Transcriptome analysis of the symbiotic response of Arabidopsis at different temperatures.

High ambient temperature regulated the plant systemic response to the beneficial endophytic fungus Serendipita indica. Most plants in nature establish symbiotic associations with endophytic fungi in soil. Beneficial endophytic fungi induce a systemic response in the aboveground parts of the host plant, thus promoting the growth and fitness of host plants. Meanwhile, temperature elevation from climate change widely affects global plant biodiversity as well as crop quality and yield. Over the past decades, great progresses have been made in the response of plants to high ambient temperature and to symbiosis with endophytic fungi. However, little is known about their synergistic effect on host plants. The endophytic fungus Serendipita indica colonizes the roots of a wide range of plants, including Arabidopsis. Based on the Arabidopsis-S. indica symbiosis experimental system, we analyzed the synergistic effect of high ambient temperature and endophytic fungal symbiosis on host plants. By transcriptome analysis, we found that DNA replication-related genes were significantly upregulated during the systemic response of Arabidopsis aboveground parts to S. indica colonization. Plant hormones, such as jasmonic acid (JA) and ethylene (ET), play important roles in plant growth and systemic responses. We found that high ambient temperature repressed the JA and ET signaling pathways of Arabidopsis aboveground parts during the systemic response to S. indica colonization in roots. Meanwhile, PIF4 is the central hub transcription factor controlling plant thermosensory growth under high ambient temperature in Arabidopsis. PIF4 is also involving JA and/or ET signaling pathway. We found that PIF4 target genes overlapped with many differentially expressed genes (DEGs) during the systemic response, and further showed that the growth promotion efficiency of S. indica on the pif4 mutant was higher than that on the wild type plants. Overall design: The aboveground parts of S. indica-inoculated Arabidopsis at 7 dpi were harvested for transcriptome. Arabidopsis was grown on half-strength MS medium with 1.2% sucrose (½MS). The seeds were stratified at 4°C for 3 days and then first grown at 22°C under short-day growth condition (12 h: 12 h, day: night photoperiod, 7000 LX light) in growth chambers. Serendipita indica (syn. Piriformospora indica, DSM11827) fungus were grown and conserved in PDA medium (200 g L-1 potato, 20 g L-1 dextrose and 20 g L-1 agar). For cocultivation with S. indica, 9-day-old Arabidopsis seedlings were inoculated with S. indica in PNM medium plates. S. indica-incubated (Si) and control (CK) samples were grown at 22°C, 25°C or 28°C under short-day growth condition.