org/10.1016/0885-5765(87)90039-7 (1987).

CAS  Article  Google Scholar 

Buchwaldt, L. & Green, H. Phytotoxicity of destruxin B and its possible role in the pathogenesis of Alternaria brassicae. Plant Pathol. 41, 55–63. https://doi.org/10.1111/j.1365-3059.1992.tb02316.x (1992).

CAS  Article  Google Scholar 

Pedras, M. S. C. & Khallaf, I. Molecular interactions of the phytotoxins destruxin B and sirodesmin PL with crucifers and cereals: Metabolism and elicitation of plant defenses. Phytochemistry 77, 129–139. https://doi.org/10.1016/j.phytochem.2012.02.010 (2012).

CAS  Article  PubMed  Google Scholar 

van Kan, J. A. L. Licensed to kill: The lifestyle of a necrotrophic plant pathogen. Trends Plant Sci. 11, 247–253. https://doi.org/10.1016/j.tplants.2006.03.005 (2006).

CAS  Article  PubMed  Google Scholar 

Choquer, M. et al. Botrytis cinerea virulence factors: New insights into a necrotrophic and polyphageous pathogen. FEMS Microbiol. Lett. 277, 1–10. https://doi.org/10.1111/j.1574-6968.2007.00930.x (2007).

CAS  Article  PubMed  Google Scholar 

Doorduin, L. J. & Vrieling, K. A review of the phytochemical support for the shifting defence hypothesis. Phytochem. Rev. 10, 99–106. https://doi.org/10.1007/s11101-010-9195-8 (2011).

CAS  Article  PubMed  Google Scholar 

Müller, C. Evolution of competitive ability and shifting defence hypotheses. In Invasion Biology: Hypotheses and Evidence (eds Jeschke, J. M. & Heger, T.) 103–123 (CABI Publishing, Wallingford, 2018).

Google Scholar 

Ugolini, L., Martini, C., Lazzeri, L., D’Avino, L. & Mari, M. Control of postharvest grey mould (Botrytis cinerea Per.: Fr.) on strawberries by glucosinolate-derived allyl-isothiocyanate treatments. Postharvest Biol. Technol. 90, 34–39. https://doi.org/10.1016/j.postharvbio.2013.12.002 (2014).

CAS  Article  Google Scholar 

Tierens, K. F. M. J. et al. Study of the role of antimicrobial glucosinolate-derived isothiocyanates in resistance of Arabidopsis to microbial pathogens. Plant Physiol. 125, 1688–1699. https://doi.org/10.1104/pp.125.4.1688 (2001).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Brader, G., Mikkelsen, M. D., Halkier, B. A. & Palva, E. T. Altering glucosinolate profiles modulates disease resistance in plants. Plant J. 46, 758–767. https://doi.org/10.1111/j.1365-313X.2006.02743.x (2006).

CAS  Article  PubMed  Google Scholar 

Juniper, B. E. The leaf from the inside and the outside: a microbe’s perspective. In Microbial Ecology of Leaves (eds Andrews, J. H. & Hirano, S. S.) 21–42 (Springer, Berlin, 1991).

Google Scholar 

Müller, C. & Riederer, M. Review: Plant surface properties in chemical ecology. J. Chem. Ecol. 31, 2621–2651. https://doi.org/10.1007/s10886-005-7617-7 (2005).

CAS  Article  PubMed  Google Scholar 

Meena, P. D., Awasthi, R. P., Chattopadhyay, C., Kolte, S. J. & Kumar, A. Alternaria blight: A chronic disease in rapeseed-mustard. J. Oilseed Brassica 1, 1–11 (2010).

Google Scholar 

Levin, D. A. The role of trichomes in plant defense. Q. Rev. Biol. 48, 3–15. https://doi.org/10.1086/407484 (1973).

Article  Google Scholar 

Hanley, M. E., Lamont, B. B., Fairbanks, M. M. & Rafferty, C. M. Plant structural traits and their role in anti-herbivore defence. Perspect. Plant Ecol. 8, 157–178. https://doi.org/10.1016/j.ppees.2007.01.001 (2007).

Article  Google Scholar 

Gessner, M. O. & Schmitt, A. L. Use of solid-phase extraction to determine ergosterol concentrations in plant tissue colonized by fungi. Appl. Environ. Microbiol. 62, 415–419 (1996).

CAS  Article  Google Scholar 

Beni, A., Soki, E., Lajtha, K. & Fekete, I. An optimized HPLC method for soil fungal biomass determination and its application to a detritus manipulation study. J. Microbiol. Meth. 103, 124–130. https://doi.org/10.1016/j.mimet.2014.05.022 (2014).

CAS  Article  Google Scholar 

Hadacek, F. & Greger, H. Testing of antifungal natural products: Methodologies, comparability of results and assay choice. Phytochem. Anal. 11, 137–147. https://doi.org/10.1002/(sici)1099-1565(200005/06)11:3<137::aid-pca514>3.0.co;2-i (2000).

CAS  Article  Google Scholar 

Schrieber, K., Schweiger, R., Kröner, L. & Müller, C. Inbreeding diminishes herbivore-induced metabolic responses in native and invasive plant populations. J. Ecol. 107, 923–936. https://doi.org/10.1111/1365-2745.13068 (2019).

Article  Google Scholar 

R Core Team. R: A language and environment for statistical computing. R foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (2018).

Bates, D., Mächler, M., Bolker, B. M. & Walker, S. C. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48. https://doi.org/10.18637/jss.v067.i01 (2015).

Article  Google Scholar 

Arnholt, A. T. & Evans, B. BSDA: Basic statistics and data analysis. R package version 1.2.0. https://CRAN.R-project.org/package=BSDA (2017).

Fox, J. & Weisberg, S. An {R} companion to applied regression. 2 edn. (Sage, 2011) https://socialsciences.mcmaster.ca/jfox/Books/Companion/ (2018).