Avoiding Effective Defenses: Strategies Employed by Phloem-Feeding Insects

Abstract

Phytophages breach the integrity of plant tissues to recover nutrients from foliage, seeds, pollen, nectar, roots, or shoots. While many herbivores cause extensive damage, phloem-feeding insects, such as aphids and whiteflies, cause modest to barely perceptible damage, respectively. Phloem-feeding insects provide additional challenges to plants as they deplete photosynthates, vector viruses, and introduce chemical and/or protein effectors that alter plant defense signaling, infestation symptoms, and plant development (Kaloshian and Walling, 2005). When these attributes are combined with broad host ranges, breeding strategies that promote invasiveness, highly evolved feeding strategies, the ability to adapt to a wide range of plant habitats, and the emergence of insecticide-resistant strains, it is not surprising that phloem-feeding insects cause heavy losses in agriculture and horticulture (Goggin, 2007). With the tools of cell and molecular biology, genetics, genomics, electrophysiology, and biochemistry, investigators are providing novel insights into the complexity and dynamics of plant-herbivore interactions. Many of the reviews in this issue describe the initial events in perception, as well as the defense signals and biochemical reprogramming that influence direct (antibiotic and antixenotic) and indirect (interactions with natural enemies) defenses to tissue-damaging herbivores. This review will highlight intricacies of plant-/phloem-feeding insect interactions, with a primary focus on whiteflies and comparisons to aphids. Hemipteran development and SLWF-plant interactions. A, SLWF adult with arcs of eggs deposited on the abaxial side of an Arabidopsis ecotype Columbia leaf. Scale bar = 1 mm. B, Silverleaf symptoms on squash caused by a severe infestation in Riverside, CA. C, SLWF eggs and first, second, third, and early fourth instar nymphs on Arabidopsis leaves after 23 d of infestation. Scale bar = 0.7 mm. D, SLWF red-eye nymphs (late fourth instar) on Arabidopsis leaves after 28 d of SLWF infestation. Scale bar = 0.5 mm. E, Bluegreen aphid female giving birth to a nymph (John Klinger, University of Arizona). Scale bar = 1 mm. Aphids and whiteflies take advantage of their adept feeding strategies and avoid or deter many plant defenses. These insects disguise themselves and deceive their hosts and natural enemies by using their stylets to deliver salivary chemicals and/or proteins into the plant to influence wound healing, defense-signaling pathways, and volatile emissions. Similar deceptive strategies are routinely employed by phytopathogenic microbes to avoid recognition and combat plant defenses (da Cunha et al., 2007). Pathogens introduce effectors into plant cells manipulating many biochemical and cellular processes to enhance phytopathogen success on host plants. In plant-biotroph interactions, effectors influence three stages of interaction (pre-entry, entry, and colonization). These interaction stages will form the framework for discussing adaptations and evasive strategies employed by phloem-feeding insects. The plant selection mechanisms used by phloem-feeding insects vary. Whiteflies use color, while aphids use both visual and olfactory cues to direct flight responses to host plants (Gerling, 1990; Powell et al., 2006). Upon landing, adults evaluate the tactile and chemical cues of the plant surface to determine the suitability of a plant as shelter or as a feeding and/or oviposition host. For insects that have sessile instars, like whiteflies, the plant chosen for egg deposition is a crucial maternal decision. On a good host, the next generation will thrive; on a poor host, insect populations will decline. While on the leaf surface, insects are exposed to chemicals that are imbedded in the hydrophobic cuticular waxes, including nonvolatile secondary metabolites, as well as volatile and semivolatile compounds (i.e. monoterpenes and glucosinolate-derived volatiles), which serve to attract or repel insects (Müller and Riederer, 2005). Leaf trichomes contribute to this complex environment by exuding secondary metabolites and proteins that have antibiotic or antixenotic effects (Wagner et al., 2004). Glandular trichome exudates deter whitefly settling and entrap whiteflies, providing one of the most effective whitefly-resistance mechanisms known to date. Surprisingly, whiteflies prefer plants with nonglandular trichomes over glabrous plants and preferentially oviposit near trichome bases (Neal and Bentz, 1999). These trichomes provide shelter for the sessile nymphs, and trichome exudates deter natural enemies. Whiteflies are not perturbed by these exudates because whiteflies shed particles of wax from their coat to form a physical barrier to trichome exudates. Interestingly, trichomes also induce a beneficial polyphenism in whiteflies (Guershon and Gerling, 2006). On glabrous leaves, all whitefly nymph cases are flat. On leaves with trichomes, most of the fourth-instar cases are decorated w