Oxylipins and Plant Palatability

Oxylipins are a large family of oxygenated fatty acids that play important roles in plant development and responses to physical damage caused by herbivores, insects, and attack by pathogenic microorganisms (Howe and Jander, 2008; Wu and Baldwin, 2010). Pathogen attack activates lipases that release unsaturated fatty acids, initiating the synthesis of oxylipins. One of the more widely known oxylipins is jasmonic acid, a signaling molecule aiding plant survival in response to insect and pathogen challenges (Browse, 2009). A critical step in oxylipin synthesis is the formation of fatty acid hydroperoxides, a reaction catalyzed by lipoxygenase (LOX) enzymes.

Arabidopsis thaliana has six LOX genes, four of which encode 13-LOX enzymes (numbered for the carbon at which oxygen is introduced). 13-LOXs catalyze the first step in the synthesis of oxylipins such as jasmonic acid. The other two LOX genes, LOX1 and LOX5, encode 9-LOX enzymes that have roles in plant development and defense.

Here, Nalam et al. (pages 1643–1653) show that feeding by the green peach aphid (GPA) (see figure, left panel) on Arabidopsis shoots stimulates expression of LOX5 in roots within 3 h. Infestation of shoots with GPAs resulted in increased levels of LOX5-synthesized 9-hydroperoxy- and 9-hydroxy-fatty acids (9-HPs). In lox5 mutant plants, the increase in 9-HPs was significantly less, associated with a decrease in the GPA population size.

Feeding on Arabidopsis shoots by the GPA (left) induces LOX5 expression in roots (right). This produces LOX5-derived oxylipins, such as 9-HP, which then move to the shoots and facilitate xylem phase feeding (XP), sieve element phase feeding (SEP), and insect survival. Bar = 2 mm. (Left panel courtesy of Vijay Singh; right panel reprinted from Nalam et al. [2012].)

Whereas petiole exudates of intact wild-type plants contain an activity that limits GPA population size, petiole exudates from GPA-infested plants increased the insect population size on an artificial diet. These latter exudates were enriched in oxylipins synthesized by LOX5. These results suggest that GPA feeding alters the host plant to make its vascular sap more palatable to insects. In agreement, petiole exudates from GPA-infested lox5 mutant plants were less effective at stimulating this increase in population.

To determine how the LOX5 genotype in roots affects aphid performance on the shoots, the authors produced reciprocal micrografts using LOX5 versus lox5 as the rootstock or scion, with LOX5/LOX5 and lox5/lox5 self-grafts as controls. Presence of the lox5 rootstock significantly limited the GPA population. By contrast, in plants with a LOX5 rootstock, GPA populations were significantly higher, demonstrating that root expression of LOX5 facilitates GPA colonization of shoots. The authors conclude that LOX5 is required for the infestation-induced changes in the vascular sap that make it more palatable to GPAs.

The authors also used electrical penetration graph analysis to monitor GPA feeding behavior on Arabidopsis plants. Using individual electrically wired insects, they were able to monitor feeding behavior on wild-type versus lox5 mutant plants. Relative to wild-type plants, GPAs on lox5 mutants spent less time consuming sap from the xylem and sieve elements.

The authors present the following model (see figure, right panel) showing how LOX5-synthesized oxylipins derived from the root act as susceptibility factors in GPA infestation. In response to GPA infestation, a plant- and/or insect-derived signal from the shoots travels to the roots and stimulates LOX5 expression and subsequent synthesis of 9-HPs by LOX5. These 9-HPs travel to the shoot, where they facilitate insect feeding, water consumption, and fecundity. The authors also suggest the possibility that these root-derived oxylipins may counteract or diminish a host defense against GPAs. As work like this helps us to learn more about the complex interactions between insect herbivores and their hosts, we will be better prepared to develop strategies to control insect pests and produce resistant host plants.