Exploring the causes of small effective population sizes in cyst nematodes using artificial Globodera pallida populations.

The effective size of a population is the size of an ideal population which would undergo genetic drift at the same rate as the real population. The balance between selection and genetic drift depends on the effective population size ( Ne), rather than the real numbers of individuals in the population ( N). The objectives of the present study were to estimate Ne in the potato cyst nematode Globodera pallida and to explore the causes of a low Ne/ N ratio in cyst nematodes using artificial populations. Using a temporal analysis of 24 independent populations, the median Ne was 58 individuals (min Ne = 25 and max Ne = 228). Ne is commonly lower than N but in the case of cyst nematodes, the Ne/ N ratio was extremely low. Using artificial populations showed that this low ratio did not result from migration, selection and overlapping generations, but could be explain by the fact that G. pallida populations deviate in structure from the assumptions of the ideal population by having unequal sex ratios, high levels of inbreeding and a high variance in family sizes. The consequences of a low Ne, resulting in a strong intensity of genetic drift, could be important for their control because G. pallida populations will have a low capacity to adapt to changing environments.

The coexistence of generalist and specialist clonal lineages in natural populations of the Irish Famine pathogen Phytophthora infestans explains local adaptation to potato and tomato.

Phytophthora infestans, causing late blight on Solanaceae, is a serious threat to potato and tomato crops worldwide. P. infestans populations sampled on either potato or tomato differ in genotypes and pathogenicity, suggesting niche exclusion in the field. We hypothesized that such niche separation can reflect differential host exploitation by different P. infestans genotypes. We thus compared genotypes and phenotypes in 21 isolates sampled on potato (n = 11) or tomato (n = 10). Typing at 12 microsatellite loci assigned potato isolates to the 13_A2, 6_A1 and 1_A1 lineages, and tomato isolates to the 23_A1, 2_A1 and unclassified multilocus genotypes. Cross-inoculations on potato and tomato leaflets showed that all isolates were pathogenic on both hosts. However, tomato isolates performed much better on tomato than did potato isolates, which performed better on potato than did tomato isolates, thus revealing a clear pattern of local adaptation. Potato isolates were significantly fitter on potato than on tomato, and are best described as potato specialists; tomato isolates appear to be generalists, with similar pathogenicity on both hosts. Niche separation in the field may thus result mainly from the large fitness gap on tomato between generalists and unadapted potato specialists, while the small, but significant fitness difference on potato between both types of isolates may prevent population invasion by generalists. Extreme specialization to potato seems very costly relative to performance loss on the alternative host. This study therefore shows that local adaptation and niche separation, commonly expected to involve and generate specialists, can occur with generalists.

The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals insights into the basis of parasitism and virulence.

BACKGROUND: The yellow potato cyst nematode, Globodera rostochiensis, is a devastating plant pathogen of global economic importance. This biotrophic parasite secretes effectors from pharyngeal glands, some of which were acquired by horizontal gene transfer, to manipulate host processes and promote parasitism. G. rostochiensis is classified into pathotypes with different plant resistance-breaking phenotypes. RESULTS: We generate a high quality genome assembly for G. rostochiensis pathotype Ro1, identify putative effectors and horizontal gene transfer events, map gene expression through the life cycle focusing on key parasitic transitions and sequence the genomes of eight populations including four additional pathotypes to identify variation. Horizontal gene transfer contributes 3.5 % of the predicted genes, of which approximately 8.5 % are deployed as effectors. Over one-third of all effector genes are clustered in 21 putative 'effector islands' in the genome. We identify a dorsal gland promoter element motif (termed DOG Box) present upstream in representatives from 26 out of 28 dorsal gland effector families, and predict a putative effector superset associated with this motif. We validate gland cell expression in two novel genes by in situ hybridisation and catalogue dorsal gland promoter element-containing effectors from available cyst nematode genomes. Comparison of effector diversity between pathotypes highlights correlation with plant resistance-breaking. CONCLUSIONS: These G. rostochiensis genome resources will facilitate major advances in understanding nematode plant-parasitism. Dorsal gland promoter element-containing effectors are at the front line of the evolutionary arms race between plant and parasite and the ability to predict gland cell expression a priori promises rapid advances in understanding their roles and mechanisms of action.

And the nasty ones lose in the end: foliar pathogenicity trades off with asexual transmission in the Irish famine pathogen Phytophthora infestans.

