Extent and complexity of RNA processing in the development of honey bee queen and worker castes revealed by Nanopore direct RNA sequencing

The distinct honey bee (Apis mellifera) worker and queen castes have become a model for the study of genomic mechanisms of phenotypic plasticity. Prior studies have explored differences in gene expression and methylation during development of the two castes, but thus far no study has performed a genome-wide analysis of differences in RNA processing. To address this here we performed a Nanopore-based direct RNA sequencing with exceptionally long reads to compare the mRNA transcripts between honey bee queen and workers at three points during their larval development. We found thousands of significantly differentially expressed isoforms (DEIs) between queen and worker larvae. Most DEIs contained alternative splicing, and many of them contained at least two types of alternative splicing patterns, indicating complex RNA processing in honey bee caste differentiation. We found a negative correlation between poly(A) length and DEI expression, suggesting that poly(A) tails participate in the regulation of isoform expression. Hundreds of isoforms uniquely expressed in either queens or workers during their larval development, and isoforms were expressed at different points in queen and worker larval development demonstrating a dynamic relationship between isoform expression and developmental mechanisms. These findings show the full complexity of RNA processing and transcript expression in honey bee phenotypic plasticity.

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Changes in Alternative Splicing in Apis Mellifera Bees Fed Apis Cerana Royal Jelly

Journal of Apicultural Science ◽

10.2478/jas-2014-0019 ◽

2014 ◽

Vol 58 (2) ◽

pp. 25-31 ◽

Cited By ~ 1

Author(s):

Yuan Yuan Shi ◽

Zachary Y. Huang ◽

Xiao Bo Wu ◽

Zi Long Wang ◽

Wei Yu Yan ◽

...

Keyword(s):

Alternative Splicing ◽

Apis Mellifera ◽

Honey Bee ◽

Royal Jelly ◽

Intron Retention ◽

Tricarboxylic Acid Cycle ◽

Apis Cerana ◽

Causative Factor ◽

Caste Differentiation ◽

Splice Sites

Abstract The Western honey bee (Apis mellifera) is a social insect characterized by caste differentiation in which the queen bee and worker bees display marked differences in morphology, behavior, reproduction, and longevity despite their identical genomes. The main causative factor in caste differentiation is the food fed to queen larvae, termed royal jelly (RJ). Alternative splicing (AS) is an important RNA-mediated post-transcriptional process in eukaryotes. Here we report AS changes in A. mellifera after being fed either A. mellifera RJ or A. cerana RJ. The results demonstrated that the RJ type affected 4 types of AS in adult A. mellifera: exon skipping, intron retention, alternative 5’ splice sites, and alternative 3’splice sites. After feeding with A. cerana RJ, AS occurred in many genes in adult A. mellifera that encode proteins involved in development, growth, the tricarboxylic acid cycle, and substance metabolism. This study provides the first evidence that heterospecific RJ can influence the AS of many genes related to honey bee development and growth.

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Integration of lncRNA–miRNA–mRNA reveals novel insights into oviposition regulation in honey bees

PeerJ ◽

10.7717/peerj.3881 ◽

2017 ◽

Vol 5 ◽

pp. e3881 ◽

Cited By ~ 14

Author(s):

Xiao Chen ◽

Ce Ma ◽

Chao Chen ◽

Qian Lu ◽

Wei Shi ◽

...

Keyword(s):

Candidate Genes ◽

Honey Bee ◽

Honey Bees ◽

Critical Role ◽

Noncoding Rnas ◽

Differentially Expressed ◽

Integrated Analysis ◽

Ovary Activation ◽

A Genome ◽

Honey Bee Queen

Background The honey bee (Apis mellifera) is a highly diverse species commonly used for honey production and pollination services. The oviposition of the honey bee queen affects the development and overall performance of the colony. To investigate the ovary activation and oviposition processes on a molecular level, a genome-wide analysis of lncRNAs, miRNAs and mRNA expression in the ovaries of the queens was performed to screen for differentially expressed coding and noncoding RNAs. Further analysis identified relevant candidate genes or RNAs. Results The analysis of the RNA profiles in different oviposition phase of the queens revealed that 740 lncRNAs, 81 miRNAs and 5,481 mRNAs were differently expressed during the ovary activation; 88 lncRNAs, 13 miRNAs and 338 mRNAs were differently expressed during the oviposition inhibition process; and finally, 100 lncRNAs, four miRNAs and 497 mRNAs were differently expressed during the oviposition recovery process. In addition, functional annotation of differentially expressed RNAs revealed several pathways that are closely related to oviposition, including hippo, MAPK, notch, Wnt, mTOR, TGF-beta and FoxO signaling pathways. Furthermore, in the QTL region for ovary size, 73 differentially expressed genes and 14 differentially expressed lncRNAs were located, which are considered as candidate genes affecting ovary size and oviposition. Moreover, a core set of genes served as bridges among different miRNAs were identified through the integrated analysis of lncRNA-miRNA-mRNA network. Conclusion The observed dramatic expression changes of coding and noncoding RNAs suggest that they may play a critical role in honey bee queens’ oviposition. The identified candidate genes for oviposition activation and regulation could serve as a resource for further studies of genetic markers of oviposition in honey bees.

