Transcriptome Analyses of Mosaic (MSC) Mitochondrial Mutants of Cucumber in a Highly Inbred Nuclear Background

Cucumber (Cucumis sativus L.) has a large, paternally transmitted mitochondrial genome. Cucumber plants regenerated from cell cultures occasionally show paternally transmitted mosaic (MSC) phenotypes, characterized by slower growth, chlorotic patterns on the leaves and fruit, lower fertility, and re...

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Main Authors: Tomasz L. Mróz, Sebastian Eves-van den Akker, Agata Bernat, Agnieszka Skarzyńska, Leszek Pryszcz, Madeline Olberg, Michael J. Havey, Grzegorz Bartoszewski
Format: Article
Language:English
Published: Oxford University Press 2018-03-01
Series:G3: Genes, Genomes, Genetics
Subjects:
Online Access:http://g3journal.org/lookup/doi/10.1534/g3.117.300321
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spelling doaj-0f775c47168246889819981f7e54f05e2021-07-02T06:39:43ZengOxford University PressG3: Genes, Genomes, Genetics2160-18362018-03-018395396510.1534/g3.117.30032120Transcriptome Analyses of Mosaic (MSC) Mitochondrial Mutants of Cucumber in a Highly Inbred Nuclear BackgroundTomasz L. MrózSebastian Eves-van den AkkerAgata BernatAgnieszka SkarzyńskaLeszek PryszczMadeline OlbergMichael J. HaveyGrzegorz BartoszewskiCucumber (Cucumis sativus L.) has a large, paternally transmitted mitochondrial genome. Cucumber plants regenerated from cell cultures occasionally show paternally transmitted mosaic (MSC) phenotypes, characterized by slower growth, chlorotic patterns on the leaves and fruit, lower fertility, and rearrangements in their mitochondrial DNAs (mtDNAs). MSC lines 3, 12, and 16 originated from different cell cultures all established using the highly inbred, wild-type line B. These MSC lines possess different rearrangements and under-represented regions in their mtDNAs. We completed RNA-seq on normalized and non-normalized cDNA libraries from MSC3, MSC12, and MSC16 to study their nuclear gene-expression profiles relative to inbred B. Results from both libraries indicated that gene expression in MSC12 and MSC16 were more similar to each other than MSC3. Forty-one differentially expressed genes (DEGs) were upregulated and one downregulated in the MSC lines relative to B. Gene functional classifications revealed that more than half of these DEGs are associated with stress-response pathways. Consistent with this observation, we detected elevated levels of hydrogen peroxide throughout leaf tissue in all MSC lines compared to wild-type line B. These results demonstrate that independently produced MSC lines with different mitochondrial polymorphisms show unique and shared nuclear responses. This study revealed genes associated with stress response that could become selection targets to develop cucumber cultivars with increased stress tolerance, and further support of cucumber as a model plant to study nuclear-mitochondrial interactions.http://g3journal.org/lookup/doi/10.1534/g3.117.300321Cucumis sativusmitochondrial mutantnuclear–mitochondrial interactionplant mitochondriaRNA-seq
collection DOAJ
language English
format Article
sources DOAJ
author Tomasz L. Mróz
Sebastian Eves-van den Akker
Agata Bernat
Agnieszka Skarzyńska
Leszek Pryszcz
Madeline Olberg
Michael J. Havey
Grzegorz Bartoszewski
spellingShingle Tomasz L. Mróz
Sebastian Eves-van den Akker
Agata Bernat
Agnieszka Skarzyńska
Leszek Pryszcz
Madeline Olberg
Michael J. Havey
Grzegorz Bartoszewski
Transcriptome Analyses of Mosaic (MSC) Mitochondrial Mutants of Cucumber in a Highly Inbred Nuclear Background
G3: Genes, Genomes, Genetics
Cucumis sativus
mitochondrial mutant
nuclear–mitochondrial interaction
plant mitochondria
RNA-seq
author_facet Tomasz L. Mróz
Sebastian Eves-van den Akker
Agata Bernat
Agnieszka Skarzyńska
Leszek Pryszcz
Madeline Olberg
Michael J. Havey
Grzegorz Bartoszewski
author_sort Tomasz L. Mróz
title Transcriptome Analyses of Mosaic (MSC) Mitochondrial Mutants of Cucumber in a Highly Inbred Nuclear Background
title_short Transcriptome Analyses of Mosaic (MSC) Mitochondrial Mutants of Cucumber in a Highly Inbred Nuclear Background
title_full Transcriptome Analyses of Mosaic (MSC) Mitochondrial Mutants of Cucumber in a Highly Inbred Nuclear Background
title_fullStr Transcriptome Analyses of Mosaic (MSC) Mitochondrial Mutants of Cucumber in a Highly Inbred Nuclear Background
title_full_unstemmed Transcriptome Analyses of Mosaic (MSC) Mitochondrial Mutants of Cucumber in a Highly Inbred Nuclear Background
title_sort transcriptome analyses of mosaic (msc) mitochondrial mutants of cucumber in a highly inbred nuclear background
publisher Oxford University Press
series G3: Genes, Genomes, Genetics
issn 2160-1836
publishDate 2018-03-01
description Cucumber (Cucumis sativus L.) has a large, paternally transmitted mitochondrial genome. Cucumber plants regenerated from cell cultures occasionally show paternally transmitted mosaic (MSC) phenotypes, characterized by slower growth, chlorotic patterns on the leaves and fruit, lower fertility, and rearrangements in their mitochondrial DNAs (mtDNAs). MSC lines 3, 12, and 16 originated from different cell cultures all established using the highly inbred, wild-type line B. These MSC lines possess different rearrangements and under-represented regions in their mtDNAs. We completed RNA-seq on normalized and non-normalized cDNA libraries from MSC3, MSC12, and MSC16 to study their nuclear gene-expression profiles relative to inbred B. Results from both libraries indicated that gene expression in MSC12 and MSC16 were more similar to each other than MSC3. Forty-one differentially expressed genes (DEGs) were upregulated and one downregulated in the MSC lines relative to B. Gene functional classifications revealed that more than half of these DEGs are associated with stress-response pathways. Consistent with this observation, we detected elevated levels of hydrogen peroxide throughout leaf tissue in all MSC lines compared to wild-type line B. These results demonstrate that independently produced MSC lines with different mitochondrial polymorphisms show unique and shared nuclear responses. This study revealed genes associated with stress response that could become selection targets to develop cucumber cultivars with increased stress tolerance, and further support of cucumber as a model plant to study nuclear-mitochondrial interactions.
topic Cucumis sativus
mitochondrial mutant
nuclear–mitochondrial interaction
plant mitochondria
RNA-seq
url http://g3journal.org/lookup/doi/10.1534/g3.117.300321
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