Contrasting Sex-and Caste-Dependent piRNA Profiles in the Transposon Depleted Haplodiploid Honeybee Apis mellifera

Weiwen Wang, Regan Ashby, Hua Ying, Ryszard Maleszka, Sylvain Forêt

Research output: Contribution to journalArticle

5 Citations (Scopus)
11 Downloads (Pure)

Abstract

Protecting genome integrity against transposable elements is achieved by intricate molecular mechanisms involving PIWI proteins, their associated small RNAs (piRNAs), and epigenetic modifiers such as DNA methylation. Eusocial bees, in particular the Western honeybee, Apis mellifera, have one of the lowest contents of transposable elements in the animal kingdom, and, unlike other animals with a functional DNA methylation system, appear not to methylate their transposons. This raises the question of whether the PIWI machinery has been retained in this species. Using comparative genomics, mass spectrometry, and expressional profiling, we present seminal evidence that the piRNA system is conserved in honeybees. We show that honey bee piRNAs contain a 2'-O-methyl modification at the 3' end, and have a bias towards a 5' terminal U, which are signature features of their biogenesis. Both piRNA repertoire and expression levels are greater in reproductive individuals than in sterile workers. Haploid males, where the detrimental effects of transposons are dominant, have the greatest piRNA levels, but surprisingly, the highest expression of transposons. These results show that even in a transposon-depleted species, the piRNA system is required to guard the vulnerable haploid genome and reproductive castes against transposon-associated genomic instability. This also suggests that dosage plays an important role in the regulation of transposons and piRNAs expression in haplo-diploid systems.

Original languageEnglish
Pages (from-to)1341-1356
Number of pages16
JournalGenome Biology and Evolution
Volume9
Issue number5
DOIs
Publication statusPublished - 1 Jun 2017

Fingerprint

caste
honeybee
Bees
methylation
Apis mellifera
Social Class
bee
transposons
Small Interfering RNA
honey bees
genomics
genome
DNA
DNA Transposable Elements
gender
animal
Haploidy
honey
DNA Methylation
machinery

Cite this

Wang, Weiwen ; Ashby, Regan ; Ying, Hua ; Maleszka, Ryszard ; Forêt, Sylvain. / Contrasting Sex-and Caste-Dependent piRNA Profiles in the Transposon Depleted Haplodiploid Honeybee Apis mellifera. In: Genome Biology and Evolution. 2017 ; Vol. 9, No. 5. pp. 1341-1356.
@article{bb5a07bb68314d91b27c77f2054b8dc1,
title = "Contrasting Sex-and Caste-Dependent piRNA Profiles in the Transposon Depleted Haplodiploid Honeybee Apis mellifera",
abstract = "Protecting genome integrity against transposable elements is achieved by intricate molecular mechanisms involving PIWI proteins, their associated small RNAs (piRNAs), and epigenetic modifiers such as DNA methylation. Eusocial bees, in particular the Western honeybee, Apis mellifera, have one of the lowest contents of transposable elements in the animal kingdom, and, unlike other animals with a functional DNA methylation system, appear not to methylate their transposons. This raises the question of whether the PIWI machinery has been retained in this species. Using comparative genomics, mass spectrometry, and expressional profiling, we present seminal evidence that the piRNA system is conserved in honeybees. We show that honey bee piRNAs contain a 2'-O-methyl modification at the 3' end, and have a bias towards a 5' terminal U, which are signature features of their biogenesis. Both piRNA repertoire and expression levels are greater in reproductive individuals than in sterile workers. Haploid males, where the detrimental effects of transposons are dominant, have the greatest piRNA levels, but surprisingly, the highest expression of transposons. These results show that even in a transposon-depleted species, the piRNA system is required to guard the vulnerable haploid genome and reproductive castes against transposon-associated genomic instability. This also suggests that dosage plays an important role in the regulation of transposons and piRNAs expression in haplo-diploid systems.",
keywords = "piRNA, Honeybee, Caste determination, Transposon, Haploid, Diploid",
author = "Weiwen Wang and Regan Ashby and Hua Ying and Ryszard Maleszka and Sylvain For{\^e}t",
note = "{\circledC} The Author 2017. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.",
year = "2017",
month = "6",
day = "1",
doi = "10.1093/gbe/evx087",
language = "English",
volume = "9",
pages = "1341--1356",
journal = "Genome Biology and Evolution",
issn = "1759-6653",
publisher = "Oxford University Press",
number = "5",

