Abstract

Aphids are economically important pest insects that damage plants by phloem feeding and the transmission of plant viruses. Their ability to feed exclusively on nutritionally poor phloem sap is dependent on the obligatory symbiotic bacterium Buchnera aphidicola, but additional facultative symbionts may also be present, a common example of which is Serratia symbiotica. Many Serratia species secrete extracellular enzymes, so we hypothesised that S. symbiotica may produce proteases that help aphids to feed on plants. Molecular analysis, including fluorescence in situ hybridization (FISH), revealed that S. symbiotica colonises the gut, salivary glands and mouthparts (including the stylet) of the pea aphid Acyrthosiphon pisum, providing a mechanism to transfer the symbiont into host plants. S. symbiotica was also detected in plant tissues wounded by the penetrating stylet and was transferred to naïve aphids feeding on plants containing this symbiont. The maintenance of S. symbiotica by repeated transmission via plants may explain the high frequency of this symbiont in aphid populations. Proteomic analysis of the supernatant from a related but cultivable S. symbiotica strain cultured in liquid medium revealed the presence of known and novel proteases including metalloproteases. The corresponding transcripts encoding these S. symbiotica enzymes were detected in A. pisum and in plants carrying the symbiont, although the mRNA was much more abundant in the aphids. Our data suggest that enzymes from S. symbiotica may facilitate the digestion of plant proteins, thereby helping to suppress plant defense, and that the symbionts are important mediators of aphid–plant interactions.

Highlights

  • Aphids are major crop pests, causing both direct feeding damage and the transmission of important plant viruses (Van Emden and Harrington, 2017)

  • The same PCR showed that S. symbiotica was present in V. faba plants infested with Serratia-positive aphids, whereas no symbionts were detected in the plants exposed to the Serratia-free aphid line (Figure 1)

  • We were unable to determine whether S. symbiotica was present in one or both canals, but in either case our results indicated its route into aphids with the phloem sap or outward with the saliva

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Summary

Introduction

Aphids are major crop pests, causing both direct feeding damage and the transmission of important plant viruses (Van Emden and Harrington, 2017). The pea aphid (Acyrthosiphon pisum Harris) is a model for the analysis of symbiosis, and its genome sequence was the first to be published among hemipteran insects (Consortium, 2010; Oliver et al, 2014). Facultative symbionts are found in multiple aphid tissues (including the haemolymph, gut, and reproductive system), and are sometimes co-localised with B. aphidicola within specialised structures known as bacteriomes (Moran et al, 2005; Skaljac et al, 2018). The complex horizontal transmission routes include shared plants and parasitoids, resulting in the acquisition of novel ecological traits by the host (Russell et al, 2003; Chiel et al, 2009; CaspiFluger et al, 2012; Gehrer and Vorburger, 2012; Gonella et al, 2015; Chrostek et al, 2017)

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