Abstract

Plants continuously adjust their strategies to optimize the balance between growth and defense under ever changing environmental conditions. In Arabidopsis, global surveillance to remove aberrant transcripts is mainly maintained by nonsense-mediated mRNA decay (NMD), in which UP-FRAMESHIFT (UPF) 1 and 3 play a vital role. Though it has been known that NMD regulates a subgroup of nucleotide-binding (NB), leucine-rich repeat (LRR) receptors (NLRs) to repress autoimmunity, little is known about NMD -mediated NLR regulation under different temperatures and its role to repress autoimmunity. Also, whether NMD regulates downstream components of these NLRs, still remains elusive.

Here we showed that when NMD is defective, plants shift prioritization toward defense from growth/development at low temperatures. upf1-5 upf3-1 mutants showed a hypersensitive growth arrest response only at a low temperature. Gene ontology terms related to defense were gradually enriched in upf1-5 upf3-1 mutants as temperature decreased, whereas terms related to growth/development were gradually depleted. upf1-5 upf3-1 mutants accumulate high levels of salicylic acid that leads to hypersensitivity at 16°C and inhibition of SA biosynthesis rescued the hypersensitivity. upf1-5 upf3-1 mutants showed upregulation of genes involved in defense and SA biosynthesis/signaling. Hypersensitivity seen at a low temperature in upf1-5 upf3-1 mutants required light. Four nucleotide-binding, leucine-rich repeat genes (two Toll-Interleukin-Resistance domain-containing proteins, ADR1 -LIKE 2, and a TIR -NBS-LRR protein) are important for the hypersensitive response and they were under temperature-dependent NMD regulation. NMD also regulates the downstream components such as EDS1 , SARD1 and WRKY transcription factors.

Taken together, our data suggest that both temperature-dependent NMD and light are important for maintaining the balance between growth/development and defense to optimize plant fitness.