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Antibiotic properties of the glucosinolates of Brassica oleracea var. acephala similarly affect generalist and specialist larvae of two lepidopteran pests

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Abstract

Glucosinolates may deter generalist insect feeding as their toxicity causes fitness damage, whereas insects specialized in brassicaceous plants may circumvent the toxic effect. By using no-choice leaf tests, we investigated whether larval development time, body weight, mortality and feeding rate of the generalist Mamestra brassicae (Lepidoptera, Noctuidae) and the specialist Pieris rapae (Lepidoptera, Pieridae), were affected by six genotypes of Brassica oleracea var. acephala, selected for having high or low concentration of sinigrin, glucoiberin (aliphatics) and glucobrassicin (indole). Two phenological plant stages were used. On young plants, M. brassicae most consumed the high sinigrin and low glucoiberin genotypes. Larvae weighed more on the high sinigrin plants. Development time took longer on the low glucoiberin genotype. On mature plants, consumption rate decreased on the high glucoiberin genotype. Larval weight decreased on the high sinigrin, glucoiberin and glucobrassicin genotypes, and development time increased with high glucobrassicin concentration. Pupal weight and mortality rate increased on mature plants, irrespective of the genotype. Pieris rapae fed most on young plants with high sinigrin, and larval weight increased on the high glucoiberin genotype. Mortality increased with low glucoiberin and low glucobrassicin. On mature plants, larval weight decreased with high sinigrin and glucoiberin. The high glucoiberin genotype was the less consumed and also induced a longer development time. High content of aliphatic glucosinolates offered mature plants significant antibiosis defence against both the lepidopterans, whereas the indole glucosinolate was marginally effective. Young plants were more consumed and increased larval weight likely because glucosinolate concentration was still not optimal.

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References

  • Agrawal AA, Kurashige NS (2003) A role for isothiocyanates in plant resistance against the specialist herbivore Pieris rapae. J Chem Ecol 29:1403–1415

    Article  CAS  PubMed  Google Scholar 

  • Ali JG, Agrawal AA (2012) Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci 17:293–302

    Article  CAS  PubMed  Google Scholar 

  • Bekaert M, Edger PP, Hudson CM, Pires JC, Conant GC (2012) Metabolic and evolutionary costs of herbivory defense: systems biology of glucosinolate synthesis. New Phytol 196:596–605

    Article  Google Scholar 

  • Benrey B, Denno RF (1997) The slow-growth–high-mortality hypothesis: a test using the cabbage butterfly. Ecology 78:987–999

    Google Scholar 

  • Bowers MD, Stamp NE (1993) Effects of plant age, genotype and herbivory on plantago performance and chemistry. Ecology 74:1778–1791

    Article  Google Scholar 

  • Campos WG, Schoereder JH, Picanço MC (2003) Performance of an oligophagous insect in relation to the age of the host plant. Neotrop Entomol 32:671–676

    Google Scholar 

  • Cartea ME, Velasco P, Obregón S, Padilla G, de Haro A (2008) Seasonal variation in glucosinolate content in Brassica oleracea crops grown in northwestern Spain. Phytochemistry 69:403–410

    Article  CAS  PubMed  Google Scholar 

  • Cartea ME, Soengas P, Ordás A, Velasco P (2009) Resistance of kale varieties to attack by Mamestra brassicae. Agric For Entomol 11:153–160

    Article  Google Scholar 

  • Clancy KM, Price PW (1987) Rapid herbivore growth enhances enemy attack: sublethal plant defenses remain a paradox. Ecology 68:733–737

    Article  Google Scholar 

  • Cole RA (1997) The relative importance of glucosinolates and amino acids to the development of two aphid pests Brevicoryne brassicae and Myzus persicae on wild and cultivated brassica species. Entomol Exp Appl 85:121–133

