Molecular sabotage of plant defense by aphid saliva

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...

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Published in:	Proceedings of the National Academy of Sciences - PNAS Vol. 104; no. 25; pp. 10536 - 10541
Main Authors:	Will, Torsten, Tjallingii, W. Fred, Thönnessen, Alexandra, van Bel, Aart J.E
Format:	Journal Article
Language:	English
Published:	United States National Academy of Sciences 19-06-2007 National Acad Sciences
Subjects:	Animals Aphididae Aphids - anatomy & histology Aphids - chemistry Aphids - metabolism Aphids - physiology Biological Sciences Botany Calcium Calcium - metabolism Calcium - physiology calcium-binding proteins defense mechanisms Diet Electric Conductivity Flowers & plants forisomes gel-electrophoresis Gels gossypii Ingestion insect pests insect proteins Insects Megoura viciae membrane penetration Phloem Plant ecology Plant Physiological Phenomena Plant Proteins - metabolism Plant Proteins - physiology plant-insect relations Plants Plants - anatomy & histology Plants - chemistry Plants - metabolism Plants - parasitology polyacrylamide gels potentials resistance Saliva Saliva - chemistry Saliva - metabolism Saliva - physiology sap sieve element occlusion Sieve plates sieve tube plugging Sieve tubes stylets Vicia faba Waveforms
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Summary:	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 calcium-triggered 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 ⁴⁵Ca²⁺ 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.
Bibliography:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Edited by Nancy A. Moran, University of Arizona, Tucson, AZ, and approved May 3, 2007 Author contributions: T.W. and A.J.E.v.B. designed research; T.W. and A.T. performed research; T.W. and W.F.T. analyzed data; and T.W., W.F.T., A.T., and A.J.E.v.B. wrote the paper.
ISSN:	0027-8424 1091-6490
DOI:	10.1073/pnas.0703535104