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Pathogen-Associated Molecular Pattern-Triggered Immunity Involves Proteolytic Degradation of Core Nonsense-Mediated
Ho Won Jung1, Gagan Kumar Panigrahi2,3,4, Ga Young Jung1
1Department of Applied Bioscience, Dong-A University, Busan 49315, Korea.
Abstract:
Nonsense-mediated mRNA decay (NMD), an mRNA quality control process, is thought to function in plant immunity. A subset of fully spliced (FS) transcripts of Arabidopsis (Arabidopsis thaliana) resistance (R) genes are upregulated during bacterial infection. Here, we report that 81.2% and 65.1% of FS natural TIR-NBS-LRR (TNL) and CC-NBS-LRR transcripts, respectively, retain characteristics of NMD regulation, as their transcript levels could be controlled posttranscriptionally. Both bacterial infection and the perception of bacteria by pattern recognition receptors initiated the destruction of core NMD factors UP-FRAMESHIFT1 (UPF1), UPF2, and UPF3 in Arabidopsis within 30 min of inoculation via the independent ubiquitination of UPF1 and UPF3 and their degradation via the 26S proteasome pathway. The induction of UPF1 and UPF3 ubiquitination was delayed in mitogen-activated protein kinase3 (mpk3) and mpk6, but not in salicylic acid-signaling mutants, during the early immune response. Finally, previously uncharacterized TNL-type R transcripts accumulated in upf mutants and conferred disease resistance to infection with a virulent Pseudomonas strain in plants. Our findings demonstrate that NMD is one of the main regulatory processes through which PRRs fine-tune R transcript levels to reduce fitness costs and achieve effective immunity.
Insights
Nonsense-mediated mRNA decay (NMD) regulates plant immunity by controlling resistance (R) gene transcript levels. Bacterial infection triggers NMD factor degradation, enhancing plant defense responses.
Area of Science:
- Plant molecular biology
- Plant immunity
- mRNA regulation
Background:
- Nonsense-mediated mRNA decay (NMD) is a crucial mRNA quality control pathway.
- NMD is implicated in plant immune responses, but its precise role remains unclear.
- Certain resistance (R) gene transcripts increase during bacterial infections in Arabidopsis.
Purpose of the Study:
- To investigate the role of NMD in regulating R gene expression during plant-bacterial interactions.
- To elucidate the molecular mechanisms by which NMD factors are regulated during early plant immune responses.
Main Methods:
- Analysis of transcript levels of fully spliced (FS) transcripts from TIR-NBS-LRR and CC-NBS-LRR genes.
- Investigating the degradation of core NMD factors (UPF1, UPF2, UPF3) upon bacterial inoculation.
- Utilizing Arabidopsis mutants (mpk3, mpk6, salicylic acid signaling, upf mutants) to dissect signaling pathways.
- Assessing disease resistance in upf mutants challenged with Pseudomonas.
Main Results:
- A significant proportion of FS TNL and CC-NBS-LRR transcripts exhibit NMD regulation.
- Bacterial infection and pattern recognition receptor (PRR) perception rapidly induce UPF1, UPF2, and UPF3 degradation via ubiquitination and proteasomal pathways.
- UPF1 and UPF3 ubiquitination are delayed in mpk3 and mpk6 mutants, indicating a role for these kinases.
- Accumulation of uncharacterized TNL-type R transcripts in upf mutants confers enhanced resistance to virulent Pseudomonas.
Conclusions:
- NMD is a key post-transcriptional regulatory mechanism controlling R gene expression in Arabidopsis immunity.
- PRRs fine-tune R transcript levels through NMD to balance fitness costs and effective immunity.
- The study reveals a novel mechanism linking NMD, MAPK signaling, and plant defense.
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