Heat-induced cell damage induces autophagy-mediated cell expansion in Arabidopsis

Plants have evolved sophisticated cellular and molecular mechanisms to acclimate to adverse environmental stresses. Here, we report that acute heat stress induces excessive cell expansion, reaching up to 13,000 µm2, in Arabidopsis thaliana. The heat-induced cell expansion progressed along with programmed cell death. Autophagy was responsible for excessive cell expansion, as evidenced by autophagic structures in the expanded cells as well as failure of heat-induced cell expansion in autophagy-related 5-1 (atg5-1) and atg7-2 mutants. We also reveal that the transcription factor ETHYLENE RESPONSE FACTOR115 (ERF115), which is activated upon neighboring cell death, is involved in heat-induced cell expansion. ERF115 accumulation in response to heat possibly activated the expression of several ATGs by directly binding to gene promoters. In agreement, the erf115 phytochrome a signal transduction1-2 (pat1-2) double mutant exhibited reduced cell expansion under heat stress with diminished autophagic activity. Overall, our findings indicate that heat-stress-induced cell death triggers autophagy-mediated cell expansion in plant leaves, which may compensate for the death of nearby cells. Overall design: Total RNA was extracted with a Plant RNA extraction kit (Takara, 9769B) from 1st and 2nd rosette leaves at 1 and 48 h after wound or heat treatment. Three biological replicates were collected. Sequencing libraries were constructed with a TruSeq standard mRNA library kit followed by 100-bp paired-end sequencing using the Illumina NovaSeq platform.