Transcriptome-wide identification and characterization of genes exhibit allele-specific imprinting in maize embryo and endosperm

Abstract Background Genomic imprinting refers to a subset of genes that are expressed from only one parental allele during seed development in plants. Studies on genomic imprinting have revealed that intraspecific variations in genomic imprinting expression exist in naturally genetic varieties. Howe...

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Main Authors: Xiaomei Dong, Haishan Luo, Wenjing Bi, Hanyu Chen, Shuai Yu, Xiaoyu Zhang, Yuxin Dai, Xipeng Cheng, Yupeng Xing, Xiaoqin Fan, Yanbin Zhu, Yanling Guo, Dexuan Meng
Format: Article
Language:English
Published: BMC 2023-10-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-023-04473-8
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author Xiaomei Dong
Haishan Luo
Wenjing Bi
Hanyu Chen
Shuai Yu
Xiaoyu Zhang
Yuxin Dai
Xipeng Cheng
Yupeng Xing
Xiaoqin Fan
Yanbin Zhu
Yanling Guo
Dexuan Meng
author_facet Xiaomei Dong
Haishan Luo
Wenjing Bi
Hanyu Chen
Shuai Yu
Xiaoyu Zhang
Yuxin Dai
Xipeng Cheng
Yupeng Xing
Xiaoqin Fan
Yanbin Zhu
Yanling Guo
Dexuan Meng
author_sort Xiaomei Dong
collection DOAJ
description Abstract Background Genomic imprinting refers to a subset of genes that are expressed from only one parental allele during seed development in plants. Studies on genomic imprinting have revealed that intraspecific variations in genomic imprinting expression exist in naturally genetic varieties. However, there have been few studies on the functional analysis of allele-specific imprinted genes. Results Here, we generated three reciprocal crosses among the B73, Mo17 and CAU5 inbred lines. Based on the transcriptome-wide analysis of allele-specific expression using RNA sequencing technology, 305 allele-specific imprinting genes (ASIGs) were identified in embryos, and 655 ASIGs were identified in endosperms from three maize F1 hybrids. Of these ASIGs, most did not show consistent maternal or paternal bias between the same tissue from different hybrids or different tissues from one hybrid cross. By gene ontology (GO) analysis, five and eight categories of GO exhibited significantly higher functional enrichments for ASIGs identified in embryo and endosperm, respectively. These functional categories indicated that ASIGs are involved in intercellular nutrient transport, signaling pathways, and transcriptional regulation of kernel development. Finally, the mutation and overexpression of one ASIG (Zm305) affected the length and width of the kernel. Conclusion In this study, our data will be helpful in gaining further knowledge of genes exhibiting allele-specific imprinting patterns in seeds. The gain- and loss-of-function phenotypes of ASIGs associated with agronomically important seed traits provide compelling evidence for ASIGs as crucial targets to optimize seed traits in crop plants.
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spelling doaj.art-362b1d737be34e7abb43188aa920fe2d2023-11-26T12:47:28ZengBMCBMC Plant Biology1471-22292023-10-0123111210.1186/s12870-023-04473-8Transcriptome-wide identification and characterization of genes exhibit allele-specific imprinting in maize embryo and endospermXiaomei Dong0Haishan Luo1Wenjing Bi2Hanyu Chen3Shuai Yu4Xiaoyu Zhang5Yuxin Dai6Xipeng Cheng7Yupeng Xing8Xiaoqin Fan9Yanbin Zhu10Yanling Guo11Dexuan Meng12College of Bioscience and Biotechnology, Shenyang Agricultural UniversityCollege of Agronomy, Shenyang Agricultural UniversityCollege of Agronomy, Shenyang Agricultural UniversityCollege of Agronomy, Shenyang Agricultural UniversityCollege of Bioscience and Biotechnology, Shenyang Agricultural UniversityCollege of Bioscience and Biotechnology, Shenyang Agricultural UniversityCollege of Bioscience and Biotechnology, Shenyang Agricultural UniversityCollege of Bioscience and Biotechnology, Shenyang Agricultural UniversityCollege of Bioscience and Biotechnology, Shenyang Agricultural UniversityManas Agricultural Experimental Station of Xinjiang Academy of Agricultural SciencesNational Key Laboratory of Maize Biological Breeding, Key Laboratory of Genetics and Breeding of Main Crops in Northeast Region, Ministry of Agriculture and Rural Affairs, Liaoning Dongya Seed Industry Co., LtdNational Key Laboratory of Maize Biological Breeding, Key Laboratory of Genetics and Breeding of Main Crops in Northeast Region, Ministry of Agriculture and Rural Affairs, Liaoning Dongya Seed Industry Co., LtdCollege of Agronomy, Shenyang Agricultural UniversityAbstract Background Genomic imprinting refers to a subset of genes that are expressed from only one parental allele during seed development in plants. Studies on genomic imprinting have revealed that intraspecific variations in genomic imprinting expression exist in naturally genetic varieties. However, there have been few studies on the functional analysis of allele-specific imprinted genes. Results Here, we generated three reciprocal crosses among the B73, Mo17 and CAU5 inbred lines. Based on the transcriptome-wide analysis of allele-specific expression using RNA sequencing technology, 305 allele-specific imprinting genes (ASIGs) were identified in embryos, and 655 ASIGs were identified in endosperms from three maize F1 hybrids. Of these ASIGs, most did not show consistent maternal or paternal bias between the same tissue from different hybrids or different tissues from one hybrid cross. By gene ontology (GO) analysis, five and eight categories of GO exhibited significantly higher functional enrichments for ASIGs identified in embryo and endosperm, respectively. These functional categories indicated that ASIGs are involved in intercellular nutrient transport, signaling pathways, and transcriptional regulation of kernel development. Finally, the mutation and overexpression of one ASIG (Zm305) affected the length and width of the kernel. Conclusion In this study, our data will be helpful in gaining further knowledge of genes exhibiting allele-specific imprinting patterns in seeds. The gain- and loss-of-function phenotypes of ASIGs associated with agronomically important seed traits provide compelling evidence for ASIGs as crucial targets to optimize seed traits in crop plants.https://doi.org/10.1186/s12870-023-04473-8MaizeAllele-specific imprintingEmbryoEndospermKernel development
spellingShingle Xiaomei Dong
Haishan Luo
Wenjing Bi
Hanyu Chen
Shuai Yu
Xiaoyu Zhang
Yuxin Dai
Xipeng Cheng
Yupeng Xing
Xiaoqin Fan
Yanbin Zhu
Yanling Guo
Dexuan Meng
Transcriptome-wide identification and characterization of genes exhibit allele-specific imprinting in maize embryo and endosperm
BMC Plant Biology
Maize
Allele-specific imprinting
Embryo
Endosperm
Kernel development
title Transcriptome-wide identification and characterization of genes exhibit allele-specific imprinting in maize embryo and endosperm
title_full Transcriptome-wide identification and characterization of genes exhibit allele-specific imprinting in maize embryo and endosperm
title_fullStr Transcriptome-wide identification and characterization of genes exhibit allele-specific imprinting in maize embryo and endosperm
title_full_unstemmed Transcriptome-wide identification and characterization of genes exhibit allele-specific imprinting in maize embryo and endosperm
title_short Transcriptome-wide identification and characterization of genes exhibit allele-specific imprinting in maize embryo and endosperm
title_sort transcriptome wide identification and characterization of genes exhibit allele specific imprinting in maize embryo and endosperm
topic Maize
Allele-specific imprinting
Embryo
Endosperm
Kernel development
url https://doi.org/10.1186/s12870-023-04473-8
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