Advertisement

Evolutionary Ecology

, Volume 31, Issue 3, pp 305–316 | Cite as

Clonal integration and heavy-metal stress: responses of plants with contrasting evolutionary backgrounds

  • Michal Gruntman
  • Clarissa Anders
  • Anubhav Mohiley
  • Tanja Laaser
  • Stephan Clemens
  • Stephan Höreth
  • Katja Tielbörger
Original Paper

Abstract

Physiological integration between ramets can ameliorate the growth and survival of clonal plants in spatially-heterogeneous environments, as ramets from favourable patches can provide support to those found in stressful patches. However, the advantage conferred by clonal integration might also depend on the evolutionary history of plants with regards to the presented stress. Here, we compared the benefit of clonal integration in response to the distribution of a heavy metal as a stress factor, and asked if this benefit would differ between ecotypes that have either undergone selection to tolerate heavy metals or not. In a greenhouse experiment, we grew pairs of connected and severed ramets of the metal hyperaccumulator Arabidopsis halleri, which originated from populations of either metalliferous or non-metalliferous soils. The ramets were grown in paired pots, which were contaminated with cadmium (Cd) either heterogeneously (100 or 0 ppm Cd per pot) or homogenously (50 ppm Cd per each pot). A. halleri ecotypes that originated from non-metalliferous soils performed better when ramets were connected and the distribution of Cd was heterogeneous. However, clonal integration had no effect on the performance of genotypes from metalliferous soils, regardless of the distribution of Cd. These results support the hypothesis that clonal integration is beneficial in stressful environments as long as the stress is patchily distributed, and particularly for plants that did not undergo selection to withstand it.

Keywords

Arabidopsis halleri Clonal integration Heavy metal tolerance Metal hyperaccumulation Local adaptation 

Notes

Acknowledgments

We are grateful to Ute Krämer and Ricardo Stein for providing information on A. halleri populations, and to Mira Hoch, Bettina Springer and Anne Rysavy for the collection of A. halleri and soil in the field, the preparation of contaminated soil, and propagation of A. halleri in the greenhouse. We also wish to thank Peter Kühn and Sabine Flaiz from the Physical Geography Department at Tübingen University for the Zn and Cd soil-content analyses, and Jitka Klimešova and two anonymous reviewers for helpful suggestions on the manuscript. This study was supported by the SPP 1529 priority program “Adaptomics” grant of the German Research Foundation (DFG) to KT and MG (TI 338/10-2) and to SC (CL 152/9-2).

