Comparative transcriptome analysis provides molecular insights into heterosis of waterlogging tolerance in Chrysanthemum indicum

Abstract Background Heterosis breeding is one of the most important breeding methods for chrysanthemum. To date, the genetic mechanisms of heterosis for waterlogging tolerance in chrysanthemum are still unclear. This study aims to analyze the expression profiles and potential heterosis-related genes...

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Main Authors: Jiangshuo Su, Limin Zhao, Yingnan Yang, Yang Yang, Xuefeng Zhang, Zhiyong Guan, Weimin Fang, Fadi Chen, Fei Zhang
Format: Article
Language:English
Published: BMC 2024-04-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-024-04954-4
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author Jiangshuo Su
Limin Zhao
Yingnan Yang
Yang Yang
Xuefeng Zhang
Zhiyong Guan
Weimin Fang
Fadi Chen
Fei Zhang
author_facet Jiangshuo Su
Limin Zhao
Yingnan Yang
Yang Yang
Xuefeng Zhang
Zhiyong Guan
Weimin Fang
Fadi Chen
Fei Zhang
author_sort Jiangshuo Su
collection DOAJ
description Abstract Background Heterosis breeding is one of the most important breeding methods for chrysanthemum. To date, the genetic mechanisms of heterosis for waterlogging tolerance in chrysanthemum are still unclear. This study aims to analyze the expression profiles and potential heterosis-related genes of two hybrid lines and their parents with extreme differences in waterlogging tolerance under control and waterlogging stress conditions by RNA-seq. Results A population of 140 F1 progeny derived from Chrysanthemum indicum (Nanchang) (waterlogging-tolerant) and Chrysanthemum indicum (Nanjing) (waterlogging-sensitive) was used to characterize the extent of genetic variation in terms of seven waterlogging tolerance-related traits across two years. Lines 98 and 95, respectively displaying positive and negative overdominance heterosis for the waterlogging tolerance traits together with their parents under control and waterlogging stress conditions, were used for RNA-seq. In consequence, the maximal number of differentially expressed genes (DEGs) occurred in line 98. Gene ontology (GO) enrichment analysis revealed multiple stress-related biological processes for the common up-regulated genes. Line 98 had a significant increase in non-additive genes under waterlogging stress, with transgressive up-regulation and paternal-expression dominant patterns being the major gene expression profiles. Further, GO analysis identified 55 and 95 transgressive up-regulation genes that overlapped with the up-regulated genes shared by two parents in terms of responses to stress and stimulus, respectively. 6,640 genes in total displaying maternal-expression dominance patterns were observed in line 95. In addition, 16 key candidate genes, including SAP12, DOX1, and ERF017 which might be of significant importance for the formation of waterlogging tolerance heterosis in line 98, were highlighted. Conclusion The current study provides a comprehensive overview of the root transcriptomes among F1 hybrids and their parents under waterlogging stress. These findings lay the foundation for further studies on molecular mechanisms underlying chrysanthemum heterosis on waterlogging tolerance.
