Genome-wide association of rice response to blast fungus identifies loci for robust resistance under high nitrogen

Mathias Frontini, Arnaud Boisnard, Julien Frouin, Malika Ouikene, Jean Benoit Morel, Elsa Ballini

Nitrogen fertilization is known to increase disease susceptibility, a phenomenon called Nitrogen-Induced Susceptibility (NIS). In rice, this phenomenon has been observed in infections with the blast fungus Magnaporthe oryzae. A previous classical genetic study revealed a locus (NIS1) that enhances susceptibility to rice blast under high nitrogen fertilization. In order to further address the underlying genetics of plasticity in susceptibility to rice blast after fertilization, we analyzed NIS under greenhouse-controlled conditions in a panel of 139 temperate japonica rice strains. A genome-wide association analysis was conducted to identify loci potentially involved in NIS by comparing susceptibility loci identified under high and low nitrogen conditions, an approach allowing for the identification of loci validated across different nitrogen environments. We also used a novel NIS Index to identify loci potentially contributing to plasticity in susceptibility under different nitrogen fertilization regimes. A global NIS effect was observed in the population, with the density of lesions increasing by 8%, on average, under high nitrogen fertilization. Three new QTL, other than NIS1, were identified. A rare allele of the RRobN1 locus on chromosome 6 provides robust resistance in high and low nitrogen environments. A frequent allele of the NIS2 locus, on chromosome 5, exacerbates blast susceptibility under the high nitrogen condition. Finally, an allele of NIS3, on chromosome 10, buffers the increase of susceptibility arising from nitrogen fertilization but increases global levels of susceptibility. This allele is almost fixed in temperate japonicas, as a probable consequence of genetic hitchhiking with a locus involved in cold stress adaptation. Our results extend to an entire rice subspecies the initial finding that nitrogen increases rice blast susceptibility. We demonstrate the usefulness of estimating plasticity for the identification of novel loci involved in the response of rice to the blast fungus under different nitrogen regimes.