Advertisement

Oecologia

, Volume 178, Issue 2, pp 369–378 | Cite as

Is there a trade-off between glucosinolate-based organic and inorganic defences in a metal hyperaccumulator in the field?

  • Ardeshir Kazemi-Dinan
  • Jan Sauer
  • Ricardo J. Stein
  • Ute Krämer
  • Caroline Müller
Population ecology - Original research

Abstract

Several plant species are able to not only tolerate but also hyperaccumulate heavy metals in their aboveground tissues. Thus, in addition to secondary metabolites acting as organic defences, metal hyperaccumulators possess an elemental defence that can act as protection against antagonists. Whereas several laboratory studies have determined potential relationships or trade-offs between organic and inorganic defences, little is known about whether these traits are interconnected in the field and which factors determine the compositions of organic defences and elements of leaf tissues most. To target these questions, we collected young leaves of Arabidopsis halleri, a Brassicaceae capable of hyperaccumulating Cd and Zn, as well as soil samples in the field from 16 populations. We detected wide variation in the composition of glucosinolates—the characteristic secondary metabolites of this plant family—among plants, with two distinct chemotypes occurring. Distance-based redundancy analyses revealed that variation in glucosinolate composition was determined mainly by population affiliation and to a lesser degree by geographic distance. Likewise, elemental composition of the leaves was mainly influenced by the location at which samples were collected. Therefore, the particular abiotic and biotic conditions and potential genetic relatedness at a particular locality affect the plant tissue chemistry. A slight indication of a trade-off between glucosinolate-based organic and inorganic defences was found, but only in the less abundant chemotype. A large variation in defence composition and potential joint effects of different defences may be highly adaptive ways of protecting against a wide arsenal of biotic antagonists.

Keywords

Metal hyperaccumulation Glucosinolates Trade-off Joint effects 

Notes

Acknowledgments

This work was supported by the grant MU1829/11-1 to CM and metal analysis by the grant KR1967/10-1 to UK as part of the priority program SPP 1529 Adaptomics of the Deutsche Forschungsgemeinschaft (DFG). JS was financed by the grant SA 2228/1 from the DFG.

