Physiological integration of roots and shoots in plant defense strategies links above- and belowground herbivory

Ecology Letters

Volumn 11, Issue 8, 2008, Pages 841-851

  Kaplan, Ian ^a   Halitschke, Rayko ^b   Kessler, Andre ^b   Rehill, Brian J ^c   Sardanelli, Sandra ^a   Denno, Robert F ^a  

^a Bldg 142   (United States)

^b Department of Obstetrics Gynecology   (United States)

^c UNITED STATES NAVAL ACADEMY   (United States)

Author keywords

Indirect effects; Phytoparasitic nematode; Plant mediated interactions; Resistance; Root herbivory; Sink strength; Stable isotope; Tolerance

Indexed keywords

CARBON; NICOTINE;

ANTIHERBIVORE DEFENSE; HERBIVORY; INSECT; METABOLISM; NEMATODE; PHYSIOLOGY; PLANT-HERBIVORE INTERACTION; RESOURCE ALLOCATION; ROOT SYSTEM; SHOOT; TOBACCO; TOLERANCE;

ANIMAL; ARTICLE; BIOSYNTHESIS; FEEDING BEHAVIOR; GENETICS; METABOLISM; MOTH; NEMATODE; PHYSIOLOGY; PLANT; PLANT ROOT; TOBACCO;

ANIMALS; CARBON; FEEDING BEHAVIOR; MOTHS; NEMATODA; NICOTINE; PLANT ROOTS; PLANT SHOOTS; TOBACCO;

HEXAPODA; NEMATODA; NICOTIANA TABACUM;

EID: 47249109793     PISSN: 1461023X     EISSN: 14610248     Source Type: Journal    
DOI: 10.1111/j.1461-0248.2008.01200.x     Document Type: Article

References (53)

