Context-dependent transmission of a generalist plant pathogen: host species and pathogen strain mediate insect vector competence

The specificity of pathogen–vector–host interactions is an important element of disease epidemiology. For generalist pathogens, different pathogen strains, vector species, or host species may all contribute to variability in disease incidence. One such pathogen is Xylella fastidiosa Wells et al., a xylem-limited bacterium that infects dozens of crop, ornamental, and native plants in the USA. This pathogen also has a diverse vector complex and multiple biologically distinct strains. We studied the implications of diversity in this pathogen–vector–host system, by quantifying variability in transmission efficiency of different X. fastidiosa strains (isolates from almond and grape genetic groups) for different host plants (grape, almond, and alfalfa) by two of the most important vectors in California: glassy-winged sharpshooter [ Homalodisca vitripennis (Germar)] and green sharpshooter ( Draeculacephala minerva Ball) (both Hemiptera: Cicadellidae). Transmission of isolates of the almond strain by H. vitripennis did not differ significantly, whereas transmission varied significantly among isolates from the grape strain (15–90%). Host plant species did not affect H. vitripennis transmission. Conversely, D. minerva efficiency was mediated by both host plant species and pathogen strain. No acquisition of an almond isolate occurred regardless of plant type (0/122), whereas acquisition of a grape isolate from alfalfa was 10-fold higher than from grape or almond plants. These results suggest that pathogen, vector, and host diversity impose contingencies on the transmission ecology of this complex disease system. Studies aimed at the development of management strategies for X. fastidiosa diseases should consider the complexity of these interactions as they relate to disease spread.     

Temperature mediates vector transmission efficiency: inoculum supply and plant infection dynamics

Climate, particularly environmental temperature, frequently plays an important role in disease epidemiology. This study investigated the role of environmental temperature on transmission of the generalist plant pathogen Xylella fastidiosa by its leafhopper vectors. In this system temperature is known to influence both vector performance and feeding rate, yet the implications for pathogen transmission have not been documented. Experiments were conducted over a range of temperatures to document effects on transmission efficiency of the California native Graphocephala atropunctata (blue–green sharpshooter) and the invasive Homalodisca vitripennis (glassy-winged sharpshooter). Inoculation efficiency of H. vitripennis was positively related to temperature. Graphocephala atropunctata mortality and transmission responded non-linearly to temperature, with the highest rates of both at the highest temperature. The experiment also evaluated whether differences in inoculum supply contributed to plant infection level using quantitative PCR. Although total X. fastidiosa population within G. atropunctata was not related to plant infection, the number of infectious vectors was a strong predictor of plant infection level–suggesting that the number of inoculation events is important in the development of systemic infection of X. fastidiosa in grapevines. These results, along with existing evidence from the literature, point to wide-ranging impacts of climate on the epidemiology of X. fastidiosa diseases.     

Impact of duration versus frequency of probing by Homalodisca vitripennis (Hemiptera: Cicadellidae) on inoculation of Xylella fastidiosa

Successful infection of the plant pathogenic bacterium Xylella fastidiosa (Wells) from an infected plant to a new host involves three main steps: 1) acquisition of the bacterium by a vector; 2) inoculation of a noninfected host plant by the vector; and 3) establishment of sufficient titers of X. fastidiosa in the host plant to sustain a chronic infection. Understanding the basic biology of the transmission process is a key to limiting the spread of plant diseases induced by X. fasdidiosa and reducing agricultural losses, especially those experienced in California since the introduction of a new vector, Homalodisca vitripennis (Germar) (Hemiptera, Cicadellidae) (formerly H. coagulata Say), the glassy-winged sharpshooter. In this study, H. vitripennis adults that acquired X. fastidiosa were allowed access to chrysanthemum plant cuttings for 30, 60, 90, or 120 min. The numbers of X. fastidiosa acquired (i.e., cells present in the insect foregut) and the number inoculated to the plant cuttings were separately determined using quantitative real-time polymerase chain reaction (PCR). In addition, the number of times glassy-winged sharpshooter stylets probed plant cuttings and the amount of time glassy-winged sharpshooter spent actively ingesting were monitored using video surveillance. Linear regression did not indicate a relationship between the number of X. fastidiosa cells inoculated into the plant cutting and either the titer of pathogen present in the insect or amount of time spent ingesting per probe. However, the number of probes significantly influenced the number of X. fastidiosa cells inoculated. Due to the highly variable nature of transmission, our model could not account for all observed variation as indicated by low R2 values. However, our results suggest that the mechanism of transmission is dependent on probing behaviors more than ingestion duration.     

