Infection of tobacco plants by a begomovirus improves nutritional assimilation by a whitefly

The majority of described plant viruses are transmitted by insects of the Hemipteroid assemblage that includes aphids, whiteflies, leafhoppers, planthoppers, and thrips. In this review we highlight progress made in research on vector interactions of the more than 200 plant viruses that are transmitted by hemipteroid insects beginning a few hours or days after acquisition and for up to the life of the insect, i.e., in a persistent-circulative or persistent-propagative mode. These plant viruses move through the insect vector, from the gut lumen into the hemolymph or other tissues and finally into the salivary glands, from which these viruses are introduced back into the plant host during insect feeding. The movement and/or replication of the viruses in the insect vectors require specific interactions between virus and vector components. Recent investigations have resulted in a better understanding of the replication sites and tissue tropism of several plant viruses that propagate in insect vectors. Furthermore, virus and insect proteins involved in overcoming transmission barriers in the vector have been identified for some virus-vector combinations.

The basal defenses important in curtailing the development of the phloem-feeding silverleaf whitefly (Bemisia tabaci type B; SLWF) on Arabidopsis (Arabidopsis thaliana) were investigated. Sentinel defense gene RNAs were monitored in SLWF-infested and control plants. Salicylic acid (SA)-responsive gene transcripts accumulated locally (PR1, BGL2, PR5, SID2, EDS5, PAD4) and systemically (PR1, BGL2, PR5) during SLWF nymph feeding. In contrast, jasmonic acid (JA)- and ethylene-dependent RNAs (PDF1.2, VSP1, HEL, THI2.1, FAD3, ERS1, ERF1) were repressed or not modulated in SLWF-infested leaves. To test for a role of SA and JA pathways in basal defense, SLWF development on mutant and transgenic lines that constitutively activate or impair defense pathways was determined. By monitoring the percentage of SLWF nymphs in each instar, we show that mutants that activate SA defenses (cim10) or impair JA defenses (coi1) accelerated SLWF nymphal development. Reciprocally, mutants that activate JA defenses (cev1) or impair SA defenses (npr1, NahG) slowed SLWF nymphal development. Furthermore, when npr1 plants, which do not activate downstream SA defenses, were treated with methyl jasmonate, a dramatic delay in nymph development was observed. Collectively, these results showed that SLWF-repressed, JA-regulated defenses were associated with basal defense to the SLWF.

The incidence of phloem sap feeding by animals appears paradoxical. Although phloem sap is nutrient-rich compared with many other plant products and generally lacking in toxins and feeding deterrents, it is consumed as the dominant or sole diet by a very restricted range of animals, exclusively insects of the order Hemiptera. These insects display two sets of adaptations. First, linked to the high ratio of non-essential:essential amino acids in phloem sap, these insects contain symbiotic micro-organisms which provide them with essential amino acids. For example, bacteria of the genus Buchnera contribute up to 90% of the essential amino acids required by the pea aphid Acyrthosiphon pisum feeding on Vicia faba. Second, the insect tolerance of the very high sugar content and osmotic pressure of phloem sap is promoted by their possession in the gut of sucrase-transglucosidase activity, which transforms excess ingested sugar into long-chain oligosaccharides voided via honeydew. Various other animals consume phloem sap by proxy, through feeding on the honeydew of phloem-feeding hemipterans. Honeydew is physiologically less extreme than phloem sap, with a higher essential:non-essential amino acid ratio and lower osmotic pressure. Even so, ant species strongly dependent on honeydew as food may benefit from nutrients derived from their symbiotic bacteria Blochmannia.