    Article  CAS  Google Scholar 

  • de Vos M, Kriksunov KL, Jander G (2008) Indole-3-acetonitrile production from indole glucosinolates deters oviposition by Pieris rapae (white cabbage butterfly). Plant Physiol 146:916–926

    Article  PubMed Central  PubMed  Google Scholar 

  • Gols R, Bukovinszky T, van Dam N, Dicke M, Bullock JM, Harvey JA (2008a) Genetic variation in defence chemistry in wild cabbages affects herbivores and their endoparasitoids. Ecology 89:1616–1626

    Article  PubMed  Google Scholar 

  • Gols R, Bukovinszky T, van Dam N, Dicke M, Bullock JM, Harvey JA (2008b) Performance of generalist and specialist herbivores and their endoparasitoids differs on cultivated and wild Brassica populations. J Chem Ecol 34:132–143

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Harvey JA, Gols R (2011) Population-related variation in plant defense more strongly affects survival of an herbivore than its solitary parasitoid wasp. J Chem Ecol 37:1081–1090

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Harvey JA, Gols R, Wagenaar R, Bezemer TM (2007) Development of an insect herbivore and its pupal parasitoid reflect differences in direct plant defense. J Chem Ecol 33:1556–1569

    Article  CAS  PubMed  Google Scholar 

  • Hopkins RJ, van Dam N, van Loon JJA (2009) Role of glucosinolates in insect–plant relationships and multitrophic interactions. Annu Rev Entomol 54:57–83

    Article  CAS  PubMed  Google Scholar 

  • Kliebenstein DJ, Lambrix V, Reichelt M, Gershenzon J, Mitchell-Olds T (2001) Gene duplication and the diversification of secondary metabolism: side chain modification of glucosinolates in Arabidopsis thaliana. Plant Cell 13:681–693

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lankau RA (2007) Specialist and generalist herbivores exert opposing selection on a chemical defense. New Phytol 175:176–184

    Article  PubMed  Google Scholar 

  • Lankau RA, Kliebenstein DJ (2009) Competition, herbivory and genetics interact to determine the accumulation and fitness consequences of a defence metabolite. J Ecol 97:78–88

    Article  Google Scholar 

  • Lankau RA, Strauss SY (2008) Community complexity drives patterns of natural selection on a chemical defence of Brassica nigra. Am Nat 171:150–161

    Article  PubMed  Google Scholar 

  • Loader C, Damman H (1991) Nitrogen content of food plants and vulnerability of P. rapae to natural enemies. Ecology 72:1586–1590

    Article  Google Scholar 

  • Müller C, Agerbirk N, Olsen CE (2003) Lack of sequestration of host plant glucosinolates in Pieris rapae and P. brassicae. Chemoecology 13:47–54

    Article  Google Scholar 

  • Newton EL, Bullock JM, Hodgson DJ (2009) Glucosinolate polymorphism in wild cabbage (Brassica oleracea) influences the structure of herbivore communities. Oecologia 160:63–76

    Article  PubMed  Google Scholar 

  • Newton EL, Bullock JM, Hodgson DJ (2010) Temporal consistency in herbivore responses to glucosinolate polymorphism in populations of wild cabbage (Brassica oleracea). Oecologia 164:689–699

    Article  PubMed  Google Scholar 

  • Ode P (2006) Plant chemistry and natural enemy fitness: effect on herbivore and natural enemy interactions. Annu Rev Entomol 51:163–185

    Article  CAS  PubMed  Google Scholar 

  • Poelman EH, Galiart RJFH, Raajimakers CE, van Loon JJA, van Dam N (2008) Performance of specialist and generalist herbivores feeding on cabbage cultivars is not explained by glucosinolate profiles. Entomol Exp Appl 127:218–228

    Article  Google Scholar 

  • Poelman EH, van Dam N, van Loon JJA, Vet LEM, Dicke M (2009) Chemical diversity in Brassica oleracea affects biodiversity of insect herbivores. Ecology 90:1863–1877

