Oecologia

, Volume 147, Issue 3, pp 461–468 | Cite as

Members only: induced systemic resistance to herbivory in a clonal plant network

Plant Animal Interactions

Abstract

The stoloniferous herb Trifolium repens was used to study the expression of induced systemic resistance (ISR) to the generalist caterpillar Spodoptera exigua in interconnected ramets of clonal fragments. The ISR was assessed as caterpillar preference in dual choice tests between control and systemically induced plants. The ISR was detected in young ramets, after inducing older sibling ramets on the same stolon by a controlled herbivore attack. However, older ramets did not receive a defense induction signal from younger ramets unless the predominant phloem flow was reversed by means of basal shading. This provides evidence for the notion that in T. repens the clone-internal expression of ISR is coupled to phloem transport and follows source–sink gradients. The inducibility of the genotypes was not linked to their constitutive ability to produce cyanide, implying the absence of a trade-off between these two defense traits. To our knowledge, this is the first study that explores ISR to herbivory in the context of physiological integration in potentially extensive clonal plant networks.

Keywords

Inducible defense Plant communication Source–sink transport Spodoptera exigua Trifolium repens 

References

  1. Akhtar Y, Isman MB (2004) Comparative growth inhibitory and antifeedant effects of plant extracts and pure allelochemicals on four phytophagous insect species. J App Ent 128:32–38CrossRefGoogle Scholar
  2. Alpert P (1996) Nutrient sharing in natural clonal fragments of Fragaria chiloensis. J Ecol 84:395–406CrossRefGoogle Scholar
  3. Alpert P, Stuefer JF (1997) Division of labour in clonal plants. In: de Kroon H, van Groenendael J (eds) The ecology and evolution of clonal plants. Backhuys Publishers, The Netherlands, pp 137–154Google Scholar
  4. Arnold T, Appel H, Patel V, Stocum E, Kavalier A, Schultz J (2004) Carbohydrate translocation determines the phenolic content of Populus foliage: a test of the sink–source model of plant defense. New Phytol 164:157–164CrossRefGoogle Scholar
  5. Biere A, Marak HB, van Damme JMM (2004) Plant chemical defense against herbivores and pathogens: generalized defense or trade-offs? Oecologia 140:430–441PubMedCrossRefGoogle Scholar
  6. Chamberlain K, Guerrieri E, Pennacchio F, Pettersson J, Pickett JA, Poppy GM, Powell W, Wadhams LJ, Woodcock CM (2001) Can aphid-induced plant signals be transmitted aerially and through the rhizosphere? Biochem Syst Ecol 29:1063–1074CrossRefGoogle Scholar
  7. Chapman DF, Robson MJ, Snaydon RW (1990) Short-term effects of manipulating the source–sink ratio of White Clover (Trifolium repens) plants on export of carbon from, and morphology of, developing leaves. Phys Plant 80:262–266CrossRefGoogle Scholar
  8. Chapman DF, Robson MJ, Snaydon RW (1992a) Physiological integration in the clonal perennial herb Trifolium repens L. Oecologia 89:338–347Google Scholar
  9. Chapman DF, Robson MJ, Snaydon RW (1992b) The carbon economy of clonal plants of Trifolium repens L. J Exp Bot 43:427–434CrossRefGoogle Scholar
  10. Chen SX, Petersen BL, Olsen CE, Schulz A, Halkier BA (2001) Long-distance phloem transport of glucosinolates in Arabidopsis. Plant Physiol 127:194–201PubMedCrossRefGoogle Scholar
  11. Davis JM, Gordon MP, Smit BA (1991) Assimilate movement dictates remote sites of wound-induced gene-expression in Poplar leaves. Proc Natl Acad Sci USA 88:2393–2396PubMedCrossRefGoogle Scholar
  12. Dicke M, Bruin J (2001) Chemical information transfer between plants: back to the future. Biochem Syst Ecol 29:981–994CrossRefGoogle Scholar
  13. Dirzo R, Harper JL (1982a) Experimental studies on slug–plant interactions. 3. Differences in the acceptability of individual plants of Trifolium repens to slugs and snails. J Ecol 70:101–117CrossRefGoogle Scholar
  14. Dirzo R, Harper JL (1982b) Experimental studies on slug–plant interactions. 4. The performance of cyanogenic and acyanogenic morphs of Trifolium repens in the field. J Ecol 70:119–138CrossRefGoogle Scholar
  15. Dolch R, Tscharntke T (2000) Defoliation of alders (Alnus glutinosa) affects herbivory by leaf beetles on undamaged neighbours. Oecologia 125:504–511CrossRefGoogle Scholar
  16. Fenner M, Hanley ME, Lawrence R (1999) Comparison of seedling and adult palatability in annual and perennial plants. Funct Ecol 13:546–551CrossRefGoogle Scholar
  17. Guerrieri E, Poppy GM, Powell W, Rao R, Pennacchio F (2002) Plant-to-plant communication mediating in-flight orientation of Aphidius ervi. J Chem Ecol 28:1703–1715PubMedCrossRefGoogle Scholar
  18. Hamilton NRS, Hay MJM (1998) Vascular architecture of a large-leafed genotype of Trifolium repens. Ann Bot 81:441–448CrossRefGoogle Scholar
  19. Hayden KJ, Parker IM (2002) Plasticity in cyanogenesis of Trifolium repens L.: inducibility, fitness costs and variable expression. Evol Ecol Res 4:155–168Google Scholar