References

  1. Alpert P (1990) Water sharing among ramets in a desert population of Distichlis spicata (Poaceae). Am J Bot 77:1648–1651CrossRefGoogle Scholar
  2. Alpert P (1991) Nitrogen sharing among ramets increases clonal growth in Fragaria chiloensis. Ecology 72:69–80CrossRefGoogle Scholar
  3. Alpert P (1999) Clonal integration in Fragaria chiloensis differs between populations: ramets from grassland are selfish. Oecologia 120:69–76CrossRefPubMedGoogle Scholar
  4. Alpert P, Mooney H (1986) Resource sharing among ramets in the clonal herb, Fragaria chiloensis. Oecologia 70:227–233CrossRefPubMedGoogle Scholar
  5. Armas C, Ordiales R, Pugnaire FI (2004) Measuring plant interactions: a new comparative index. Ecology 85:2682–2686CrossRefGoogle Scholar
  6. Baker AJ (1981) Accumulators and excluders-strategies in the response of plants to heavy metals. J Plant Nutr 3:643–654CrossRefGoogle Scholar
  7. Baker A (1987) Metal tolerance. New Phytol 106:93–111CrossRefGoogle Scholar
  8. Bert V, Macnair M, De Laguerie P et al (2000) Zinc tolerance and accumulation in metallicolous and nonmetallicolous populations of Arabidopsis halleri (Brassicaceae). New Phytol 146:225–233CrossRefGoogle Scholar
  9. Bert V, Bonnin I, Saumitou-Laprade P et al (2002) Do Arabidopsis halleri from nonmetallicolous populations accumulate zinc and cadmium more effectively than those from metallicolous populations? New Phytol 155:47–57CrossRefGoogle Scholar
  10. Brady KU, Kruckeberg AR, Bradshaw Jr H (2005) Evolutionary ecology of plant adaptation to serpentine soils. Annu Rev Ecol Evol Syst 36:243–266CrossRefGoogle Scholar
  11. Caraco T, Kelly CK (1991) On the adaptive value of physiological integraton in clonal plants. Ecology 72:81–93CrossRefGoogle Scholar
  12. Chen J-S, Lei N-F, Yu D et al (2006) Differential effects of clonal integration on performance in the stoloniferous herb Duchesnea indica, as growing at two sites with different altitude. Plant Ecol 183:147–156CrossRefGoogle Scholar
  13. de Kroon H, Hutchings MJ (1995) Morphological plasticity in clonal plants—the foraging concept reconsidered. J Ecol 83:143–152CrossRefGoogle Scholar
  14. Ernst W, Schat H, Verkleij J (1990) Evolutionary biology of metal resistance in Silene vulgaris. Evolut Trends Plants 4:45–51Google Scholar
  15. Gardner SN, Mangel M (1999) Modeling investments in seeds, clonal offspring, and translocation in a clonal plant. Ecology 80:1202–1220CrossRefGoogle Scholar
  16. Hartnett D, Bazzaz F (1983) Physiological integration among intraclonal ramets in Solidago canadensis. Ecology 64:779–788CrossRefGoogle Scholar
  17. Hutchings M (1999) Clonal plants as cooperative systems: benefits in heterogeneous environments. Plant Species Biol 14:1–10CrossRefGoogle Scholar
  18. Hutchings MJ, Wijesinghe DK (1997) Patchy habitats, division of labour and growth dividends in clonal plants. Trends Ecol Evol 12:390–394CrossRefPubMedGoogle Scholar
  19. Jónsdóttir IS, Callaghan TV (1989) Localized defoliation stress and the movement of 14 C between tillers of Carex bigelowii. Oikos 54:211–219CrossRefGoogle Scholar
  20. Kazakou E, Dimitrakopoulos P, Baker A et al (2008) Hypotheses, mechanisms and trade-offs of tolerance and adaptation to serpentine soils: from species to ecosystem level. Biol Rev 83:495–508PubMedGoogle Scholar
  21. Kazemi-Dinan A, Thomaschky S, Stein RJ et al (2014) Zinc and cadmium hyperaccumulation act as deterrents towards specialist herbivores and impede the performance of a generalist herbivore. New Phytol 202:628–639CrossRefPubMedGoogle Scholar
  22. Kemball W, Marshall C (1995) Clonal integration between parent and branch stolons in white clover: a developmental study. New Phytol 129:513–521CrossRefGoogle Scholar
  23. Koivunen S, Saikkonen K, Vuorisalo T et al (2004) Heavy metals modify costs of reproduction and clonal growth in the stoloniferous herb Potentilla anserina. Evol Ecol 18:541–561CrossRefGoogle Scholar
  24. Krämer U (2010) Metal hyperaccumulation in plants. Annu Rev Plant Biol 61:517–534CrossRefPubMedGoogle Scholar
