Abstract
Freezing tolerance is a significant trait in plants that grow in cold environments and survive through the winter. Apple (Malus domestica Borkh.) is a cold-tolerant fruit tree, and the cold tolerance of its bark is important for its survival at low temperatures. However, little is known about the gene activity related to its freezing tolerance. To better understand the gene expression and regulation properties of freezing tolerance in dormant apple trees, we analyzed the transcriptomic divergences in the bark from 1-year-old branches of two apple cultivars, “Golden Delicious” (G) and “Jinhong” (H), which have different levels of cold resistance, under chilling and freezing treatments. “H” can safely overwinter below −30 °C in extremely low-temperature regions, whereas “G” experiences severe freezing damage and death in similar environments. Based on 28 bark transcriptomes (from the epidermis, phloem, and cambium) from 1-year-old branches under seven temperature treatments (from 4 to −29 °C), we identified 4173 and 7734 differentially expressed genes (DEGs) in “G” and “H”, respectively, between the chilling and freezing treatments. A gene coexpression network was constructed according to this expression information using weighted gene correlation network analysis (WGCNA), and seven biologically meaningful coexpression modules were identified from the network. The expression profiles of the genes from these modules suggested the gene regulatory pathways that are responsible for the chilling and freezing stress responses of “G” and/or “H.” Module 7 was probably related to freezing acclimation and freezing damage in “H” at the lower temperatures. This module contained more interconnected hub transcription factors (TFs) and cold-responsive genes (CORs). Modules 6 and 7 contained C-repeat binding factor (CBF) TFs, and many CBF-dependent homologs were identified as hub genes. We also found that some hub TFs had higher intramodular connectivity (KME) and gene significance (GS) than CBFs. Specifically, most hub TFs in modules 6 and 7 were activated at the beginning of the early freezing stress phase and maintained upregulated expression during the whole freezing stress period in “G” and “H”. The upregulation of DEGs related to methionine and carbohydrate biosynthetic processes in “H” under more severe freezing stress supported the maintenance of homeostasis in the cellular membrane. This study improves our understanding of the transcriptional regulation patterns underlying freezing tolerance in the bark of apple branches.
Highlights
The domesticated apple (Malus domestica Borkh.: Rosaceae) is one of the most abundant fruit crops in the world[1,2]
To detect the differences in cold tolerance between “Golden Delicious” (“G”) and “Jinhong” (“H”) (Fig. 1A–C), we estimated the electrolyte leakage rates (ELR) of 1-year-old branches of “G” and “H” that were treated for 24 h at seven low temperatures, from 4 to −29 °C (Fig. 1D)
The results showed that the ELR of “G” was similar to that of “H” at 4, −4, −9, −14, and −19 °C; the ELRs of the two cultivars were significantly different at both −24 and −29 °C
Summary
The domesticated apple (Malus domestica Borkh.: Rosaceae) is one of the most abundant fruit crops in the world[1,2]. Many temperate plant species have evolved a sophisticated process, called cold acclimation, by which plants can acquire freezing tolerance after being exposed to low and nonfreezing temperatures[9,10]. This process involves many physiological and biochemical changes and allows hardy plants to activate expression of many transcription factors (TFs) and cold-responsive genes (CORs) to resist freezing stress[9,10,11]. More than twothirds of COR genes are coregulated by two or three
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