Estimating Xylella fastidiosa transmission parameters: decoupling sharpshooter number and feeding period

Compared to human- and wildlife-transmitted pathogens, less emphasis has been placed on developing models of plant pathogen transmission by insects. Here, we describe the transmission ecology of the bacterium Xylella fastidiosa Wells et al., the causal agent of Pierce's disease in grapevines, by its leafhopper vectors. First, we performed a meta-analysis of transmission studies of X. fastidiosa by its two most important vectors in the Western USA, the invasive glassy-winged sharpshooter, Homalodisca vitripennis Germar, and the native blue-green sharpshooter, Graphocephala atropunctata Signoret (both Hemiptera: Cicadellidae). The importance of vector number, pathogen acquisition period, and inoculation access period (IAP) for transmission differed between the two species. We fit these transmission datasets to two biologically derived transmission models, i.e., a binomial and a Poisson probability model. The Poisson model provided substantially better fit and produced estimates of H. vitripennis transmission efficiency that were dramatically lower than for G. atropunctata . We also conducted a separate pair of experiments that decoupled vector number from IAP. These experiments supported the results of the meta-analysis. Interestingly, high vector loads not only increased transmission rate, but also shortened X. fastidiosa incubation period in grapevines. This work provides quantitative estimates of transmission of an economically important pathogen that is analogous to risk models for arthropod-vectored human and wildlife diseases. In addition, this work suggests that heterogeneous vector loads may accelerate the disease cycle, increasing the potential for secondary spread in vineyards.     

Disrupting the transmission of a vector-borne plant pathogen

Approaches to control vector-borne diseases rarely focus on the interface between vector and microbial pathogen, but strategies aimed at disrupting the interactions required for transmission may lead to reductions in disease spread. We tested if the vector transmission of the plant-pathogenic bacterium Xylella fastidiosa was affected by three groups of molecules: lectins, carbohydrates, and antibodies. Although not comprehensively characterized, it is known that X. fastidiosa adhesins bind to carbohydrates, and that these interactions are important for initial cell attachment to vectors, which is required for bacterial transmission from host to host. Lectins with affinity to substrates expected to occur on the cuticular surface of vectors colonized by X. fastidiosa, such as wheat germ agglutinin, resulted in statistically significant reductions in transmission rate, as did carbohydrates with N-acetylglucosamine residues. Presumably, lectins bound to receptors on the vector required for cell adhesion/colonization, while carbohydrate-saturated adhesins on X. fastidiosa's cell surface. Furthermore, antibodies against X. fastidiosa whole cells, gum, and afimbrial adhesins also resulted in transmission blockage. However, no treatment resulted in the complete abolishment of transmission, suggesting that this is a complex biological process. This work illustrates the potential to block the transmission of vector-borne pathogens without directly affecting either organism.     

Transmission efficiency of Xylella fastidiosa by sharpshooters (Hemiptera: Cicadellidae) in coffee and citrus

