Silicon-mediated resistance to Spodoptera frugiperda in rice modulates growth and defense processes via transcriptional reprogramming

Abstract

Accumulation of silicon (Si) is known to confer resistance in plants against abiotic and biotic stresses; however, questions remain about the underlying mechanisms of Si-mediated resistance against insect herbivores. We investigated the Si-mediated resistance mechanisms in rice against fall armyworm, Spodoptera frugiperda, using the OsLsi1 mutant rice (cv. Nipponbare) lines deficient in Si uptake from the soil. We investigated these questions using a multidisciplinary approach, combining bioassays of insect and plant growth and biochemical quantification of defense metabolites, phytohormones, and volatiles. Further, we studied constitutive and herbivory-induced gene expression in Os Lsi1 rice mutants relative to the wild type (WT). Moreover, we detected high-impact SNPs/InDels associated with plant–insect interactions, and integrated these variants with expression signatures across mutants and WT. Si played a key role in mediating constitutive resistance to FAW, but Si content did not substantially alter induced responses. High Si content promoted compensatory growth post-herbivory and had no effect on constitutive or induced activities of peroxidases, polyphenol oxidases, trypsin inhibitors, and jasmonic acid. Low Si plants constitutively emitted higher levels of certain terpene volatiles. Comparative transcriptomics across mutants and WT showed that Si modulates gene expression under both constitutive and post-herbivory. Plants with high Si levels appear well defended but also capable of allocating resources to re-growth than low Si plants. Genes including OsbHLH024, OsLsi1, OsMSH3 , OsARC5, OsCKX2 , and OsBBX3 are candidates for engineering rice varieties with enhanced herbivory resistance. These results suggest that Si-deficient rice lines are genetically and transcriptionally less equipped to resistance.