Molecular sabotage of plant defense by aphid saliva

Abstract

Aphids, which constitute one of the most important groups of agricultural pests, ingest nutrients from sieve tubes, the photoassimilate transport conduits in plants. Aphids are able to successfully puncture sieve tubes with their piercing mouthparts (stylets) and ingest phloem sap without eliciting the sieve tubes' normal occlusion response to injury. Occlusion mechanisms are calciumtriggered and may be prevented by chemical constituents in aphid saliva injected into sieve tubes before and during feeding. We recorded aphid feeding behavior with the electrical penetration graph (EPG) technique and then experimentally induced sieve tube plugging. Initiation of sieve tube occlusion caused a change in aphid behavior from phloem sap ingestion to secretion of watery saliva. Direct proof of ''unplugging'' properties of aphid saliva was provided by the effect of aphid saliva on forisomes. Forisomes are proteinaceous inclusions in sieve tubes of legumes that show calcium-regulated changes in conformation between a contracted state (below calcium threshold) that does not occlude the sieve tubes and a dispersed state (above calcium threshold) that occludes the sieve tubes. We demonstrated in vitro that aphid saliva induces dispersed forisomes to revert back to the nonplugging contracted state. Labeling Western-blotted saliva proteins with 45 Ca 2؉ or ruthenium red inferred the presence of calcium-binding domains. These results demonstrate that aphid saliva has the ability to prevent sieve tube plugging by molecular interactions between salivary proteins and calcium. This provides aphids with access to a continuous flow of phloem sap and is a critical adaptation instrumental in the evolutionary success of aphids.calcium-binding ͉ plant-aphid interaction ͉ plugging ͉ saliva proteins ͉ sieve element

Male-derived butterfly anti-aphrodisiac mediates induced indirect plant defense

“…In cowpea, perception of Spodoptera frugiperda herbivory is mediated by fragments of ATP synthase that induce a targeted defense mechanism (27). Interestingly, herbivore saliva is not only able to elicit plant defense but is also able to suppress it (33)(34)(35). Aphid saliva was demonstrated to contain proteins with calcium-binding properties, which thereby prevent sieve tube occlusion, the normal plant defense response to injury of sieve tubes (34).…”

“…Interestingly, herbivore saliva is not only able to elicit plant defense but is also able to suppress it (33)(34)(35). Aphid saliva was demonstrated to contain proteins with calcium-binding properties, which thereby prevent sieve tube occlusion, the normal plant defense response to injury of sieve tubes (34). Elicitors isolated from plant pathogens and their interactions with the plant surface have been studied more intensively than herbivore-released elicitors.…”

Predicted Effector Molecules in the Salivary Secretome of the Pea Aphid (Acyrthosiphon pisum): A Dual Transcriptomic/Proteomic Approach

“…23 Direct MS analysis of pea aphid salivary proteins identified a candidate calcium-binding protein, regucalcin, 28 which we have not identified in our analyses of the salivary gland. Four additional secreted calcium-binding proteins were predicted by our salivary gland ESTs and proteome (an endoplasmin, calreticulain and two calnexins), but were then not found to be enriched in the salivary gland cDNA libraries (Table S6, Supporting Information).…”

“…Aphids initially secrete a gelling saliva that hardens and forms a protective sheath around the mouthparts, followed by watery saliva which is secreted into the phloem immediately before and during feeding but also into cells as the tip of the mouthparts progress toward the phloem. 21,22 A number of strategies have been employed in an attempt to catalogue and characterize the salivary proteins of various aphid species and include mass spectrometry of collected saliva, 27,28 RNA interference, 29 salivary gland EST analysis, 30 in planta analysis of phloem occlusion mechanisms, 23 plant differential gene expression studies 31 in response to aphid salivary concentrates and in planta expression of candidate salivary effector proteins. 32 The availability of a genome sequence for the pea aphid, Acyrthosiphon pisum, has made this species a particularly good candidate for saliva studies.…”

“…Many pathogens have specific secretion systems that enable the delivery of these effectors, such as the type III secretion system in bacteria [15][16][17] or the RXLR system in oomycetes. [18][19][20] By the nature of their feeding, aphids are thought to deliver effectors in their saliva, [21][22][23] as is the case for plant pathogenic nematodes. [24][25][26] However, little is known about the bioactive components of aphid saliva.…”