Xylella fastidiosa (Wells, Raju, Hung, Weisburg, Mandelco-Paul, and Brenner) is a bacterial pathogen transmitted by several sharpshooters in two tribes of Cicadellinae (Proconiini and Cicadellini). Here, we compared the transmission efficiency of X. fastidiosa in coffee (Coffea arabica L.) and citrus [Citrus sinensis (L.) Osbeck] by Cicadellini [Bucephalogonia xanthophis (Berg) and Dilobopterus costalimai Young] and Proconiini [Homalodisca ignorata Melichar and Oncometopia facialis (Signoret)] sharpshooters that occur in both crops. At different seasons, healthy adults of each species were submitted to a 48-h acquisition access period on citrus or coffee source plants infected with X. fastidiosa isolates that cause Citrus variegated chlorosis (CVC) and Coffee leaf scorch (CLS), respectively, and then confined on healthy seedlings of the corresponding host plant for a 48-h inoculation access period. No significant effect of inoculation season was observed when comparing infection rates of citrus or coffee plants inoculated by vectors at different times of the year. In citrus, the transmission rate by single insects was significantly higher for H. ignorata (30%) in relation to B. xanthophis (5%) and O. facialis (1.1%), but there was no difference among vector species in coffee, whose transmission rates ranged from 1.2 to 7.2%. Comparing host plants, H. ignorata was more effective in transmitting X. fastidiosa to citrus (30%) in relation to coffee (2.2%), whereas the other vectors transmitted the bacterium to both hosts with similar efficiencies. Despite these variations, vector efficiency in coffee and citrus is lower than that reported in other hosts.     

Interactive effects of water stress and xylem-limited bacterial infection on the water relations of a host vine

Xylella fastidiosa, a xylem-limited bacterial pathogen that causes bacterial leaf scorch in its hosts, has a diverse and extensive host range among plant species worldwide. Previous work has shown that water stress enhances leaf scorch symptom severity and progression along the stem in Parthenocissus quinquefolia infected by X. fastidiosa. The objective here was to investigate the mechanisms underlying the interaction of water stress and infection by X. fastidiosa. Using the eastern deciduous forest vine, P. quinquefolia, infection and water availability were manipulated while measuring leaf water potentials (psi(L)), stomatal conductance (g(s)), whole shoot hydraulic conductance (K(h)), per cent xylem embolism, and xylem vessel dimensions. No significant differences in any of the physiological measurements were found between control and infected plants prior to drought. Drought treatment significantly reduced psi(L) and g(s) at all leaf positions throughout the day in late summer in both years of the study. In addition, infection significantly reduced psi(L) and g(s) in the most basal leaf positions in late summer in both years. Whole shoot hydraulic conductance was reduced by both low water and infection treatments. However, per cent embolized vessels and mean vessel diameter were affected by drought treatment only. These results imply that the major effect of infection by X. fastidiosa occurs due to reduced hydraulic conductance caused by clogging of the vessels, and not increased cavitation and embolism of xylem elements. The reduced K(h) caused by X. fastidiosa infection acts additively with the water limitation imposed by Drought stress.     

Differentiation of Xylella fastidiosa strains via multilocus sequence analysis of environmentally mediated genes (MLSA-E)

Isolates of the plant pathogen Xylella fastidiosa are genetically very similar, but studies on their biological traits have indicated differences in virulence and infection symptomatology. Taxonomic analyses have identified several subspecies, and phylogenetic analyses of housekeeping genes have shown broad host-based genetic differences; however, results are still inconclusive for genetic differentiation of isolates within subspecies. This study employs multilocus sequence analysis of environmentally mediated genes (MLSA-E; genes influenced by environmental factors) to investigate X. fastidiosa relationships and differentiate isolates with low genetic variability. Potential environmentally mediated genes, including host colonization and survival genes related to infection establishment, were identified a priori. The ratio of the rate of nonsynonymous substitutions to the rate of synonymous substitutions (dN/dS) was calculated to select genes that may be under increased positive selection compared to previously studied housekeeping genes. Nine genes were sequenced from 54 X. fastidiosa isolates infecting different host plants across the United States. Results of maximum likelihood (ML) and Bayesian phylogenetic (BP) analyses are in agreement with known X. fastidiosa subspecies clades but show novel within-subspecies differentiation, including geographic differentiation, and provide additional information regarding host-based isolate variation and specificity. dN/dS ratios of environmentally mediated genes, though <1 due to high sequence similarity, are significantly greater than housekeeping gene dN/dS ratios and correlate with increased sequence variability. MLSA-E can more precisely resolve relationships between closely related bacterial strains with low genetic variability, such as X. fastidiosa isolates. Discovering the genetic relationships between X. fastidiosa isolates will provide new insights into the epidemiology of populations of X. fastidiosa, allowing improved disease management in economically important crops.     

