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Full-length transcriptome profiling reveals insight into the cold response of two kiwifruit genotypes (A. arguta) with contrasting freezing tolerances

BACKGROUND: Kiwifruit (Actinidia Lindl.) is considered an important fruit species worldwide. Due to its temperate origin, this species is highly vulnerable to freezing injury while under low-temperature stress. To obtain further knowledge of the mechanism underlying freezing tolerance, we carried ou...

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Autores principales: Sun, Shihang, Lin, Miaomiao, Qi, Xiujuan, Chen, Jinyong, Gu, Hong, Zhong, Yunpeng, Sun, Leiming, Muhammad, Abid, Bai, Danfeng, Hu, Chungen, Fang, Jinbao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8356467/
https://www.ncbi.nlm.nih.gov/pubmed/34380415
http://dx.doi.org/10.1186/s12870-021-03152-w
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author Sun, Shihang
Lin, Miaomiao
Qi, Xiujuan
Chen, Jinyong
Gu, Hong
Zhong, Yunpeng
Sun, Leiming
Muhammad, Abid
Bai, Danfeng
Hu, Chungen
Fang, Jinbao
author_facet Sun, Shihang
Lin, Miaomiao
Qi, Xiujuan
Chen, Jinyong
Gu, Hong
Zhong, Yunpeng
Sun, Leiming
Muhammad, Abid
Bai, Danfeng
Hu, Chungen
Fang, Jinbao
author_sort Sun, Shihang
collection PubMed
description BACKGROUND: Kiwifruit (Actinidia Lindl.) is considered an important fruit species worldwide. Due to its temperate origin, this species is highly vulnerable to freezing injury while under low-temperature stress. To obtain further knowledge of the mechanism underlying freezing tolerance, we carried out a hybrid transcriptome analysis of two A. arguta (Actinidi arguta) genotypes, KL and RB, whose freezing tolerance is high and low, respectively. Both genotypes were subjected to − 25 °C for 0 h, 1 h, and 4 h. RESULTS: SMRT (single-molecule real-time) RNA-seq data were assembled using the de novo method, producing 24,306 unigenes with an N50 value of 1834 bp. Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analysis of DEGs showed that they were involved in the ‘starch and sucrose metabolism’, the ‘mitogen-activated protein kinase (MAPK) signaling pathway’, the ‘phosphatidylinositol signaling system’, the ‘inositol phosphate metabolism’, and the ‘plant hormone signal transduction’. In particular, for ‘starch and sucrose metabolism’, we identified 3 key genes involved in cellulose degradation, trehalose synthesis, and starch degradation processes. Moreover, the activities of beta-GC (beta-glucosidase), TPS (trehalose-6-phosphate synthase), and BAM (beta-amylase), encoded by the abovementioned 3 key genes, were enhanced by cold stress. Three transcription factors (TFs) belonging to the AP2/ERF, bHLH (basic helix-loop-helix), and MYB families were involved in the low-temperature response. Furthermore, weighted gene coexpression network analysis (WGCNA) indicated that beta-GC, TPS5, and BAM3.1 were the key genes involved in the cold response and were highly coexpressed together with the CBF3, MYC2, and MYB44 genes. CONCLUSIONS: Cold stress led various changes in kiwifruit, the ‘phosphatidylinositol signaling system’, ‘inositol phosphate metabolism’, ‘MAPK signaling pathway’, ‘plant hormone signal transduction’, and ‘starch and sucrose metabolism’ processes were significantly affected by low temperature. Moreover, starch and sucrose metabolism may be the key pathway for tolerant kiwifruit to resist low temperature damages. These results increase our understanding of the complex mechanisms involved in the freezing tolerance of kiwifruit under cold stress and reveal a series of candidate genes for use in breeding new cultivars with enhanced freezing tolerance. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-03152-w.
