Targets of selection in a disease resistance network in wild tomatoes

Rose, Laura; Grzeskowiak, Lukasz; Hörger, Anja C.; Groth, Martin; Stephan, Wolfgang

doi:10.1111/j.1364-3703.2011.00720.x

Cited by 25 publications

(33 citation statements)

References 36 publications

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“…More effective seed banks slow down the rate of evolution (5, 7), potentially explaining the lack of evidence for genomic signatures of positive directional selection for abiotic stress tolerance in this species (26,31). Conversely, small germination rates promote genetic diversity at host and parasite genes involved in coevolutionary interactions (14), making balancing selection at plant R-genes more likely to occur and to be observable in S. peruvianum (41).…”

Section: Resultsmentioning

confidence: 99%

Inference of seed bank parameters in two wild tomato species using ecological and genetic data

Tellier¹,

Laurent²,

Lainer³

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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112

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Seed and egg dormancy is a prevalent life-history trait in plants and invertebrates whose storage effect buffers against environmental variability, modulates species extinction in fragmented habitats, and increases genetic variation. Experimental evidence for reliable differences in dormancy over evolutionary scales (e.g., differences in seed banks between sister species) is scarce because complex ecological experiments in the field are needed to measure them. To cope with these difficulties, we developed an approximate Bayesian computation (ABC) framework that integrates ecological information on population census sizes in the priors of the parameters, along with a coalescent model accounting simultaneously for seed banks and spatial genetic structuring of populations. We collected SNP data at seven nuclear loci (over 300 SNPs) using a combination of three spatial sampling schemes: population, pooled, and species-wide samples. We provide evidence for the existence of a seed bank in two wild tomato species (Solanum chilense and Solanum peruvianum) found in western South America. Although accounting for uncertainties in ecological data, we infer for each species (i) the past demography and (ii) ecological parameters, such as the germination rate, migration rates, and minimum number of demes in the metapopulation. The inferred difference in germination rate between the two species may reflect divergent seed dormancy adaptations, in agreement with previous population genetic analyses and the ecology of these two sister species: Seeds spend, on average, a shorter time in the soil in the specialist species (S. chilense) than in the generalist species (S. peruvianum).Bayesian analysis | bet-hedging | coalescent theory T he effective size of a population or species (N e ) defines its evolutionary potential because it determines the rate at which adaptive substitutions appear and get fixed (1), as well as the vulnerability to loss of genetic diversity by genetic drift. A fundamental question in plant evolutionary biology, and of practical relevance for conservation biology, is to understand how the census size of a population above ground (N cs ) is affected by ecological disturbances and how this process, in turn, affects the N e (2). Habitat loss and fragmentation attributable to human activities are indeed acute problems for conservation of spatially structured populations because they reduce deme sizes (N e and N cs ) and gene flow among demes. The genetic diversity, reflected by the N e , of many plant (and invertebrate) species, can be seen as an iceberg. The tip of the iceberg is composed of individuals observable above ground (N cs ), whereas the major part of the diversity is accounted for by among-population differences (3, 4) and seed banks (5-8).Most, if not all, plant and animal species exist as spatially structured populations (metapopulations) with many demes linked by migration, which may be subjected to extinction/ recolonization (9). Depending on extinction/recolonization rates and the type of group fo...

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Section: Resultsmentioning

confidence: 99%

Inference of seed bank parameters in two wild tomato species using ecological and genetic data

Tellier¹,

Laurent²,

Lainer³

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

112

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“…Previous studies of other resistance genes in this species indicate that pathogen pressure is a significant evolutionary force, at least in some parts of the species range [33]–[35]. Moreover, high levels of polymorphism in this species provide sufficient power for population genetic analyses.…”

Section: Introductionmentioning

confidence: 83%

Balancing Selection at the Tomato RCR3 Guardee Gene Family Maintains Variation in Strength of Pathogen Defense

et al. 2012

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Coevolution between hosts and pathogens is thought to occur between interacting molecules of both species. This results in the maintenance of genetic diversity at pathogen antigens (or so-called effectors) and host resistance genes such as the major histocompatibility complex (MHC) in mammals or resistance (R) genes in plants. In plant–pathogen interactions, the current paradigm posits that a specific defense response is activated upon recognition of pathogen effectors via interaction with their corresponding R proteins. According to the “Guard-Hypothesis,” R proteins (the “guards”) can sense modification of target molecules in the host (the “guardees”) by pathogen effectors and subsequently trigger the defense response. Multiple studies have reported high genetic diversity at R genes maintained by balancing selection. In contrast, little is known about the evolutionary mechanisms shaping the guardee, which may be subject to contrasting evolutionary forces. Here we show that the evolution of the guardee RCR3 is characterized by gene duplication, frequent gene conversion, and balancing selection in the wild tomato species Solanum peruvianum. Investigating the functional characteristics of 54 natural variants through in vitro and in planta assays, we detected differences in recognition of the pathogen effector through interaction with the guardee, as well as substantial variation in the strength of the defense response. This variation is maintained by balancing selection at each copy of the RCR3 gene. Our analyses pinpoint three amino acid polymorphisms with key functional consequences for the coevolution between the guardee (RCR3) and its guard (Cf-2). We conclude that, in addition to coevolution at the “guardee-effector” interface for pathogen recognition, natural selection acts on the “guard-guardee” interface. Guardee evolution may be governed by a counterbalance between improved activation in the presence and prevention of auto-immune responses in the absence of the corresponding pathogen.

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“…Additionally, several studies exist suggesting that bacterial resistance-associated genes are under selective pressure (Rose et al, 2005; Rose et al, 2011; Rose, Michelmore & Langley, 2007). S. chilense is native in South America, ranging from southern Peru to central Chile, and colonised a broad range of habitats.…”

Section: Introductionmentioning

confidence: 99%

The wild tomato speciesSolanum chilenseshows variation in pathogen resistance between geographically distinct populations

Stam

Scheikl

Tellier

2017

PeerJ

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Wild tomatoes are a valuable source of disease resistance germplasm for tomato (Solanum lycopersicum) breeders. Many species are known to possess a certain degree of resistance against certain pathogens; however, evolution of resistance traits is yet poorly understood. For some species, like Solanum chilense, both differences in habitat and within species genetic diversity are very large. Here we aim to investigate the occurrence of spatially heterogeneous coevolutionary pressures between populations of S. chilense. We investigate the phenotypic differences in disease resistance within S. chilense against three common tomato pathogens (Alternaria solani, Phytophthora infestans and a Fusarium sp.) and confirm high degrees of variability in resistance properties between selected populations. Using generalised linear mixed models, we show that disease resistance does not follow the known demographic patterns of the species. Models with up to five available climatic and geographic variables are required to best describe resistance differences, confirming the complexity of factors involved in local resistance variation. We confirm that within S. chilense, resistance properties against various pathogens show a mosaic pattern and do not follow environmental patterns, indicating the strength of local pathogen pressures. Our study can form the basis for further investigations of the genetic traits involved.

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Targets of selection in a disease resistance network in wild tomatoes

Cited by 25 publications

References 36 publications

Inference of seed bank parameters in two wild tomato species using ecological and genetic data

Inference of seed bank parameters in two wild tomato species using ecological and genetic data

Balancing Selection at the Tomato RCR3 Guardee Gene Family Maintains Variation in Strength of Pathogen Defense

The wild tomato speciesSolanum chilenseshows variation in pathogen resistance between geographically distinct populations

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