Transcriptome analysis of tree peony under high temperature treatment and functional verification of PsDREB2A gene

Plant Physiol Biochem. 2024 Dec 15:219:109405. doi: 10.1016/j.plaphy.2024.109405. Online ahead of print.

Abstract

Paeonia suffruticosa is a plant of Paeonia in Paeoniaceae. It is an important woody ornamental flower in the world. High temperature in summer hinders the growth of tree peony and reduces its ornamental quality, which restricts the cultivation and application of tree peony in Jiangnan area of China. Paeonia suffruticosa 'Hu Hong' is a traditional Chinese tree peony variety with high ornamental value. It is an excellent parent material for cultivating heat-resistant peony. This paper selected the tree peony variety 'Hu Hong' as the material. The transcriptome data of Paeonia suffruticosa 'Hu Hong' at 0, 2, 6, 12 and 24 h after high temperature treatment were analyzed by RNA-Seq method. At each time point, a large number of significantly differentially expressed genes(DEGs) were screened between tree peony cultured at high temperature and room temperature. The analysis of the common DEGs in the four comparison groups showed that the differential genes were mainly enriched in the GO terms ' protein processing in endoplasmic reticulum', 'Pentose and glucuronate interconversions ', ' plant-pathogen interaction ', ' zeatin biosynthesis ', ' fatty acid elongation ', and ' plant hormone signal transduction ' pathways. Abscisic acid(ABA), ethylene(ET) and brassinosteroid(BR) signaling related genes were significantly up-regulated in 'Hu Hong' to resist high temperature treatment. In the auxin(IAA), cytokinin(CTK), gibberellin(GA), salicylic acid(SA) pathways, compared with the control group, the down-regulated expression was involved in hormone signal transduction to respond to high temperature treatment. A total of 62 TFs from 28 different families were annotated, with the AP2/ERF family annotating the largest number. Among the TFs annotated to the AP2/ERF family, the highest expression gene PsDREB2A was found. Overexpression of PsDREB2A Arabidopsis plants improved heat tolerance under high temperature treatment. However, silencing PsDREB2A in tree peony resulted in a heat-intolerant phenotype. PsDREB2A can directly bind to the DRE-core motif in the PsHSFA3 promoter to initiate its expression. In addition, PsHSFA3-overexpressing plants showed higher heat resistance, while PsHSFA3-silenced plants showed lower heat resistance. This study provides a scientific basis for in-depth study of the molecular mechanism of high temperature treatment response in tree peony, improving the heat signal transduction regulation network of tree peony, and mining heat-resistant related genes.

Keywords: DREB2A; HSFA3; High temperature treatment; Transcriptome analysis; Tree peony.