The genome of the thin-necked bladder worm Taenia hydatigena reveals evolutionary strategies for helminth survival

Taenia hydatigena is a widespread gastrointestinal helminth that causes significant health problems in livestock industry. This parasite can survive in a remarkably wide range of intermediate hosts and affects the transmission dynamics of zoonotic parasites. T. hydatigena is therefore of particular interest to researchers interested in studying zoonotic diseases and the evolutionary strategies of parasites. Herein we report a high-quality draft genome for this tapeworm, characterized by some hallmarks (e.g., expanded genome size, wide integrations of viral-like sequences and extensive alternative splicing during development), and specialized adaptations related to its parasitic fitness (e.g., adaptive evolutions for teguments and lipid metabolism). Importantly, in contrast with the evolutionarily close trematodes, which achieve gene diversification associated with immunosuppression by gene family expansions, in T. hydatigena and other cestodes, this is accomplished by alternative splicing and gene loss. This indicates that these two classes have evolved different mechanisms for survival. In addition, molecular targets for diagnosis and intervention were identified to facilitate the development of control interventions. Overall, this work uncovers new strategies by which helminths evolved to interact with their hosts.

High Relative Parasitic Fitness of G22 Derivatives is Associated with the Epidemic Potential of Wheat Stripe Rust in China

In total, 13 commercial wheat cultivars around China and four races of Puccinia striiformis f. sp. tritici (namely, CYR32, CYR33, G22-9, and G22-14) were employed for a test of relative parasitic fitness (RPF) using the drop method. The RPF values were measured, including the urediniospore germination rate, the latent period, the uredinial length, the uredinial density, the infection area, the sporulation intensity, the lesion expansion speed, and the sporulation period. The results indicated that the parameters of relative parasitic fitness of the four P. striiformis f. sp. tritici races on the 13 wheat cultivars were significantly different (P = 0.00) in sporulation intensity, lesion expansion speed, uredinial length, sporulation period, uredinial density, and latent period. The urediniospore germination rates of the four P. striiformis f. sp. tritici races for the test were significantly different (P = 0.00), whereas no correlation with the different cultivars was observed (P = 1.00). The infection areas of the tested races on the different cultivars were significantly different (P = 0.00) but there were no obvious manifestations among the various races (P = 0.20). Principal component analysis (PCA) showed that the sporulation intensity represented sporulation capacity and scalability, the latent period indicated infection ability, and the urediniospore germination rate represented urediniospore vigor, all of which fully contributed to the RPF in the interaction of the four races and 13 wheat cultivars, which was calculated by the following formula: RPF = (sporulation intensity × urediniospore germination rate)/latent period. The sporulation and infection of G22-9 on the 13 large-scale cultivated cultivars were the highest, and the RPF of G22-9 was higher than that of the predominant races, CYR32 and CYR33. This result suggested that G22-9 could become a new predominant race and potentially cause epidemics of wheat stripe rust in China. To prevent potential epidemics, susceptible wheat cultivars should be withdrawn from production and breeding programs should reduce the use of Yr10 and Yr26 and use other more effective resistance genes in combination with nonrace-specific resistance for developing wheat cultivars with durable resistance to stripe rust.

Parasitic Fitness of Fungicide-Resistant and -Sensitive Isolates of Alternaria solani

Resistance to chemistries of the succinate dehydrogenase inhibiting (SDHI) and quinone outside inhibiting (QoI) fungicides has developed rapidly in populations of Alternaria solani, the cause of early blight of potato. Reduced sensitivity to the anilinopyrimidine (AP) fungicide pyrimethanil has also been identified recently, determining that resistance to three chemical classes of fungicides is present within the A. solani population. Although no mutations have been characterized to confer resistance to APs, in A. solani five point mutations on three AsSdh genes have been determined to convey resistance to SDHIs, and the substitution of phenylalanine with leucine at position 129 (F129L) in the cytb gene confers resistance to QoIs. The objective of this study was to investigate the parasitic fitness of A. solani isolates with resistance to one or more of these chemical classes. A total of 120 A. solani isolates collected from various geographical locations around the United States were chosen for in vitro assessment, and 60 of these isolates were further evaluated in vivo. Fitness parameters measured were (i) spore germination in vitro, (ii) mycelial expansion in vitro, and (iii) aggressiveness in vivo. No significant differences in spore germination or mycelial expansion (P = 0.44 and 0.51, respectively) were observed among wild-type and fungicide-resistant isolates in vitro. Only A. solani isolates possessing the D123E mutation were shown to be significantly more aggressive in vivo (P < 0.0001) compared with wild-type isolates. These results indicate that fungicide-resistant A. solani isolates have no significant fitness penalties compared with sensitive isolates under the parameters evaluated regardless of the presence or absence of reduced sensitivity to multiple chemical classes. Results of these studies suggest that A. solani isolates with multiple fungicide resistances may compete successfully with wild-type isolates under field conditions.

