Aberrant growth and lethality of Arabidopsis deficient in nonsense-mediated RNA decay factors is caused by autoimmune-like response.

Nonsense-mediated RNA decay (NMD) is an evolutionarily conserved RNA quality control mechanism that eliminates transcripts containing nonsense mutations. NMD has also been shown to affect the expression of numerous genes, and inactivation of this pathway is lethal in higher eukaryotes. However, despite relatively detailed knowledge of the molecular basis of NMD, our understanding of its physiological functions is still limited and the underlying causes of lethality are unknown. In this study, we examined the importance of NMD in plants by analyzing an allelic series of Arabidopsis thaliana mutants impaired in the core NMD components SMG7 and UPF1. We found that impaired NMD elicits a pathogen defense response which appears to be proportional to the extent of NMD deficiency. We also demonstrate that developmental aberrations and lethality of the strong smg7 and upf1 alleles are caused by constitutive pathogen response upregulation. Disruption of pathogen signaling suppresses the lethality of the upf1-3 null allele and growth defects associated with SMG7 dysfunction. Interestingly, infertility and abortive meiosis observed in smg7 mutants is not coupled with impaired NMD suggesting a broader function of SMG7 in cellular metabolism. Taken together, our results uncover a major physiological consequence of NMD deficiency in Arabidopsis and revealed multifaceted roles of SMG7 in plant growth and development.

Nonsense-mediated mRNA decay modulates immune receptor levels to regulate plant antibacterial defense.

Nonsense-mediated mRNA decay (NMD) is a conserved eukaryotic RNA surveillance mechanism that degrades aberrant mRNAs. NMD impairment in Arabidopsis is linked to constitutive immune response activation and enhanced antibacterial resistance, but the underlying mechanisms are unknown. Here we show that NMD contributes to innate immunity in Arabidopsis by controlling the turnover of numerous TIR domain-containing, nucleotide-binding, leucine-rich repeat (TNL) immune receptor-encoding mRNAs. Autoimmunity resulting from NMD impairment depends on TNL signaling pathway components and can be triggered through deregulation of a single TNL gene, RPS6. Bacterial infection of plants causes host-programmed inhibition of NMD, leading to stabilization of NMD-regulated TNL transcripts. Conversely, constitutive NMD activity prevents TNL stabilization and impairs plant defense, demonstrating that host-regulated NMD contributes to disease resistance. Thus, NMD shapes plant innate immunity by controlling the threshold for activation of TNL resistance pathways.