Frequency Of Virulence Alleles Research Articles

Combining Masculinizing Resistance, Rotation, and Biocontrol to Achieve Durable Suppression of the Potato Pale Cyst Nematode: A Model

ABSTRACTThe pale cyst nematode, Globodera pallida, is a pest that poses a significant threat to potato crops worldwide. The most effective chemical nematicides are toxic to nontarget organisms and are now banned. Alternative control methods are therefore required. Crop rotation and biological control methods have limitations for effectively managing nematodes. The use of genetically resistant cultivars is a promising alternative, but nematode populations evolve, and virulent mutants can break resistance after just a few years. Masculinizing resistances, preventing avirulent nematodes from producing females, might be more durable than blocking resistances, preventing infection. Our demo‐genetic model, tracking both nematode population densities and virulence allele frequencies, shows that virulence against masculinizing resistance may not be fixed in the pest population under realistic agricultural conditions. Avirulence may persist despite the uniform use of resistance. This is because avirulent male nematodes may transmit avirulent alleles to their progeny by mating with virulent females. Additionally, because avirulent nematodes do not produce females themselves, they weaken the reproductive rate of the nematode population, leading to a reduction in its density by at least 20%. This avirulence load can even lead to the collapse of the nematode population in theory. Overall, our model showed that combining masculinizing resistance, rotation, and biocontrol may achieve durable suppression of G. pallida in a reasonable time frame. Our work is supported by an online interactive interface allowing users (i.e., growers, plant health authorities, researchers) to test their own control combinations.

Short communication: Virulence of barley leaf rust in the South of Russia in 2017-2019

Aim of study: To analyze the structure of Puccinia hordei populations by virulence in southern Russia during 2017-2019. Area of study: South of Russia, the leading Russian region for barley production where barley leaf rust is an important foliar disease. Material and methods: Uredinial samples of P. hordei were collected at the production sites of winter barley in the south of Russia. Single uredinial isolates (total 95) were tested for virulence with 17 differentials with Rph resistance genes. Main results: No isolates were found virulent to the host line with the Rph13 gene. There was a decrease in the number of fungal isolates virulent to the host lines with Rph5 and Rph7 genes. In 2017 and 2019, isolates containing a large number of virulence alleles (from 11 to 15) prevailed. In 2018, isolates with low (1-5) and medium (6-10) frequency of virulent alleles prevailed, as well as avirulent isolates. The values of the Nei index via diversity showed high similarity of the pathogen populations in 2017-2018 (N = 0.05) and minor differences in 2017-2019 and 2018-2019 (N = 0.13 and 0.16, respectively). The greatest frequency of virulence alleles in accordance with the Nei (Hs) index was noted for the 2018 population (Hs = 0.36). For the 2017 and 2019 populations, this indicator was on average Hs = 0.29 and 0.20, respectively. Research highlights: Analysis of genetics of the P. hordei population is important for the strategy of varietal distribution in the region and development of rust-resistant cultivars.

Rotating and stacking genes can improve crop resistance durability while potentially selecting highly virulent pathogen strains

Rotating crop cultivars with different resistance genes could slow the evolution of virulent strains of fungal pathogens, but could also produce highly virulent pathogen strains. We present a new model that links polycyclic pathogen epidemiology and population genetics in order to predict how different strategies of rotating cultivars with different resistances will affect the evolution of pathogen virulence and the breakdown of crop resistance. We modelled a situation where there were four different resistance genes that can be deployed within each crop cultivar, and four virulence genes that may be present within the pathogen. We simulated four different rotational management strategies: (i) no rotation; (ii) a different gene every year; (iii) a different gene every 5 years; and (iv) a different combination of two stacked genes each year. Results indicate that rotating cultivars can lead to longer periods of disease suppression but also to the selection of highly virulent strains. The efficacy and relative advantage of different resistant cultivar rotation strategies depended on the fitness penalties, initial virulence allele frequencies, and ability of non-virulent pathogen genotypes to grow and reproduce on resistant cultivars. By capturing the essential processes involved, our model provides a useful new tool for investigating the evolutionary dynamics of pathogen virulence and crop resistance breakdown.

Reduced Fitness of Virulent Aphis glycines (Hemiptera: Aphididae) Biotypes May Influence the Longevity of Resistance Genes in Soybean

Sustainable use of insect resistance in crops require insect resistance management plans that may include a refuge to limit the spread of virulence to this resistance. However, without a loss of fitness associated with virulence, a refuge may not prevent virulence from becoming fixed within a population of parthenogenetically reproducing insects like aphids. Aphid-resistance in soybeans (i.e., Rag genes) prevent outbreaks of soybean aphid (Aphis glycines), yet four biotypes defined by their capacity to survive on aphid-resistant soybeans (e.g., biotype-2 survives on Rag1 soybean) are found in North America. Although fitness costs are reported for biotype-3 on aphid susceptible and Rag1 soybean, it is not clear if virulence to aphid resistance in general is associated with a decrease in fitness on aphid susceptible soybeans. In laboratory assays, we measured fitness costs for biotype 2, 3 and 4 on an aphid-susceptible soybean cultivar. In addition, we also observed negative cross-resistance for biotype-2 on Rag3, and biotype-3 on Rag1 soybean. We utilized a simple deterministic, single-locus, four compartment genetic model to account for the impact of these findings on the frequency of virulence alleles. When a refuge of aphid susceptible was included within this model, fitness costs and negative cross-resistance delayed the increase of virulence alleles when virulence was inherited recessively or additively. If virulence were inherited additively, fitness costs decreased the frequency of virulence. Combined, these results suggest that a refuge may prevent virulent A. glycines biotypes from overcoming Rag genes if this aphid-resistance were used commercially in North America.

