Disease interactions in a shared host plant: effects of pre-existing viral infection on cucurbit plant defense responses and resistance to bacterial wilt disease.

Both biotic and abiotic stressors can elicit broad-spectrum plant resistance against subsequent pathogen challenges. However, we currently have little understanding of how such effects influence broader aspects of disease ecology and epidemiology in natural environments where plants interact with multiple antagonists simultaneously. In previous work, we have shown that healthy wild gourd plants (Cucurbita pepo ssp. texana) contract a fatal bacterial wilt infection (caused by Erwinia tracheiphila) at significantly higher rates than plants infected with Zucchini yellow mosaic virus (ZYMV). We recently reported evidence that this pattern is explained, at least in part, by reduced visitation of ZYMV-infected plants by the cucumber beetle vectors of E. tracheiphila. Here we examine whether ZYMV-infection may also directly elicit plant resistance to subsequent E. tracheiphila infection. In laboratory studies, we assayed the induction of key phytohormones (SA and JA) in single and mixed infections of these pathogens, as well as in response to the feeding of A. vittatum cucumber beetles on healthy and infected plants. We also tracked the incidence and progression of wilt disease symptoms in plants with prior ZYMV infections. Our results indicate that ZYMV-infection slightly delays the progression of wilt symptoms, but does not significantly reduce E. tracheiphila infection success. This observation supports the hypothesis that reduced rates of wilt disease in ZYMV-infected plants reflect reduced visitation by beetle vectors. We also documented consistently strong SA responses to ZYMV infection, but limited responses to E. tracheiphila in the absence of ZYMV, suggesting that the latter pathogen may effectively evade or suppress plant defenses, although we observed no evidence of antagonistic cross-talk between SA and JA signaling pathways. We did, however, document effects of E. tracheiphila on induced responses to herbivory that may influence host-plant quality for (and hence pathogen acquisition by) cucumber beetles.

Outcomes of co-infection by two potyviruses: implications for the evolution of manipulative strategies.

Recent studies have documented effects of plant viruses on host plants that appear to enhance transmission by insect vectors. But, almost no empirical work has explored the implications of such apparent manipulation for interactions among co-infecting pathogens. We examined single and mixed infections of two potyviruses, watermelon mosaic virus (WMV) and zucchini yellow mosaic virus (ZYMV), that frequently co-occur in cucurbitaceae populations and share the same aphid vectors. We found that ZYMV isolates replicated at similar rates in single and mixed infections, whereas WMV strains accumulated to significantly lower levels in the presence of ZYMV. Furthermore, ZYMV induced changes in leaf colour and volatile emissions that enhanced aphid (Aphis gossypii) recruitment to infected plants. By contrast, WMV did not elicit strong effects on plant-aphid interactions. Nevertheless, WMV was still readily transmitted from mixed infections, despite fairing poorly in in-plant competition. These findings suggest that pathogen effects on host-vector interactions may well influence competition among co-infecting pathogens. For example, if non-manipulative pathogens benefit from the increased vector traffic elicited by manipulative competitors, their costs of competition may be mitigated to some extent. Conversely, the benefits of manipulation may be limited by free-rider effects in systems where there is strong competition among pathogens for host resources and/or access to vectors.

Effects of the virus satellite gene ßC1 on host plant defense signaling and volatile emission.

Tomato Yellow Leaf Curl China virus spreads together with its invasive vector, the silverleaf whitefly B biotype, which exhibits higher growth rates on infected plants. Previous studies indicate that the virus satellite gene ßC1 accounts for the visible symptoms of infection and inhibits the constitutive expression of jasmonic acid (JA)--a phytohormone involved in plant defense against whiteflies--and of some JA-regulated genes. Here we present new details of the effects of on plant signaling and defense, obtained with (non-host) transgenic Arabidopsis thaliana and Nicotiana benthamiana plants. We found that JA induction in response to wounding was reduced in plants expressing ßC1. This result implies that ßC1 acts on conserved plant regulation mechanisms and might impair the entire JA defense pathway. Furthermore, transformed N. benthamiana plants exhibited elevated emissions of the volatile compound linalool, suggesting that ßC1 also influences plant-derived olfactory cues available to vector and non-vector insects.

Variation in Arabidopsis developmental responses to oomycete infection: resilience vs changes in life history traits.

Although plant resistance to aggressors has been well described, there is still little knowledge about the mechanisms underlying their tolerance to pathogens. Tolerance often appears to be mediated by changes in life history traits, shifting host resource investment from growth to reproduction, but whether host phenotype modifications induced after attack are adaptive is not always clear. Here, we investigated the details of the impact of Hyaloperonospora arabidopsidis infection on several biomass, phenology and architectural traits of Arabidopsis thaliana, for three pathogen genotypes and three host plant genotypes that have been shown previously to differ greatly in fecundity and tolerance to infection. We found that, although host genotype explains most of the variance in life history traits, these three lines differ critically in their response to infection, with delays and biomass losses at bolting, together with changes in inflorescence architecture, observed at one extreme host line, and an advantage at bolting for infected plants and no inflorescence alteration for the other. These results suggest that the differences in tolerance observed previously in this pathosystem do not involve plasticity in inflorescence architecture, but may arise from induced changes at the vegetative stage, before plant transition to reproduction.

