Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush

Abstract The possibility of communication between plants was proposed nearly 20 years ago, although previous demonstrations have suffered from methodological problems and have not been widely accepted. Here we report the first rigorous, experimental evidence demonstrating that undamaged plants respond to cues released by neighbors to induce higher levels of resistance against herbivores in nature. Sagebrush plants that were clipped in the field released a pulse of an epimer of methyl jasmonate that has been shown to be a volatile signal capable of inducing resistance in wild tobacco. Wild tobacco plants with clipped sagebrush neighbors had increased levels of the putative defensive oxidative enzyme, polyphenol oxidase, relative to control tobacco plants with unclipped sagebrush neighbors. Tobacco plants near clipped sagebrush experienced greatly reduced levels of leaf damage by grasshoppers and cutworms during three field seasons compared to unclipped controls. This result was not caused by an altered light regime experienced by tobacco near clipped neighbors. Barriers to soil contact between tobacco and sagebrush did not reduce the difference in leaf damage although barriers that blocked air contact negated the effect.

[1]  M. Stout,et al.  Antinutritive and toxic components of plant defense against insects , 1996 .

[2]  M. J. Mueller,et al.  Quantification of jasmonic acid by capillary gas chromatography-negative chemical ionization-mass spectrometry. , 1994, Analytical biochemistry.

[3]  P. Wells.  An Ecological Investigation of Two Desert Tobaccos , 1959 .

[4]  Ilya Raskin,et al.  Airborne signalling by methyl salicylate in plant pathogen resistance , 1997, Nature.

[5]  J. Schultz,et al.  Rapid Changes in Tree Leaf Chemistry Induced by Damage: Evidence for Communication Between Plants , 1983, Science.

[6]  J. Rodman,et al.  INSECT HERBIVORY AS A MAJOR FACTOR IN THE SHADE DISTRIBUTION OF A NATIVE CRUCIFER (CARDAMINE CORDIFOLIA A. GRAY, BITTERCRESS) , 1996 .

[7]  J. H. Tumlinson,et al.  Herbivore-infested plants selectively attract parasitoids , 1998, Nature.

[8]  E. Farmer,et al.  Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[9]  J. Ward,et al.  Jasmonates: key players in the plant defence. , 1998, Natural product reports.

[10]  C. P. Constabel,et al.  A survey of wound- and methyl jasmonate-induced leaf polyphenol oxidase in crop plants , 1998 .

[11]  Richard Karban,et al.  Induced Responses to Herbivory , 1997 .

[12]  Dennis D. Murphy,et al.  Sun, slope, and butterflies: topographic determinants of habitat quality for Euphydryas editha , 1988 .

[13]  I. Baldwin.  Jasmonate-induced responses are costly but benefit plants under attack in native populations. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[14]  T. Shiraishi,et al.  Involvement of Volatile Substances in Systemic Resistance of Barley Against Erysiphe graminis f. sp. hordei Induced by Pruning of Leaves , 1987 .

[15]  J. Draper,et al.  Jasmonic Acid Accumulation in Tobacco Hypersensitive Response Lesions , 1999 .

[16]  J. Lawton,et al.  Rapidly Induced Defenses and Talking Trees: The Devil's Advocate Position , 1985, The American Naturalist.

[17]  G. Felton,et al.  Impact of oxidized plant phenolics on the nutritional quality of dietar protein to a noctuid herbivore, Spodoptera exigua , 1992 .

[18]  D. F. Rhoades.  Responses of Alder and Willow to Attack by Tent Caterpillars and Webworms: Evidence for Pheromonal Sensitivity of Willows , 1983 .

[19]  I. Baldwin,et al.  Induced responses in Nicotiana attenuata affect behavior and growth of the specialist herbivore Manduca sexta , 2000, Oecologia.

[20]  Texa Biophysics.  Jasmonate is essential for insect defense in Arabidopsis , 1997 .

[21]  J. Quail,et al.  Importance of the Chiral Centers of Jasmonic Acid in the Responses of Plants (Activities and Antagonism between Natural and Synthetic Analogs) , 1997, Plant physiology.

[22]  I. Baldwin,et al.  Quantification, correlations and manipulations of wound-induced changes in jasmonic acid and nicotine in Nicotiana sylvestris , 1997, Planta.

[23]  B. Vick,et al.  Biosynthesis of jasmonic Acid by several plant species. , 1984, Plant physiology.

[24]  E. Farmer,et al.  Fatty acid signaling in Arabidopsis , 1998, Planta.

[25]  M. Dicke,et al.  Ecology of infochemical use by natural enemies in a tritrophic context. , 1992 .