Detection and differentiation of Xylella fastidiosa strains acquired and retained by glassy-winged sharpshooters (Hemiptera: Cicadellidae) using a mixture of strain-specific primer sets

Xylella fastidiosa Wells is a bacterial pathogen that causes a variety of plant diseases, including Pierce's disease (PD) of grapevine, almond leaf scorch, alfalfa dwarf, citrus variegated chlorosis, and oleander leaf scorch (OLS). Numerous strains of this pathogen have been genetically characterized, and several different strains occur in the United States. The dominant vector in southern California is the glassy-winged sharpshooter, Homalodisca coagulata (Say) (Hemiptera: Cicadellidae). The high mobility of this insect, and its use of large numbers of host plant species, provides this vector with ample exposure to multiple strains of X. fastidiosa during its lifetime. To learn more about the ability of this vector to acquire, retain, and transmit multiple strains of the pathogen, we developed a polymerase chain reaction (PCR)-based method to detect and differentiate strains of X. fastidiosa present in individual glassy-winged sharpshooter adults. Insects were sequentially exposed to plants infected with a PD strain in grapevine and an OLS strain in oleander. After sequential exposure, a few insects tested positive for both strains (7%); however, in most cases individuals tested positive for only one strain (29% PD, 41% OLS). In transmission studies, individual adults transmitted either the PD or OLS strain of the pathogen at a rate (39%) similar to that previously reported after exposure to a single strain, but no single individual transmitted both strains of the pathogen. PD and OLS strains of X. fastidiosa remained detectable in glassy-winged sharpshooter, even when insects were fed on a plant species that was not a host of the strain for 1 wk.     

Biological traits of Xylella fastidiosa strains from grapes and almonds

Xylella fastidiosa is a xylem-limited bacterium that causes various diseases, among them Pierce's disease of grapevine (PD) and almond leaf scorch (ALS). PD and ALS have long been considered to be caused by the same strain of this pathogen, but recent genetic studies have revealed differences among X. fastidiosa isolated from these host plants. We tested the hypothesis that ALS is caused by PD and ALS strains in the field and found that both groups of X. fastidiosa caused ALS and overwintered within almonds after mechanical inoculation. Under greenhouse conditions, all isolates caused ALS and all isolates from grapes caused PD. However, isolates belonging to almond genetic groupings did not cause PD in inoculated grapes but systemically infected grapes with lower frequency and populations than those belonging to grape strains. Isolates able to cause both PD and ALS developed 10-fold-higher concentrations of X. fastidiosa in grapes than in almonds. In the laboratory, isolates from grapes overwintered with higher efficiency in grapes than in almonds and isolates from almonds overwintered better in almonds than in grapes. We assigned strains from almonds into groups I and II on the basis of their genetic characteristics, growth on PD3 solid medium, and bacterial populations within inoculated grapevines. Our results show that genetically distinct strains from grapes and almonds differ in population behavior and pathogenicity in grapes and in the ability to grow on two different media.     

Genetic structure and biology of Xylella fastidiosa strains causing disease in citrus and coffee in Brazil

Xylella fastidiosa is a vector-borne, plant-pathogenic bacterium that causes disease in citrus (citrus variegated chlorosis [CVC]) and coffee (coffee leaf scorch [CLS]) plants in Brazil. CVC and CLS occur sympatrically and share leafhopper vectors; thus, determining whether X. fastidiosa isolates can be dispersed from one crop to another and cause disease is of epidemiological importance. We sought to clarify the genetic and biological relationships between CVC- and CLS-causing X. fastidiosa isolates. We used cross-inoculation bioassays and microsatellite and multilocus sequence typing (MLST) approaches to determine the host range and genetic structure of 26 CVC and 20 CLS isolates collected from different regions in Brazil. Our results show that citrus and coffee X. fastidiosa isolates are biologically distinct. Cross-inoculation tests showed that isolates causing CVC and CLS in the field were able to colonize citrus and coffee plants, respectively, but not the other host, indicating biological isolation between the strains. The microsatellite analysis separated most X. fastidiosa populations tested on the basis of the host plant from which they were isolated. However, recombination among isolates was detected and a lack of congruency among phylogenetic trees was observed for the loci used in the MLST scheme. Altogether, our study indicates that CVC and CLS are caused by two biologically distinct strains of X. fastidiosa that have diverged but are genetically homogenized by frequent recombination.     

