Barley Anther and Meiocyte Transcriptome Dynamics in Meiotic Prophase I

In flowering plants, successful germinal cell development and meiotic recombination depend upon a combination of environmental and genetic factors. To gain insights into this specialized reproductive development program we used short- and long-read RNA-sequencing (RNA-seq) to study the temporal dyna...

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Main Authors: Abdellah Barakate, Jamie Orr, Miriam Schreiber, Isabelle Colas, Dominika Lewandowska, Nicola McCallum, Malcolm Macaulay, Jenny Morris, Mikel Arrieta, Pete E. Hedley, Luke Ramsay, Robbie Waugh
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-01-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2020.619404/full
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spelling doaj-8b2c544d0d8c43de8ac4d0b070dc018e2021-01-12T05:31:08ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-01-011110.3389/fpls.2020.619404619404Barley Anther and Meiocyte Transcriptome Dynamics in Meiotic Prophase IAbdellah Barakate0Jamie Orr1Miriam Schreiber2Isabelle Colas3Dominika Lewandowska4Nicola McCallum5Malcolm Macaulay6Jenny Morris7Mikel Arrieta8Pete E. Hedley9Luke Ramsay10Robbie Waugh11Robbie Waugh12Robbie Waugh13Cell and Molecular Sciences, The James Hutton Institute, Dundee, United KingdomCell and Molecular Sciences, The James Hutton Institute, Dundee, United KingdomCell and Molecular Sciences, The James Hutton Institute, Dundee, United KingdomCell and Molecular Sciences, The James Hutton Institute, Dundee, United KingdomCell and Molecular Sciences, The James Hutton Institute, Dundee, United KingdomCell and Molecular Sciences, The James Hutton Institute, Dundee, United KingdomCell and Molecular Sciences, The James Hutton Institute, Dundee, United KingdomCell and Molecular Sciences, The James Hutton Institute, Dundee, United KingdomCell and Molecular Sciences, The James Hutton Institute, Dundee, United KingdomCell and Molecular Sciences, The James Hutton Institute, Dundee, United KingdomCell and Molecular Sciences, The James Hutton Institute, Dundee, United KingdomCell and Molecular Sciences, The James Hutton Institute, Dundee, United KingdomSchool of Life Sciences, University of Dundee, Dundee, United KingdomSchool of Agriculture and Wine, University of Adelaide, Adelaide, SA, AustraliaIn flowering plants, successful germinal cell development and meiotic recombination depend upon a combination of environmental and genetic factors. To gain insights into this specialized reproductive development program we used short- and long-read RNA-sequencing (RNA-seq) to study the temporal dynamics of transcript abundance in immuno-cytologically staged barley (Hordeum vulgare) anthers and meiocytes. We show that the most significant transcriptional changes in anthers occur at the transition from pre-meiosis to leptotene–zygotene, which is followed by increasingly stable transcript abundance throughout prophase I into metaphase I–tetrad. Our analysis reveals that the pre-meiotic anthers are enriched in long non-coding RNAs (lncRNAs) and that entry to meiosis is characterized by their robust and significant down regulation. Intriguingly, only 24% of a collection of putative meiotic gene orthologs showed differential transcript abundance in at least one stage or tissue comparison. Argonautes, E3 ubiquitin ligases, and lys48 specific de-ubiquitinating enzymes were enriched in prophase I meiocyte samples. These developmental, time-resolved transcriptomes demonstrate remarkable stability in transcript abundance in meiocytes throughout prophase I after the initial and substantial reprogramming at meiosis entry and the complexity of the regulatory networks involved in early meiotic processes.https://www.frontiersin.org/articles/10.3389/fpls.2020.619404/fullbarleyanthermeiocytetranscriptomemeiosisargonaute
collection DOAJ
language English
format Article
sources DOAJ
author Abdellah Barakate
Jamie Orr
Miriam Schreiber
Isabelle Colas
Dominika Lewandowska
Nicola McCallum
Malcolm Macaulay
Jenny Morris
Mikel Arrieta
Pete E. Hedley
Luke Ramsay
Robbie Waugh
Robbie Waugh
Robbie Waugh
spellingShingle Abdellah Barakate
Jamie Orr
Miriam Schreiber
Isabelle Colas
Dominika Lewandowska
Nicola McCallum
Malcolm Macaulay
Jenny Morris
Mikel Arrieta
Pete E. Hedley
Luke Ramsay
Robbie Waugh
Robbie Waugh
Robbie Waugh
Barley Anther and Meiocyte Transcriptome Dynamics in Meiotic Prophase I
Frontiers in Plant Science
barley
anther
meiocyte
transcriptome
meiosis
argonaute
author_facet Abdellah Barakate
Jamie Orr
Miriam Schreiber
Isabelle Colas
Dominika Lewandowska
Nicola McCallum
Malcolm Macaulay
Jenny Morris
Mikel Arrieta
Pete E. Hedley
Luke Ramsay
Robbie Waugh
Robbie Waugh
Robbie Waugh
author_sort Abdellah Barakate
title Barley Anther and Meiocyte Transcriptome Dynamics in Meiotic Prophase I
title_short Barley Anther and Meiocyte Transcriptome Dynamics in Meiotic Prophase I
title_full Barley Anther and Meiocyte Transcriptome Dynamics in Meiotic Prophase I
title_fullStr Barley Anther and Meiocyte Transcriptome Dynamics in Meiotic Prophase I
title_full_unstemmed Barley Anther and Meiocyte Transcriptome Dynamics in Meiotic Prophase I
title_sort barley anther and meiocyte transcriptome dynamics in meiotic prophase i
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2021-01-01
description In flowering plants, successful germinal cell development and meiotic recombination depend upon a combination of environmental and genetic factors. To gain insights into this specialized reproductive development program we used short- and long-read RNA-sequencing (RNA-seq) to study the temporal dynamics of transcript abundance in immuno-cytologically staged barley (Hordeum vulgare) anthers and meiocytes. We show that the most significant transcriptional changes in anthers occur at the transition from pre-meiosis to leptotene–zygotene, which is followed by increasingly stable transcript abundance throughout prophase I into metaphase I–tetrad. Our analysis reveals that the pre-meiotic anthers are enriched in long non-coding RNAs (lncRNAs) and that entry to meiosis is characterized by their robust and significant down regulation. Intriguingly, only 24% of a collection of putative meiotic gene orthologs showed differential transcript abundance in at least one stage or tissue comparison. Argonautes, E3 ubiquitin ligases, and lys48 specific de-ubiquitinating enzymes were enriched in prophase I meiocyte samples. These developmental, time-resolved transcriptomes demonstrate remarkable stability in transcript abundance in meiocytes throughout prophase I after the initial and substantial reprogramming at meiosis entry and the complexity of the regulatory networks involved in early meiotic processes.
topic barley
anther
meiocyte
transcriptome
meiosis
argonaute
url https://www.frontiersin.org/articles/10.3389/fpls.2020.619404/full
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