References

  1. Agerbirk N, Olsen CE, Nielsen JK (2001) Seasonal variation in leaf glucosinolates and insect resistance in two types of Barbarea vulgaris ssp. arcuata. Phytochemistry 58:91–100. doi: 10.1016/S0031-9422(01)00151-0 CrossRefPubMedGoogle Scholar
  2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46. doi: 10.1111/j.1442-9993.2001.01070.pp.x Google Scholar
  3. Anderson MJ (2004) DISTML v.5: a FORTRAN computer program to calculate a distance-based multivariate analysis for a linear model. Department of Statistics, University of Auckland, AucklandGoogle Scholar
  4. 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. doi: 10.1111/j.1469-8137.2012.04302.x CrossRefPubMedGoogle Scholar
  5. Bennett RN, Rosa EAS, Mellon FA, Kroon PA (2006) Ontogenic profiling of glucosinolates, flavonoids, and other secondary metabolites in Eruca sativa (salad rocket), Diplotaxis erucoides (wall rocket), Diplotaxis tenuifolia (wild rocket), and Bunias orientalis (Turkish rocket). J Agr Food Chem 54:4005–4015. doi: 10.1021/jf052756t CrossRefGoogle Scholar
  6. Boyd RS (2004) Ecology of metal hyperaccumulation. New Phytol 162:563–567. doi: 10.1111/j.1469-8137.2004.01079.x CrossRefGoogle Scholar
  7. Boyd R (2007) The defense hypothesis of elemental hyperaccumulation: status, challenges and new directions. Plant Soil 293:153–176. doi: 10.1007/s11104-007-9240-6 CrossRefGoogle Scholar
  8. Boyd RS (2012) Plant defense using toxic inorganic ions: conceptual models of the defensive enhancement and joint effects hypotheses. Plant Sci 195:88–95. doi: 10.1016/j.plantsci.2012.06.012 CrossRefPubMedGoogle Scholar
  9. Boyd RS (2013) Exploring tradeoffs in hyperaccumulator ecology and evolution. New Phytol 199:871–872. doi: 10.1111/nph.12398 CrossRefPubMedGoogle Scholar
  10. Cole R (1996) Abiotic induction of changes to glucosinolate profiles in Brassica species and increased resistance to the specialist aphid Brevicoryne brassicae. Entomol Exp Appl 80:228–230. doi: 10.1007/978-94-009-1720-0_52 CrossRefGoogle Scholar
  11. Coolong TW, Randle WM, Toler HD, Sams CE (2004) Zinc availability in hydroponic culture influences glucosinolate concentrations in Brassica rapa. HortScience 39:84–86Google Scholar
  12. Core Team R (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  13. Dahmani-Muller H, van Oort F, Gelie B, Balabane M (2000) Strategies of heavy metal uptake by three plant species growing near a metal smelter. Environ Pollut 109:231–238. doi: 10.1093/dnares/dsu024 CrossRefPubMedGoogle Scholar
  14. Davis MA, Boyd RS (2000) Dynamics of Ni-based defence and organic defences in the Ni hyperaccumulator, Streptanthus polygaloides (Brassicaceae). New Phytol 146:211–217. doi: 10.1046/j.1469-8137.2000.00632.x CrossRefGoogle Scholar
  15. Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insect-specific plant reactions. Trend Plant Sci 17:250–259. doi: 10.1016/j.tplants.2012.01.003 CrossRefGoogle Scholar
  16. Ernst WHO (1990) Ecological aspects of sulfur metabolism. In: Rennenberg H, Brunold C, de Kok LJ, Stulen I (eds) Sulfur nutrition and sulfur assimilation in higher plants. SPB Academic, The Hague, pp 131–144Google Scholar
  17. Ernst WHO, Krauss GJ, Verkleij JAC, Wesenberg D (2008) Interaction of heavy metals with the sulphur metabolism in angiosperms from an ecological point of view. Plant Cell Environ 31:123–143. doi: 10.1111/j.1365-3040.2007.01746.x PubMedGoogle Scholar
  18. Fahey JW, Zalcmann AT, Talalay P (2001) The chemical diversity and distribution of glucosinolates and isothiocyanates among plants. Phytochemistry 56:5–51. doi: 10.1016/S0031-9422(00)00316-2 CrossRefPubMedGoogle Scholar
  19. Fones HN, Preston GM (2013) Trade-offs between metal hyperaccumulation and induced disease resistance in metal hyperaccumulator plants. Plant Pathol 62:63–71. doi: 10.1111/ppa.12171 CrossRefGoogle Scholar
  20. Fraley C, Raftery AE (1998) How many clusters? Which clustering method? Answers via model-based cluster analysis. Comput J 41:578–588. doi: 10.1093/comjnl/41.8.578 CrossRefGoogle Scholar
