Plant phloem sap, the principal food of aphids, is a grossly unbalanced diet for animals, with high ratios of sugars:amino acids, non-essential:essential amino acids and K + :Na + and exceptionally low lipid levels. The chief digestive function of the alimentary tract is hydrolysis of phloem sugars, usually sucrose to glucose and fructose. Additionally, multiple complex sugars, including oligosaccharides of ≤20 hexose units are synthesized in the gut and these transformations contribute to the reduction in osmotic pressure of ingested phloem sap, such that the voided honeydew is isosmotic with the haemolymph. Sugars assimilated into aphid tissues are allocated principally to respiration and lipid synthesis. Aphids derive their nitrogen requirement from the phloem amino acids and symbiotic bacteria, Buchnera , which provide essential amino acids. Buchnera may also contribute to aphid nitrogen nutrition by recycling aphid waste nitrogen. Recent advances in analytical techniques and molecular biology/genomics provide the basis to explore the processes by which nutrient provisioning by Buchnera is integrated into the wider nutritional physiology of aphids and to identify the physiological traits of Hemiptera which contribute to the predisposition of these insects to evolve the phloem sap feeding habit.

The Nutritional Physiology of Aphids

E ndosymbiosis has been proposed as an evolutionary innovation that underlies the success and diversification of some groups of organisms by enabling them to exploit new ecological niches (e.g., Margulis and Fester 1991, Maynard Smith and Szathmary 1995). Three kinds of information are needed to evaluate this proposal. First, it is necessary to know something of the role played by symbionts in the lives of hosts: Are their effects ones that allow use of novel ecological niches? Second, information is needed on the evolutionary history of endosymbioses: How old are they and, in particular, do endosymbiotic infections predate diversification of major host groups? Finally, the evolutionary consequences for hosts of acquiring new capabilities in the form of symbiotic associations must be evaluated: Are these novel traits stable? Do they impose constraints as well as new capabilities on hosts? Recent studies have begun to shed light on these questions for bacteriocyte-associated endosymbioses in insects. Bacteriocytes (or mycetocytes) are cells of animal hosts that are positioned at characteristic locations in the body and appear to be specialized for housing bacteria (Figure 1; Buchner 1965, Dasch et al.

Bacteriocyte-Associated Endosymbionts of Insects

The complex interactions between aphids and their host plant are species-specific and involve multiple layers of recognition and defense. Aphid salivary proteins, which are released into the plant during phloem feeding, are a likely mediator of these interactions. In an approach to identify aphid effectors that facilitate feeding from host plants, eleven Myzus persicae (green peach aphid) salivary proteins and the GroEL protein of Buchnera aphidicola, a bacterial endosymbiont of this aphid species, were expressed transiently in Nicotiana tabacum (tobacco). Whereas two salivary proteins increased aphid reproduction, expression of three other aphid proteins and GroEL significantly decreased aphid reproduction on N. tabacum. These effects were recapitulated in stable transgenic Arabidopsis thaliana plants. Further experiments with A. thaliana expressing Mp55, a salivary protein that increased aphid reproduction, showed lower accumulation of 4-methoxyindol-3-ylmethylglucosinolate, callose and hydrogen peroxide in response to aphid feeding. Mp55-expressing plants also were more attractive for aphids in choice assays. Silencing Mp55 gene expression in M. persicae using RNA interference approaches reduced aphid reproduction on N. tabacum, A. thaliana, and N. benthamiana. Together, these results demonstrate a role for Mp55, a protein with as-yet-unknown molecular function, in the interaction of M. persicae with its host plants.

https://apsjournals.apsnet.org/doi/pdf/10.1094/MPMI-01-14-0018-R

Suppression of plant defenses by a Myzus persicae (green peach aphid) salivary effector protein.

Large-scale label-free quantitative proteomics of the pea aphid-Buchnera symbiosis

The symbiotic bacteria Buchnera sp. provide aphids with essential amino acids, nutrients in short supply in the aphid diet of plant phloem sap. The contribution of Buchnera-derived amino acids to net protein growth of the aphid Aphis fabae was quantified from the protein growth of aphids reared on chemically defined diets lacking individual amino acids. The amino acid production rates varied among the nine essential amino acids over the range 8-156 pmol microg(-1)protein day(-1) (for tryptophan and leucine, respectively), equivalent to 0.02-0.33 fmol Buchnera(-1)day(-1). In a complementary metabolic analysis, the aphids incorporated radioactivity from dietary [(14)C]glutamic acid into the essential amino acids isoleucine, lysine and threonine. Incorporation into isoleucine was significantly elevated by the omission of dietary isoleucine, indicating that dietary supply may affect the biosynthetic rates of certain amino acids by Buchnera. Aphids experimentally deprived of Buchnera did not synthesize essential amino acids from dietary glutamic acid. The mortality of aposymbionts was high over 7 days on the phenylalanine-free diet, and their assimilation of dietary leucine was depressed on the complete diet, suggesting that both the absence of bacteria-derived amino acids and the low rates of assimilation of certain dietary amino acids may contribute to the poor growth of these insects.

Quantifying nutrient production by the microbial symbionts in an aphid.

The population of symbiotic Buchnera bacteria in parthenogenetic females of the pea aphid Acyrthosiphon pisum was determined by quantitative hybridization of a DNA probe (groESL) to aphid homogenates. The aphids bore 1 x 10(sup7) to 2 x 10(sup7) bacterial cells per mg (fresh weight). In teneral aphids (i.e., aphids that had moulted to adulthood but that had not initiated reproduction), >75% of the bacteria were in the embryos, and the density of bacteria in the embryos was consistently greater than that in the maternal tissues. The bacterial density in teneral aphids increased from 1.3 x 10(sup7) to 2.0 x 10(sup7) cells mg (fresh weight) of aphids(sup-1) with temperature between 15 and 25(deg)C. This variation could be attributed to a temperature-dependent increase in both the density of bacteria in the embryos and embryo content of the aphids.

Partitioning of Symbiotic Bacteria between Generations of an Insect: a Quantitative Study of a Buchnera sp. in the Pea Aphid (Acyrthosiphon pisum) Reared at Different Temperatures

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Partitioning of Symbiotic Bacteria between Generations of an Insect: a Quantitative Study of a Buchnera sp. in the Pea Aphid (Acyrthosiphon pisum) Reared at Different Temperatures