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spelling doaj.art-d96010d0c6784f8c8e32b5d20061823e2024-04-14T11:11:59ZengBMCBMC Plant Biology1471-22292024-04-0124111610.1186/s12870-024-04954-4Comparative transcriptome analysis provides molecular insights into heterosis of waterlogging tolerance in Chrysanthemum indicumJiangshuo Su0Limin Zhao1Yingnan Yang2Yang Yang3Xuefeng Zhang4Zhiyong Guan5Weimin Fang6Fadi Chen7Fei Zhang8State Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, Key Laboratory of Biology of Ornamental Plants in East China, College of Horticulture, National Forestry and Grassland Administration, Nanjing Agricultural UniversityState Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, Key Laboratory of Biology of Ornamental Plants in East China, College of Horticulture, National Forestry and Grassland Administration, Nanjing Agricultural UniversityState Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, Key Laboratory of Biology of Ornamental Plants in East China, College of Horticulture, National Forestry and Grassland Administration, Nanjing Agricultural UniversityState Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, Key Laboratory of Biology of Ornamental Plants in East China, College of Horticulture, National Forestry and Grassland Administration, Nanjing Agricultural UniversityState Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, Key Laboratory of Biology of Ornamental Plants in East China, College of Horticulture, National Forestry and Grassland Administration, Nanjing Agricultural UniversityState Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, Key Laboratory of Biology of Ornamental Plants in East China, College of Horticulture, National Forestry and Grassland Administration, Nanjing Agricultural UniversityState Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, Key Laboratory of Biology of Ornamental Plants in East China, College of Horticulture, National Forestry and Grassland Administration, Nanjing Agricultural UniversityState Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, Key Laboratory of Biology of Ornamental Plants in East China, College of Horticulture, National Forestry and Grassland Administration, Nanjing Agricultural UniversityState Key Laboratory of Crop Genetics & Germplasm Enhancement and Utilization, Key Laboratory of Biology of Ornamental Plants in East China, College of Horticulture, National Forestry and Grassland Administration, Nanjing Agricultural UniversityAbstract Background Heterosis breeding is one of the most important breeding methods for chrysanthemum. To date, the genetic mechanisms of heterosis for waterlogging tolerance in chrysanthemum are still unclear. This study aims to analyze the expression profiles and potential heterosis-related genes of two hybrid lines and their parents with extreme differences in waterlogging tolerance under control and waterlogging stress conditions by RNA-seq. Results A population of 140 F1 progeny derived from Chrysanthemum indicum (Nanchang) (waterlogging-tolerant) and Chrysanthemum indicum (Nanjing) (waterlogging-sensitive) was used to characterize the extent of genetic variation in terms of seven waterlogging tolerance-related traits across two years. Lines 98 and 95, respectively displaying positive and negative overdominance heterosis for the waterlogging tolerance traits together with their parents under control and waterlogging stress conditions, were used for RNA-seq. In consequence, the maximal number of differentially expressed genes (DEGs) occurred in line 98. Gene ontology (GO) enrichment analysis revealed multiple stress-related biological processes for the common up-regulated genes. Line 98 had a significant increase in non-additive genes under waterlogging stress, with transgressive up-regulation and paternal-expression dominant patterns being the major gene expression profiles. Further, GO analysis identified 55 and 95 transgressive up-regulation genes that overlapped with the up-regulated genes shared by two parents in terms of responses to stress and stimulus, respectively. 6,640 genes in total displaying maternal-expression dominance patterns were observed in line 95. In addition, 16 key candidate genes, including SAP12, DOX1, and ERF017 which might be of significant importance for the formation of waterlogging tolerance heterosis in line 98, were highlighted. Conclusion The current study provides a comprehensive overview of the root transcriptomes among F1 hybrids and their parents under waterlogging stress. These findings lay the foundation for further studies on molecular mechanisms underlying chrysanthemum heterosis on waterlogging tolerance.https://doi.org/10.1186/s12870-024-04954-4ChrysanthemumHeterosisWaterlogging toleranceRNA-seqOverdominant expression
spellingShingle Jiangshuo Su
Limin Zhao
Yingnan Yang
Yang Yang
Xuefeng Zhang
Zhiyong Guan
Weimin Fang
Fadi Chen
Fei Zhang
Comparative transcriptome analysis provides molecular insights into heterosis of waterlogging tolerance in Chrysanthemum indicum
BMC Plant Biology
Chrysanthemum
Heterosis
Waterlogging tolerance
RNA-seq
Overdominant expression
title Comparative transcriptome analysis provides molecular insights into heterosis of waterlogging tolerance in Chrysanthemum indicum
title_full Comparative transcriptome analysis provides molecular insights into heterosis of waterlogging tolerance in Chrysanthemum indicum
title_fullStr Comparative transcriptome analysis provides molecular insights into heterosis of waterlogging tolerance in Chrysanthemum indicum
title_full_unstemmed Comparative transcriptome analysis provides molecular insights into heterosis of waterlogging tolerance in Chrysanthemum indicum
title_short Comparative transcriptome analysis provides molecular insights into heterosis of waterlogging tolerance in Chrysanthemum indicum
title_sort comparative transcriptome analysis provides molecular insights into heterosis of waterlogging tolerance in chrysanthemum indicum
topic Chrysanthemum
Heterosis
Waterlogging tolerance
RNA-seq
Overdominant expression
url https://doi.org/10.1186/s12870-024-04954-4
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