Blocking the Transmission of a Noncirculative Vector-Borne Plant Pathogenic Bacterium.

The successful control of insect-borne plant pathogens is often difficult to achieve due to the ecologically complex interactions among pathogens, vectors, and host plants. Disease management often relies on pesticides and other approaches that have limited long-term sustainability. To add a new tool to control vector-borne diseases, we attempted to block the transmission of a bacterial insect-transmitted pathogen, the bacterium Xylella fastidiosa, by disrupting bacteria-insect vector interactions. X. fastidiosa is known to attach to and colonize the cuticular surface of the mouthparts of vectors; a set of recombinant peptides was generated and the chemical affinities of these peptides to chitin and related carbohydrates was assayed in vitro. Two candidates, the X. fastidiosa hypothetical protein PD1764 and an N-terminal region of the hemagglutinin-like protein B (HxfB) showed affinity for these substrates. These proteins were provided to vectors via an artificial diet system in which insects acquire X. fastidiosa, followed by an inoculation access period on plants under greenhouse conditions. Both PD1764 and HxfAD1-3 significantly blocked transmission. Furthermore, bacterial populations within insects over a 10-day period demonstrated that these peptides inhibited cell adhesion to vectors but not bacterial multiplication, indicating that the mode of action of these peptides is restricted to limiting cell adhesion to insects, likely via competition for adhesion sites. These results open a new venue in the search for sustainable disease-control strategies that are pathogen specific and may have limited nontarget effects

Blocking the Transmission of a Noncirculative Vector-Borne Plant Pathogenic Bacterium.

The successful control of insect-borne plant pathogens is often difficult to achieve due to the ecologically complex interactions among pathogens, vectors, and host plants. Disease management often relies on pesticides and other approaches that have limited long-term sustainability. To add a new tool to control vector-borne diseases, we attempted to block the transmission of a bacterial insect-transmitted pathogen, the bacterium Xylella fastidiosa, by disrupting bacteria-insect vector interactions. X. fastidiosa is known to attach to and colonize the cuticular surface of the mouthparts of vectors; a set of recombinant peptides was generated and the chemical affinities of these peptides to chitin and related carbohydrates was assayed in vitro. Two candidates, the X. fastidiosa hypothetical protein PD1764 and an N-terminal region of the hemagglutinin-like protein B (HxfB) showed affinity for these substrates. These proteins were provided to vectors via an artificial diet system in which insects acquire X. fastidiosa, followed by an inoculation access period on plants under greenhouse conditions. Both PD1764 and HxfAD1-3 significantly blocked transmission. Furthermore, bacterial populations within insects over a 10-day period demonstrated that these peptides inhibited cell adhesion to vectors but not bacterial multiplication, indicating that the mode of action of these peptides is restricted to limiting cell adhesion to insects, likely via competition for adhesion sites. These results open a new venue in the search for sustainable disease-control strategies that are pathogen specific and may have limited nontarget effects

Data from: Museum specimen data reveal emergence of a plant disease may be linked to increases in the insect vector population

The emergence rate of new plant diseases is increasing due to novel introductions, climate change, and changes in vector populations, posing risks to agricultural sustainability. Assessing and managing future disease risks depends on understanding the causes of contemporary and historical emergence events. Since the mid-1990s, potato growers in the western United States, Mexico, and Central America have experienced severe yield loss from Zebra Chip disease and have responded by increasing insecticide use to suppress populations of the insect vector, the potato psyllid, Bactericera cockerelli (Hemiptera: Triozidae). Despite the severe nature of Zebra Chip outbreaks, the causes of emergence remain unknown. We tested the hypotheses that 1) B. cockerelli occupancy has increased over the last century in California and 2) such increases are related to climate change, specifically warmer winters. We compiled a dataset of 87,000 museum specimen occurrence records across the order Hemiptera collected between 1900 and 2014. We then analyzed changes in B. cockerelli distribution using a hierarchical occupancy model using changes in background species lists to correct for collecting effort. We found evidence that B. cockerelli occupancy has increased over the last century. However, these changes appear to be unrelated to climate changes, at least at the scale of our analysis. To the extent that species occupancy is related to abundance, our analysis provides the first quantitative support for the hypothesis that B. cockerelli population abundance has increased, but further work is needed to link B. cockerelli population dynamics to Zebra Chip epidemics. Finally, we demonstrate how this historical macro-ecological approach provides a general framework for comparative risk assessment of future pest and insect vector outbreaks

Bayesian vector transmission model detects conflicting interactions from transgenic disease-resistant grapevines