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A genome-wide analysis of alternative splicing in tissues and distinct neuronal subtypes in C. elegans

10.26226/morressier.5ebd45acffea6f735881af04 ◽

2020 ◽

Author(s):

Bina Koterniak

Keyword(s):

Alternative Splicing ◽

Genome Wide Analysis ◽

C Elegans ◽

Genome Wide ◽

A Genome

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Analysis of RNA processing and m6A modification using nanopore direct RNA sequencing.

10.26226/morressier.5ebd45acffea6f735881af26 ◽

2020 ◽

Author(s):

Matthew Parker

Keyword(s):

Rna Sequencing ◽

Rna Processing

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A Genome-Wide Analysis of the Gene Expression and Alternative Splicing Events in a Whole-Body Hypoxic Preconditioning Mouse Model

Neurochemical Research ◽

10.1007/s11064-021-03241-0 ◽

2021 ◽

Vol 46 (5) ◽

pp. 1101-1111

Author(s):

Jun Li ◽

Hongyu Zhao ◽

Yongqiang Xing ◽

Tongling Zhao ◽

Lu Cai ◽

...

Keyword(s):

Gene Expression ◽

Alternative Splicing ◽

Mouse Model ◽

Hypoxic Preconditioning ◽

Whole Body ◽

Genome Wide Analysis ◽

Genome Wide ◽

A Genome ◽

Alternative Splicing Events

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Deep RNA sequencing reveals a high frequency of alternative splicing events in the fungus Trichoderma longibrachiatum

BMC Genomics ◽

10.1186/s12864-015-1251-8 ◽

2015 ◽

Vol 16 (1) ◽

pp. 54 ◽

Cited By ~ 23

Author(s):

Bin-Bin Xie ◽

Dan Li ◽

Wei-Ling Shi ◽

Qi-Long Qin ◽

Xiao-Wei Wang ◽

...

Keyword(s):

Alternative Splicing ◽

Rna Sequencing ◽

High Frequency ◽

Trichoderma Longibrachiatum ◽

Alternative Splicing Events

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Production and transmission of honey bee queen (Apis mellifera L.) mandibular gland pheromone

Behavioral Ecology and Sociobiology ◽

10.1007/bf00165956 ◽

1991 ◽

Vol 29 (5) ◽

pp. 321-332 ◽

Cited By ~ 84

Author(s):

Ken Naumann ◽

Mark L. Winston ◽

Keith N. Slessor ◽

Glenn D. Prestwich ◽

Francis X. Webster

Keyword(s):

Apis Mellifera ◽

Honey Bee ◽

Mandibular Gland ◽

Honey Bee Queen

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Abstract 12192: MBNL1 Directly Regulates the Alternative Splicing of mRNAs That Promote Myofibroblast Differentiation

Circulation ◽

10.1161/circ.130.suppl_2.12192 ◽

2014 ◽

Vol 130 (suppl_2) ◽

Author(s):

Jennifer Davis ◽

Michelle Sargent ◽

Jianjian Shi ◽

Lei Wei ◽

Maurice S Swanson ◽

...

Keyword(s):

Alternative Splicing ◽

Molecular Mechanisms ◽

Rna Binding ◽

Transforming Growth Factor ◽

Ventricular Remodeling ◽

Cardiac Injury ◽

Myofibroblast Differentiation ◽

Genome Wide ◽

A Genome

Rationale: During the cardiac injury response fibroblasts differentiate into myofibroblasts, a cell type that enhances extracellular matrix production and facilitates ventricular remodeling. To better understand the molecular mechanisms whereby myofibroblasts are generated in the heart we performed a genome-wide screen with 18,000 cDNAs, which identified the RNA-binding protein muscleblind-like splicing regulator 1 (MBNL1), suggesting a novel association between mRNA alternative splicing and the regulation of myofibroblast differentiation. Objective: To determine the mechanism whereby MBNL1 regulates myofibroblast differentiation and the cardiac fibrotic response. Methods and Results: Confirming the results from our genome wide screen, adenoviral-mediated overexpression of MBNL1 promoted transformation of rat cardiac fibroblasts and mouse embryonic fibroblasts (MEFs) into myofibroblasts, similar to the level of conversion obtained by the profibrotic agonist transforming growth factor β (TGFβ). Antithetically, Mbnl1 -/- MEFs were refractory to TGFβ-induced myofibroblast differentiation. MBNL1 expression is induced in transforming fibroblasts in response to TGFβ and angiotensin II. These results were extended in vivo by analysis of dermal wound healing, a process dependent on myofibroblast differentiation and their proper activity. By day 6 control mice had achieved 82% skin wound closure compared with only 40% in Mbnl1 -/- mice. Moreover, Mbnl1 -/- mice had reduced survival following myocardial infarction injury due to defective fibrotic scar formation and healing. High throughput RNA sequencing (RNAseq) and RNA immunoprecipitation revealed that MBNL1 directly regulates the alternative splicing of transcripts for myofibroblast signaling factors and cytoskeletal-assembly elements. Functional analysis of these factors as mediators of MBNL1 activity is also described here. Conclusions: Collectively, our data suggest that MBNL1 coordinates myofibroblast transformation by directly mediating the alternative splicing of an array of mRNAs encoding differentiation-specific signaling transcripts, which then alter the fibroblast proteome for myofibroblast structure and function.

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