    Article  PubMed  Google Scholar 

  • Ratzka A, Vogel H, Kliebenstein DJ, Mitchell-Olds T, Kroymann J (2002) Disarming the mustard oil bomb. Proc Natl Acad Sci USA 99:11223–11228

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rosa E, Heaney R (1996) Seasonal variation in protein, mineral and glucosinolate composition of Portuguese cabbages and kale. Anim Feed Sci Tech 57:111–127

    Article  CAS  Google Scholar 

  • Santolamazza-Carbone S, Velasco P, Soengas P, Cartea ME (2014) Bottom-up and top-down herbivore regulation mediated by glucosinolates in Brassica oleracea var. acephala. Oecologia 174:893–907

    Article  PubMed  Google Scholar 

  • Schramm K, Giggings Vassão D, Reichelt M, Gershenzon J, Wittstock U (2012) Metabolism of glucosinolate-derived isothiocyanates to glutathione conjugates in generalist lepidopteran herbivores. Insect Biochem Mol 42:174–182

    Article  CAS  Google Scholar 

  • Soler R, Bezemer TM, Van der Putten WH, Vet LEM, Harvey JA (2005) Root herbivore effects on above-ground herbivore parasitoid and hyperparasitoid performance changes in plant quality. J Anim Ecol 74:1121–1130

    Article  Google Scholar 

  • Stauber EJ, Kuczka P, van Ohlen M, Vogt B, Janowitz T et al (2012) Turning the ‘mustard oil bomb’ into a ‘cyanide bomb’: aromatic glucosinolate metabolism in a specialist insect herbivore. PLoS ONE 7(4):e35545. doi:10.1371/journal.pone.0035545

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Traw MB, Dawson TE (2002) Reduced performance of two specialist herbivores (Lepidoptera: Pieridae, Coleoptera: Chrysomelidae) on new leaves of damaged black mustard plants. Environ Entomol 31:714–722

    Article  Google Scholar 

  • Velasco P, Cartea ME, González C, Vilar M, Ordás A (2007) Factors affecting the glucosinolate content of kale (Brassica oleracea acephala group). J Agric Food Chem 55:955–962

    Article  CAS  PubMed  Google Scholar 

  • Wentzell AM, Kliebenstein DJ (2008) Genotype, age, tissue, and environment regulate the structural outcome of glucosinolate activation. Plant Physiol 147:415–428

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Research was supported by the National Plan for Research and Development (AGL2012-35539). Authors thank Fatima Nogueira Míguez, Rosaura Abilleira, and César González, for their valuable help during laboratory bioassays. Serena Santolamazza-Carbone acknowledges a post-doctoral research contract (JAE-Doc) from the Consejo Superior de Investigaciones Científicas (CSIC). Tamara Sotelo acknowledges a pre-doctoral grant from the Spanish Ministerio de Economia y Competitividad.

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Authors and Affiliations

  1. Group of Genetics, Breeding and Biochemistry of Brassicas, Misión Biológica de Galicia, Consejo Superior de Investigaciones Científicas (MBG-CSIC), P.O. Box 28, 36080, Pontevedra, Spain

    Serena Santolamazza-Carbone, Tamara Sotelo, Pablo Velasco & María Elena Cartea

Authors
  1. Serena Santolamazza-Carbone
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  2. Tamara Sotelo
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  3. Pablo Velasco
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  4. María Elena Cartea
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Correspondence to Serena Santolamazza-Carbone.

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Communicated by S. T. Jaronski.

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Santolamazza-Carbone, S., Sotelo, T., Velasco, P. et al. Antibiotic properties of the glucosinolates of Brassica oleracea var. acephala similarly affect generalist and specialist larvae of two lepidopteran pests. J Pest Sci 89, 195–206 (2016). https://doi.org/10.1007/s10340-015-0658-y

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  • DOI: https://doi.org/10.1007/s10340-015-0658-y

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