Subsets of NLR genes show differential signatures of adaptation during colonization of new habitats

Stam, Remco; Silva‐Arias, Gustavo A.; Tellier, Aurélien

doi:10.1111/nph.16017

Cited by 57 publications

(92 citation statements)

References 79 publications

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“…In sharp contrast, MADA sequences appear to have degenerated over time in sensor CC-NLRs as these proteins specialized in pathogen detection and lost the capacity to execute the immune response without their helper mates. Consistent with this view, NRCs are known to be more highly conserved than their NRC-S partners within the Solanaceae Stam et al, 2019). Future analyses will determine whether MADA-CC-NLRs are generally more evolutionarily constrained than non-MADA containing NLRs.…”

Section: Discussionmentioning

confidence: 76%

An N-terminal motif in NLR immune receptors is functionally conserved across distantly related plant species

Adachi

Contreras

Harant

et al. 2019

Preprint

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The molecular codes underpinning the functions of plant NLR immune receptors are poorly understood. We used in vitro Mu transposition to generate a random truncation library and identify the minimal functional region of NLRs. We applied this method to NRC4-a helper NLR that functions with multiple sensor NLRs within a Solanaceae receptor network. This revealed that the NRC4 N-terminal 29 amino acids are sufficient to induce hypersensitive cell death. This region is defined by the consensus MADAxVSFxVxKLxxLLxxEx (MADA motif) that is conserved at the N-termini of NRC family proteins and ~20% of coiled-coil (CC)-type plant NLRs. The MADA motif matches the N-terminal 1 helix of Arabidopsis NLR protein ZAR1, which undergoes a conformational switch during resistosome activation. Immunoassays revealed that the MADA motif is functionally conserved across NLRs from distantly related plant species. NRC-dependent sensor NLRs lack MADA sequences indicating that this motif has degenerated in sensor NLRs over evolutionary time.

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Section: Discussionmentioning

confidence: 76%

An N-terminal motif in NLR immune receptors is functionally conserved across distantly related plant species

Adachi

Contreras

Harant

et al. 2019

Preprint

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“…Therefore, we envision that the gene dataset can be divided into two categories of genes in hosts and parasites a priori: pairs of candidate loci possibly under coevolution, and pairs of other randomly selected genes. For example, the candidates can be resistance genes in the host plant [4][5][6][12][13][14][15][16] and the corresponding predicted effectors in the parasite [17,18]. The second category can be composed of genes involved in processes such as housekeeping, abiotic stress responses or photosynthesis in plants, and housekeeping genes and/or degrading enzymes with non-specific activities in parasites.…”

Section: Accuracy Of Inferencementioning

confidence: 99%

“…Hereby, allele frequencies either converge towards a stable equilbrium or they fluctuate persistently over time. Based on these classic expectations, genomic studies have unravelled positive and balancing selection signatures at various resistance genes [4][5][6][12][13][14][15][16] and effector genes [17,18].…”

Section: Introductionmentioning

confidence: 99%

Inference of coevolutionary dynamics and parameters from host and parasite polymorphism data of repeated experiments

