Eighty years of gene-for-gene relationship and its applications in identification and utilization of R genes

Antagonistic coevolution between plants and pathogens has generated a broad array of attack and defense mechanisms. In the classical avirulence (Avr) gene-for-gene model, the pathogen gene evolves to escape host recognition while the host resistance (R) gene evolves to track the evolving pathogen elicitor. In the case of host-specific toxins (HST), the evolutionary arms race may be inverted, with the gene encoding the pathogen toxin evolving to maintain recognition of the host sensitivity target while the host sensitivity gene evolves to escape binding with the toxin. Pathogen effector genes, including those encoding Avr elicitors and HST, often show elevated levels of polymorphism reflecting the coevolutionary arms race between host and pathogen. However, selection can also eliminate variation in the coevolved gene and its neighboring regions when advantageous alleles are swept to fixation. The distribution and diversity of corresponding host genes will have a major impact on the distribution and diversity of effectors in the pathogen population. Population genetic analyses including both hosts and their pathogens provide an essential tool to understand the diversity and dynamics of effector genes. Here, we summarize current knowledge about the population genetics of fungal and oomycete effector genes, focusing on recent studies that have used both spatial and temporal collections to assess the diversity and distribution of alleles and to monitor changes in allele frequencies over time. These studies illustrate that effector genes exhibit a significant degree of diversity at both small and large sampling scales, suggesting that local selection plays an important role in their evolution. They also illustrate that Avr elicitors and HST may be recognizing the same R genes in plants, leading to evolutionary outcomes that differ for necrotrophs and biotrophs while affecting the evolution of the corresponding R genes. Under this scenario, the optimal number of R genes in a plant genome may be determined by the relative abundance of necrotrophic and biotrophic pathogens in the plant's environment.

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

Biomics ◽

10.31301/2221-6197.bmcs.2020-22 ◽

2020 ◽

Vol 12 (3) ◽

pp. 343-351

Author(s):

S.V. Veselova ◽

G.F. Burkhanova ◽

S.D. Rumyantsev ◽

T.V. Nuzhnaya

Keyword(s):

Host Plant ◽

Transcriptional Activity ◽

Susceptibility Gene ◽

Stagonospora Nodorum ◽

Quantitative Composition ◽

Host Genotype ◽

Mrna Accumulation ◽

Gene System ◽

Compatible Interactions ◽

Gene For Gene

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.

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Differential resistance to tuber late blight in potato cultivars without R-genes

Potato Research ◽

10.1007/bf02358089 ◽

1991 ◽

Vol 34 (1) ◽

pp. 3-8 ◽

Cited By ~ 18

Author(s):

T. Bjor ◽

K. Mulelid

Keyword(s):

Late Blight ◽

Differential Resistance ◽

Potato Cultivars ◽

R Genes

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Isolation and Characterization Of Rice R Genes: Evidence for Distinct Evolutionary Paths in Rice and Maize

Genetics ◽

10.1093/genetics/142.3.1021 ◽

1996 ◽

Vol 142 (3) ◽

pp. 1021-1031 ◽

Cited By ~ 3

Author(s):

Jianping Hu ◽

Beth Anderson ◽

Susan R Wessler

Keyword(s):

Gene Family ◽

Gene Families ◽

Chromosome 1 ◽

R Gene ◽

R Genes ◽

Helix Loop Helix ◽

Isolation And Characterization ◽

Undetermined Function ◽

Evolutionary Paths

Abstract R and B genes and their homologues encode basic helix-loop-helix (bHLH) transcriptional activators that regulate the anthocyanin biosynthetic pathway in flowering plants. In maize, R/B genes comprise a very small gene family whose organization reflects the unique evolutionary history and genome architecture of maize. To know whether the organization of the R gene family could provide information about the origins of the distantly related grass rice, we characterized members of the R gene family from rice Oryza sativa. Despite being a true diploid, O. sativa has at least two R genes. An active homologue (Ra) with extensive homology with other R genes is located at a position on chromosome 4 previously shown to be in synteny with regions of maize chromosomes 2 and 10 that contain the B and R loci, respectively. A second rice R gene (Rb) of undetermined function was identified on chromosome 1 and found to be present only in rice species with AA genomes. All non-AA species have but one R gene that is Ra-like. These data suggest that the common ancestor shared by maize and rice had a single R gene and that the small R gene families of grasses have arisen recently and independently.

