Identification of long non-coding RNAs and microRNAs involved in anther development in the tropical Camellia oleifera

Abstract Background Explored the molecular science of anther development is important for improving productivity and overall yield of crops. Although the role of regulatory RNAs, including long non-coding RNAs (lncRNAs) and microRNAs (miRNAs), in regulating anther development has been established, t...

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Main Authors: Lingshan Kong, Yanjing Zhuo, Jieru Xu, Xiangxu Meng, Yue Wang, Wenxiu Zhao, Hanggui Lai, Jinhui Chen, Jian Wang
Format: Article
Language:English
Published: BMC 2022-08-01
Series:BMC Genomics
Subjects:
Online Access:https://doi.org/10.1186/s12864-022-08836-7
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author Lingshan Kong
Yanjing Zhuo
Jieru Xu
Xiangxu Meng
Yue Wang
Wenxiu Zhao
Hanggui Lai
Jinhui Chen
Jian Wang
author_facet Lingshan Kong
Yanjing Zhuo
Jieru Xu
Xiangxu Meng
Yue Wang
Wenxiu Zhao
Hanggui Lai
Jinhui Chen
Jian Wang
author_sort Lingshan Kong
collection DOAJ
description Abstract Background Explored the molecular science of anther development is important for improving productivity and overall yield of crops. Although the role of regulatory RNAs, including long non-coding RNAs (lncRNAs) and microRNAs (miRNAs), in regulating anther development has been established, their identities and functions in Camellia oleifera, an important industrial crop, have yet not been clearly explored. Here, we report the identification and characterization of genes, lncRNAs and miRNAs during three stages of the tropical C. oleifera anther development by single-molecule real-time sequencing, RNA sequencing and small RNA sequencing, respectively. Results These stages, viz. the pollen mother cells stage, tetrad stage and uninucleate pollen stage, were identified by analyzing paraffin sections of floral buds during rapid expansion periods. A total of 18,393 transcripts, 414 putative lncRNAs and 372 miRNAs were identified, of which 5,324 genes, 115 lncRNAs, and 44 miRNAs were differentially accumulated across three developmental stages. Of these, 44 and 92 genes were predicted be regulated by 37 and 30 differentially accumulated lncRNAs and miRNAs, respectively. Additionally, 42 differentially accumulated lncRNAs were predicted as targets of 27 miRNAs. Gene ontology enrichment indicated that potential target genes of lncRNAs were enriched in photosystem II, regulation of autophagy and carbohydrate phosphatase activity, which are essential for anther development. Functional annotation of genes targeted by miRNAs indicated that they are relevant to transcription and metabolic processes that play important roles in microspore development. An interaction network was built with 2 lncRNAs, 6 miRNAs and 10 mRNAs. Among these, miR396 and miR156 family were up-regulated, while their targets, genes (GROWTH REGULATING FACTORS and SQUAMOSA PROMOTER BINDING PROTEIN-LIKE genes) and lncRNAs, were down-regulated. Further, the trans-regulated targets of these lncRNAs, like wall-associated kinase2 and phosphomannose isomerase1, are involved in pollen wall formation during anther development. Conclusions This study unravels lncRNAs, miRNAs and miRNA-lncRNA-mRNA networks involved in development of anthers of the tropical C. oleifera lays a theoretical foundation for further elucidation of regulatory roles of lncRNAs and miRNAs in anther development.
