Early interactions during the encounter of plants, aphids and arboviruses

Abstract

Aphids infest many plants and cause damage by depriving them of nutrients and by transmitting many viral diseases. Aphid infestation and arbovirus transmission are controlled by establishment (or not) of a compatible reaction between the insects and the plants. This reaction is the result of defense reactions of the plant and counter-defense reactions of the parasite. Contrarily to plant-bacteria, plant-fungi and plant-herbivorous insects pathosystems, the plant-aphid pathosystem is understudied, although recent advances have begun to uncover some of its details. Especially the very early steps in plant-aphid interactions are hardly known. We here resume the present knowledge of these interactions. We discuss further how an aphid-transmitted plant virus that is transmitted during the first moments of the plant-aphid encounter, might help to study the very early plant aphid interactions.

Keywords: ROS; aphid; arbovirus; calcium; effector; elicitor; immunity; plant; signaling; transmission; virus.

Figure 1. CaMV exploits early plant-aphid interactions for transmission. (A) The CaMV transmissible complex is composed of the virus particle (V) and the viral helper protein P2 (red) that binds to a receptor (mauve) in the common canal (CC) in the stylet tips. AC, alimentary canal; SC, salivary canal. (B) An aphid inserts its stylets into the tissue where they meander in between the cells. During the stylet movement sheath saliva is constantly secreted that polymerizes to form a sheath (magenta). Some cells are punctured by the stylets. In this case, the aphid secrets some watery saliva (yellow) into the cell and then aspires some cytoplasm. The stylets will penetrate further into the tissue until they are inserted into the sieve tubes (not shown), or if the interaction is incompatible, the stylets will be retracted and the aphid either tries to puncture elsewhere on the same plant or it takes off for another plant. Aphid elicitors and/or effectors can be sheath or watery saliva components that are recognized by plant pattern recognition receptors and result in a recognition reaction (light magenta). CaMV forms in infected plant cells transmission bodies (TB, red circles) that contain basically the viral helper protein P2. The mechanical and/or chemical stress provoked by the aphid stylet activity triggers an early plant response (membrane depolarization, calcium and other ion fluxes, elicitor-plant pattern recognition receptor interactions). This early response is “sensed” by the TB, which disintegrates instantly and redistributes its P2 contents onto microtubules (red hatches in touched and penetrated cells). This P2 morph is acquirable by the aphid and allows for efficient transmission. After departure of the vector, the TBs reform (not shown). The TB reaction is detected easily by immunofluorescence microscopy and might be used to screen for aphid elicitors and effectors.