Effect of rotation of canola (Brassica napus) cultivars with different complements of blackleg resistance genes on disease severity

Blackleg disease (phoma stem canker) caused by the fungus Leptosphaeria maculans is a major disease of canola (oilseed rape, Brassica napus) worldwide. Canola plants in pots were exposed to blackleg‐infested stubble of canola with different complements of resistance genes and then assessed for disease. Plant mortality was reduced when plants were exposed to stubble from a cultivar with a different complement of resistance genes compared to stubble of a cultivar with the same resistance gene. These findings were consistent with 7 years of field surveys, which showed that changes in selection pressure as a result of extensive sowing of cultivars with major‐gene resistance, termed ‘sylvestris resistance’, dramatically influenced the frequency of virulent isolates in the population towards particular resistance genes, and therefore disease severity. All these data were supported by PCR‐genotyping surveys of fungal populations whereby the frequency of virulence alleles of avirulence genes AvrLm1 and AvrLm4 changed significantly depending on the resistance gene present in the cultivar from which the isolates were cultured. This is the first example of a study showing that sowing of canola cultivars with different complements of resistance genes in subsequent years, i.e. rotation of resistance genes, minimizes disease pressure by manipulating fungal populations. This approach provides a valuable disease management strategy for canola growers and is likely to be applicable to other plant diseases.

Evolution of linked avirulence effectors in Leptosphaeria maculans is affected by genomic environment and exposure to resistance genes in host plants.

Brassica napus (canola) cultivars and isolates of the blackleg fungus, Leptosphaeria maculans interact in a ‘gene for gene’ manner whereby plant resistance (R) genes are complementary to pathogen avirulence (Avr) genes. Avirulence genes encode proteins that belong to a class of pathogen molecules known as effectors, which includes small secreted proteins that play a role in disease. In Australia in 2003 canola cultivars with the Rlm1 resistance gene suffered a breakdown of disease resistance, resulting in severe yield losses. This was associated with a large increase in the frequency of virulence alleles of the complementary avirulence gene, AvrLm1, in fungal populations. Surprisingly, the frequency of virulence alleles of AvrLm6 (complementary to Rlm6) also increased dramatically, even though the cultivars did not contain Rlm6. In the L. maculans genome, AvrLm1 and AvrLm6 are linked along with five other genes in a region interspersed with transposable elements that have been degenerated by Repeat-Induced Point (RIP) mutations. Analyses of 295 Australian isolates showed deletions, RIP mutations and/or non-RIP derived amino acid substitutions in the predicted proteins encoded by these seven genes. The degree of RIP mutations within single copy sequences in this region was proportional to their proximity to the degenerated transposable elements. The RIP alleles were monophyletic and were present only in isolates collected after resistance conferred by Rlm1 broke down, whereas deletion alleles belonged to several polyphyletic lineages and were present before and after the resistance breakdown. Thus, genomic environment and exposure to resistance genes in B. napus has affected the evolution of these linked avirulence genes in L. maculans.

Pedigreed crosses to estimate recessive virulence allele frequencies in natural populations of gall midges

AbstractMonitoring changes in rare, recessive allele frequencies in natural populations can be accomplished using pedigreed individuals sampled from these populations. A pedigree keeps track of and limits the mating of sampled individuals, to preserve information about the genotype of the sampled individual in the phenotypes of its descendents. To estimate allele frequencies in a natural population using pedigreed crosses, four relations must be specified: (1) a method to determine whether the pedigreed line carries the desired allele; (2) a method to estimate the phenotypic frequency of the trait among the pedigreed lines and a credibility limit for the estimate; (3) the genetic relation between the phenotype frequency among the lines and the allele frequency in the natural population; and (4) a method to estimate the probability that the first method did not detect the trait, assuming that the allele was present in the sampled individual. Knowledge about the segregation patterns of the allele enables specification of (3) and (4). Bayesian statistics were used to estimate the phenotypic frequency of the trait among the pedigreed lines. The method determining whether the pedigreed line carries the desired allele will vary with the species and trait of concern. We focused on monitoring of vGm1, a recessive autosomal allele, and vGm2, a recessive sex‐linked allele, which provide virulence against certain rice resistance genes in rice gall midge, Orseolia oryzae (Wood‐Mason) (Diptera: Cecidomyiidae). We show how three pedigrees can be used to estimate these allele frequencies. An F1 field screen challenges the F1 offspring of sampled individuals on the rice differentials. A P1 test‐cross mates the sampled individual with a homozygous lab colony for the allele of interest, and evaluates their offspring on the rice differentials. A conditional F1 test‐cross takes the offspring from pedigrees that were negative in an F1 field screen, and test‐crosses these offspring with the homozygous laboratory colony. We also indicate how to test for independent assortment when a double (or multiple) homozygote laboratory colony is used in a test‐cross, how to test for differences among samples, and how to pool data to produce a single estimate based on a larger number of pedigreed lines. These methods may encourage the development of a variety of pedigreed monitoring strategies that could improve and prolong the use of scarce plant resistance alleles in rice and other plants.