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spelling doaj.art-fbef2c266abc49afa4a279d1f4a18c0b2022-12-22T02:34:51ZengBMCBMC Genomics1471-21642022-08-0123111810.1186/s12864-022-08836-7Identification of long non-coding RNAs and microRNAs involved in anther development in the tropical Camellia oleiferaLingshan Kong0Yanjing Zhuo1Jieru Xu2Xiangxu Meng3Yue Wang4Wenxiu Zhao5Hanggui Lai6Jinhui Chen7Jian Wang8Sanya Nanfan Research Institute of Hainan UniversitySchool of Public Administration, Hainan UniversitySanya Nanfan Research Institute of Hainan UniversitySanya Nanfan Research Institute of Hainan UniversitySanya Nanfan Research Institute of Hainan UniversitySanya Nanfan Research Institute of Hainan UniversitySchool of Tropical Crops, Hainan UniversitySanya Nanfan Research Institute of Hainan UniversitySanya Nanfan Research Institute of Hainan UniversityAbstract Background Explored the molecular science of anther development is important for improving productivity and overall yield of crops. Although the role of regulatory RNAs, including long non-coding RNAs (lncRNAs) and microRNAs (miRNAs), in regulating anther development has been established, their identities and functions in Camellia oleifera, an important industrial crop, have yet not been clearly explored. Here, we report the identification and characterization of genes, lncRNAs and miRNAs during three stages of the tropical C. oleifera anther development by single-molecule real-time sequencing, RNA sequencing and small RNA sequencing, respectively. Results These stages, viz. the pollen mother cells stage, tetrad stage and uninucleate pollen stage, were identified by analyzing paraffin sections of floral buds during rapid expansion periods. A total of 18,393 transcripts, 414 putative lncRNAs and 372 miRNAs were identified, of which 5,324 genes, 115 lncRNAs, and 44 miRNAs were differentially accumulated across three developmental stages. Of these, 44 and 92 genes were predicted be regulated by 37 and 30 differentially accumulated lncRNAs and miRNAs, respectively. Additionally, 42 differentially accumulated lncRNAs were predicted as targets of 27 miRNAs. Gene ontology enrichment indicated that potential target genes of lncRNAs were enriched in photosystem II, regulation of autophagy and carbohydrate phosphatase activity, which are essential for anther development. Functional annotation of genes targeted by miRNAs indicated that they are relevant to transcription and metabolic processes that play important roles in microspore development. An interaction network was built with 2 lncRNAs, 6 miRNAs and 10 mRNAs. Among these, miR396 and miR156 family were up-regulated, while their targets, genes (GROWTH REGULATING FACTORS and SQUAMOSA PROMOTER BINDING PROTEIN-LIKE genes) and lncRNAs, were down-regulated. Further, the trans-regulated targets of these lncRNAs, like wall-associated kinase2 and phosphomannose isomerase1, are involved in pollen wall formation during anther development. Conclusions This study unravels lncRNAs, miRNAs and miRNA-lncRNA-mRNA networks involved in development of anthers of the tropical C. oleifera lays a theoretical foundation for further elucidation of regulatory roles of lncRNAs and miRNAs in anther development.https://doi.org/10.1186/s12864-022-08836-7Anther developmentMicroRNAsLong non-coding RNAsNetworkCamellia oleifera
spellingShingle Lingshan Kong
Yanjing Zhuo
Jieru Xu
Xiangxu Meng
Yue Wang
Wenxiu Zhao
Hanggui Lai
Jinhui Chen
Jian Wang
Identification of long non-coding RNAs and microRNAs involved in anther development in the tropical Camellia oleifera
BMC Genomics
Anther development
MicroRNAs
Long non-coding RNAs
Network
Camellia oleifera
title Identification of long non-coding RNAs and microRNAs involved in anther development in the tropical Camellia oleifera
title_full Identification of long non-coding RNAs and microRNAs involved in anther development in the tropical Camellia oleifera
title_fullStr Identification of long non-coding RNAs and microRNAs involved in anther development in the tropical Camellia oleifera
title_full_unstemmed Identification of long non-coding RNAs and microRNAs involved in anther development in the tropical Camellia oleifera
title_short Identification of long non-coding RNAs and microRNAs involved in anther development in the tropical Camellia oleifera
title_sort identification of long non coding rnas and micrornas involved in anther development in the tropical camellia oleifera
topic Anther development
MicroRNAs
Long non-coding RNAs
Network
Camellia oleifera
url https://doi.org/10.1186/s12864-022-08836-7
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