}

Contrasting Sex-and Caste-Dependent piRNA Profiles in the Transposon Depleted Haplodiploid Honeybee Apis mellifera. / Wang, Weiwen; Ashby, Regan; Ying, Hua; Maleszka, Ryszard; Forêt, Sylvain.

In: Genome Biology and Evolution, Vol. 9, No. 5, 01.06.2017, p. 1341-1356.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Contrasting Sex-and Caste-Dependent piRNA Profiles in the Transposon Depleted Haplodiploid Honeybee Apis mellifera

AU - Wang, Weiwen

AU - Ashby, Regan

AU - Ying, Hua

AU - Maleszka, Ryszard

AU - Forêt, Sylvain

N1 - © The Author 2017. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.

PY - 2017/6/1

Y1 - 2017/6/1

N2 - Protecting genome integrity against transposable elements is achieved by intricate molecular mechanisms involving PIWI proteins, their associated small RNAs (piRNAs), and epigenetic modifiers such as DNA methylation. Eusocial bees, in particular the Western honeybee, Apis mellifera, have one of the lowest contents of transposable elements in the animal kingdom, and, unlike other animals with a functional DNA methylation system, appear not to methylate their transposons. This raises the question of whether the PIWI machinery has been retained in this species. Using comparative genomics, mass spectrometry, and expressional profiling, we present seminal evidence that the piRNA system is conserved in honeybees. We show that honey bee piRNAs contain a 2'-O-methyl modification at the 3' end, and have a bias towards a 5' terminal U, which are signature features of their biogenesis. Both piRNA repertoire and expression levels are greater in reproductive individuals than in sterile workers. Haploid males, where the detrimental effects of transposons are dominant, have the greatest piRNA levels, but surprisingly, the highest expression of transposons. These results show that even in a transposon-depleted species, the piRNA system is required to guard the vulnerable haploid genome and reproductive castes against transposon-associated genomic instability. This also suggests that dosage plays an important role in the regulation of transposons and piRNAs expression in haplo-diploid systems.

AB - Protecting genome integrity against transposable elements is achieved by intricate molecular mechanisms involving PIWI proteins, their associated small RNAs (piRNAs), and epigenetic modifiers such as DNA methylation. Eusocial bees, in particular the Western honeybee, Apis mellifera, have one of the lowest contents of transposable elements in the animal kingdom, and, unlike other animals with a functional DNA methylation system, appear not to methylate their transposons. This raises the question of whether the PIWI machinery has been retained in this species. Using comparative genomics, mass spectrometry, and expressional profiling, we present seminal evidence that the piRNA system is conserved in honeybees. We show that honey bee piRNAs contain a 2'-O-methyl modification at the 3' end, and have a bias towards a 5' terminal U, which are signature features of their biogenesis. Both piRNA repertoire and expression levels are greater in reproductive individuals than in sterile workers. Haploid males, where the detrimental effects of transposons are dominant, have the greatest piRNA levels, but surprisingly, the highest expression of transposons. These results show that even in a transposon-depleted species, the piRNA system is required to guard the vulnerable haploid genome and reproductive castes against transposon-associated genomic instability. This also suggests that dosage plays an important role in the regulation of transposons and piRNAs expression in haplo-diploid systems.

KW - piRNA

KW - Honeybee

KW - Caste determination

KW - Transposon

KW - Haploid

KW - Diploid

UR - http://www.scopus.com/inward/record.url?scp=85026642319&partnerID=8YFLogxK

U2 - 10.1093/gbe/evx087

DO - 10.1093/gbe/evx087

M3 - Article

VL - 9

SP - 1341

EP - 1356

JO - Genome Biology and Evolution

JF - Genome Biology and Evolution

SN - 1759-6653

IS - 5

ER -