How phloem-feeding insects face the challenge of phloem-located defenses

Abstract

Due to the high content of nutrient, sieve tubes are a primary target for pests, e.g., most phytophagous hemipteran. To protect the integrity of the sieve tubes as well as their content, plants possess diverse chemical and physical defense mechanisms. The latter mechanisms are important because they can potentially interfere with the food source accession of phloem-feeding insects. Physical defense mechanisms are based on callose as well as on proteins and often plug the sieve tube. Insects that feed from sieve tubes are potentially able to overwhelm these defense mechanisms using their saliva. Gel saliva forms a sheath in the apoplast around the stylet and is suggested to seal the stylet penetration site in the cell plasma membrane. In addition, watery saliva is secreted into penetrated cells including sieve elements; the presence of specific enzymes/effectors in this saliva is thought to interfere with plant defense responses. Here we detail several aspects of plant defense and discuss the interaction of plants and phloem-feeding insects. Recent agro-biotechnological phloem-located aphid control strategies are presented.

Keywords: P-proteins; aphid saliva; aphid-plant interactions; phloem; plant defense; sieve element occlusion.

FIGURE 1

Interaction of plants and aphids. (A) Aphids penetrate the plant with their stylet and move it through the apoplast toward the sieve tubes. The stylet contains a salivary (Sc) and nutrition channel (Nc). Before plant penetration and during stylet movement, aphids secrete gel saliva (gray), which forms a salivary sheath (Ss) around the stylet. The Ss remains in the plant’s apoplast after stylet retraction and show empty stylet canals (Esc). After penetrating a sieve tube, aphids secrete watery saliva (light blue) prior to ingestion. Both saliva types are produced in the salivary glands (Sg). Proteases (violet dots) located in the stomach (S) are assumed to digest phloem-sap proteins. (B) The sieve tube penetration of the stylet without secretion of any saliva type would activate mechano-sensitive Ca²⁺ channels (dark green ovals) in the plasma membrane of sieve elements (SE). The consequence is a Ca²⁺ influx (dark green dots) from the apoplast and potentially from the endoplasmaic reticulum (ER) into the SE lumen. P-proteins (P, red) including the forisome and callose produced from the callose synthase (CalS; inset shows a higher magnification) lead to Ca²⁺ dependent sieve-element occlusion. (C) The secretion of gel and watery saliva most likely leads to an absence of wound-induced reaction of SEOs by Ca²⁺-binding. Beside Ca²⁺-binding, aphids are able to suppress further plant defense responses due to salivary effectors (red triangles). Furthermore, plant defense responses are induced in parenchyma cells (PCs), among others, by producing cell wall degradation products that act as pathogen-induced molecular patterns (red circles). Saliva proteins may act as pathogen-associated molecular patterns (red squares). E, epidermis; C, cortex; CC, companion cell; CF, condensed forisome; Cp, cell penetration; CW, cell wall; DF, dispersed forisome; Hg, hint gut; SP, sieve plate.