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 a Fusarium-Alternaria pathosystem. By using an Advanced Intercross Recombinant Inbred Line (AI-RIL) mapping population of N. attenuata planted 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 identified RLXL (intracellular ribonuclease LX-like) as an important factor underlying plant pathogen resistance. Virus-induced silencing of RLXL reduced leaf wilting in plants inoculated with an in vitro culture of Fusarium species. Assessing the significance of the RLXL-associated allele in mixed field populations indicated that, among 4-plant subpopulations, those harboring a single plant with the RLXL-deficiency allele exhibited the highest survival rates. Within these populations, a living RLXL-deficient plant improved the survival of RLXL-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 representing RLXL presence or absence.