1. Agrawal, A.A. (1999). Induced responses to herbivory in wild radish: effects on several herbivores and plant fitness. Ecology, 80, 1713 1723.
2. Agrawal, A.A. Karban, R. (2000). Specificity of constitutive and induced resistance: pigment glands influence mites and caterpillars on cotton plants. Entomol. Exp. Appl., 96, 39 49.
3. Babst, B.A., Ferrieri, R.A., Gray, D.W., Lerdau, M., Schlyer, D.J., Schueller, M. et al. (2005). Jasmonic acid induces rapid changes in carbon transport and partitioning in Populus. New Phytol., 167, 63 72.
4. Bais, H.P., Park, S.W., Weir, T.L., Callaway, R.M. Vivanco, J.M. (2004). How plants communicate using the underground information superhighway. Trends Plant Sci., 9, 26 32.
5. Baldwin, I.T. (1988). Damage-induced alkaloids in tobacco: pot-bound plants are not inducible. J. Chem. Ecol., 14, 1113 1121.
6. Baldwin, I.T. (1991). Damage-induced alkaloids in wild tobacco. In : Phytochemical Induction by Herbivores (eds Tallamy, D.W. Raupp, M.J.). John Wiley & Sons, New York, pp. 47 69.
7. Barker, K.R. Lucas, G.B. (1984). Nematode parasites of tobacco. In : Plant and Insect Nematodes (ed. Nickle, W.R.). Marcel Dekker, Inc., New York, pp. 213 242.
8. Barker, K.R. Weeks, W.W. (1991). Relationships between soil and levels of Meloidogyne incognita and tobacco yield and quality. J. Nematol., 23, 82 90.
9. Bezemer, T.M. van Dam, N.M. (2005). Linking aboveground and belowground interactions via induced plant defenses. Trends Ecol. Evol., 20, 617 624.
10. Bezemer, T.M., Wagenaar, R., van Dam, N.M. Wäckers, F.L. (2003). Interactions between above- and belowground insect herbivores as mediated by the plant defense system. Oikos, 101, 555 562.
11. Bezemer, T.M., Wagenaar, R., van Dam, N.M., van der Putten, W.H. Wäckers, F.L. (2004). Above- and below-ground terpenoid aldehyde induction in cotton, Gossypium herbaceum, following root and leaf injury. J. Chem. Ecol., 30, 53 67.
12. Brown, V.K. Gange, A.C. (1990). Insect herbivory below-ground. Adv. Ecol. Res., 20, 1 58.
13. Coleman, D.C., Crossley, D.A. Hendrix, P.F. (2004). Fundamentals of Soil Ecology, 2nd edn. Academic Press, New York.
14. van Dam, N.M. Bezemer, T.M. (2006). Chemical communication between roots and shoots: towards an integration of aboveground and belowground induced responses in plants. In : Chemical Ecology: From Gene to Ecosystem (eds Dicke, M. Takken, W.). Springer, The Netherlands, pp. 127 143.
15. van Dam, N.M., Harvey, J.A., Wäckers, F.L., Bezemer, T.M., van der Putten, W.H. Vet, L.E.M. (2003). Interactions between aboveground and belowground induced responses against phytophages. Basic Appl. Ecol., 4, 63 77.
16. van Dam, N.M., Raaijmakers, C.E. van der Putten, W.H. (2005). Root herbivory reduces growth and survival of the shoot feeding specialist Pieris rapae on Brassica nigra. Entomol. Exp. Appl., 115, 161 170.
17. Dawson, R.F. (1941). The localization of the nicotine synthetic mechanism in the tobacco plant. Science, 94, 396 397.
18. Dawson, T.E., Mambelli, S., Plamboeck, A.H., Templer, P.H. Tu, K.P. (2002). Stable isotopes in plant ecology. Ann. Rev. Ecol. System., 33, 507 559.
19. Denno, R.F. Kaplan, I. (2007). Plant-mediated interactions in herbivorous insects: mechanisms, symmetry, and challenging the paradigms of competition past. In : Ecological Communities: Plant Mediation in Indirect Interaction Webs (eds Ohgushi, T., Craig, T.P. Price, P.W.). Cambridge University Press, Cambridge, pp. 19 50.
20. Erb, M., Ton, J., Degenhardt, J. Turlings, T.C.J. (2008). Interactions between arthropod-induced aboveground and belowground defenses in plants. Plant Phys., 146, 867 874.
21. Halitschke, R., Gase, K., Hui, D.Q., Schmidt, D.D. Baldwin, I.T. (2003). Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. VI. Microarray analysis reveals that most herbivore-specific transcriptional changes are mediated by fatty acid-amino acid conjugates. Plant Physiol., 131, 1894 1902.
22. Hanounik, S.B. Osborne, W.W. (1975). Influence of Meloidogyne incognita on the content of amino acids and nicotine in tobacco grown under gnotobiotic conditions. J. Nematol., 7, 332 336.
23. Hanounik, S.B. Osborne, W.W. (1977). The relationship between population density of Meloidogyne incognita and nicotine content of tobacco. Nematologica, 23, 147 152.
24. 14-labeled gossypol. J. Biol. Chem., 237, 2643 2646.
25. Herms, D.A. (2002). Effects of fertilization on insect resistance of woody ornamental plants: reassessing an entrenched paradigm. Environ. Entomol., 31, 923 933.
