Insects As Alternative Hosts for Phytopathogenic Bacteria Geetanchaly Nadarasah1 & John Stavrinides1

REVIEW ARTICLE Insects as alternative hosts for phytopathogenic bacteria Geetanchaly Nadarasah1 & John Stavrinides1 1Department of Biology, University of Regina, Regina, Saskatchewan, Canada Correspondence: John Stavrinides, Abstract Department of Biology, University of Regina, 3737 Wascana Parkway, Regina, Phytopathogens have evolved specialized pathogenicity determinants that enable Saskatchewan, Canada S4S0A2. Tel.: 11 306 them to colonize their specific plant hosts and cause disease, but their intimate 337 8478; fax: 11 306 337 2410; e-mail: associations with plants also predispose them to frequent encounters with [email protected] herbivorous insects, providing these phytopathogens with ample opportunity to colonize and eventually evolve alternative associations with insects. Decades of Received 8 September 2010; revised 15 research have revealed that these associations have resulted in the formation of December 2010; accepted 22 December 2010. bacterial–vector relationships, in which the insect mediates dissemination of the Final version published online 15 February plant pathogen. Emerging research, however, has highlighted the ability of plant 2011. pathogenic bacteria to use insects as alternative hosts, exploiting them as they DOI:10.1111/j.1574-6976.2011.00264.x would their primary plant host. The identification of specific bacterial genetic determinants that mediate the interaction between bacterium and insect suggests Editor: Colin Berry that these interactions are not incidental, but have likely arisen following the repeated association of microorganisms with particular insects over evolutionary Keywords time. This review will address the biology and ecology of phytopathogenic bacteria plant pathogens; insects; pathogenicity; that interact with insects, including the traditional role of insects as vectors, as well transmission; vector; alternative hosts. as the newly emerging paradigm of insects serving as alternative primary hosts. Also discussed is one case where an insect serves as both host and vector, which may represent a transitionary stage in the evolution of insect–phytopathogen associations. the hidden ecology and true pathogenic potential of many Introduction bacteria that have long been considered strict and very Plant pathogenic bacteria are responsible for some of the dedicated phytopathogens. most devastating losses of major agricultural crops and vital The exploration of phytopathogen life histories is often fruit trees, causing millions of dollars in damage annually. trumped by the striking and often contrasting disease Their agricultural and economic impact has afforded them symptomology that develops on host plants as a conse- significant attention over the last 30 years, resulting in quence of disease. Traditionally, this has resulted in an enormous strides in the exploration of their epidemiology almost exclusive focus on the biology, ecology, and genetics and specialized disease strategies. Research of plant patho- of specific plant–phytopathogen relationships, often to the genic bacteria has not only seeded our understanding of the exclusion of other potentially relevant yet presumably less genetics of disease, epidemiology, and the factors contribut- obvious associations. Even the most intimate association ing to emerging infectious diseases, but has also led to the between pathogen and plant host in the natural environ- development of effective control and prevention measures ment, whether occurring at the interface of the phyllosphere for many plant diseases (Woolhouse et al., 2002; Gardan or within plant tissues, is still subject to incursions by other et al., 2003). More recently, however, there has been a shift in ecological players. Phytophagous insects, in particular, the exploration of the plant pathogens to a broader com- which graze frequently and recurrently on plant tissues that munity level, which moves beyond the traditional single may be colonized by epiphytic or plant pathogenic bacteria, MICROBIOLOGY REVIEWS MICROBIOLOGY host–single pathogen model to a wider and more encom- are often neglected as key ecological players, despite the fact passing view of the evolution and ecology of plant patho- that they are most likely to have repeated encounters and genic bacteria. Much of this research has expanded the field associations with phytopathogenic bacteria that reside in or into a new direction, and has resulted in the unearthing of on their preferred host plants. FEMS Microbiol Rev 35 (2011) 555–575 c 2011 Federation of European Microbiological Societies Published by Blackwell Publishing Ltd. All rights reserved 556 G. Nadarasah & J. Stavrinides There are numerous potential interactions that can result and then the saliva, and may be delivered into