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Recent Findings Unravel Genes and Genetic Factors Underlying Leptosphaeria maculans Resistance in Brassica napus and Its Relatives

International Journal of Molecular Sciences ◽

10.3390/ijms22010313 ◽

2020 ◽

Vol 22 (1) ◽

pp. 313

Author(s):

Aldrin Y. Cantila ◽

Nur Shuhadah Mohd Saad ◽

Junrey C. Amas ◽

David Edwards ◽

Jacqueline Batley

Keyword(s):

Brassica Napus ◽

Genetic Factors ◽

Quantitative Resistance ◽

Genetic Resistance ◽

Leptosphaeria Maculans ◽

Gene Interaction ◽

R Gene ◽

R Genes ◽

Blackleg Resistance ◽

Avr Gene

Among the Brassica oilseeds, canola (Brassica napus) is the most economically significant globally. However, its production can be limited by blackleg disease, caused by the fungal pathogen Lepstosphaeria maculans. The deployment of resistance genes has been implemented as one of the key strategies to manage the disease. Genetic resistance against blackleg comes in two forms: qualitative resistance, controlled by a single, major resistance gene (R gene), and quantitative resistance (QR), controlled by numerous, small effect loci. R-gene-mediated blackleg resistance has been extensively studied, wherein several genomic regions harbouring R genes against L. maculans have been identified and three of these genes were cloned. These studies advance our understanding of the mechanism of R gene and pathogen avirulence (Avr) gene interaction. Notably, these studies revealed a more complex interaction than originally thought. Advances in genomics help unravel these complexities, providing insights into the genes and genetic factors towards improving blackleg resistance. Here, we aim to discuss the existing R-gene-mediated resistance, make a summary of candidate R genes against the disease, and emphasise the role of players involved in the pathogenicity and resistance. The comprehensive result will allow breeders to improve resistance to L. maculans, thereby increasing yield.

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Mutations introduced in susceptibility genes through CRISPR/Cas9 genome editing confer increased late blight resistance in potatoes

Scientific Reports ◽

10.1038/s41598-021-83972-w ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Nam Phuong Kieu ◽

Marit Lenman ◽

Eu Sheng Wang ◽

Bent Larsen Petersen ◽

Erik Andreasson

Keyword(s):

Late Blight ◽

Late Blight Resistance ◽

Susceptibility Genes ◽

Blight Resistance ◽

R Genes ◽

Guide Rnas ◽

Knockout Mutants ◽

Growth Phenotype ◽

Allelic Deletion ◽

S Genes

AbstractThe use of pathogen-resistant cultivars is expected to increase yield and decrease fungicide use in agriculture. However, in potato breeding, increased resistance obtained via resistance genes (R-genes) is hampered because R-gene(s) are often specific for a pathogen race and can be quickly overcome by the evolution of the pathogen. In parallel, susceptibility genes (S-genes) are important for pathogenesis, and loss of S-gene function confers increased resistance in several plants, such as rice, wheat, citrus and tomatoes. In this article, we present the mutation and screening of seven putative S-genes in potatoes, including two DMR6 potato homologues. Using a CRISPR/Cas9 system, which conferred co-expression of two guide RNAs, tetra-allelic deletion mutants were generated and resistance against late blight was assayed in the plants. Functional knockouts of StDND1, StCHL1, and DMG400000582 (StDMR6-1) generated potatoes with increased resistance against late blight. Plants mutated in StDND1 showed pleiotropic effects, whereas StDMR6-1 and StCHL1 mutated plants did not exhibit any growth phenotype, making them good candidates for further agricultural studies. Additionally, we showed that DMG401026923 (here denoted StDMR6-2) knockout mutants did not demonstrate any increased late blight resistance, but exhibited a growth phenotype, indicating that StDMR6-1 and StDMR6-2 have different functions. To the best of our knowledge, this is the first report on the mutation and screening of putative S-genes in potatoes, including two DMR6 potato homologues.

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Molecular evolution of the plant R regulatory gene family.

Genetics ◽

10.1093/genetics/138.3.849 ◽

1994 ◽

Vol 138 (3) ◽

pp. 849-854

Author(s):

M D Purugganan ◽

S R Wessler

Keyword(s):

Molecular Evolution ◽

Gene Family ◽

Plant Species ◽

Regulatory Gene ◽

Nonsynonymous Substitution ◽

R Genes ◽

Nucleotide Substitutions ◽

Variable Regions ◽

Helix Loop Helix ◽

Regulatory Loci

Abstract Anthocyanin pigmentation patterns in different plant species are controlled in part by members of the myc-like R regulatory gene family. We have examined the molecular evolution of this gene family in seven plant species. Three regions of the R protein show sequence conservation between monocot and dicot R genes. These regions encode the basic helix-loop-helix domain, as well as conserved N-terminal and C-terminal domains; mean replacement rates for these conserved regions are 1.02 x 10(-9) nonsynonymous nucleotide substitutions per site per year. More than one-half of the protein, however, is diverging rapidly, with nonsynonymous substitution rates of 4.08 x 10(-9) substitutions per site per year. Detailed analysis of R homologs within the grasses (Poaceae) confirm that these variable regions are indeed evolving faster than the flanking conserved domains. Both nucleotide substitutions and small insertion/deletions contribute to the diversification of the variable regions within these regulatory genes. These results demonstrate that large tracts of sequence in these regulatory loci are evolving at a fairly rapid rate.

