Inverse relationship between systemic resistance of plants to microorganisms and to insect herbivory

Abstract

Pre-inoculation of plants with a pathogen that induces necrosis leads to the development of systemic acquired resistance (SAR) to subsequent pathogen attack [1]. The phenylpropanoid-derived compound salicylic acid (SA) is necessary for the full expression of both local resistance and SAR [2] [3]. A separate signaling pathway involving jasmonic acid (JA) is involved in systemic responses to wounding and insect herbivory [4] [5]. There is evidence both supporting and opposing the idea of cross-protection against microbial pathogens and insect herbivores [6] [7]. This is a controversial area because pharmacological experiments point to negative cross-talk between responses to systemic pathogens and responses to wounding [8] [9] [10], although this has not been demonstrated functionally in vivo. Here, we report that reducing phenylpropanoid biosynthesis by silencing the expression of phenylalanine ammonialyase (PAL) reduces SAR to tobacco mosaic virus (TMV), whereas overexpression of PAL enhances SAR. Tobacco plants with reduced SAR exhibited more effective grazing-induced systemic resistance to larvae of Heliothis virescens, but larval resistance was reduced in plants with elevated phenylpropanoid levels. Furthermore, genetic modification of components involved in phenylpropanoid synthesis revealed an inverse relationship between SA and JA levels. These results demonstrate phenylpropanoid-mediated cross-talk in vivo between microbially induced and herbivore-induced pathways of systemic resistance.

Transgene-Mediated and Elicitor-Induced Perturbation of Metabolic Channeling at the Entry Point into the Phenylpropanoid Pathway

“…It is tempting to speculate that salicylic acid is synthesized via an uncoupled form of PAL, for example, nonmicrosomally associated PAL2 in tobacco. However, tobacco PAL1 could be equally involved in salicylic acid biosynthesis, because overexpression of bean PAL, which, like tobacco PAL1, is localized both cytoplasmically and microsomally in transgenic tobacco stem tissue, results in increased salicylic acid production and corresponding increases in disease resistance in intact tobacco plants (Felton et al, 1999).…”

“…It is tempting to speculate that salicylic acid is synthesized via an uncoupled form of PAL, for example, nonmicrosomally associated PAL2 in tobacco. However, tobacco PAL1 could be equally involved in salicylic acid biosynthesis, because overexpression of bean PAL, which, like tobacco PAL1, is localized both cytoplasmically and microsomally in transgenic tobacco stem tissue, results in increased salicylic acid production and corresponding increases in disease resistance in intact tobacco plants (Felton et al, 1999).Our results obtained in experiments with PAL-overexpressing tobacco cell cultures and elicited wild-type cultures do not support the idea that a loss of channeling leads directly to a higher accumulation of salicylic acid produced from unchanneled trans-cinnamic acid, because the levels of salicylic acid are the same as those in wild-type tobacco cells. However, a marked difference can be seen in the accumulation of the vanillin derivative, which is 10 times higher in PAL-overexpressing tobacco cells when compared with wild-type cells, although it is not significantly induced by elicitation.…”

Regulation of tradeoffs between plant defenses against pathogens with different lifestyles

“…Moreover, genetically engineered plants with a silenced phenyl-ammonia-lyase gene have reduced levels of SA, but higher levels of JA, compared with WT. Accordingly, resistance against tobacco mosaic virus was lost, whereas resistance to an herbivorous insect was boosted (32).…”

Signaling in Plant Resistance Responses: Divergence and Cross-Talk of Defense Pathways

“…A similar phenomenon was observed by Preston et al (1999) who demonstrated that TMV-infected tobacco plants induced for SAR display higher sensitivity to tobacco hornworm (Manduca sexta) grazing when compared with noninduced control plants. Furthermore, it has been shown that transgenic tobacco plants with reduced SA levels, caused by silencing of the PAL gene, exhibit reduced SAR against TMV but enhanced herbivore-induced resistance to Heliothis virescens larvae (Felton et al, 1999). In a converse manner, PAL-overexpressing tobacco displays a strong reduction of herbivore-induced insect resistance, while TMVinduced SAR was enhanced in these plants.…”