Breaching the Sieve Element—The Role of Saliva as the Molecular Interface Between Aphids and the Phloem

Abstract

Aphids (order Hemiptera; suborder Sternorrhyncha) are fast becoming an excellent system for studying molecular interactions between sap feeding insects and their host plants. This has been facilitated, in part, by the recent completion of the pea aphid (Acyrthosiphon pisum) genome project (IAGC, 2010) and the development of high throughput genomic resources such as preliminary genomes and large-scale EST libraries for a number of other aphid species. Coupled with a strong tradition as a model system for investigating insect-plant interactions more generally, the recent increase in the number of studies involving aphids has lead to greater insights into the complexity of plant-aphid interactions and has provided a tantalizing preview of the intricate molecular mechanisms that govern this intimate association. Aphids and other sap-feeding hemipterans (e.g., whiteflies) have evolved specialized mouthparts, the stylets, which penetrate through plant tissues to feed directly from a single sieve element within the phloem. The feeding pathway, mechanism of penetration, and insect behavior associated with feeding have been well described (reviewed by Powell et al., 2006), but the role of the copious amounts of saliva that is continuously secreted during feeding remains obscure. Two types of saliva are recognized: a "gelling" saliva that constitutes the salivary sheath that is left in situ following stylet withdrawal from plant tissues, and a "watery" saliva that is secreted intracellularly either when the stylets briefly puncture cells during probing or immediately before and during sap ingestion (Martin et al., 1997). The gelling saliva is thought to provide mechanical support to the delicate stylets and to offer a degree of molecular concealment from plant defenses (Miles, 1999; Tjallingii, 2006; Will et al., 2007), although the assignment of function to the various types of saliva remains speculative, largely because of difficulties with collection and analysis of aphid saliva in general.

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

“…Gel saliva forms a salivary flange on the plant surface prior to plant penetration ( Figure 1A ; Will et al, 2012b), which is suggested to stabilize the stylet before initiating stylet penetration of the plant (Pollard, 1973; Tjallingii, 2006). When the stylet moves, small amounts of gel saliva are secreted; these harden and are then penetrated by the stylet (McLean and Kinsey, 1965).…”

“…When the stylet moves, small amounts of gel saliva are secreted; these harden and are then penetrated by the stylet (McLean and Kinsey, 1965). This continuous secretion of gel saliva leads to the formation of a solid salivary sheath that envelops the stylet and is left in situ after it is withdrawn from plant tissues (Will et al, 2012b). Sheath formation was assumed to be associated with the oxidation of protein sulphydryl groups, e.g., present in the amino acid cysteine (Miles, 1965; Tjallingii, 2006).…”

“…Potential candidates for PIMP production are cell-wall-degrading enzymes, such as cellulase and pectinase, which were detected in aphid saliva (Ma et al, 1990; Cherqui and Tjallingii, 2000). Whether the protein or peptide components of gel saliva act in a similar manner to, e.g., flg22 from bacteria (Zipfel, 2008) as pathogen-associated molecular patterns (PAMPs; Figure 1C ) that trigger plant defense responses in a gene-to-gene interaction can be speculated (Will et al, 2012b). It may be that aphid gel saliva on one hand induces plant defense in cortex cells along the stylet track and on the other hand suppresses defense inside penetrated sieve tubes ( Figure 1C ; Will and van Bel, 2008; Louis et al, 2012).…”

Profiling Diuraphis noxia (Hemiptera: Aphididae) Transcript Expression of the Biotypes SA1 and SAM Feeding on Various Triticum aestivum Varieties

“…The intimate relationship between an aphid and its host is mediated by the secretion of abundant amounts of saliva during all the stages of feeding, including probing and ingestion (Will et al 2013). Two types of saliva are secreted during feeding, the "sheath saliva"-once secreted, although initially in liquid form, hardens around the stylet to form a path in the plant cells and remains in the plant; and the second form that remains as a liquid to facilitate feeding-known as "watery saliva."…”

Pea Aphid (Acyrthosiphon pisum) Host Races Reduce Heat-Induced Forisome Dispersion in Vicia faba and Trifolium pratense

“…Aphids typically cause little damage to plant tissue because they use their stylets to navigate in between plant cells [18][19][20]. During this process, aphids inject saliva into the plant [21,22]. One type of saliva, called gelling saliva, is secreted into the apoplastic space where it gelatinizes, and the aphid subsequently pushes its stylet through the gel so that the gel forms a sheath [23].…”