A multigene phylogenetic study of clonal diversity and divergence in North American strains of the plant pathogen Xylella fastidiosa

Xylella fastidiosa is a pathogen that causes leaf scorch and related diseases in over 100 plant species, including Pierce's disease in grapevines (PD), phony peach disease (PP), plum leaf scald (PLS), and leaf scorch in almond (ALS), oak (OAK), and oleander (OLS). We used a high-resolution DNA sequence approach to investigate the evolutionary relationships, geographic variation, and divergence times among the X. fastidiosa isolates causing these diseases in North America. Using a large data set of 10 coding loci and 26 isolates, the phylogeny of X. fastidiosa defined three major clades. Two of these clades correspond to the recently identified X. fastidiosa subspecies piercei (PD and some ALS isolates) and X. fastidiosa subsp. multiplex (OAK, PP, PLS, and some ALS isolates). The third clade grouped all of the OLS isolates into a genetically distinct group, named X. fastidiosa subsp. sandyi. These well-differentiated clades indicate that, historically, X. fastidiosa has been a clonal organism. Based on their synonymous-site divergence ( approximately 3%), these three clades probably originated more than 15,000 years ago, long before the introduction of the nonnative plants that characterize most infections. The sister clades of X. fastidiosa subsp. sandyi and X. fastidiosa subsp. piercei have synonymous-site evolutionary rates 2.9 times faster than X. fastidiosa subsp. multiplex, possibly due to generation time differences. Within X. fastidiosa subsp. multiplex, a low level ( approximately 0.1%) of genetic differentiation indicates the recent divergence of ALS isolates from the PP, PLS, and OAK isolates due to host plant adaptation and/or allopatry. The low level of variation within the X. fastidiosa subsp. piercei and X. fastidiosa subsp. sandyi clades, despite their antiquity, suggests strong selection, possibly driven by host plant adaptation.     

Host heterogeneity in susceptibility and disease dynamics: tests of a mathematical model

Most mathematical models of disease assume that transmission is linearly dependent on the densities of host and pathogen. Recent data for animal diseases, however, have cast doubt on this assumption, without assessing the usefulness of alternative models. In this article, we use a combination of laboratory dose-response experiments, field transmission experiments, and observations of naturally occurring populations to show that virus transmission in gypsy moths is a nonlinear function of virus density, apparently because of heterogeneity among individual gypsy moth larvae in their susceptibility to the virus. Dose-response experiments showed that larvae from a laboratory colony of gypsy moths are substantially less heterogeneous in their susceptibility to the virus than are larvae from feral populations, and field experiments showed that there is a more strongly nonlinear relationship between transmission and virus density for feral larvae than for lab larvae. This nonlinearity in transmission changes the dynamics of the virus in natural populations so that a model incorporating host heterogeneity in susceptibility to the virus gives a much better fit to data on virus dynamics from large-scale field plots than does a classical model that ignores host heterogeneity. Our results suggest that heterogeneity among individuals has important effects on the dynamics of disease in insects at several spatial and temporal scales and that heterogeneity in susceptibility may be of general importance in the ecology of disease.     

Effect of host plant tissue on the vector transmission of grapevine leafroll-associated virus 3