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Organization, Expression and Evolution of a Disease Resistance Gene Cluster in Soybean

Genetics ◽

10.1093/genetics/162.4.1961 ◽

2002 ◽

Vol 162 (4) ◽

pp. 1961-1977

Author(s):

Michelle A Graham ◽

Laura Fredrick Marek ◽

Randy C Shoemaker

Keyword(s):

Disease Resistance ◽

Resistance Gene ◽

Resistance Genes ◽

Developmental Stages ◽

Gene Evolution ◽

Pcr Amplification ◽

Disease Resistance Genes ◽

Disease Resistance Gene ◽

R Genes ◽

Specific Primers

Abstract PCR amplification was previously used to identify a cluster of resistance gene analogues (RGAs) on soybean linkage group J. Resistance to powdery mildew (Rmd-c), Phytophthora stem and root rot (Rps2), and an ineffective nodulation gene (Rj2) map within this cluster. BAC fingerprinting and RGA-specific primers were used to develop a contig of BAC clones spanning this region in cultivar “Williams 82” [rps2, Rmd (adult onset), rj2]. Two cDNAs with homology to the TIR/NBD/LRR family of R-genes have also been mapped to opposite ends of a BAC in the contig Gm_Isb001_091F11 (BAC 91F11). Sequence analyses of BAC 91F11 identified 16 different resistance-like gene (RLG) sequences with homology to the TIR/NBD/LRR family of disease resistance genes. Four of these RLGs represent two potentially novel classes of disease resistance genes: TIR/NBD domains fused inframe to a putative defense-related protein (NtPRp27-like) and TIR domains fused inframe to soybean calmodulin Ca2+-binding domains. RT-PCR analyses using gene-specific primers allowed us to monitor the expression of individual genes in different tissues and developmental stages. Three genes appeared to be constitutively expressed, while three were differentially expressed. Analyses of the R-genes within this BAC suggest that R-gene evolution in soybean is a complex and dynamic process.

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Multiyear Evaluation of the Durability of the Resistance Conferred by Ma and RMia Genes to Meloidogyne incognita in Prunus Under Controlled Conditions

Phytopathology ◽

10.1094/phyto-09-12-0228-r ◽

2013 ◽

Vol 103 (8) ◽

pp. 833-840 ◽

Cited By ~ 5

Author(s):

Samira Khallouk ◽

Roger Voisin ◽

Ulysse Portier ◽

Joël Polidori ◽

Cyril Van Ghelder ◽

...

Keyword(s):

Meloidogyne Incognita ◽

Economic Losses ◽

R Gene ◽

R Genes ◽

Tomato Plants ◽

Controlled Conditions ◽

Meloidogyne Spp ◽

Resistance Breakdown ◽

Susceptible Tomato ◽

Prunus Spp

Root-knot nematodes (RKNs) (Meloidogyne spp.) are highly polyphagous pests that parasitize Prunus crops in Mediterranean climates. Breeding for RKN-resistant Prunus cultivars, as an alternative to the now-banned use of nematicides, is a real challenge, because the perennial nature of these trees increases the risk of resistance breakdown. The Ma plum resistance (R) gene, with a complete spectrum, and the RMia peach R gene, with a more restricted spectrum, both provide total control of Meloidogyne incognita, the model parthenogenetic species of the genus and the most important RKN in terms of economic losses. We investigated the durability of the resistance to this nematode conferred by these genes, comparing the results obtained with those for the tomato Mi-1 reference gene. In multiyear experiments, we applied a high and continuous nematode inoculum pressure by cultivating nematode-infested susceptible tomato plants with either Prunus accessions carrying Ma or RMia R genes, or with resistant tomato plants carrying the Mi-1 gene. Suitable conditions for Prunus development were achieved by carrying out the studies in a glasshouse, in controlled conditions allowing a short winter leaf fall and dormancy. We first assessed the plum accession ‘P.2175’, which is heterozygous for the Ma gene, in two successive 2-year evaluations, for resistance to two M. incognita isolates. Whatever the isolate used, no nematodes reproducing on P.2175 were detected, whereas galls and nematodes reproducing on tomato plants carrying Mi-1 were observed. In a second experiment with the most aggressive isolate, interspecific full-sib material (P.2175 × [‘Garfi’ almond × ‘Nemared’ peach]), carrying either Ma or RMia (from Nemared) or both (in the heterozygous state) or neither of these genes, was evaluated for 4 years. No virulent nematodes developed on Prunus spp. carrying R genes, whereas galling and virulent individuals were observed on Mi-1-resistant tomato plants. Thus, the resistance to M. incognita conferred by Ma in Prunus material in both a pure-plum and an interspecific genetic background, or by RMia in an interspecific background, appears to be durable, highlighting the value of these two genes for the creation of Prunus rootstock material.

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Identification of expressed R-genes associated with leaf spot diseases in cultivated peanut

Molecular Biology Reports ◽

10.1007/s11033-018-4464-5 ◽

2018 ◽

Vol 46 (1) ◽

pp. 225-239 ◽

Cited By ~ 4

Author(s):

Phat M. Dang ◽

Marshall C. Lamb ◽

Kira L. Bowen ◽

Charles Y. Chen

Keyword(s):

Leaf Spot ◽

R Genes ◽

Cultivated Peanut

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