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Article|01 Dec 2020|OPEN
Transcriptional regulation of bark freezing tolerance in apple (Malus domestica Borkh.)
Yinghai Liang1, Shanshan Wang1, Chenhui Zhao1, Xinwei Ma2, Yiyong Zhao3, Jing Shao1, Yuebo Li1, Honglian Li1, Hongwei Song1, Hong Ma2, Hao Li2,, Bingbing Zhang1, & Liangsheng Zhang4
1Institute of Pomology, Jilin Academy of Agricultural Sciences, 136100 Gongzhuling, People’s Republic of China
2Department of Biology, Eberly College of Science, and The Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA 16802, USA
3Ministry of Education Key Laboratory of Biodiversity Sciences and Ecological Engineering, Collaborative Innovation Center for Genetics and Development, Institute of Biodiversity Sciences, Institute of Plant Biology, Center for Evolutionary Biology, School of Life Sciences, Fudan University, 200438 Shanghai, People’s Republic of China
4Genomics and Genetic Engineering Laboratory of Ornamental Plants, College of Agriculture and Biotechnology, Zhejiang University, 310058 Hangzhou, People’s Republic of China

Horticulture Research 7,
Article number: 205 (2020)
doi: 10.1038/hortres.2020.205
Views: 328

Received: 14 Apr 2020
Revised: 01 Oct 2020
Accepted: 06 Oct 2020
Published online: 01 Dec 2020


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.