Genomic and cytogenetic analyses reveal satellite repeat signature in allotetraploid okra (Abelmoschus esculentus)

Abstract Background Satellite repeats are one of the most rapidly evolving components in eukaryotic genomes and play vital roles in genome regulation, genome evolution, and speciation. As a consequence, the composition, abundance and chromosome distribution of satellite repeats often exhibit variabi...

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Main Authors: Jiarui Liu, Xinyi Lin, Xiaojie Wang, Liqing Feng, Shixin Zhu, Runmeng Tian, Jingping Fang, Aifen Tao, Pingping Fang, Jianmin Qi, Liwu Zhang, Yongji Huang, Jiantang Xu
Format: Article
Language:English
Published: BMC 2024-01-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-024-04739-9
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author Jiarui Liu
Xinyi Lin
Xiaojie Wang
Liqing Feng
Shixin Zhu
Runmeng Tian
Jingping Fang
Aifen Tao
Pingping Fang
Jianmin Qi
Liwu Zhang
Yongji Huang
Jiantang Xu
author_facet Jiarui Liu
Xinyi Lin
Xiaojie Wang
Liqing Feng
Shixin Zhu
Runmeng Tian
Jingping Fang
Aifen Tao
Pingping Fang
Jianmin Qi
Liwu Zhang
Yongji Huang
Jiantang Xu
author_sort Jiarui Liu
collection DOAJ
description Abstract Background Satellite repeats are one of the most rapidly evolving components in eukaryotic genomes and play vital roles in genome regulation, genome evolution, and speciation. As a consequence, the composition, abundance and chromosome distribution of satellite repeats often exhibit variability across various species, genome, and even individual chromosomes. However, we know little about the satellite repeat evolution in allopolyploid genomes. Results In this study, we investigated the satellite repeat signature in five okra (Abelmoschus esculentus) accessions using genomic and cytogenetic methods. In each of the five accessions, we identified eight satellite repeats, which exhibited a significant level of intraspecific conservation. Through fluorescence in situ hybridization (FISH) experiments, we observed that the satellite repeats generated multiple signals and exhibited variations in copy number across chromosomes. Intriguingly, we found that five satellite repeats were interspersed with centromeric retrotransposons, signifying their involvement in centromeric satellite repeat identity. We confirmed subgenome-biased amplification patterns of these satellite repeats through existing genome assemblies or dual-color FISH, indicating their distinct dynamic evolution in the allotetraploid okra subgenome. Moreover, we observed the presence of multiple chromosomes harboring the 35 S rDNA loci, alongside another chromosomal pair carrying the 5 S rDNA loci in okra using FISH assay. Remarkably, the intensity of 35 S rDNA hybridization signals varied among chromosomes, with the signals predominantly localized within regions of relatively weak DAPI staining, associated with GC-rich heterochromatin regions. Finally, we observed a similar localization pattern between 35 S rDNA and three satellite repeats with high GC content and confirmed their origin in the intergenic spacer region of the 35 S rDNA. Conclusions Our findings uncover a unique satellite repeat signature in the allotetraploid okra, contributing to our understanding of the composition, abundance, and chromosomal distribution of satellite repeats in allopolyploid genomes, further enriching our understanding of their evolutionary dynamics in complex allopolyploid genomes.
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spelling doaj.art-daf8d4134da4459daa449abd557051902024-03-05T16:24:48ZengBMCBMC Plant Biology1471-22292024-01-0124111610.1186/s12870-024-04739-9Genomic and cytogenetic analyses reveal satellite repeat signature in allotetraploid okra (Abelmoschus esculentus)Jiarui Liu0Xinyi Lin1Xiaojie Wang2Liqing Feng3Shixin Zhu4Runmeng Tian5Jingping Fang6Aifen Tao7Pingping Fang8Jianmin Qi9Liwu Zhang10Yongji Huang11Jiantang Xu12Scientific Observing and Experimental Station of Southeastern kenaf & jute, Ministry of Agriculture and Rural Affairs of the People’s Republic of China, Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, Fujian Provincial Key Laboratory of Crop Breeding by Design, National Engineering Research Center for Sugarcane, College of Agriculture, Fujian Agriculture and Forestry UniversityScientific Observing and Experimental Station of Southeastern kenaf & jute, Ministry of Agriculture and Rural Affairs of the People’s Republic of China, Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, Fujian Provincial Key Laboratory of Crop Breeding by Design, National Engineering Research Center for Sugarcane, College of Agriculture, Fujian Agriculture and Forestry UniversityCollege of Life Science, Fujian Agriculture and Forestry UniversityCollege of Life Science, Fujian Normal UniversityScientific Observing and Experimental Station of Southeastern kenaf & jute, Ministry of Agriculture and Rural Affairs of the People’s Republic of China, Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, Fujian Provincial Key Laboratory of Crop Breeding by Design, National Engineering Research Center for Sugarcane, College of Agriculture, Fujian Agriculture and Forestry UniversityScientific Observing and Experimental Station of Southeastern kenaf & jute, Ministry of Agriculture and Rural Affairs of the People’s Republic of China, Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, Fujian Provincial Key Laboratory of Crop Breeding by Design, National Engineering Research Center for Sugarcane, College of Agriculture, Fujian Agriculture and Forestry UniversityCollege of Life Science, Fujian Normal UniversityScientific Observing and Experimental Station of Southeastern kenaf & jute, Ministry of Agriculture and Rural Affairs of the People’s