Interplant communication revisited

Ecology, Dec, 1995 by Irene Shonle, Joy Bergelson

Originally proposed as pheromonal sensitivity in red alders and willows (Rhoades 1983), and further corroborated in a study using poplars and maples (Baldwin and Schultz 1983), the idea that plants might warn each other about an imminent attack was quite exciting because of the clear advantage that forewarning would mean for plants. It would remove the window of vulnerability that plants would otherwise suffer due to the lag in induced response. The excitement was, however, short-lived. Since the persuasive criticisms put forth by Fowler and Lawton (1985), only a few papers mention plant communication (but see Karban and Meyers 1989, Chessin and Zipf 1990) or have attempted to test it (but see Haukioja et al. 1985, Zeringue 1987, Parsons et al. 1989). As neither mechanisms nor messengers were known at the time, interest in "talking trees" faded (J. Lawton, personal communication).

Recently, however, molecular biologists have revealed a signal that might mediate interplant communication. In 1990, Farmer and Ryan showed that methyl jasmonate (MJ) is a volatile chemical messenger that diffuses through the air from wounded plants, is potent in very small quantities, and starts a general signal cascade for increased production of defense chemicals in a wide range of plant families. The plant defenses include proteinase inhibitor proteins (which limit the ability of insects to digest plant proteins, Green and Ryan 1972), phenolics, alkaloids, and glucosinolates. This intriguing finding that MJ might mediate inter-plant communication fills a gap that ecologists faced when originally interpreting the results of experimental manipulations. In light of this new evidence, we believe that the phenomenon of interplant communication warrants further ecological characterization and testing.

The Jasmonates

Molecular and chemical work shows that the jasmonates are lipid-derived molecules, which are synthesized from alpha-linoleic acid by a lipoxygenase-mediated oxygenation (Staswick 1992). MJ and/or jasmonic acid (JA) occur in plant tissues in quantities of 10 ng-3 [[micro]gram]/g fresh mass (Staswick 1992), and are considered to be intercellular signal molecules in the systemic resistance of plants against herbivory. The signal cascade begins when insect damage activates membrane-associated lipases causing linoleic acid to be released and converted to JA. JA then moves through the phloem and induces defense genes throughout the plant, either directly or through induction of the signal molecule systemin (Enyedi et al. 1992, Baldwin et al. 1994). Some JA is also converted to MJ, which is volatile at room temperature, potentially allowing it to affect both remote parts of the releaser plant as well as nearby plants. In addition, MJ appears to affect its own (and JA's) biosynthesis autocatalytically. Airborne jasmonate molecules are thought to enter the plant either through the stomata or by diffusing into the leaf cell cytoplasm (Farmer and Ryan 1990).

Perhaps the most intriguing aspect of methyl jasmonate is that it elicits a response in very low quantities with concentrations as low as 10 nL (Farmer and Ryan 1990, Aerts et al. 1994). This is much more potent than the well known gaseous phytohormone, ethylene (Falkenstein et al. 1991), raising the possibility that sufficient quantities could diffuse to relatively distant neighbors. It may be found that MJ is yet more potent, because the more biologically active of the four possible stereoisomers, (-)jasmonate, readily interconverts to the less active ( )jasmonate in commercial preparations. As commercial preparations are generally used in experiments, the effective jasmonate concentrations may often be overestimated (Staswick 1992).

Jasmonates Affect a Wide Range of Plant Secondary Compounds

What has methyl jasmonate actually been shown to do? Farmer and Ryan (1990) incubated tomato plants with MJ or with conspecifics that had previously been sprayed with MJ, and found that proteinase inhibitor genes were induced. This interesting discovery has since been found to apply to a much wider range of plant defenses. Indeed, JA/MJ apparently acts as an integral part of the signal transduction system regulating most defense genes in plants. For example, Gundlach et al. (1992) found that MJ induced the production of six unique secondary compounds in cell suspension cultures of six plant species from different families. The increases were impressive; metabolite levels were 9-30 fold higher than controls. Gundlach and coworkers also applied MJ to 36 additional cell suspension cultures in which the secondary compound was less well defined, and all responded with the accumulation of low molecular mass compounds. While extrapolating results from cell suspension culture studies to real-world plants requires caution, results have been mirrored with intact plant studies. In addition to species studied in the original Farmer and Ryan study, Aerts et al. (1994) found that atmospheric MJ increased alkaloid production in the pharmaceutically important plants, Cinchona and Catharanthus.