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spelling pubmed-83564672021-08-16 Full-length transcriptome profiling reveals insight into the cold response of two kiwifruit genotypes (A. arguta) with contrasting freezing tolerances Sun, Shihang Lin, Miaomiao Qi, Xiujuan Chen, Jinyong Gu, Hong Zhong, Yunpeng Sun, Leiming Muhammad, Abid Bai, Danfeng Hu, Chungen Fang, Jinbao BMC Plant Biol Research BACKGROUND: Kiwifruit (Actinidia Lindl.) is considered an important fruit species worldwide. Due to its temperate origin, this species is highly vulnerable to freezing injury while under low-temperature stress. To obtain further knowledge of the mechanism underlying freezing tolerance, we carried out a hybrid transcriptome analysis of two A. arguta (Actinidi arguta) genotypes, KL and RB, whose freezing tolerance is high and low, respectively. Both genotypes were subjected to − 25 °C for 0 h, 1 h, and 4 h. RESULTS: SMRT (single-molecule real-time) RNA-seq data were assembled using the de novo method, producing 24,306 unigenes with an N50 value of 1834 bp. Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analysis of DEGs showed that they were involved in the ‘starch and sucrose metabolism’, the ‘mitogen-activated protein kinase (MAPK) signaling pathway’, the ‘phosphatidylinositol signaling system’, the ‘inositol phosphate metabolism’, and the ‘plant hormone signal transduction’. In particular, for ‘starch and sucrose metabolism’, we identified 3 key genes involved in cellulose degradation, trehalose synthesis, and starch degradation processes. Moreover, the activities of beta-GC (beta-glucosidase), TPS (trehalose-6-phosphate synthase), and BAM (beta-amylase), encoded by the abovementioned 3 key genes, were enhanced by cold stress. Three transcription factors (TFs) belonging to the AP2/ERF, bHLH (basic helix-loop-helix), and MYB families were involved in the low-temperature response. Furthermore, weighted gene coexpression network analysis (WGCNA) indicated that beta-GC, TPS5, and BAM3.1 were the key genes involved in the cold response and were highly coexpressed together with the CBF3, MYC2, and MYB44 genes. CONCLUSIONS: Cold stress led various changes in kiwifruit, the ‘phosphatidylinositol signaling system’, ‘inositol phosphate metabolism’, ‘MAPK signaling pathway’, ‘plant hormone signal transduction’, and ‘starch and sucrose metabolism’ processes were significantly affected by low temperature. Moreover, starch and sucrose metabolism may be the key pathway for tolerant kiwifruit to resist low temperature damages. These results increase our understanding of the complex mechanisms involved in the freezing tolerance of kiwifruit under cold stress and reveal a series of candidate genes for use in breeding new cultivars with enhanced freezing tolerance. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-03152-w. BioMed Central 2021-08-11 /pmc/articles/PMC8356467/ /pubmed/34380415 http://dx.doi.org/10.1186/s12870-021-03152-w Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Sun, Shihang
Lin, Miaomiao
Qi, Xiujuan
Chen, Jinyong
Gu, Hong
Zhong, Yunpeng
Sun, Leiming
Muhammad, Abid
Bai, Danfeng
Hu, Chungen
Fang, Jinbao
Full-length transcriptome profiling reveals insight into the cold response of two kiwifruit genotypes (A. arguta) with contrasting freezing tolerances
title Full-length transcriptome profiling reveals insight into the cold response of two kiwifruit genotypes (A. arguta) with contrasting freezing tolerances
title_full Full-length transcriptome profiling reveals insight into the cold response of two kiwifruit genotypes (A. arguta) with contrasting freezing tolerances
title_fullStr Full-length transcriptome profiling reveals insight into the cold response of two kiwifruit genotypes (A. arguta) with contrasting freezing tolerances
title_full_unstemmed Full-length transcriptome profiling reveals insight into the cold response of two kiwifruit genotypes (A. arguta) with contrasting freezing tolerances
title_short Full-length transcriptome profiling reveals insight into the cold response of two kiwifruit genotypes (A. arguta) with contrasting freezing tolerances
title_sort full-length transcriptome profiling reveals insight into the cold response of two kiwifruit genotypes (a. arguta) with contrasting freezing tolerances
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8356467/
https://www.ncbi.nlm.nih.gov/pubmed/34380415
http://dx.doi.org/10.1186/s12870-021-03152-w
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