Functional Genomics and Comparative Lineage-Specific Region Analyses Reveal Novel Insights into Race Divergence in Verticillium dahliae

Deciphering the gene-for-gene relationships during host-pathogen interactions is the basis of modern plant resistance breeding. In the Verticillium dahliae -tomato pathosystem, two races (races 1 and 2) and their corresponding avirulence ( Avr ) genes have been identified, but strains that lacked these two Avr genes exist in nature.

Novel Fusarium Wilt Resistance Genes Uncovered in the Wild Progenitors and Heirloom Cultivars of Strawberry

Fusarium wilt, a soilborne disease caused by Fusarium oxysporum f. sp. fragariae, poses a significant threat to strawberry (Fragaria × ananassa) production in many parts of the world. This pathogen causes wilting, collapse, and death in susceptible genotypes. We previously identified a dominant gene (FW1) on chromosome 2B that confers resistance to race 1 of the pathogen and hypothesized that gene-for-gene resistance to Fusarium wilt was widespread in strawberry. To explore this, a genetically diverse collection of heirloom and modern cultivars and wild octoploid ecotypes were screened for resistance to Fusarium wilt races 1 and 2. Here we show that resistance to both races is widespread and that resistance to race 1 is mediated by dominant genes (FW1, FW2, FW3, FW4, and FW5) on three non-homoeologous chromosomes (1A, 2B, and 6B). The resistance proteins encoded by these genes are not yet known; however, plausible candidates were identified that encode pattern recognition receptor or other proteins known to mediate gene-for-gene resistance in plants. High-throughput genotyping assays for SNPs in linkage disequilibrium with FW1-FW5 were developed to facilitate marker-assisted selection and accelerate the development of race 1 resistant cultivars. This study laid the foundation for identifying the genes encoded by FW1-FW5, in addition to exploring the genetics of resistance to race 2 and other races of the pathogen, as a precaution to averting a Fusarium wilt pandemic.

Sustained coevolution of phage Lambda and Escherichia coli involves inner as well as outer membrane defenses and counter-defenses

Bacteria often evolve resistance to phage through the loss or modification of cell-surface receptors. In Escherichia coli and phage λ, such resistance can catalyze a coevolutionary arms race focused on host and phage structures that interact at the outer membrane. Here, we analyze another facet of this arms race involving interactions at the inner membrane, whereby E. coli evolves mutations in mannose permease-encoding genes manY and manZ that impair λ’s ability to eject its DNA into the cytoplasm. We show that these man mutants arose concurrently with the arms race at the outer membrane. We tested the hypothesis that λ evolved an additional counter-defense that allowed them to infect bacteria with deleted man genes. The deletions severely impaired the ancestral λ, but some evolved phage grew well on the deletion mutants, indicating they regained infectivity by evolving the ability to infect hosts independently of the mannose permease. This coevolutionary arms race fulfills the model of an inverse-gene-for-gene infection network. Taken together, the interactions at both the outer and inner membranes reveal that coevolutionary arms races can be richer and more complex than is often appreciated.IMPACT STATEMENTLaboratory studies of coevolution help us understand how host defenses and pathogen counter-defenses change over time, which is often essential for predicting the future dynamics of host-pathogen interactions. One particular model, termed “inverse-gene-for-gene” coevolution, predicts that coevolution proceeds through alternating steps, whereby hosts lose the features exploited by pathogens, and pathogens evolve to exploit alternative features. Using a classic model system in molecular biology, we describe the nature and timing of a previously overlooked step in the coevolution of E. coli and bacteriophage lambda. Our work demonstrates that this mode of coevolution can profoundly re-shape the interactions between bacteria and phage.

Sensitivity genes in wheat and corresponding effector genes in necrotrophs exhibiting inverse gene-for-gene relationship

In wheat, genes for resistance (R) as well as susceptibility (S) are now known for several diseases. The S genes also include sensitivity genes like Tsn1 in wheat. R genes follow a gene-for-gene (GFG) relationship and generally involve biotrophs and S genes particularly sensitivity genes, follow an inverse gene-for-gene relationship (IGFG), generally involving necrotroph or hemi-biotroph pathogens. The toxin (virulence factor) genes of the pathogen and the corresponding sensitivity genes have been described in some detail for the following three pathogens: (i) Paratagonospora nodorum (causing Septoria nodorum blotch or SNB); (ii) Pyrenophora tritici-repentis (tan spot) and (iii) Bipolaris sorokiniana (spot blotch). These and some other pathogens produce several necrotrophic effectors (NEs), which interact directly or indirectly with the products of S genes in the host and produce disease symptoms like necrosis and/or chlorosis. In this article we present a critical review of all the relevant information about the interactions between NEs of the above three pathogens and the corresponding S genes in wheat. The gaps in knowledge and possibilities for future research are also discussed.