Effective management of vector-borne plant pathogens often relies on disease-resistant cultivars. While heterogeneity in host resistance and in pathogen population density at the host population level plays important and well-recognized roles in epidemiology, the effects of resistance traits on pathogen distribution at the individual host level, and the epidemiological consequences in turn, are poorly understood. Transgenic disease-resistant plants that produce bacterial diffusible signaling factor (DSF) could provide resistance to the vector-borne bacterium Xylella fastidiosa by impeding plant colonization and reducing virulence. However, the effects of constitutive in planta production of DSF on insect vector transmission have remained unresolved. We investigated the transmission biology of X. fastidiosa in DSF and wild-type (WT) grapevines with the efficient vector Graphocephala atropunctata. We also developed a novel Bayesian hierarchical model to improve statistical inference on the multiple components of the vector transmission process. We found that insect vectors had a greater colonization efficiency on DSF plants—meaning they acquired a greater population size of X. fastidiosa—than on WT plants. However, DSF plants also maintained much lower X. fastidiosa populations. These apparently conflicting processes resulted in a lower but highly variable probability of transmission from DSF plants compared to WT plants. Our Bayesian model improved statistical inference compared to widely used frequentist statistics in part by estimating and correcting for imperfect detection of X. fastidiosa in plant and insect tissues. Overall, our results support current models on the roles that DSF plays in vector transmission of X. fastidiosa. In line with our hypothesis, DSF production reduced mean X. fastidiosa population density but increased heterogeneity within host plants. While DSF-producing plants could potentially improve disease management, our results suggest that they could, under some conditions, facilitate X. fastidiosa spread.Peer reviewe

Museum specimen data reveal emergence of a plant disease may be linked to increases in the insect vector population.

The emergence rate of new plant diseases is increasing due to novel introductions, climate change, and changes in vector populations, posing risks to agricultural sustainability. Assessing and managing future disease risks depends on understanding the causes of contemporary and historical emergence events. Since the mid-1990s, potato growers in the western United States, Mexico, and Central America have experienced severe yield loss from Zebra Chip disease and have responded by increasing insecticide use to suppress populations of the insect vector, the potato psyllid, Bactericera cockerelli (Hemiptera: Triozidae). Despite the severe nature of Zebra Chip outbreaks, the causes of emergence remain unknown. We tested the hypotheses that (1) B. cockerelli occupancy has increased over the last century in California and (2) such increases are related to climate change, specifically warmer winters. We compiled a data set of 87,000 museum specimen occurrence records across the order Hemiptera collected between 1900 and 2014. We then analyzed changes in B. cockerelli distribution using a hierarchical occupancy model using changes in background species lists to correct for collecting effort. We found evidence that B. cockerelli occupancy has increased over the last century. However, these changes appear to be unrelated to climate changes, at least at the scale of our analysis. To the extent that species occupancy is related to abundance, our analysis provides the first quantitative support for the hypothesis that B. cockerelli population abundance has increased, but further work is needed to link B. cockerelli population dynamics to Zebra Chip epidemics. Finally, we demonstrate how this historical macro-ecological approach provides a general framework for comparative risk assessment of future pest and insect vector outbreaks

Data from: Bayesian vector transmission model detects conflicting interactions from transgenic disease‐resistant grapevines

Vector transmission from DSF grapevines data set Data from vector transmission experiment for Xylella fastidiosa from DSF transgenic grapevines. File is an .rds file for loading directly into R. The file is a list of length 2. The first item in the list is metadata describing each variable of the data set, including total sample size. The second item is the data set itself. zeilinger_dsf_transmission_dataset.rdsEffective management of vector-borne plant pathogens often relies on disease-resistant cultivars. While heterogeneity in host resistance and in pathogen population density at the host population level play important and well-recognized roles in epidemiology, the effects of resistance traits on pathogen distribution at the individual host level, and the epidemiological consequences in turn, are poorly understood. Transgenic disease-resistant plants that produce bacterial Diffusible Signaling Factor (DSF) could provide resistance to the vector-borne bacterium Xylella fastidiosa by impeding plant colonization and reducing virulence. However, the effects of constitutive in planta production of DSF on insect vector transmission has remained unresolved. We investigated the transmission biology of X. fastidiosa in DSF and wild-type (WT) grapevines with the efficient vector Graphocephala atropunctata. We also developed a novel Bayesian hierarchical model to improve statistical inference on the multiple components of the vector transmission process. We found that insect vectors had a greater colonization efficiency on DSF plants—meaning they acquired a greater population size of X. fastidiosa—than on WT plants. However, DSF plants also maintained much lower X. fastidiosa populations. These apparently conflicting processes resulted in a lower but highly variable probability of transmission from DSF plants compared to WT plants. Our Bayesian model improved statistical inference compared to widely used frequentist statistics in part by estimating and correcting for imperfect detection of X. fastidiosa in plant and insect tissues. Overall, our results support current models on the roles that DSF plays in vector transmission of X. fastidiosa. In line with our hypothesis, DSF production reduced mean X. fastidiosa population density but increased heterogeneity within host plants. While DSF-producing plants could potentially improve disease management, our results suggest that they could, under some conditions, facilitate X. fastidiosa spread.Peer reviewe