26. Herms, D.A. Mattson, W.J. (1992). The dilemma of plants: to grow or defend. Quart. Rev. Biol., 67, 283 335.
27. Hibi, N., Higashiguchi, S., Hashimoto, T. Yamada, Y. (1994). Gene expression in tobacco low-nicotine mutants. Plant Cell, 6, 723 735.
28. Huberty, A.F. Denno, R.F. (2004). Plant water stress and its consequences for herbivorous insects: a new synthesis. Ecology, 85, 1383 1398.
29. Hussey, R.S. Barker, K.R. (1973). A comparison of methods of collecting inocula of Meloidogyne spp., including a new technique. Plant Disease Rep., 57, 1025 1028.
30. Johnson, S.N., Birch, A.N.E., Gregory, P.J. Murray, P.J. (2006). The 'mother knows best' principle: should soil insects be included in the preference-performance debate? Ecol. Entomol., 31, 395 401.
31. Kaplan, I. Denno, R.F. (2007). Interspecific interactions in phytophagous insects revisited: a quantitative assessment of competition theory. Ecol. Lett., 10, 977 994.
32. Kaplan, I., Halitschke, R., Kessler, A., Sardanelli, S. Denno, R.F. (2008). Constitutive and induced defenses to herbivory in above- and belowground plant tissues. Ecology, 89, 392 406.
33. Karban, R. Baldwin, I.T. (1997). Induced Responses to Herbivory. University of Chicago Press, Chicago, IL.
34. Keinänen, M., Oldham, N.J. Baldwin, I.T. (2001). Rapid HPLC screening of jasmonate-induced increases in tobacco alkaloids, phenolics, and diterpene glycosides in Nicotiana attenuata. J. Agric. Food Chem., 49, 3553 3558.
35. Krischik, V.A., Goth, R.W. Barbosa, P. (1991). Generalized plant defense: effects on multiple species. Oecologia, 85, 562 571.
36. McCully, M.E. (1999). Roots in soil: unearthing the complexities of roots and their rhizospheres. Ann. Rev. Plant Phys. Plant Mol. Biol., 50, 695 718.
37. Meisner, J., Ishaaya, I., Ascher, K.R.S. Zur, M. (1978). Gossypol inhibits protease and amylase activity of Spodoptera littoralis larvae. Ann. Entomol. Soc. Am., 71, 5 8.
38. Öpik, H. Rolfe, S. (2005). The Physiology of Flowering Plants, 4th edn. Cambridge University Press, New York.
39. Parrott, W.L. (1990). Plant resistance to insects in cotton. Fla. Entomol., 73, 392 396.
40. Preisser, E.L., Gibson, S.E., Adler, L.S. Lewis, E.E. (2007). Underground herbivory and the costs of constitutive defense in tobacco. Acta Oecol., 31, 210 215.
41. van der Putten, W.H., Vet, L.E.M., Harvey, J.A. Wäckers, F.L. (2001). Linking above- and belowground multitrophic interactions of plants, herbivores, pathogens, and their antagonists. Trends Ecol. Evol., 16, 547 554.
42. Rasmann, S. Turlings, T.C.J. (2007). Simultaneous feeding by aboveground and belowground herbivores attenuates plant-mediated attraction of their respective natural enemies. Ecol. Lett., 10, 926 936.
43. Rehill, B.J. Schultz, J.C. (2003). Enhanced invertase activities in the galls of Hormaphis hamamelidis. J. Chem. Ecol., 29, 2703 2720.
44. Roitsch, T. González, M.C. (2004). Function and regulation of plant invertases: sweet sensations. Trends Plant Sci., 9, 606 613.
45. SAS 2001). SAS for Windows, Version 9.1. SAS Institute, Cary, North Carolina, USA.
46. Schenk, H.J. (2006). Root competition: beyond resource depletion. J. Ecol., 94, 725 739.
47. Schwachtje, J., Minchin, P.E.H., Jahnke, S., van Dongen, J.T., Schittko, U. Baldwin, I.T. (2006). SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots. Proc. Natl. Acad. Sci. U S A., 103, 12935 12940.
48. Smith, F.H. (1961). Biosynthesis of gossypol by excised cotton roots. Nature, 192, 888 889.
49. Soler, R., Bezemer, T.M., van der Putten, W.H., Vet, L.E.M. Harvey, J.A. (2005). Root herbivore effects on above-ground herbivore, parasitoid and hyperparasitoid performance via changes in plant quality. J. Anim. Ecol., 74, 1121 1130.
50. Soler, R., Bezemer, T.M., Cortesero, A.M., van der Putten, W.H., Vet, L.E.M. Harvey, J.A. (2007). Impact of foliar herbivory on the development of a root-feeding insect and its parasitoid. Oecologia, 152, 257 264.
51. Steppuhn, A., Gase, K., Krock, B., Halitschke, R. Baldwin, I.T. (2004). Nicotine's defensive function in nature. PLoS Biol., 2, 1074 1080.
52. Turlings, T.C.J. Tumlinson, J.H. (1992). Systemic release of chemical signals by herbivore-injured corn. Proc. Natl. Acad. Sci. USA., 89, 8399 8402.
53. Wink, M. Theile, V. (2002). Alkaloid tolerance in Manduca sexta and phylogenetically related sphingids (Lepidoptera: Sphingidae). Chemoecology, 12, 29 46.