  21. Gonzáles-Megías A, Müller C (2010) Root herbivores and detritivores shape the aboveground multitrophic assemblage through plant mediated effects. J Anim Ecol 79:923–931. doi: 10.1111/j.1365-2656.2010.01681.x Google Scholar
  22. Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Ann Rev Plant Biol 57:303–333. doi: 10.1146/annurev.arplant.57.032905.105228 CrossRefGoogle Scholar
  23. Hausdorf B, Hennig C (2003) Biotic element analysis in biogeography. Syst Biol 52:717–723. doi: 10.1080/10635150390235584 CrossRefPubMedGoogle Scholar
  24. Hausdorf B, Hennig C (2010) Species delimitation using dominant and codominant multilocus markers. Syst Biol 59:491–503. doi: 10.1093/sysbio/syq039 CrossRefPubMedGoogle Scholar
  25. Hennig C, Hausdorf B (2012) The prabclus package version 2.2-4. Department of Statistical Science, University College London, London. http://www.cran.r-project.org/web/packages/prabclus/
  26. Herbette S et al (2006) Genome-wide transcriptome profiling of the early cadmium response of Arabidopsis roots and shoots. Biochimie 88:1751–1765. doi: 10.1016/j.biochi.2006.04.018 CrossRefPubMedGoogle Scholar
  27. Hopkins RJ, van Dam NM, van Loon JJA (2009) Role of glucosinolates in insect–plant relationships and multitrophic interactions. Ann Rev Entomol 54:57–83. doi: 10.1146/annurev.ento.54.110807.090623
  28. Jhee EM, Boyd RS, Eubanks MD, Davis MA (2006) Nickel hyperaccumulation by Streptanthus polygaloides protects against the folivore Plutella xylostella (Lepidoptera: Plutellidae). Plant Ecol 183:91–104. doi: 10.1007/s11258-005-9009-z CrossRefGoogle Scholar
  29. Kazemi-Dinan A, Thomaschky S, Stein RJ, Krämer U, Müller C (2014) Zn and Cd hyperaccumulation act as deterrents towards specialist herbivores and impede the performance of a generalist herbivore. New Phytol 202:628–639. doi: 10.1111/nph.12663 CrossRefPubMedGoogle Scholar
  30. Kazemi-Dinan A, Barwinski A, Stein RJ, Krämer U, Müller C (2015) Metal hyperaccumulation mediates defence against herbivores in the field and improved growth. Entomol Exp Appl (in review)Google Scholar
  31. Kleine S, Müller C (2011) Intraspecific plant chemical diversity and its effects on herbivores. Oecologia 166:175–186. doi: 10.1007/s00442-010-1827-6 CrossRefPubMedGoogle Scholar
  32. Koch MA, Matschinger M (2007) Evolution and genetic differentiation among relatives of Arabidopsis thaliana. Proc Natl Acad Sci USA 104:6272–6277. doi: 10.1073/pnas.0701338104 CrossRefPubMedCentralPubMedGoogle Scholar
  33. Kruskal J (1964) Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29:1–27. doi: 10.1007/BF02289565 CrossRefGoogle Scholar
  34. Kusznierewicz B et al (2012) The dose-dependent influence of zinc and cadmium contamination of soil on their uptake and glucosinolate content in white cabbage (Brassica oleracea var. capitata f. alba). Environ Toxicol Chem 31:2482–2489. doi: 10.1002/etc.1977 CrossRefPubMedGoogle Scholar
  35. Legendre P, Anderson MJ (1999) Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecol Monogr 69:1–24. doi: 10.1890/0012-9615(1999)069[0001:dbratm]2.0.co;2CrossRefGoogle Scholar
  36. Llugany M, Martin SR, Barcelo J, Poschenrieder C (2013) Endogenous jasmonic and salicylic acids levels in the Cd-hyperaccumulator Noccaea (Thlaspi) praecox exposed to fungal infection and/or mechanical stress. Plant Cell Rep 32:1243–1249. doi: 10.1007/s00299-013-1427-0 CrossRefPubMedGoogle Scholar
  37. Maksymiec W (2007) Signaling responses in plants to heavy metal stress. Acta Physiol Plant 29:177–187. doi: 10.1007/s11738-007-0036-3 CrossRefGoogle Scholar
  38. Mathys W (1977) Role of malate, oxalate, and mustard oil glucosides in evolution of zinc resistance in herbage plants. Physiol Plant 40:130–136. doi: 10.1111/j.1399-3054.1977.tb01509.x
  39. Metz J, Ribbers K, Tielbörger K, Müller C (2014) Long- and medium-term effects of aridity on the chemical defence of a widespread Brassicaceae in the Mediterranean. Environ Exp Bot 105:39–45. doi: 10.1016/j.envexpbot.2014.04.007 CrossRefGoogle Scholar