Many biotic and abiotic factors affect the transmission efficiency of vector-borne plant pathogens. Insect vector within-plant distribution and host tissue preference are known to affect pathogen acquisition and inoculation rates. In this study, we first investigated whether feeding tissue affects the transmission of Grapevine leafroll-associated virus 3 by Planococcus ficus (Signoret) (Hemiptera: Pseudococcidae) and the effect of mealybug within-plant distribution on virus transmission under greenhouse conditions. Results showed no significant effect on transmission efficiency after insect confinement on leaf blades, petioles or stems of virus source or healthy test plants for either acquisition or inoculation trials. Transmission efficiency of a single mealybug varied from 4 to 25% in those trials. Second, we tested whether leaf position affected transmission efficiency due to potentially variable virus populations within acquisition plant tissues. No significant differences of transmission rate among acquisition leaf position were observed, probably because there were no differences in the virus population within source tissues. Finally, we examined the seasonality of the virus in field-collected samples and found that GLRaV-3 prevalence varied along a growing season, such that GLRaV-3 translocated along expanding shoots to leaves. Similarly, mealybug populations are known to increase in spring, and then mealybugs spread to cordons and leaves. This coordination of spatial and temporal dynamics of the virus and its vector may increase the risk of GLRaV-3 transmission during late spring and early summer. Further integration of information about pathogen populations in plants, vector feeding behavior and vector population seasonality could lead to more effective management practices.     

Use of a green fluorescent strain for analysis of Xylella fastidiosa colonization of Vitis vinifera

Xylella fastidiosa causes Pierce's disease of grapevine as well as several other major agricultural diseases but is a benign endophyte in most host plants. X. fastidiosa colonizes the xylem vessels of host plants and is transmitted by xylem sap-feeding insect vectors. To understand better the pattern of host colonization and its relationship to disease, we engineered X. fastidiosa to express a green fluorescent protein (Gfp) constitutively and performed confocal laser-scanning microscopic analysis of colonization in a susceptible host, Vitis vinifera. In symptomatic leaves, the fraction of vessels colonized by X. fastidiosa was fivefold higher than in nearby asymptomatic leaves. The fraction of vessels completely blocked by X. fastidiosa colonies increased 40-fold in symptomatic leaves and was the feature of colonization most dramatically linked to symptoms. Therefore, the extent of vessel blockage by bacterial colonization is highly likely to be a crucial variable in symptom expression. Intriguingly, a high proportion (>80%) of colonized vessels were not blocked in infected leaves and instead had small colonies or solitary cells, suggesting that vessel blockage is not a colonization strategy employed by the pathogen but, rather, a by-product of endophytic colonization. We present evidence for X. fastidiosa movement through bordered pits to neighboring vessels and propose that vessel-to-vessel movement is a key colonization strategy whose failure results in vessel plugging and disease.     

Evaluation of Arabidopsis thaliana as a model host for Xylella fastidiosa

The bacterium Xylella fastidiosa causes a number of plant diseases of significant economic impact. To date, progress determining mechanisms of host-plant susceptibility, tolerance, or resistance has been slow, due in large part to the long generation time and limited available genetic resources for grape, almond, and other known hosts of X. fastidiosa. To overcome many of these limitations, Arabidopsis thaliana has been evaluated as a host for X. fastidiosa. A pin-prick inoculation method has been developed to infect Arabidopsis with X. fastidiosa. Following infection, X. fastidiosa multiplies and can be detected by microscopy, polymerase chain reaction, and isolation. The ecotypes Van-0, LL-0, and Tsu-1 all allow more growth of strain X. fastidiosa Temecula than the reference ecotype Col-0. Affymetrix ATH1 microarray analysis of inoculated vs. noninoculated Tsu-1 reveals gene expression changes that differ greatly from changes seen after infection with apoplast-colonizing bacteria such as Psuedomonas syringae pvs. tomato or syringae. Many genes responsive to oxidative stress are differentially regulated, while classic pathogenesis-related genes are not induced by X. fastidiosa infection.     

Spatiotemporal Model of Barley and Cereal Yellow Dwarf Virus Transmission Dynamics with Seasonality and Plant Competition

Many generalist pathogens are influenced by the spatial distributions and relative abundances of susceptible host species. The spatial structure of host populations can influence patterns of infection incidence (or disease outbreaks), and the effects of a generalist pathogen on host community dynamics in a spatially heterogeneous community may differ from predictions derived via simple models. In this paper, we model the transmission of a generalist pathogen within a patch framework that incorporates the movement of vectors between discrete host patches to investigate the effects of local host community composition and vector movement rates on disease dynamics.     

