Integrative DNA methylome and transcriptome analysis illuminate leaf phenotype alterations in tetraploid citrus

Abstract Whole-genome duplication (WGD) in plants triggers profound morphological and physiological changes, with DNA modification being a key epigenetic factor that helps neo-polyploids overcome challenges and gain adaptive advantages. Tetraploids were previously mined from diploid citrus seedlings...

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Main Authors: Hu Gao, Gong-Ao Xiao, Yi Bao, Qiang-Ming Xia, Kai-Dong Xie, Xiao-Meng Wu, Wen-Wu Guo
Format: Article
Language:English
Published: Springer 2024-11-01
Series:Horticulture Advances
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Online Access:https://doi.org/10.1007/s44281-024-00051-6
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author Hu Gao
Gong-Ao Xiao
Yi Bao
Qiang-Ming Xia
Kai-Dong Xie
Xiao-Meng Wu
Wen-Wu Guo
author_facet Hu Gao
Gong-Ao Xiao
Yi Bao
Qiang-Ming Xia
Kai-Dong Xie
Xiao-Meng Wu
Wen-Wu Guo
author_sort Hu Gao
collection DOAJ
description Abstract Whole-genome duplication (WGD) in plants triggers profound morphological and physiological changes, with DNA modification being a key epigenetic factor that helps neo-polyploids overcome challenges and gain adaptive advantages. Tetraploids were previously mined from diploid citrus seedlings, showing enhanced environmental adaptability and potential as rootstocks. These tetraploids exhibited increased leaf and cell wall thickness compared to their diploid counterparts. To explore the impact of WGD, transcriptomic and whole-genome bisulfite sequencing (WGBS) were conducted on two pairs of citrus tetraploids and their diploid controls, revealing significant molecular changes. Notably, tetraploid citrus displayed lower CG methylation levels in gene and transposable element (TE) bodies relative to diploids. Differentially methylated genes (DMGs) between tetraploids and diploids were primarily associated with immune stress, organ development, metabolic pathways, and secondary metabolism. In Trifoliate orange (Poncirus trifoliata L. Raf.) and Ziyang Xiangcheng (Citrus junos Sieb. ex Tanaka), only 150 and 58 differentially expressed genes (DEGs) were identified, respectively, with enrichment in critical cellular processes such as cell wall synthesis, plastid development, and pathways modulating chloroplasts and plasma membranes. A total of 70 genes showed both differential methylation and expression, including ACN1, Nac036, and ASMT1, which are involved in stomatal development, leaf morphology, and melatonin synthesis, respectively, offering insight into the regulatory mechanisms of phenotype alterations after polyploidization. These findings reveal the epigenetic modifications in polyploid citrus and highlight the role of polyploidization-induced methylation in driving phenotypic changes.
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spelling doaj-art-1cbb12258dfd4b4a9e16b38288c664982025-08-20T02:50:07ZengSpringerHorticulture Advances2948-11042024-11-012111510.1007/s44281-024-00051-6Integrative DNA methylome and transcriptome analysis illuminate leaf phenotype alterations in tetraploid citrusHu Gao0Gong-Ao Xiao1Yi Bao2Qiang-Ming Xia3Kai-Dong Xie4Xiao-Meng Wu5Wen-Wu Guo6National Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityNational Key Laboratory for Germplasm Innovation & Utilization of Horticultural Crops, College of Horticulture and Forestry Sciences, Huazhong Agricultural UniversityAbstract Whole-genome duplication (WGD) in plants triggers profound morphological and physiological changes, with DNA modification being a key epigenetic factor that helps neo-polyploids overcome challenges and gain adaptive advantages. Tetraploids were previously mined from diploid citrus seedlings, showing enhanced environmental adaptability and potential as rootstocks. These tetraploids exhibited increased leaf and cell wall thickness compared to their diploid counterparts. To explore the impact of WGD, transcriptomic and whole-genome bisulfite sequencing (WGBS) were conducted on two pairs of citrus tetraploids and their diploid controls, revealing significant molecular changes. Notably, tetraploid citrus displayed lower CG methylation levels in gene and transposable element (TE) bodies relative to diploids. Differentially methylated genes (DMGs) between tetraploids and diploids were primarily associated with immune stress, organ development, metabolic pathways, and secondary metabolism. In Trifoliate orange (Poncirus trifoliata L. Raf.) and Ziyang Xiangcheng (Citrus junos Sieb. ex Tanaka), only 150 and 58 differentially expressed genes (DEGs) were identified, respectively, with enrichment in critical cellular processes such as cell wall synthesis, plastid development, and pathways modulating chloroplasts and plasma membranes. A total of 70 genes showed both differential methylation and expression, including ACN1, Nac036, and ASMT1, which are involved in stomatal development, leaf morphology, and melatonin synthesis, respectively, offering insight into the regulatory mechanisms of phenotype alterations after polyploidization. These findings reveal the epigenetic modifications in polyploid citrus and highlight the role of polyploidization-induced methylation in driving phenotypic changes.https://doi.org/10.1007/s44281-024-00051-6CitrusPolyploidDNA methylationTranscriptomeDMG
spellingShingle Hu Gao
Gong-Ao Xiao
Yi Bao
Qiang-Ming Xia
Kai-Dong Xie
Xiao-Meng Wu
Wen-Wu Guo
Integrative DNA methylome and transcriptome analysis illuminate leaf phenotype alterations in tetraploid citrus
Horticulture Advances
Citrus
Polyploid
DNA methylation
Transcriptome
DMG
title Integrative DNA methylome and transcriptome analysis illuminate leaf phenotype alterations in tetraploid citrus
title_full Integrative DNA methylome and transcriptome analysis illuminate leaf phenotype alterations in tetraploid citrus
title_fullStr Integrative DNA methylome and transcriptome analysis illuminate leaf phenotype alterations in tetraploid citrus
title_full_unstemmed Integrative DNA methylome and transcriptome analysis illuminate leaf phenotype alterations in tetraploid citrus
title_short Integrative DNA methylome and transcriptome analysis illuminate leaf phenotype alterations in tetraploid citrus
title_sort integrative dna methylome and transcriptome analysis illuminate leaf phenotype alterations in tetraploid citrus
topic Citrus
Polyploid
DNA methylation
Transcriptome
DMG
url https://doi.org/10.1007/s44281-024-00051-6
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