Evolutionary Systems Biology Identifies Genetic Trade-offs in Rice Defense against Aboveground and Belowground Attackers

Like other plants, wild and domesticated rice species (Oryza nivara, O. rufipogon, and O. 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 aboveground and belowground herbivores, the fall armyworm (Spodoptera frugiperda) and the southern root-knot nematode (Meloidogyne incognita), and comparison with rice responses to microbial pathogens, we identify potential genetic trade-offs at the KSL8 and MG1 loci on chromosome 11. KSL8 encodes the first committed step toward the biosynthesis of either stemarane-type or stemodane-type diterpenoids through the japonica (KSL8-jap) or indica (KSL8-ind) allele. Knocking out KSL8-jap and CPS4, encoding an enzyme that acts upstream in diterpenoid synthesis, in japonica rice cultivars increased resistance to S. frugiperda and decreased resistance to M. incognita. Furthermore, MG1 resides in a haplotype that provided resistance to M. incognita, while alternative haplotypes are involved in mediating resistance to the rice blast fungus Magnaporthe oryzae and other pests and pathogens. Finally, KSL8 and MG1 alleles are located within trans-species polymorphic haplotypes and may be evolving under long-term balancing selection. Our data are consistent with a hypothesis that polymorphisms at KSL8 and MG1 may be maintained through complex and diffuse community interactions.