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.

Meiosis is a modified cell division that produces four haploid nuclei from a single diploid cell in two rounds of chromosome segregation. Here, we analyze the role of Arabidopsis thaliana SUPPRESSOR WITH MORPHOGENETIC EFFECTS ON GENITALIA7 (SMG7), THREE DIVISION MUTANT1 (TDM1), and TARDY ASYNCHRONOUS MEIOSIS (TAM) in meiotic progression. SMG7 is a conserved nonsense-mediated mRNA decay factor that is also, in Arabidopsis, essential for completion of meiosis. Examination of activating CYCLIN DEPENDENT KINASE A;1 phosophorylation at Thr-161 suggests that the meiotic arrest observed in smg7 mutants is likely caused by a failure to downregulate cyclin-dependent kinase (CDK) activity at the end of the second meiotic division. Genetic analysis indicates that SMG7 and TDM1 act in the same pathway to facilitate exit from meiosis. We further demonstrate that the cyclin TAM is specifically expressed in meiosis I and has both stimulatory and inhibitory effects on progression to meiosis II. TAM knockouts skip the second meiotic division producing unreduced gametes, but inactivation of SMG7 or TDM1 alleviates TAM's requirement for entry into meiosis II. We propose a model that meiotic progression in Arabidopsis pollen mother cells is driven by a yet to be identified cyclin-CDK activity that is modulated by regulatory interactions between TDM1, SMG7, and TAM.