a new host from the association between a microorganism and an plant when the insect feeds (Kwon et al., 1999). Noncircula- insect, all of which are defined by the relative effects on the tive and nonpropagative microorganisms are those that fitness of the individual organisms (referred to as sym- generally form a physical association with the insect and are bionts). Mutualisms may form between the two organisms, subsequently mechanically transmitted to the plant host where both derive a benefit from their interaction. Mutual- (infection by an insect stylet that is coated with a pathogen, isms may be defensive, where the microorganisms provides for example) (James & Perry, 2004). protection to the insect host (Wilkinson et al., 2000), or Over the last decade, the exploration of phytopathogenic nutritional, where the microorganism supplements the diet bacteria and their interactions with insects has expanded of the insect host with key nutrients (Barbosa & Letourneau, beyond the traditional phytopathogen–vector relationship 1988). Parasitisms may also develop between microorgan- to include cases where phytopathogens exhibit entomo- isms and insects, where the microorganism benefits by pathogenic associations. Most of these relationships have extracting nutrients from its host, but at a cost to its host. been characterized only recently, and represent a new In the latter case, the microorganism may impair or disrupt paradigm in bacterial–insect interactions. Certainly, this the physiology and normal functioning of the insect host, has not lessened the focus on the traditional plant–microor- resulting in specific disease symptomology. A commensal- ganism or vector–microorganism association, or the use of ism describes the association between insect and microor- genomic and high-throughput approaches for exploring ganism where the microorganism benefits and the insect is these interactions. Instead, these studies have uncovered unaffected. Commensalisms likely characterize many of the hidden alternative interactions for plant pathogenic bacter- interactions that exist in the natural environment, but are ia, ultimately providing additional breadth to our under- most likely to go unnoticed. Both commensalistic and standing of their biology, ecology, and evolution. This parasitic symbioses can range from highly specific to non- review will examine the alternative associations of phyto- specific, with the development of more specific interactions pathogenic bacteria with insects, focusing on the genetics being favoured in cases where specialist microorganism and ecological relevance of those insects that can serve as encounter specialist insects recurrently over long periods of either a transport host/vector, an insect that serves as a time, and more general interactions in cases where generalist carrier of the pathogen, or a primary host, an insect that the or transient insects encounter specialist bacterial pathogens pathogen can colonize, replicate in, and disperse from. Also (or vice versa). examined is one special interaction where the microorgan- Phytopathogenic bacteria have evolved to harness insects ism exploits a single insect as both host and vector. This as vectors to effect their dissemination and delivery directly unusual association may represent a rare transitionary phase onto or into their preferred plant hosts. These partnerships in the evolution of phytopathogen–insect associations. can either be commensalistic or slightly parasitic to the insect, but in either case, the insect performs as a living Insects as vectors for phytopathogenic carrier that transmits the microorganism to its final (defini- bacteria tive) host. Many of these symbioses are highly specific, and The evolution of effective and stable phytopathogen–insect are categorized by the ability of the bacterium to replicate in vector partnerships is dependent largely on the opportunity and move through its vector. The ability to replicate within for the insect and the microorganism to encounter each the insect vector can be classified as either propagative or other frequently. Generally, the dependence of many insects nonpropagative, and the ability of the microorganism to and phytopathogens on plants as their primary source move through its vector can be classified as circulative or of nutrition may lead to an overlap of ecological niche, noncirculative (Blanc, 2004). In circulative nonpropagative providing the necessary conditions for insects to encounter, transmission, the microorganism is ingested by its insect contact, or ingest phytopathogenic bacteria. In this section, vector as it feeds on the host plant, after which it migrates we describe the best-characterized symbioses between in- into the midgut or the hindgut epithelium, and is then sects and phytopathogens

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