Spatial and Temporal Distribution of Mutations Conferring QoI and SDHI Resistance in Alternaria solani Across the United States

The application of succinate dehydrogenase inhibiting (SDHI) and quinone outside inhibiting (QoI) fungicide chemistries is a primary tactic in the management of early blight of potato, caused by Alternaria solani. Resistance to QoIs in A. solani has been attributed to the F129L mutation, while resistance to SDHIs is conferred by five different known point mutations on three AsSdh genes. In total, 1,323 isolates were collected from 2013 through 2015 across 11 states to determine spatial and temporal frequency distribution of these mutations. A real-time polymerase chain reaction (PCR) was used to detect the presence of the F129L mutation. Molecular detection of SDHI-resistant isolates was performed using SDH multiplex PCR specific for point mutations in AsSdhB, AsSdhC, or AsSdhD genes and mismatch amplification analysis PCR detecting the point mutations in AsSdhB. Previous work in our research group determined that substitutions of histidine for tyrosine (H278Y) or arginine (H278R) at codon 278 on the AsSdhB gene were the most prevalent mutations, detected in 46 and 21% of A. solani isolates, respectively, collected in 2011 to 2012, and uniformly distributed among six sampled states. In contrast, the substitution of histidine for arginine (H134R) at codon 134 in the AsSdhC gene was the most prevalent mutation in 2013 through 2015, identified in 36% of isolates, compared with 7.5% of isolates recovered in 2011 to 2012. Substitutions of histidine for arginine (H133R) at codon 133 and aspartic acid for glutamic acid (D123E) at codon 123 in the AsSdhD gene were detected in 16 and 12%, respectively, in the A. solani population by 2015 and were recovered across a wide range of states, compared with 15 and 1.5% of isolates collected in 2011 to 2012, respectively. Overall, SDHI- and QoI-resistant isolates were detected at high frequencies across all years, with evidence of significant spatial variability. Future research will investigate whether these results are due to differences in parasitic fitness.

Competitive Parasitic Fitness of Mefenoxam-Sensitive and -Resistant Isolates of Phytophthora erythroseptica under Fungicide Selection Pressure

A 2-year field and laboratory experiment was initiated to study the competitive parasitic fitness of mefenoxam-resistant (50% effective concentration [EC50] > 100 μg ml–1) and mefenoxam-sensitive (EC50 = 0.07 μg ml–1) isolates of Phytophthora erythroseptica with equal aggressiveness. The competitive ability of the mefenoxam-resistant and -sensitive isolates was tested under no selection pressure (nonfungicide treated) as well as under the influence of mefenoxam and non-mefenoxam (phosphorous acid) fungicides. P. erythroseptica isolates were combined in four ratios of mefenoxam-resistant (R) to mefenoxam-susceptible (S) (0R:0S, 1R:1S, 3R:1S, and 1R:3S) and subsequently infested into the soil at the time of planting. In-furrow mefenoxam applications were applied to the soil immediately following infestation with P. erythroseptica. Phosphorous acid was applied at tuber initiation and 14 days after tuber initiation. Noninfested, nonfungicide-treated plots served as controls. P. erythroseptica isolates recovered from field-infected pink rot tubers at harvest and 3 to 4 weeks after harvest were tested for mefenoxam sensitivity in vitro. In vivo studies were performed by challenge inoculating a zoospore suspension in the four ratios described above onto potato tubers harvested from nontreated, phosphorous acid-treated, or mefenoxam-treated field plots. These field plots were not infested with P. erythroseptica at planting. Results from both field and in vivo studies demonstrate that mefenoxam-resistant isolates of P. erythroseptica are as fit as sensitive isolates in the absence of selection pressure or in the presence of a phosphorous acid fungicide treatment. Under mefenoxam selection pressure, mefenoxam-resistant P. erythroseptica isolates were more parasitically fit than -sensitive isolates. These studies suggest the lack of an apparent fitness penalty in mefenoxam-resistant P. erythroseptica populations under field conditions and that these isolates could be stable in most agroecological systems. Based on these results, mefenoxam-based fungicides are no longer recommended for the management of pink rot once mefenoxam-resistant P. erythroseptica populations are detected in a specific field.