Monitoring virulence in Asian rice gall midge populations in India

AbstractThe Asian rice gall midge, Orseolia oryzae (Wood‐Mason) (Diptera: Cecidomyiidae), is a major pest of rice [Oryza sativa L. (Poaceae)] in India. Breeding resistant varieties and their cultivation has been the main approach to manage this pest. However, the breakdown of resistance conferred by the major genes, deployed one at a time, through evolution of virulent biotypes has become a major setback to this approach. Development of polymerase chain reaction‐based molecular markers for eight of the 10 resistance genes and their possible use in marker‐assisted selection has enabled breeders to pyramid resistance genes for achieving durable resistance. However, the choice of resistance genes needs to be made with a better understanding of the virulence composition of the pest populations in the target area and the genetics of plant resistance and insect virulence, as the rice–gall midge interaction is a gene‐for‐gene one. We adopted a single‐female test and coupled it with a modified F2 screen test to note the virulence composition of gall midge populations and estimated the frequency of virulence alleles for adaptation at three pest endemic locations in India, namely, Warangal, Ragolu, and Raipur. Results on biotype composition showed heterogeneous pest populations in all the tests and at all the locations. Tests at Warangal repeated after 8 years showed a rapid increase in frequency of the virulence allele conferring adaptation to the plant resistance gene Gm2 as compared to that of the allele for adaptation to the resistance gene Gm1. This is probably the first direct measurement of a durability parameter of plant genes conferring insect resistance. Results supported earlier observations that sex‐linked virulence against Gm2 makes it less durable. The sex ratio did not deviate from the expected 1:1 ratio at Warangal, but at Ragolu females outnumbered males.

Virulence Genes in Heterodera glycines: Allele Frequencies and Ror Gene Groups Among Field Isolates and Inbred Lines

ABSTRACT Genetic variation in field populations of Heterodera glycines is a key issue for both resistance gene deployment and basic understanding of virulence-gene flow in populations. In this study, we examined phenotypically defined genes for virulence under selection from host resistance. We separated the most common H. glycines genotypes in the United States into two virulence groups, based on their reproductive abilities on the resistant soybean plant introduction (PI) 88788. These groups correspond to previously identified virulence genes in the nematode, as follows: the dominant gene in H. glycines to PI88788, and the recessive genes to PI90763 and Pickett/Peking. Virulence allele frequencies and virulence genotype frequencies of selected field isolates were investigated by testing the host range of single-female-derived lines, which were developed through single-female inoculation on the standard susceptible soybean 'Lee 68'. By comparing virulence genotype frequencies between the original field isolates and their single-female-derived lines, we were able to determine allele frequencies in the field populations. The results suggest that tremendous variation in H. glycines virulence genes exists among field populations. Potential mechanisms of selection which could cause virulence genotype frequency increases are discussed as related to population genetics equilibrium theory.

Genotypic interaction between resistance genes in wheat and virulence genes in the Hessian fly Mayetiola destructor (Diptera: Cecidomyiidae)

The genotypic interaction between wheat resistance genes H3, H6, H7H8, H9 and virulence genes vH3, vH6, vH7vH8, vH9 of Hessian fly, Mayetiola destructor (Say), was studied in a growth chamber. Results showed that plants homozygous and heterozygous for the H3 gene expressed a high level of resistance against homozygous avirulent and heterozygous larvae carrying the vH3 virulence allele. The H7H8 genes were highly effective in the homozygous condition, but displayed a reduced level of resistance in the heterozygous condition. The H6 and H9 genes showed different levels of resistance against the reciprocal heterozygous larvae (vH6(a)vH6(A) versus vH6(A)vH6(a) and vH9(a)vH9(A) versus vH9(A)vH9(a)). Adults reared from vH6(a)vH6(A) and vH9(a)vH9(A) larvae were all males, consistent with the vH6 and vH9 X-linkage. Plants homozygous for H3, H6, H7H8, and H9 allowed for greater larval survival of heterozygous larvae, which suggests that avirulence to these resistance genes is incompletely dominant. Greater survival of homozygous avirulent larvae on heterozygous plants (H3h3, H6h6, H7h7H8h8, H9h9) suggests incomplete dominance of these wheat genes. Survival of heterozygous along with homozygous virulent larvae would reduce selection pressure for virulence in Hessian fly populations infesting fields of resistant wheat cultivars. This would be expected to slow the increase in frequency of virulence alleles that often results from deployment of resistant cultivars.