Märkle

Tellier

2020

PLoS Comput Biol

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There is a long-standing interest in understanding host-parasite coevolutionary dynamics and associated fitness effects. Increasing amounts of genomic data for both interacting species offer a promising source to identify candidate loci and to infer the main parameters of the past coevolutionary history. However, so far no method exists to perform the latter. By coupling a gene-for-gene model with coalescent simulations, we first show that three types of biological costs, namely, resistance, infectivity and infection, define the allele frequencies at the internal equilibrium point of the coevolution model. These in return determine the strength of selective signatures at the coevolving host and parasite loci. We apply an Approximate Bayesian Computation (ABC) approach on simulated datasets to infer these costs by jointly integrating host and parasite polymorphism data at the coevolving loci. To control for the effect of genetic drift on coevolutionary dynamics, we assume that 10 or 30 repetitions are available from controlled experiments or several natural populations. We study two scenarios: 1) the cost of infection and population sizes (host and parasite) are unknown while costs of infectivity and resistance are known, and 2) all three costs are unknown while populations sizes are known. Using the ABC model choice procedure, we show that for both scenarios, we can distinguish with high accuracy pairs of coevolving host and parasite loci from pairs of neutrally evolving loci, though the statistical power decreases with higher cost of infection. The accuracy of parameter inference is high under both scenarios especially when using both host and parasite data because parasite polymorphism data do inform on costs applying to the host and vice-versa. As the false positive rate to detect pairs of genes under coevolution is small, we suggest that our method complements recently developed methods to identify host and parasite candidate loci for functional studies. Author summaryIt is of importance for agriculture and medicine to understand host-parasite antagonistic coevolutionary dynamics and the deleterious associated fitness effects, as well as to reveal the genes underpinning these interactions. The increasing amounts of genomic data for PLOS COMPUTATIONAL BIOLOGY PLOS Computational Biology | https://doi.hosts and parasites offer a promising source to identify such candidate loci, but also to use statistical inference methods to reconstruct the past coevolutionary history. In our study we attempt to draw inference of the past coevolutionary history at key host and parasites loci using sequence data from several individuals and across several experimental replicates. We demonstrate that using a Bayesian statistical method, it is possible to estimate the parameters driving the interaction of hosts and parasites at these loci for thousands of generations. The main parameter that can be estimated is the fitness loss by hosts upon infection. Our method and results can be applied to experimental coevolution data with seq...

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“…To test this hypothesis, we examined genome sequence data that are available for three plants, which are from representative populations of the central, southern coastal and southern highlands region (LA3111, LA2932 and LA4330 respectively) (Stam et al ., 2019a). We extracted and aligned the genomic sequences of the co-receptors SERK3a (also known as BRI1-ASSOCIATED KINASE 1, BAK1 ) and SOBIR1 , the adaptor ACIK1 , required for regulation of the complex, as well as another regulatory co-receptor of the BAK1 -containing complex, BIR2 and its homolog BIR2b (Table S2).…”

Section: Resultsmentioning

confidence: 99%

Population studies of the wild tomato species Solanum chilense reveal geographically structured major gene-mediated pathogen resistance

Kahlon

Seta

Zander

et al. 2020

Preprint

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9Natural plant populations encounter strong pathogen pressure and defense-associated genes are 2 0 known to be under different selection pressure dependent on the pressure by the pathogens. Here 2 1 we use wild tomato Solanum chilense populations to investigate natural resistance against 2 2 Cladosporium fulvum, a well-known pathogenic fungus of domesticated tomatoes. We show that 2 3 populations of S. chilense differ in resistance against the pathogen. Next, we explored the 2 4underlying molecular processes in a species wide-context. Then, focusing on recognition of the 2 5 two prominent avirulence factors secreted by C. fulvum (Avr4 and Avr9) in central and northern 2 6 populations of S. chilense we observed high complexity in the cognate homologues of 2 7Cladosporium resistance (Hcr9) locus underlying the recognition of these effectors. Presence of 2 8 canonical genomic regions coding for Cf-4 and Cf-9, two major dominant resistance genes in the 2 9Hcr9 locus recognizing Avr4 and Avr9, respectively, does not meet prediction from Avr 3 0 response phenotypes. We find both genes in varying fractions of the plant populations and we 3 1show possible co-existence of two functionally active resistance genes, previously thought to be 3 2 allelic. Additionally, we observed the complete local absence of recognition of additional Avr 3 3 proteins of C. fulvum. In the southern populations we attribute this to changes in the coregulatory 3 4 network. As a result of loss of pathogen pressure or adaptation to extreme climatic conditions. 5This may ultimately explain the observed pathogen susceptibility in the southern populations. 6This work puts major gene mediated disease resistance in an ecological context. 3 7 3 8 3 9

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Subsets of NLR genes show differential signatures of adaptation during colonization of new habitats

Cited by 57 publications

References 79 publications

An N-terminal motif in NLR immune receptors is functionally conserved across distantly related plant species

An N-terminal motif in NLR immune receptors is functionally conserved across distantly related plant species

Inference of coevolutionary dynamics and parameters from host and parasite polymorphism data of repeated experiments

Population studies of the wild tomato species Solanum chilense reveal geographically structured major gene-mediated pathogen resistance

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