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.
Highlights
Plant immunity, a counterattack mechanism against microbial infection, is exquisitely controlled by two different immune receptors known as extracellular immune receptors and intracellular immune receptors that recognize microbe-associated molecular patterns (MAMPs) and pathogenderived effectors, respectively
To determine whether the simultaneous mutation of UPF1 and UPF3 would reinforce resistance responses against bacterial infection, we analyzed the responses of wild-type, upf1-5, upf3-1, upf1-5 upf3-1, and upf3-1 upf1-5 plants to infection with PstDC3000 and Pseudomonas cannabina pv alisalensis ES4326 (PcaES4326; formerly P. syringae pv maculicola ES4326; Bull et al, 2010)
Because bacterial infection upregulates a subset of NMDsensitive transcripts (Gloggnitzer et al, 2014), we monitored the transcript levels of core Nonsense-mediated mRNA decay (NMD) factors in PstDC3000-infected wildtype leaves to detect any decrease in transcript levels upon bacterial infection
Summary
A counterattack mechanism against microbial infection, is exquisitely controlled by two different immune receptors known as extracellular immune receptors (pattern recognition receptors, PRRs) and intracellular immune receptors (resistance [R] proteins; nucleotide binding oligomerization domain– like receptors [NOD-like receptors or NLRs]; or nucleotide binding site–leucine-rich repeat [NBS-LRR] proteins) that recognize microbe-associated molecular patterns (MAMPs) and pathogenderived effectors, respectively. PTC-containing transcripts can arise from mutations or AS, and NMD is usually triggered by the presence of a downstream splice junction or long 39 untranslated region (UTR; Rebbapragada and Lykke-Andersen, 2009; Peccarelli and Kebaara, 2014). The canonical NMD process occurs when a translating ribosome encounters a PTC and fails to properly terminate translation. This leads to the phosphorylation and activation of the core NMD factor UP-FRAMESHIFT1 (UPF1), a process promoted by the interaction of UPF1 with UPF2 and UPF3, which associate with a downstream exon-junction complex (EJC; Kim et al, 2001; Banihashemi et al, 2006; Schweingruber et al, 2013). NMD is involved in flowering, Suc metabolism, and stress responses in plants (Yoine et al, 2006; Jeong et al, 2011; Rayson et al, 2012; Riehs-Kearnan et al, 2012; Shi et al, 2012; Garcia et al, 2014; Gloggnitzer et al, 2014; Filichkin et al, 2015; Sureshkumar et al, 2016)
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