Republic of China, Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, Fujian Provincial Key Laboratory of Crop Breeding by Design, National Engineering Research Center for Sugarcane, College of Agriculture, Fujian Agriculture and Forestry UniversityScientific Observing and Experimental Station of Southeastern kenaf & jute, Ministry of Agriculture and Rural Affairs of the People’s Republic of China, Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, Fujian Provincial Key Laboratory of Crop Breeding by Design, National Engineering Research Center for Sugarcane, College of Agriculture, Fujian Agriculture and Forestry UniversityScientific Observing and Experimental Station of Southeastern kenaf & jute, Ministry of Agriculture and Rural Affairs of the People’s Republic of China, Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, Fujian Provincial Key Laboratory of Crop Breeding by Design, National Engineering Research Center for Sugarcane, College of Agriculture, Fujian Agriculture and Forestry UniversityScientific Observing and Experimental Station of Southeastern kenaf & jute, Ministry of Agriculture and Rural Affairs of the People’s Republic of China, Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, Fujian Provincial Key Laboratory of Crop Breeding by Design, National Engineering Research Center for Sugarcane, College of Agriculture, Fujian Agriculture and Forestry UniversityMinisterial and Provincial Joint Innovation Centre for Safety Production of Cross-Strait Crops, College of Geography and Oceanography, Minjiang UniversityScientific Observing and Experimental Station of Southeastern kenaf & jute, Ministry of Agriculture and Rural Affairs of the People’s Republic of China, Key Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, Fujian Provincial Key Laboratory of Crop Breeding by Design, National Engineering Research Center for Sugarcane, College of Agriculture, Fujian Agriculture and Forestry UniversityAbstract Background Satellite repeats are one of the most rapidly evolving components in eukaryotic genomes and play vital roles in genome regulation, genome evolution, and speciation. As a consequence, the composition, abundance and chromosome distribution of satellite repeats often exhibit variability across various species, genome, and even individual chromosomes. However, we know little about the satellite repeat evolution in allopolyploid genomes. Results In this study, we investigated the satellite repeat signature in five okra (Abelmoschus esculentus) accessions using genomic and cytogenetic methods. In each of the five accessions, we identified eight satellite repeats, which exhibited a significant level of intraspecific conservation. Through fluorescence in situ hybridization (FISH) experiments, we observed that the satellite repeats generated multiple signals and exhibited variations in copy number across chromosomes. Intriguingly, we found that five satellite repeats were interspersed with centromeric retrotransposons, signifying their involvement in centromeric satellite repeat identity. We confirmed subgenome-biased amplification patterns of these satellite repeats through existing genome assemblies or dual-color FISH, indicating their distinct dynamic evolution in the allotetraploid okra subgenome. Moreover, we observed the presence of multiple chromosomes harboring the 35 S rDNA loci, alongside another chromosomal pair carrying the 5 S rDNA loci in okra using FISH assay. Remarkably, the intensity of 35 S rDNA hybridization signals varied among chromosomes, with the signals predominantly localized within regions of relatively weak DAPI staining, associated with GC-rich heterochromatin regions. Finally, we observed a similar localization pattern between 35 S rDNA and three satellite repeats with high GC content and confirmed their origin in the intergenic spacer region of the 35 S rDNA. Conclusions Our findings uncover a unique satellite repeat signature in the allotetraploid okra, contributing to our understanding of the composition, abundance, and chromosomal distribution of satellite repeats in allopolyploid genomes, further enriching our understanding of their evolutionary dynamics in complex allopolyploid genomes.https://doi.org/10.1186/s12870-024-04739-9Satellite repeatrDNAIntergenic spacer regionAllotetraploidAbelmoschus esculentusFluorescence in situ hybridization
spellingShingle Jiarui Liu
Xinyi Lin
Xiaojie Wang
Liqing Feng
Shixin Zhu
Runmeng Tian
Jingping Fang
Aifen Tao
Pingping Fang
Jianmin Qi
Liwu Zhang
Yongji Huang
Jiantang Xu
Genomic and cytogenetic analyses reveal satellite repeat signature in allotetraploid okra (Abelmoschus esculentus)
BMC Plant Biology
Satellite repeat
rDNA
Intergenic spacer region
Allotetraploid
Abelmoschus esculentus
Fluorescence in situ hybridization
title Genomic and cytogenetic analyses reveal satellite repeat signature in allotetraploid okra (Abelmoschus esculentus)
title_full Genomic and cytogenetic analyses reveal satellite repeat signature in allotetraploid okra (Abelmoschus esculentus)
title_fullStr Genomic and cytogenetic analyses reveal satellite repeat signature in allotetraploid okra (Abelmoschus esculentus)
title_full_unstemmed Genomic and cytogenetic analyses reveal satellite repeat signature in allotetraploid okra (Abelmoschus esculentus)
title_short Genomic and cytogenetic analyses reveal satellite repeat signature in allotetraploid okra (Abelmoschus esculentus)
title_sort genomic and cytogenetic analyses reveal satellite repeat signature in allotetraploid okra abelmoschus esculentus
topic Satellite repeat
rDNA
Intergenic spacer region
Allotetraploid
Abelmoschus esculentus
Fluorescence in situ hybridization
url https://doi.org/10.1186/s12870-024-04739-9
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