Transmission of Xylella fastidiosa to Grapevine by the Meadow Spittlebug

There is little information available on Xylella fastidiosa transmission by spittlebugs (Hemiptera, Cercopoidea). This group of insect vectors may be of epidemiological relevance in certain diseases, so it is important to better understand the basic parameters of X. fastidiosa transmission by spittlebugs. We used grapevines as a host plant and the aphrophorid Philaenus spumarius as a vector to estimate the effect of plant access time on X. fastidiosa transmission to plants; in addition, bacterial population estimates in the heads of vectors were determined and correlated with plant infection status. Results show that transmission efficiency of X. fastidiosa by P. spumarius increased with plant access time, similarly to insect vectors in another family (Hemiptera, Cicadellidae). Furthermore, a positive correlation between pathogen populations in P. spumarius and transmission to plants was observed. Bacterial populations in insects were one to two orders of magnitude lower than those observed in leafhopper vectors, and population size peaked within 3 days of plant access period. These results suggest that P. spumarius has either a limited number of sites in the foregut that may be colonized, or that fluid dynamics in the mouthparts of these insects is different from that in leafhoppers. Altogether our results indicate that X. fastidiosa transmission by spittlebugs is similar to that by leafhoppers. In addition, the relationship between cell numbers in vectors and plant infection may have under-appreciated consequences to pathogen spread

A chitinase is required for Xylella fastidiosa colonization of its insect and plant hosts

Xylella fastidiosa colonizes the xylem network of host plant species as well as the foregut of its required insect vectors to ensure efficient propagation. Disease management strategies remain inefficient due to a limited comprehension of the mechanisms governing both insect and plant colonization. It was previously shown that X. fastidiosa has a functional chitinase (ChiA), and that chitin likely serves as a carbon source for this bacterium. We expand on that research, showing that a chiA mutant strain is unable to grow on chitin as the sole carbon source. Quantitative PCR assays allowed us to detect bacterial cells in the foregut of vectors after pathogen acquisition; populations of the wild-type and complemented mutant strain were both significantly larger than the chiA mutant strain 10 days, but not 3 days, post acquisition. These results indicate that adhesion of the chiA mutant strain to vectors may not be impaired, but that cell multiplication is limited. The mutant was also affected in its transmission by vectors to plants. In addition, the chiA mutant strain was unable to colonize host plants, suggesting that the enzyme has other substrates associated with plant colonization. Lastly, ChiA requires other X. fastidiosa protein(s) for its in vitro chitinolytic activity. The observation that the chiA mutant strain is not able to colonize plants warrants future attention to be paid to the substrates for this enzyme

Plant defense against a pathogen drives nonlinear transmission dynamics through both vector preference and acquisition

Abstract Host defense against vector‐borne plant pathogens is a critical component of integrated disease management. However, theory predicts that traits that confer tolerance or partial resistance can, under certain ecological conditions, enhance the spread of pathogens and spillover to more susceptible populations or cultivars. A key component driving such epidemic risk appears to be variation in host‐selection behavior of vectors based on infection status of the host. While recent theory has further emphasized the importance of infection‐induced host‐selection behavior by insect vectors for plant disease epidemiology, experimental tests on the relationship between vector host‐selection preference and transmission are lacking. We test how host plant defense—conferred by the PdR1 gene complex—mediates vector host‐selection preference and transmission of the pathogenic bacterium Xylella fastidiosa among grapevine cultivars. We confirmed that PdR1 confers resistance against X. fastidiosa by reducing both pathogen population size and disease severity. We found that vector transmission rates to new hosts exhibited unimodal dynamics over the course of infection when both susceptible and resistant were infected and acted as sources of the pathogen. Transmission from susceptible plants initially increased and then declined as insect vectors avoided severely diseased plants. While transmission from PdR1‐resistant plants also initially increased and then declined as well, this was not due to avoidance by vectors, although the exact mechanism remains unclear. We show that (1) vector preference changes over the course of disease progression, (2) vector preference is clearly important but a poor predictor of transmission, and (3) the post‐latent incubation period—in which plant hosts are infectious but asymptomatic—is likely a key period for vector transmission of X. fastidiosa. Our results suggest that, consistent with theory, defensive traits lengthen the duration of the incubation period, increasing X. fastidiosa transmission. However, defensive traits may over the long‐term ultimately reduce spread possibly through induced resistance. Vector host‐selection preference, host resistance, and transmission are clearly dynamic, changing over the course of disease progression. Understanding these dynamics is critical for broader insights into the epidemiology of vector‐borne plant pathogens, theory development, and deploying disease‐resistant cultivars in an effective and sustainable manner