QTL mapping in field plant populations reveals a genetic basis for frequency- and spatially-specific fungal pathosystem resistance

Abstract

Fungal pathogens pose significant challenges to agro-ecosystem productivity. The wild tobacco,Nicotiana attenuata, has been grown for over two decades at an experimental field station in its native habitat, leading to the emergence of a high-mortality sudden wilt disease caused by aFusarium-Alternariapathosystem. By using an Advanced Intercross Recombinant Inbred Line (AI-RIL) mapping population ofN. attenuataplanted in the infected field site, we found two significant loci associated with plant susceptibility to the fungi. A functional characterization of several genes in these loci identifiedRLXL(intracellular ribonuclease LX-like) as an important factor underlying plant pathogen resistance. Virus-induced silencing ofRLXLreduced leaf wilting in plants inoculated with anin vitroculture ofFusariumspecies. Assessing the significance of theRLXL-associated allele in mixed field populations indicated that, among 4-plant subpopulations, those harboring a single plant with theRLXL-deficiency allele exhibited the highest survival rates. Within these populations, a livingRLXL-deficient plant improved the survival ofRLXL-producing plants located diagonally, while the mortality of the adjacent plants remained as high as in all other subpopulations. Taken together, these findings provide evidence for the genetic basis for a frequency- and spatially-dependent population pathogen resistance mechanism.Significance statementPlant pathogen resistance studies predominantly focus on single genes that reduce pathogenicity in individual plants, aiming to apply these findings to agricultural monocultures. On the other hand, ecologists have observed for decades that greater diversity drives plant population resistance and resilience to pathogens. More studies are needed to identify and characterize loci with positive effects conferred through their frequency in plant populations. We combine quantitative genetics, molecular techniques, and ecologically-informed mixed field populations to identify a novel intracellular ribonuclease LX-like (RLXL) gene with a frequency- and position-dependent effect for plant resistance. To our knowledge, this is the first detailed link between plant population protection and various percentages of plants with an allele representingRLXLpresence or absence.