Evolution of views on plant immunity: from Flor’s “gene-for-gene” theory to the “zig-zag model” developed by Jones and Dangl

The study of plant defence mechanisms in response to pathogens in the mid-20th century resulted in Harold Flor’s gene-for-gene interaction hypothesis, which became recognised as central to the study of phytoimmunity. According to this theory, the outcome of interactions in plant – pathogen phytopathosystems – i.e. compatibility or incompatibility – is controlled genetically in interacting organisms and determined by the presence of specific genes in both pathogen and plant: resistance genes in the plant and avirulence genes in pathogen. The latest achievements in phytoimmunology, obtained with the help of modern molecular biology and bioinformatics methods, have made a significant contribution to the classical understanding of plant immunity and provided grounds for a modern concept of phytoimmunity consisting in the “zig-zag model” developed by Jonathan Jones and Jefferey Dangl. Plant immunity is currently understood as being determined by an innate multi-layer immune system involving various structures and mechanisms of specific and non-specific immunity. Recognition by plant membrane receptors of conservative molecular patterns associated with microorganisms, as well as molecules produced during cell wall disruption by pathogen hydrolytic enzymes forms a basic non-specific immune response in the plant. Detection of pathogen effector molecules by plant intra-cellular receptors triggers a specific effector-triggered immunity, resulting in the development of the hypersensitive response, systemic resistance and immune memory of the plant. Virulence factors and pathogen attack strategies on the one hand, and mechanisms of plant immune protection on the other, are the result of one form of constant co-evolution, often termed an “evolutionary arms race”. This paper discusses the main principles of Flor's classical “gene-for-gene interaction” theory as well as the molecular-genetic processes of plant innate immunity, their mechanisms and participants in light of contemporary achievements in phytoimmunology.

Effect of SnTOX effectors on the virulence degree of Stagonospora nodorum isolates

Stagonospora nodorum Berk. is the causal agent of Septoria nodorum blotch (SNB) of wheat (Triticum aestivum L.). It synthesizes host-specific necrotrophic effectors (NEs), which facilitate infection process and ensure virulence of pathogen on host plant with a dominant susceptibility gene. The interaction of virulence genes products of the NEs pathogen (SnTox) with susceptibility genes products of the host plant (Snn) in the S. nodorum - wheat pathosystem is carried out in inverted gene-for-gene system and causes the development of disease. In this study, we tested three main NEs SnToxA, SnTox1, SnTox3, which have already been identified in S. nodorum at the gene level. The NEs role in the development of SNB has already been proven; however, the overall host response to SNB does not always strictly follow the inverted gene-for-gene system, as multiple SnTox-Snn interactions can be additive or epistatic. In this regard, the aim of the work was to identify the NE genes in three S. nodorum isolates and to study effect of NEs genes transcriptional activity on the isolate virulence. We have shown that all three NEs SnToxA, SnTox3 and SnTox1 played an important role in the development of the disease in compatible interactions. Effectors SnTox3 and SnTox1 exhibited epistatic interaction that was removed by a triple compatible interaction (SnTox3-Snn3, SnToxA-Tsn1 and SnTox1-Snn1). This effect was shown by us for the first time. The mechanisms of epistatic and additive interactions, as well as the virulence of the isolate were associated with the regulation of the NEs genes transcriptional activity. The avirulent isolate Sn4VD lacked transcription of all three NEs genes, and the virulent isolate Sn9MH was characterized by a high level of mRNA accumulation of all three NEs genes during infection on susceptible cultivar. We also showed that SnTox expression depended both on the host genotype in SnToxA and SnTox3 and on the number of compatible interactions exhibiting additive or epistatic interactions in SnTox1 and SnTox3. Finally, the virulence of the S. nodorum isolate depended on the qualitative and quantitative composition of NEs.

ToxA–Tsn1 Interaction for Spot Blotch Susceptibility in Indian Wheat: An Example of Inverse Gene-for-Gene Relationship

The ToxA–Tsn1 system is an example of an inverse gene-for-gene relationship. The gene ToxA encodes a host-selective toxin (HST) which functions as a necrotrophic effector and is often responsible for the virulence of the pathogen. The genomes of several fungal pathogens (e.g., Pyrenophora tritici-repentis, Parastagonospora nodorum, and Bipolaris sorokiniana) have been shown to carry the ToxA gene. Tsn1 is a sensitivity gene in the host, whose presence generally helps a ToxA-positive pathogen to cause spot blotch in wheat. Cultivars lacking Tsn1 are generally resistant to spot blotch; this resistance is attributed to a number of other known genes which impart resistance in the absence of Tsn1. In the present study, 110 isolates of B. sorokiniana strains, collected from the ME5A and ME4C megaenvironments of India, were screened for the presence of the ToxA gene; 77 (70%) were found to be ToxA positive. Similarly, 220 Indian wheat cultivars were screened for the presence of the Tsn1 gene; 81 (36.8%) were found to be Tsn1 positive. When 20 wheat cultivars (11 with Tsn1 and 9 with tsn1) were inoculated with ToxA-positive isolates, seedlings of only those carrying the Tsn1 allele (not tsn1) developed necrotic spots surrounded by a chlorotic halo. No such distinction between Tsn1 and tsn1 carriers was observed when adult plants were inoculated. This study suggests that the absence of Tsn1 facilitated resistance against spot blotch of wheat. Therefore, the selection of wheat genotypes for the absence of the Tsn1 allele can improve resistance to spot blotch.