Transcriptional regulation of bark freezing tolerance in apple (Malus domestica Borkh.)
Open Access
- 1 December 2020
- journal article
- research article
- Published by Oxford University Press (OUP) in Horticulture Research
- Vol. 7 (1), 1-16
- https://doi.org/10.1038/s41438-020-00432-8
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.Keywords
This publication has 84 references indexed in Scilit:
- A Self-Regulatory Circuit of CIRCADIAN CLOCK-ASSOCIATED1 Underlies the Circadian Clock Regulation of Temperature Responses in ArabidopsisTHE PLANT CELL ONLINE, 2012
- Ectopic expression of a novel peach (Prunus persica) CBF transcription factor in apple (Malus × domestica) results in short-day induced dormancy and increased cold hardinessPlanta, 2011
- The genome of the domesticated apple (Malus × domestica Borkh.)Nature Genetics, 2010
- HRE1 and HRE2, two hypoxia-inducible ethylene response factors, affect anaerobic responses in Arabidopsis thalianaThe Plant Journal, 2010
- edgeR: a Bioconductor package for differential expression analysis of digital gene expression dataBioinformatics, 2009
- QuickGO: a web-based tool for Gene Ontology searchingBioinformatics, 2009
- TopHat: discovering splice junctions with RNA-SeqBioinformatics, 2009
- ArabidopsisCBF1 and CBF3 have a different function than CBF2 in cold acclimation and define different gene classes in the CBF regulonProceedings of the National Academy of Sciences of the United States of America, 2007
- A central integrator of transcription networks in plant stress and energy signallingNature, 2007
- Natural Genetic Variation of Freezing Tolerance in ArabidopsisPlant Physiology, 2006