Relative Susceptibility of Vitis vinifera Cultivars to Vector-Borne Xylella fastidiosa through Time

Understanding the interactions between pathogen, crop and vector are necessary for the development of disease control practices of vector-borne pathogens. For instance, resistant plant genotypes can help constrain disease symptoms due to infections and limit pathogen spread by vectors. On the other hand, genotypes susceptible to infection may increase pathogen spread owing to their greater pathogen quantity, regardless of their symptom status. In this study, we evaluated under greenhouse conditions the relative levels of resistance (i.e. relatively lower pathogen quantity) versus tolerance (i.e. less symptom severity) of 10 commercial grapevine (Vitis vinifera) cultivars to Pierce’s disease etiological agent, the bacterium Xylella fastidiosa. Overall, no correlation was detected between pathogen quantity and disease severity, indicating the existence of among-cultivar variation in plant response to infection. Thompson Seedless and Barbera were the two most susceptible among 10 evaluated cultivars. Rubired showed the least severe disease symptoms and was categorized as one of the most resistant genotypes in this study. However, within each cultivar the degree of resistance/tolerance was not consistent across sampling dates. These cultivar and temporal differences in susceptibility to infection may have important consequences for disease epidemiology and the effectiveness of management protocols.     

The Relationship between Host Lifespan and Pathogen Reservoir Potential: An Analysis in the System Arabidopsis thaliana-Cucumber mosaic virus

Identification of the determinants of pathogen reservoir potential is central to understand disease emergence. It has been proposed that host lifespan is one such determinant: short-lived hosts will invest less in costly defenses against pathogens, so that they will be more susceptible to infection, more competent as sources of infection and/or will sustain larger vector populations, thus being effective reservoirs for the infection of long-lived hosts. This hypothesis is sustained by analyses of different hosts of multihost pathogens, but not of different genotypes of the same host species. Here we examined this hypothesis by comparing two genotypes of the plant Arabidopsis thaliana that differ largely both in life-span and in tolerance to its natural pathogen Cucumber mosaic virus (CMV). Experiments with the aphid vector Myzus persicae showed that both genotypes were similarly competent as sources for virus transmission, but the short-lived genotype was more susceptible to infection and was able to sustain larger vector populations. To explore how differences in defense against CMV and its vector relate to reservoir potential, we developed a model that was run for a set of experimentally-determined parameters, and for a realistic range of host plant and vector population densities. Model simulations showed that the less efficient defenses of the short-lived genotype resulted in higher reservoir potential, which in heterogeneous host populations may be balanced by the longer infectious period of the long-lived genotype. This balance was modulated by the demography of both host and vector populations, and by the genetic composition of the host population. Thus, within-species genetic diversity for lifespan and defenses against pathogens will result in polymorphisms for pathogen reservoir potential, which will condition within-population infection dynamics. These results are relevant for a better understanding of host-pathogen co-evolution, and of the dynamics of pathogen emergence.     

VARIATION IN PATHOGENICITY AMONG AND WITHIN POPULATIONS OF THE FUNGUS PHOMOPSIS SUBORDINARIA INFECTING PLANTAGO LANCEOLATA

Pathogenicity of isolates of the fungus Phomopsis subordinaria, sampled in three scarcely or heavily infected populations of Plantago lanceolata, was investigated on three different host genotypes. The expression of the pathogen appeared to be quantitative rather than qualitative in character, which suggests polygenic inheritance of host susceptibility. Significant statistical interaction between pathogen and host pointed to some degree of physiological specialization between them. None of the individual host-pathogen combinations was found to contribute significantly to the interaction. Differences in mean pathogenicity between the pathogen populations could not explain the different intensities of disease observed in the field. As the variation in susceptibility between populations of the host at the same three locations also cannot account for the differences in intensity of disease in the field, it can be concluded that environmental factors (in particular weevils that spread the disease) are important for the development of the disease. In one of the populations, the spatial scale at which variation within the pathogen occurs was determined. It appeared that the pathogen varied in pathogenicity in the field, even among scapes within an individual host plant. The consequences of this scale of variation in the pathogen are discussed for the dynamics and evolution of the pathosystem.