How can your parasites become your allies?

Although parasitic infection is usually detrimental, it can be beneficial to the host in some situations. Parasites could help their host by providing a new function or modifying one of the host's life-history traits. We argue that the evolution towards a lasting mutualistic relationship would be more likely when parasites endow hosts with new abilities rather than alter a trait because hosts are less likely to evolve a new capability on their own than adjust their life history by microevolutionary steps. Furthermore, we underline how evolved dependence--the host's loss of ability to live alone owing to a long history of evolution in the presence of its parasites--has shaped contemporary mutualistic relationships.

Arabidopsis thaliana and the Robin Hood parasite: a chivalrous oomycete that steals fitness from fecund hosts and benefits the poorest one?

Are parasites always harmful to their hosts? By definition, indeed, but in a few cases and particular environments, hosts experience higher fitness in the presence than in the absence of their parasites. Symbiotic associations form a continuum of interactions, from deleterious to beneficial effects on hosts. In this paper, we investigate the outcome of parasite infection of Arabidopsis thaliana by its natural pathogen Hyaloperonospora arabidopsis. This system exhibits a wide range of parasite impact on host fitness with, surprisingly, deleterious effects on high fecundity hosts and, at the opposite extreme, seemingly beneficial effects on the least fecund one. This phenomenon might result from varying levels of tolerance among host lines and even overcompensation for parasite damage analogous to what can be observed in plant-herbivore systems.

Genetic diversity in natural populations: a fundamental component of plant-microbe interactions.

Genetic diversity for plant defense against microbial pathogens has been studied either by analyzing sequences of defense genes or by testing phenotypic responses to pathogens under experimental conditions. These two approaches give different but complementary information but, till date, only rare attempts at their integration have been made. Here we discuss the advances made, because of the two approaches, in understanding plant-pathogen coevolution and propose ways of integrating the two.

Genotype-specific interactions and the trade-off between host and parasite fitness.

BACKGROUND: Evolution of parasite traits is inextricably linked to their hosts. For instance one common definition of parasite virulence is the reduction in host fitness due to infection. Thus, traits of infection must be viewed in both protagonists and may be under shared genetic and physiological control. We investigated these questions on the oomycete Hyaloperonospora arabidopsis (= parasitica), a natural pathogen of the Brassicaceae Arabidopsis thaliana. RESULTS: We performed a controlled cross inoculation experiment confronting six lines of the host plant with seven strains of the parasite in order to evaluate genetic variation for phenotypic traits of infection among hosts, parasites, and distinct combinations. Parasite infection intensity and transmission were highly variable among parasite strains and host lines but depended also on the interaction between particular genotypes of the protagonists, and genetic variation for the infection phenotype of parasites from natural populations was found even at a small spatial scale within population. Furthermore, increased parasite fitness led to a significant decrease in host fitness only on a single host line (Gb), although a trade-off between these two traits was expected because host and parasite share the same resource pool for their respective reproduction. We propose that different levels of compatibility dependent on genotype by genotype interactions might lead to different amounts of resources available for host and parasite reproduction. This variation in compatibility could thus mask the expected negative relationship between host and parasite fitness, as the total resource pool would not be constant. CONCLUSION: These results highlight the importance of host variation in the determination of parasite fitness traits. This kind of interaction may in turn decouple the relationship between parasite transmission and its negative effect on host fitness, altering theoretical predictions of parasite evolution.

Parasite-host fitness trade-offs change with parasite identity: genotype-specific interactions in a plant-pathogen system.

Simultaneous effects of host and parasite in determining quantitative traits of infection have long been neglected in theoretical and experimental investigations of host-parasite coevolution with the notable exception of gene-for-gene resistance studies. A cross-infection experiment, using five lines of the plant Arabidopsis thaliana and two strains of its oomycete pathogen Hyaloperonospora parasitica, revealed that three traits traditionally considered those of the parasite (number of infected leaves, transmission success, and time until 50% transmission), differed among specific combinations of host and parasite lines, being determined by the two protagonists of the infection. However, the two parasite strains did not differ significantly for most measured phenotypic traits of the infection. Globally, transmission increased with increasing virulence among the different host-parasite combinations, as assumed by most models of evolution of virulence. Surprisingly, however, there was no general relationship between parasite and host fitness, estimated respectively as transmission and seed production. Only one of the two strains showed the expected significant negative genetic correlation between these two variables. Our results thus highlight the importance of taking into account both host and parasite genetic variation because their interaction can lead to unexpected evolutionary outcomes.