Pea Aphid as both Host and Vector for the Phytopathogenic Bacterium Pseudomonas syringae

Abstract

Aphids are widespread agricultural pests that are capable of disseminating plant viral diseases; however, despite coming into frequent contact with epiphytic bacteria, aphids are considered to have no role in bacterial transmission. Here, we demonstrate the ability of pea aphids to vector the phytopathogen Pseudomonas syringae pv. syringae B728a (PsyB728a). While feeding on plants colonized by epiphytic bacteria, aphids acquire the bacteria, which colonize the digestive tract, multiply, and are excreted in the aphid honeydew, resulting in inoculation of the phyllosphere with up to 10 7 phytopathogenic bacteria per cm 2 . Within days of ingesting bacteria, aphids succumb to bacterial sepsis, indicating that aphids serve as an alternative, nonplant host for PsyB728a. The related strain Pseudomonas syringae pv. tomato DC3000 is >1,000-fold less virulent than PsyB728a in the pea aphid, suggesting that PsyB728a possesses strain-specific pathogenicity factors that allow it to exploit aphids as hosts. To identify these factors, we performed a mutagenesis screen and recovered PsyB728a mutants that were hypovirulent, including one defective in a gene required for flagellum formation and motility. These interactions illustrate that aphids can also vector bacterial pathogens and that even seemingly host-restricted pathogens can have alternative host specificities and lifestyles.Aphids are prolific insect pests that impact numerous agricultural crop plants (8). Although direct parasitization of their hosts can reduce plant biomass, crop quality, and crop yield, aphids are of particular importance for their role in the dissemination of plant disease (24, 30). Phytopathogenic viruses can be acquired by aphids as they probe infected plant hosts with their stylet (29,30), with the subsequent movement of infected aphids to healthy plants contributing significantly to the dissemination of plant disease (29). Surprisingly, however, aphids are considered strictly vectors of phytopathogenic viruses, despite their frequent physical contact with a variety of bacterial epiphytes (10).Upon landing on a potential host, the aphid begins to explore the plant, probing the plant tissues with its stylet and puncturing through the epidermal layers to locate and access the phloem sieve tube elements to feed (3,18,24). As it traverses the plant surface, the aphid continually evaluates the suitability of the host, with some aphid species sampling plant fluids with droplets of saliva that are expelled and reingested (3). This saliva can contact the plant surface where many bacterial epiphytes reside, such as the ubiquitous phytopathogens Pantoea agglomerans and Pseudomonas syringae (4,5,10,21,22,32).The pea aphid, Acyrthosiphon pisum, feeds on a variety of agriculturally relevant crop plants in the Fabaceae, including soybean (Glycine max), fava/broad bean (Vicia faba), pea (Pisum sativum), and snap bean (Phaseolus vulgaris) (15,28,(34)(35)(36), and has been shown to vector bean yellow mosaic virus between these hosts (15,(34)(35)(36). Several of ...

Heritable symbiosis: The advantages and perils of an evolutionary rabbit hole

“…Potentially, these losses facilitated the evolution of symbioses with Buchnera, and with numerous facultative symbionts, as supported by the observation that Buchnera cells elicit the IMD pathway in other insects (42). This reduction in immunity seems to have consequences because aphids are susceptible to infections by bacterial pathogens during feeding and during nutritional stress (43,44). The prospect that immune-system reduction paved the way for the elaborate symbioses in sap-feeding insects generally will likely be resolved from ongoing genome sequencing of additional insect species that vary in symbiotic associations.…”

Insect pathogenicity in plant-beneficial pseudomonads: phylogenetic distribution and comparative genomics

“…Insects could be especially useful as a means of dispersal, a phenomenon documented for diverse plant-pathogenic bacteria (Nadarasah and Stavrinides, 2011). Some Pseudomonas syringae strains for instance can use the pea aphid as alternative primary host where they replicate to high numbers and can be deposited onto a new plant host via excreted honeydew (Stavrinides et al, 2009). Similarly, the rhizobacterium P. chlororaphis strain L11 was found to be transmittable from one plant to another by Diabrotica undecimpunctata subsp.…”

The Facultative Symbiont Rickettsia Protects an Invasive Whitefly against Entomopathogenic Pseudomonas syringae Strains

“…To compare the effects of P. syringae on whiteflies to the effects on aphids, we performed pathogenicity assays on aphids, modeled after those done by Stavrinides et al (22). Negative-control and bacterial treatments were prepared as described above for whiteflies, except that artificial aphid diet (27) instead of sucrose solution was used.…”

“…Such pathogens may be cryptic, in that they do not produce visible symptoms, and furthermore, they may infect at a low rate, making them difficult to observe. It was recently discovered that some strains of the plant pathogen Pseudomonas syringae cause high rates of mortality after ingestion by pea aphids (22). Pseudomonas syringae is a common plant epiphyte (23,24) and is therefore likely to be encountered by whiteflies on plants.…”