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Transcriptional regulation of bark freezing tolerance in apple (Malus domestica Borkh.).

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 (K_ME) 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.

SUBMITTER: Liang Y

PROVIDER: S-EPMC7705664 | biostudies-literature | 2020 Dec

REPOSITORIES: biostudies-literature

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Transcriptional regulation of bark freezing tolerance in apple (Malus domestica Borkh.).

Liang Yinghai Y Wang Shanshan S Zhao Chenhui C Ma Xinwei X Zhao Yiyong Y Shao Jing J Li Yuebo Y Li Honglian H Song Hongwei H Ma Hong H Li Hao H Zhang Bingbing B Zhang Liangsheng L

Horticulture research 20201201 1

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 divergenc ...[more]

PMID: 33328456

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Project description:BACKGROUND: Gene duplication is central to genome evolution. In plants, genes can be duplicated through small-scale events and large-scale duplications often involving polyploidy. The apple belongs to the subtribe Pyrinae (Rosaceae), a diverse lineage that originated via allopolyploidization. Both small-scale duplications and polyploidy may have been important mechanisms shaping the genome of this species. RESULTS: This study evaluates the gene duplication and polyploidy history of the apple by characterizing duplicated genes in this species using EST data. Overall, 68% of the apple genes were clustered into families with a mean copy-number of 4.6. Analysis of the age distribution of gene duplications supported a continuous mode of small-scale duplications, plus two episodes of large-scale duplicates of vastly different ages. The youngest was consistent with the polyploid origin of the Pyrinae 37-48 MYBP, whereas the older may be related to gamma-triplication; an ancient hexapolyploidization previously characterized in the four sequenced eurosid genomes and basal to the eurosid-asterid divergence. Duplicated genes were studied for functional diversification with an emphasis on young paralogs; those originated during or after the formation of the Pyrinae lineage. Unequal assignment of single-copy genes and gene families to Gene Ontology categories suggested functional bias in the pattern of gene retention of paralogs. Young paralogs related to signal transduction, metabolism, and energy pathways have been preferentially retained. Non-random retention of duplicated genes seems to have mediated the expansion of gene families, some of which may have substantially increased their members after the origin of the Pyrinae. The joint analysis of over-duplicated functional categories and phylogenies, allowed evaluation of the role of both polyploidy and small-scale duplications during this process. Finally, gene expression analysis indicated that 82% of duplicated genes, including 80% of young paralogs, showed uncorrelated expression profiles, suggesting extensive subfunctionalization and a role of gene duplication in the acquisition of novel patterns of gene expression. CONCLUSIONS: This study reports a genome-wide analysis of the mode of gene duplication in the apple, and provides evidence for its role in genome functional diversification by characterising three major processes: selective retention of paralogs, amplification of gene families, and changes in gene expression.

Dataset Information

Transcriptional regulation of bark freezing tolerance in apple (Malus domestica Borkh.).

Publications

Transcriptional regulation of bark freezing tolerance in apple (Malus domestica Borkh.).

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