  20. Herms DA, Mattson WJ (1992) The dilemma of plants—to grow or defend. Q Rev Biol 67:283–335CrossRefGoogle Scholar
  21. Järemo J, Tuomi J, Nilsson P (1999) Adaptive status of localized and systemic defense responses in plants. In: Tollrian R, Harvell D (eds) The ecology and evolution of inducible defenses. Princeton University Press, Princeton, pp 33–44Google Scholar
  22. Jones CG, Hopper RF, Coleman JS, Krischik VA (1993) Control of systemically induced herbivore resistance by plant vascular architecture. Oecologia 93:452–456CrossRefGoogle Scholar
  23. Karban R, Baldwin IT (1997) Induced responses to herbivory. Chicago University Press, ChicagoGoogle Scholar
  24. Karban R, Agrawal AA, Thaler JS, Adler LS (1999) Induced plant responses and information content about risk of herbivory. Trend Ecol 14:443–447CrossRefGoogle Scholar
  25. Kemball WD, Palmer MJ, Marshall C (1992) The effect of local shading and darkening on branch growth, development and survival in Trifolium repens and Galium aparine. Oikos 63:366–375CrossRefGoogle Scholar
  26. Kemball WD, Marshall C (1995) Clonal integration between parent and branch stolons in White Clover—a developmental study. New Phytol 129:513–521CrossRefGoogle Scholar
  27. Kempster VN, Scott ES, Davies KA (2002) Evidence for systemic, cross-resistance in white clover (Trifolium repens) and annual medic (Medicago truncatula var truncatula) induced by biological and chemical agents. Bio Sci Tech 12:615–623CrossRefGoogle Scholar
  28. Lockwood JR (1998) On the statistical analysis of multiple-choice feeding preference experiments. Oecologia 116:475–481CrossRefGoogle Scholar
  29. Lotscher M, Hay MJM (1996) Distribution of mineral nutrient from nodal roots of Trifolium repens: Genotypic variation in intra-plant allocation of P-32 and Ca-45. Physiol Plant 97:269–276CrossRefGoogle Scholar
  30. Marshall C (1990) Source–sink relations of interconnected ramets. In: van Groenendael J, de Kroon H (eds) Clonal growth in plants: regulation and function. SPB Academic Publishing, The Hague, pp 23–41Google Scholar
  31. Marshall C, Price EAC (1997) Sectoriality and its implications for physiological integration. In: de Kroon H, van Groenendael J (eds) The ecology and evolution of clonal plants. Backhuys Publishers, Leiden, pp 79–107Google Scholar
  32. Orians CM, Pomerleau J, Ricco R (2000) Vascular architecture generates fine scale variation in systemic induction of proteinase inhibitors in tomato. J Chem Ecol 26:471–485CrossRefGoogle Scholar
  33. Orians CM (2005) Herbivores, vascular pathways, systemic induction: facts and artifacts. J Chem Ecol 31:2231–2242PubMedCrossRefGoogle Scholar
  34. Pederson GA, Brink GE (1998) Cyanogenesis effect on insect damage to seedling white clover in a bermudagrass sod. Agron J 90:208–210Google Scholar
  35. Pitelka LF, Ashmun JW (1985) Physiology and integration of ramets in clonal plants. In: Jackson JBC (ed) Population biology and evolution of clonal organisms. Yale University Press, New Haven, pp 399–435Google Scholar
  36. Prince JS, LeBlanc WG, Macia S (2004) Design and analysis of multiple choice feeding preference data. Oecologia 138:1–4PubMedCrossRefGoogle Scholar
  37. Puustinen S, Mutikainen P (2001) Host–parasite–herbivore interactions: implications of host cyanogenesis. Ecology 82:2059–2071Google Scholar
  38. Roa R (1992) Design and analysis of multiple-choice feeding-preference experiments. Oecologia 89:509–515Google Scholar
  39. Schittko U, Baldwin IT (2003) Constraints to herbivore-induced systemic responses: bidirectional signaling along orthostichies in Nicotiana attenuata. J Chem Ecol 29:763–770PubMedCrossRefGoogle Scholar
  40. Stuefer JF (1996) Potential and limitations of current concepts regarding the response of clonal plants to environmental heterogeneity. Vegetatio 127:55–70CrossRefGoogle Scholar
  41. Stuefer JF, DeKroon H, During HJ (1996) Exploitation of environmental heterogeneity by spatial division of labour in a clonal plant. Funct Ecol 10:328–334CrossRefGoogle Scholar
  42. Stuefer JF, Gómez S, van Mölken T. (2004) Clonal integration beyond resource sharing: implications for defence signalling and disease transmission in clonal plant networks. Evol Ecol 18:647–667CrossRefGoogle Scholar
  43. Till I (1987) Variability of expression of cyanogenesis in White Clover (Trifolium repens L). Heredity 59:265–271CrossRefGoogle Scholar
  44. Underwood N, Morris W, Gross K, Lockwood JR (2000) Induced resistance to Mexican bean beetles in soybean: variation among genotypes and lack of correlation with constitutive resistance. Oecologia 122:83–89CrossRefGoogle Scholar
  45. Viswanathan DV, Thaler JS (2004) Plant vascular architecture and within-plant spatial patterns in resource quality following herbivory. J Chem Ecol 30:531–543PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Experimental Plant EcologyInstitute for Wetland and Water Research, Radboud University NijmegenNijmegenThe Netherlands

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