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

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, the...

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Autores principales: Dong, Xiaomei, Luo, Haishan, Bi, Wenjing, Chen, Hanyu, Yu, Shuai, Zhang, Xiaoyu, Dai, Yuxin, Cheng, Xipeng, Xing, Yupeng, Fan, Xiaoqin, Zhu, Yanbin, Guo, Yanling, Meng, Dexuan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10557216/
https://www.ncbi.nlm.nih.gov/pubmed/37803280
http://dx.doi.org/10.1186/s12870-023-04473-8
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author Dong, Xiaomei
Luo, Haishan
Bi, Wenjing
Chen, Hanyu
Yu, Shuai
Zhang, Xiaoyu
Dai, Yuxin
Cheng, Xipeng
Xing, Yupeng
Fan, Xiaoqin
Zhu, Yanbin
Guo, Yanling
Meng, Dexuan
author_facet Dong, Xiaomei
Luo, Haishan
Bi, Wenjing
Chen, Hanyu
Yu, Shuai
Zhang, Xiaoyu
Dai, Yuxin
Cheng, Xipeng
Xing, Yupeng
Fan, Xiaoqin
Zhu, Yanbin
Guo, Yanling
Meng, Dexuan
author_sort Dong, Xiaomei
collection PubMed
description 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-023-04473-8.
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spelling pubmed-105572162023-10-07 Transcriptome-wide identification and characterization of genes exhibit allele-specific imprinting in maize embryo and endosperm Dong, Xiaomei Luo, Haishan Bi, Wenjing Chen, Hanyu Yu, Shuai Zhang, Xiaoyu Dai, Yuxin Cheng, Xipeng Xing, Yupeng Fan, Xiaoqin Zhu, Yanbin Guo, Yanling Meng, Dexuan BMC Plant Biol Research 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. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-023-04473-8. BioMed Central 2023-10-06 /pmc/articles/PMC10557216/ /pubmed/37803280 http://dx.doi.org/10.1186/s12870-023-04473-8 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This 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
Dong, Xiaomei
Luo, Haishan
Bi, Wenjing
Chen, Hanyu
Yu, Shuai
Zhang, Xiaoyu
Dai, Yuxin
Cheng, Xipeng
Xing, Yupeng
Fan, Xiaoqin
Zhu, Yanbin
Guo, Yanling
Meng, Dexuan
Transcriptome-wide identification and characterization of genes exhibit allele-specific imprinting in maize embryo and endosperm
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 Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10557216/
https://www.ncbi.nlm.nih.gov/pubmed/37803280
http://dx.doi.org/10.1186/s12870-023-04473-8
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