Evolutionary Systems Biology Identifies Genetic Trade-offs In Rice Defense Against Above- and Belowground Attackers

Abstract

AbstractLike other plants, wild and domesticated rice species (Oryza nivara, O. rufipogon, andO. sativa) evolve in environments with various biotic and abiotic stresses that fluctuate in intensity through space and time. Microbial pathogens and invertebrate herbivores such as plant-parasitic nematodes and caterpillars show geographical and temporal variation in activity patterns and may respond differently to certain plant defensive mechanisms. As such, plant interactions with multiple community members may result in conflicting selection pressures on genetic polymorphisms. Here, through assays with different above- and belowground herbivores, the fall armyworm (Spodoptera frugiperda) and the southern root-knot nematode (Meloidogyne incognita), respectively, and comparison with rice responses to microbial pathogens, we identify potential genetic trade-offs at theKSL8andMG1loci on chromosome 11.KSL8encodes the first committed step towards biosynthesis of either stemarane- or stemodane-type diterpenoids through the japonica (KSL8-jap) or indica (KSL8-ind) allele. Knocking outKSL8-japandCPS4, encoding an enzyme that acts upstream in diterpenoid synthesis, in japonica rice cultivars increased resistance toS. frugiperdaand decreased resistance toM. incognita. Furthermore,MG1resides in a haplotype that provided resistance toM. incognita, while alternative haplotypes are involved in mediating resistance to the rice blast fungusMagnaporthe oryzaeand other pests and pathogens. Finally,KSL8andMG1alleles are located within trans-species haplotypes and may be evolving under long-term balancing selection. Our data are consistent with a hypothesis that polymorphisms atKSL8andMG1may be maintained through complex and diffuse community interactions.