  25. Macnair M (1981) Tolerance of higher plants to toxic materials. In: Bishops J, Cook L (eds) Genetic consequences of man made change. Academic Press, London, pp 177–208Google Scholar
  26. Maestri E, Marmiroli M, Visioli G et al (2010) Metal tolerance and hyperaccumulation: costs and trade-offs between traits and environment. Environ Exp Bot 68:1–13CrossRefGoogle Scholar
  27. Nilsson J, D’Hertefeldt T (2007) Origin matters for level of resource sharing in the clonal herb Aegopodium podagraria. Evol Ecol 22:437–448CrossRefGoogle Scholar
  28. Outridge P, Hutchinson T (1991) Induction of cadmium tolerance by acclimation transferred between ramets of the clonal fern Salvinia minima Baker. New Phytol 117:597–605CrossRefGoogle Scholar
  29. Pauwels M, Frérot H, Bonnin I et al (2006) A broad-scale analysis of population differentiation for Zn tolerance in an emerging model species for tolerance study: Arabidopsis halleri (Brassicaceae). J Evol Biol 19:1838–1850CrossRefPubMedGoogle Scholar
  30. Pennings SC, Callaway RM (2000) The advantages of clonal integration under different ecological conditions: a community-wide test. Ecology 81:709–716CrossRefGoogle Scholar
  31. Price EAC, Hutchings MJ, Marshall C (1996) Causes and consequences of sectoriality in the clonal herb Glechoma hederacea. Vegetatio 127:41–54CrossRefGoogle Scholar
  32. Roiloa SR, Retuerto R (2006) Physiological integration ameliorates effects of serpentine soils in the clonal herb Fragaria vesca. Physiol Plant 128:662–676CrossRefGoogle Scholar
  33. Roiloa SR, Retuerto R (2012) Clonal integration in Fragaria vesca growing in metal-polluted soils: parents face penalties for establishing their offspring in unsuitable environments. Ecol Res 27:95–106CrossRefGoogle Scholar
  34. Roiloa SR, Alpert P, Tharayil N et al (2007) Greater capacity for division of labour in clones of Fragaria chiloensis from patchier habitats. J Ecol 95:397–405CrossRefGoogle Scholar
  35. Saitoh T, Seiwa K, Nishiwaki A (2002) Importance of physiological integration of dwarf bamboo to persistence in forest understorey: a field experiment. J Ecol 90:78–85CrossRefGoogle Scholar
  36. Salzman AG, Parker MA (1985) Neighbors ameliorate local salinity stress for a rhizomatous plant in a heterogeneous environment. Oecologia 65:273–277CrossRefPubMedGoogle Scholar
  37. Slade A, Hutchings M (1987) An analysis of the costs and benefits of physiological integration between ramets in the clonal perennial herb Glechoma hederacea. Oecologia 73:425–431CrossRefPubMedGoogle Scholar
  38. Stuefer JF, During HJ, de Kroon H (1994) High benefits of clonal integration in two stoloniferous species, in response to heterogeneous light environments. J Ecol 82:511–518CrossRefGoogle Scholar
  39. Stuefer J, De Kroon H, During H (1996) Exploitation of environmental hetergeneity by spatial division of labor in a clonal plant. Funct Ecol 10:328–334CrossRefGoogle Scholar
  40. Sutherland WJ, Stillman RA (1988) The foraging tactics of plants. Oikos 52:239–244CrossRefGoogle Scholar
  41. Van Kleunen M, Fischer M, Schmid B (2000) Clonal integration in Ranunculus reptans: by-product or adaptation? J Evol Biol 13:237–248CrossRefGoogle Scholar
  42. Van Rossum F, Bonnin I, Stéphane F et al (2004) Spatial genetic structure within a metallicolous population of Arabidopsis halleri, a clonal, self-incompatible and heavy-metal-tolerant species. Mol Ecol 13:2959–2967CrossRefPubMedGoogle Scholar
  43. Wijesinghe DK, Handel SN (1994) Advantages of clonal growth in heterogeneous habitats: an experiment with Potentilla simplex. J Ecol 82:495–502CrossRefGoogle Scholar
  44. Zhao F, Jiang R, Dunham S et al (2006) Cadmium uptake, translocation and tolerance in the hyperaccumulator Arabidopsis halleri. New Phytol 172:646–654CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Michal Gruntman
    • 1
  • Clarissa Anders
    • 1
  • Anubhav Mohiley
    • 1
  • Tanja Laaser
    • 1
  • Stephan Clemens
    • 2
  • Stephan Höreth
    • 2
  • Katja Tielbörger
    • 1
  1. 1.Plant Ecology Group, Institute of Evolution and EcologyUniversity of TübingenTübingenGermany
  2. 2.Department of Plant PhysiologyUniversity of BayreuthBayreuthGermany

Personalised recommendations