Most aphids possess intracellular bacteria of the genus Buchnera. The bacteria are transmitted vertically via the aphid ovary, and the association is obligate for both partners: Bacteria-free aphids grow poorly and produce few or no offspring, and Buchnera are both unknown apart from aphids and apparently unculturable. The symbiosis has a nutritional basis. Specifically, bacterial provisioning of essential amino acids has been demonstrated. Nitrogen recycling, however, is not quantitatively important to the nutrition of aphid species studied, and there is strong evidence against bacterial involvement in the lipid and sterol nutrition of aphids. Buchnera have been implicated in various non-nutritional functions. Of these, just one has strong experimental support: promotion of aphid transmission of circulative viruses. It is argued that strong parallels may exist between the nutritional interactions (including the underlying mechanisms) in the aphid-Buchnera association and other insect symbioses with intracellular microorganisms.

Nutritional Interactions in Insect-Microbial Symbioses: Aphids and Their Symbiotic Bacteria Buchnera

. Plant penetration by Aphis fabae (Scopoli) was recorded by the electrical penetration graph (EPG) technique and followed by stylectomy during wave-forms that were suspected of indicating sieve element punctures. The severed stylets in the plant tissue were subsequently processed for transmission electron microscopy (TEM) and sectioned either transverse or longitudinal to the stylets. Two completely serially sectioned probes from the epidermis to the phloem were reconstructed.



In one probe the stylet pathway went to a sieve element and showed many empty branches of salivary sheath material. Breaks in cell walls filled with sheath material demonstrated that the majority of cells bordering the track had been punctured, which supports earlier evidence from EPGs. All types of cells showed punctures and the highest number was found inside the vascular bundle. Very few cells died, which would appear to be important for virus transmission, and in others cellular reactions remained limited to some callose formation. The route of the stylets was intercellular and passed through the secondary wall material. The role of pectinase in intercellular penetration, and previous evidence for intracellular tracks are discussed. Most sieve elements had been punctured but only one was eventually accepted. Thus, reaching a sieve element in a host plant does not automatically imply its acceptance though the reason remains unclear. Gelation of phloem proteins was shown in the stylet canal.



In a second probe, plant cytological and morphological correlations with the EPG were emphasized. Probes by other aphid-plant combinations showed great similarity.

https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1365-3032.1993.tb00604.x

Fine structure of aphid stylet routes in plant tissues in correlation with EPG signals.

Insects are sensitive to chemical aspects of their environment, particularly with regard to host and mate location. Aphids can select individual or a few closely related host plant species from a wide range of nonhost vegetation (65, 71). This selection relies upon the detection of secondary plant compounds as well as primary metabolites associated with the physiological condition of the host plant (82). Use of long-range volatile chemical cues in aphid-plant and aphid-aphid interactions was formerly considered unlikely (78, 108). Never­ theless, recent work reviewed here demonstrates that olfaction plays a more extensive role in the chemical ecology of aphids than previously thought. Thc study of aphid chemical ecology involving volatile semiochemicals, particularly pheromones, has been greatly enhanced by the development of electrophysiological rccordings from aphid antennae, using the electroan­ tennograph (EAG) and single-cell recording (SCR) methods. SCR directly coupled to high-resolution capillary column gas chromatography (GC-SCR) provides a powerful tool for locating the active components in behaviorally active samples (154). Analysis by other highly sensitive techniques such as

The Chemical Ecology of Aphids

A gene that encodes systemin, a mobile 18-amino acid polypeptide inducer of proteinase inhibitor synthesis in tomato and potato leaves, has been isolated from tomato, Lycopersicon esculentum. Induction of proteinase inhibitors in plants is a response to insect or pathogen attacks. The gene has 10 introns and 11 exons, ten of which are organized as five homologous pairs with an unrelated sequence in the eleventh, encoding systemin. Systemin is proteolytically processed from a 200-amino acid precursor protein, prosystemin. Prosystemin messenger RNA was found in all organs of the plant except the roots and was systemically wound-inducible in leaves. Tomato plants transformed with an antisense prosystemin complementary DNA exhibited greatly suppressed systemic wound induction of proteinase Inhibitor I and II synthesis in leaves.

https://science.sciencemag.org/content/sci/255/5051/1570.full.pdf

Structure, expression, and antisense inhibition of the systemin precursor gene

Phloem-feeding pests cause extensive crop damage throughout the world, yet little is understood about how plants perceive and defend themselves from these threats. The silverleaf whitefly (SLWF; Bemisia tabaci type B) is a good model for studying phloem-feeding insect-plant interactions, as SLWF nymphs cause little wounding and have a long, continuous interaction with the plant. Using the Affymetrix ATH1 GeneChip to monitor the Arabidopsis (Arabidopsis thaliana) transcriptome, 700 transcripts were found to be up-regulated and 556 down-regulated by SLWF nymphs. Closer examination of the regulation of secondary metabolite (glucosinolate) and defense pathway genes after SLWF-instar feeding shows that responses were qualitatively and quantitatively different from chewing insects and aphids. In addition to the RNA profile distinctions, analysis of SLWF performance on wild-type and phytoalexin-deficient4 (pad4) mutants suggests aphid and SLWF interactions with Arabidopsis were distinct. While pad4-1 mutants were more susceptible to aphids, SLWF development on pad4-1 and wild-type plants was similar. Furthermore, although jasmonic acid genes were repressed and salicylic acid-regulated genes were induced after SLWF feeding, cytological staining of SLWF-infested tissue showed that pathogen defenses, such as localized cell death and hydrogen peroxide accumulation, were not observed. Like aphid and fungal pathogens, callose synthase gene RNAs accumulated and callose deposition was observed in SLWF-infested tissue. These results provide a more comprehensive understanding of phloem-feeding insect-plant interactions and distinguish SLWF global responses.

Arabidopsis Transcriptome Changes in Response to Phloem-Feeding Silverleaf Whitefly Nymphs. Similarities and Distinctions in Responses to Aphids

The importance of host-plant resistance of crop plants in the biological control of aphids and the formation of aphid biotypes is discussed. The rapid response of plant breeders to the formation of new aphid biotypes requires detailed knowledge on the mechanism of host-plant resistance. Current knowledge on the chemical basis of host-plant resistance to aphids is summarized. Of central importance to this relationship is the aphid-pectinase plant-pectin interdependence. Parallels between the mechanism of aphid-plant and pathogen-plant attack are pointed out and how aphid bacterial endo-symbiotes play a central role in host-plant selection.

D. L. Dreyer

Papers

Chemical basis of host-plant resistance to aphids