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

Abstract

Natural plant populations encounter strong pathogen pressure and defence-associated genes are known to be under selection dependent on the pressure by the pathogens. Here, we use populations of the wild tomato Solanum chilense to investigate natural resistance against Cladosporium fulvum , a well-known ascomycete pathogen of domesticated tomatoes. Host populations used are from distinct geographical origins and share a defined evolutionary history. We show that distinct populations of S. chilense differ in resistance against the pathogen. Screening for major resistance gene-mediated pathogen recognition throughout the whole species showed clear geographical differences between populations and complete loss of pathogen recognition in the south of the species range. In addition, we observed high complexity in a homologues of Cladosporium resistance ( Hcr ) locus, underlying the recognition of C. fulvum, in central and northern populations. Our findings show that major gene-mediated recognition specificity is diverse in a natural plant-pathosystem. We place major gene resistance in a geographical context that also defined the evolutionary history of that species. Data suggest that the underlying loci are more complex than previously anticipated, with small-scale gene recombination being possibly responsible for maintaining balanced polymorphisms in the populations that experience pathogen pressure.

Quantitative resistance differences between and within natural populations of Solanum chilense against the oomycete pathogen Phytophthora infestans

“…Our findings show an example of intraspecific variation in quantitative resistance in S. chilense plants from selected populations, in which we earlier reported variation in qualitative resistance against another pathogen (Kahlon et al, 2020). We show that this quantitative variation exists between and within the natural populations of the species and is mainly driven by the plant genotype.…”

“…Most recently, we showed that genetic diversity in the species also has immediate effect on the observed resistance phenotypes of the host populations. Two specific Cladosporium fulvum resistance gene-dependent responses show presence-absence variations between and within populations of the central geographical group of S. chilense (Kahlon et al, 2020). Interestingly, in this study, we also found complete loss of major R gene-mediated resistance responses in the southern part of the species range, which we hypothesize to be related to the extreme environments and probably absence of the pathogen in these regions.…”

“…Solanum chilense is known for its resistance against various pathogens (Tabaeizadeh et al, 1999;Griffiths & Scott, 2001;Ji et al, 2007;Verlaan et al, 2013). It has also been studied extensively in relation to habitat adaptation (Böndel et al, 2018;Fischer et al, 2013;Nosenko et al, 2016;Xia et al, 2010) and as a model for the evolution of pathogen defense mechanisms in plants (Kahlon et al, 2020;. Previously, S. chilense populations from different geographical regions were shown to express different levels of resistance against three filamentous tomato pathogens (Stam, Silva-Arias, et al, 2019).…”

Genomic patterns of structural variation among diverse genotypes of Sorghum bicolor and a potential role for deletions in local adaptation

“…There were three genes that had disease resistance functions. Cf-4A , an R gene important for resistance against the fungal disease caused by Cladosporium fulvum in tomato, had a 97 bp deletion unique to this cluster causing a frameshift mutation, which could suggest that this particular host-pathogen interaction is not as important in this region as it is in the other geographic locations ( Kahlon et al 2020 ). This cluster also had a 141 bp deletion predictably causing exon loss variant in LRR , which is well-known for disease resistance ( Goff and Ramonell 2007 ).…”

Distinct Phyllosphere Microbiome of Wild Tomato Species in Central Peru upon Dysbiosis

“…Major dominant resistance genes such as Cf-4 and Cf-9 originate from wild tomato species [91]. Homologs can be found in many wild tomato species and show remarkable diversity between populations of certain species, probably to fend off diverse pathogen strains [52,57].…”