A trade-off between pathogenicity and transmission is often postulated to explain the persistence of pathogens over time. If demonstrated, it would help to predict the evolution of pathogenicity across cropping seasons, and to develop sustainable control strategies from this prediction. Unfortunately, experimental demonstration of such trade-offs in agricultural plant pathogens remains elusive. We measured asexual transmission of Phytophthora infestans isolates differing in pathogenicity in two sets of artificial infection experiments under controlled, semi-outdoor conditions. Higher foliar pathogenicity decreased mean daughter tuber weight, increased infection severity in daughter tubers, and increased stem mortality before emergence. The most pathogenic isolates thus suffer a double penalty for asexual transmission: a lower survival probability within small and severely infected tubers; and a lower infection probability of neighbouring healthy plants due to fewer infected stems produced by surviving tubers. Moderate tuber resistance favoured transmission of the least pathogenic isolates, while high levels of resistance almost abolished transmission of all isolates. These data demonstrate a trade-off between foliar pathogenicity and asexual transmission over seasons in P. infestans, which should stabilise pathogenicity over time in the potato late blight pathosystem and possibly favour clone replacement by less pathogenic lineages after demographic bottlenecks.

Heterozygote deficits in cyst plant-parasitic nematodes: possible causes and consequences.

Deviations of genotypic frequencies from Hardy-Weinberg equilibrium (HWE) expectations could reveal important aspects of the biology of populations. Deviations from HWE due to heterozygote deficits have been recorded for three plant-parasitic nematode species. However, it has never been determined whether the observed deficits were due (i) to the presence of null alleles, (ii) to a high level of consanguinity and/or (iii) to a Wahlund effect. The aim of the present work was, while taking into the possible confounding effect of null alleles, to disentangle consanguinity and Wahlund effect in natural populations of those three economically important cyst nematodes using microsatellite markers: Globodera pallida, G. tabacum and Heterodera schachtii, pests of potato, tobacco and sugar beet, respectively. The results show a consistent pattern of heterozygote deficiency in the three nematode species sampled at the spatial scale of the host plant. We demonstrate that the prevalence of null alleles is weak and that heterozygote deficits do not have a single origin. Our results suggested that it is restricted dispersal that leads to heterozygote deficits through both consanguinity and substructure, which effects can be linked to soil movement, cyst density, and the number of generations per year. We discuss potential implications for the durability of plant resistances that are used to protect crops against parasites in which mating between relatives occur. While consanguineous mating leads to homozygosity at all loci, including loci governing avirulence/virulence, which favours the expression of virulence when recessive, the Wahlund effect is expected to have no particular effect on the adaptation of nematodes to resistances.

Genetic diversity of the golden potato cyst nematode Globodera rostochiensis and determination of the origin of populations in Quebec, Canada.

The golden cyst nematode (Globodera rostochiensis), native to South America, has been introduced in many parts of the world, including Europe and North America. Recently, it was found for the first time in the province of Quebec, Canada in the locality of St. Amable near Montreal. To date, very few studies have examined the population genetics of this pest. Consequently, there is a lack of knowledge about the genetic structure and evolution of this nematode. In this study, twelve new microsatellite markers were developed in order to explore these questions. These markers were used to genotype fifteen populations originating from different regions of the world, including five from Canada. Within populations, the highest genetic diversity was consistently observed in the populations from Bolivia, the postulated region of origin of the golden nematode, and the lowest in populations from British Columbia (Canada) and New York (USA). The two Quebec populations were very similar to each other and to the population found in Newfoundland, but surprisingly, they were significantly different from three other North American populations including those from New York and British Columbia. Based on our results, we conclude that the golden cyst nematode has been introduced in North America at least twice from distinct regions of the world.

Fitness costs associated with unnecessary virulence factors and life history traits: evolutionary insights from the potato late blight pathogen Phytophthora infestans.

BACKGROUND: In gene-for-gene models of plant-pathogen interactions, the existence of fitness costs associated with unnecessary virulence factors still represents an issue, both in evolutionary biology and agricultural sciences. Measuring such costs experimentally has proven difficult, especially in pathogens not readily amenable to genetic transformation, since the creation of isogenic lines differing only by the presence or absence of avirulence genes cannot be achieved in many organisms. Here, we circumvented this difficulty by comparing fitness traits in groups of Phytophthora infestans isolates sharing the same multilocus fingerprint, but differing by their virulence/avirulence spectrum. RESULTS: Fitness was assessed from calculations derived from the basic reproduction number, combining several life history traits (latent period, spore density and lesion growth rate) evaluated on leaflets of the potato cultivar Bintje, which is free of resistance genes. A statistically significant fitness cost was found in isolates virulent to the R10 resistance gene. That cost was due to a lower spore production in virulent isolates; however, the latent period was shorter in virulent isolates. Similar trends, although not statistically significant, were observed for the other genes tested. CONCLUSION: The data likely reflect the adaptive response of the pathogen to the cost associated with virulence. They suggest strong trade-offs between life history traits related to pathogenicity and adaptive biology of pathogens.