Abstract
Nonsense-mediated mRNA decay (NMD) removes aberrant transcripts to avoid the accumulation of truncated proteins. NMD regulates nucleotide-binding, leucine-rich repeat (NLR) genes to prevent autoimmunity; however, the function of a large number of NLRs still remains poorly understood. Here, we show that three NLR genes (AT1G72910, AT1G72940, and ADR1-LIKE 2) are important for NMD-mediated regulation of defense signaling at lower temperatures. At 16 °C, the NMD-compromised up-frameshift protein1 (upf1) upf3 mutants showed growth arrest that can be rescued by the artificial miRNA-mediated knockdown of the three NLR genes. mRNA levels of these NLRs are induced by Pseudomonas syringae inoculation and exogenous SA treatment. Mutations in AT1G72910, AT1G72940, and ADR1-LIKE 2 genes resulted in increased susceptibility to Pseudomonas syringae, whereas their overexpression resulted in severely stunted growth, which was dependent on basal disease resistance genes. The NMD-deficient upf1 upf3 mutants accumulated higher levels of NMD signature-containing transcripts from these NLR genes at 16 °C. Furthermore, mRNA degradation kinetics showed that these NMD signature-containing transcripts were more stable in upf1 upf3 mutants. Based on these findings, we propose that AT1G72910, AT1G72940, and ADR1-LIKE 2 are directly regulated by NMD in a temperature-dependent manner and play an important role in modulating plant immunity at lower temperatures.
Highlights
Plants integrate external cues, including biotic/abiotic stresses, light, and temperature during growth and development
We found that the arrested growth of upf1/3 mutants could be rescued by shifting the temperature from 16 ◦C to 27 ◦C
Two weeks after transfer to 27 ◦C, the upf1/3 mutants resumed growth and completed their life cycles (Figure 1b) and the fresh weight of upf1/3 mutants shifted to 27 ◦C and was restored to the levels of wild-type plants (Figure 1c), which is consistent with previous reports that the growth defects in nonsense-mediated mRNA decay (NMD)-deficient mutants can be rescued by high temperature [9,23]
Summary
Plants integrate external cues, including biotic/abiotic stresses, light, and temperature during growth and development. Among these environmental cues, temperature affects plant growth, development, and immunity [1]. Temperature and plant growth interact in an antagonistic manner: at higher ambient temperatures, growth is favored while immunity is generally compromised [2]. The negative association between plant immunity and ambient temperature may involve the transcriptional regulation of genes involved in plant growth [3], but the role of post-transcriptional regulation remains to be explored. In one type of post-transcriptional regulation, eukaryotes use nonsense-mediated mRNA decay (NMD) to eliminate aberrant mRNAs from cells, preventing the accumulation of truncated proteins
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