  40. Noret N, Meerts P, Vanhaelen M, Dos Santos A, Escarré J (2007) Do metal-rich plants deter herbivores? A field test of the defence hypothesis. Oecologia 152:92–100. doi: 10.1007/s00442-006-0635 CrossRefPubMedGoogle Scholar
  41. Pongrac P, Tolrà R, Vogel-Mikus K, Poschenrieder C, Barceló J, Regvar M (2010) At the crossroads of metal hyperaccumulation and glucosinolates: is there anything out there? In: Sherameti I, Varma A (eds) Soil heavy metals. Springer, Heidelberg, pp 139–162. doi: 10.1007/978-3-642-02436-8_7 CrossRefGoogle Scholar
  42. Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: how and why do they do it? And what makes them so interesting? Plant Sci 180:169–181. doi: 10.1016/j.plantsci.2010.08.016 CrossRefPubMedGoogle Scholar
  43. Reeves RD, Baker AJM (2000) Metal-accumulating plants. In: Raskin I, Ensley BD (eds) Phytoremediation of toxic metals: using plants to clean up the environment. Wiley, New York, pp 193–229Google Scholar
  44. Schoonhoven LM, van Loon JJA, Dicke M (2005) Insect–plant biology, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  45. Strauss SY, Rudgers JA, Lau JA, Irwin RE (2002) Direct and ecological costs of resistance to herbivory. Trends Ecol Evol 17:278–285. doi: 10.1016/S0169-5347(02)02483-7 CrossRefGoogle Scholar
  46. Sun XM et al (2009) Glucosinolate profiles of Arabidopsis thaliana in response to cadmium exposure. Water Air Soil Poll 200:109–117CrossRefGoogle Scholar
  47. Textor S, Gershenzon J (2009) Herbivore induction of the glucosinolate–myrosinase defense system: major trends, biochemical bases and ecological significance. Phytochem Rev 8:149–170. doi: 10.1007/s11101-008-9117-1 CrossRefGoogle Scholar
  48. Tolrà RP, Poschenrieder C, Alonso R, Barceló D, Barceló J (2001) Influence of zinc hyperaccumulation on glucosinolates in Thlaspi caerulescens. New Phytol 151:621–626. doi: 10.1046/j.0028-646x.2001.00221.x CrossRefGoogle Scholar
  49. Tolrà R, Pongrac P, Poschenrieder C, Vogel-Mikus K, Regvar M, Barcelo J (2006) Distinctive effects of cadmium on glucosinolate profiles in Cd hyperaccumulator Thlaspi praecox and non-hyperaccumulator Thlaspi arvense. Plant Soil 288:333–341. doi: 10.1007/s11104-006-9124-1 CrossRefGoogle Scholar
  50. Travers-Martin N, Müller C (2008) Matching plant defense syndromes with performance and preference of a specialist herbivore. Funct Ecol 22:1033–1043. doi: 10.1111/j.1365-2435.2008.01487.x CrossRefGoogle Scholar
  51. van Dam NM, Tytgat TOG, Kirkegaard JA (2009) Root and shoot glucosinolates: a comparison of their diversity, function and interactions in natural and managed ecosystems. Phytochem Rev 8:171–186. doi: 10.1007/s11101-008-9101-9 CrossRefGoogle Scholar
  52. van der Ent A, Baker AJM, Reeves RD, Pollard AJ, Schat H (2013) Hyperaccumulators of metal and metalloid trace elements: facts and fiction. Plant Soil 362:319–334. doi: 10.1007/s11104-012-1287-3 CrossRefGoogle Scholar
  53. van Leur H, Raaijmakers CE, van Dam NM (2006) A heritable glucosinolate polymorphism within natural populations of Barbarea vulgaris. Phytochemistry 67:1214–1223. doi: 10.1016/j.phytochem.2006.04.021 CrossRefPubMedGoogle Scholar
  54. Velasco P, Cartea ME, Gonzalez C, Vilar M, Ordas A (2007) Factors affecting the glucosinolate content of kale (Brassica oleracea acephala group). J Agr Food Chem 55:955–962. doi: 10.1021/jf0624897 CrossRefGoogle Scholar
  55. Wang AS, Angle JS, Chaney RL, Delorme TA, Reeves RD (2006) Soil pH effects on uptake of Cd and Zn by Thlaspi caerulescens. Plant Soil 281:325–337. doi: 10.1007/s11104-005-4642-9 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Ardeshir Kazemi-Dinan
    • 1
  • Jan Sauer
    • 1
  • Ricardo J. Stein
    • 2
  • Ute Krämer
    • 2
  • Caroline Müller
    • 1
  1. 1.Department of Chemical EcologyBielefeld UniversityBielefeldGermany
  2. 2.Department of Plant PhysiologyRuhr University BochumBochumGermany

Personalised recommendations