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

Tomasz L. Mróz, Sebastian Eves-van den Akker, Agata Bernat, Agnieszka Skarzyńska, Leszek Pryszcz, Madeline Olberg, Michael J. Havey, Grzegorz Bartoszewski (Lead / Corresponding author)

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Abstract

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 up- and one down-regulated 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.

Original languageEnglish
Pages (from-to)953-965
Number of pages13
JournalG3 : Genes, Genomes, Genetics
Volume8
Issue number3
Early online date12 Jan 2018
DOIs
Publication statusPublished - 29 Jan 2018

Fingerprint

Cucumis sativus
Gene Expression Profiling
Mitochondrial DNA
Genes
Cell Culture Techniques
Mitochondrial Genome
Plant Cells
Gene Library
Transcriptome
Hydrogen Peroxide
Libraries
Fertility
Fruit
RNA
Phenotype
Gene Expression
Growth

Keywords

  • Journal article
  • Cucumis Sativus
  • Mitochondrial mutant
  • Nuclear-mitochondrial interaction
  • Plant mitochondria
  • RNA-SEQ
  • Nuclear- mitochondrial interaction
  • RNA-seq
  • Cucumis sativus
  • Cucumis sativus/genetics
  • Transcriptome
  • DNA, Mitochondrial
  • Gene Expression Profiling
  • Computational Biology/methods
  • Cell Nucleus/genetics
  • Gene Expression Regulation, Plant
  • Inbreeding
  • Gene Library
  • Signal Transduction
  • Molecular Sequence Annotation
  • Phenotype
  • Mitochondria/genetics
  • Mosaicism
  • High-Throughput Nucleotide Sequencing
  • Genome, Mitochondrial
  • Mutation

Cite this

Mróz, T. L., Eves-van den Akker, S., Bernat, A., Skarzyńska, A., Pryszcz, L., Olberg, M., ... Bartoszewski, G. (2018). Transcriptome Analyses of Mosaic (MSC) Mitochondrial Mutants of Cucumber in a Highly Inbred Nuclear Background. G3 : Genes, Genomes, Genetics, 8(3), 953-965. https://doi.org/10.1534/g3.117.300321
Mróz, Tomasz L. ; Eves-van den Akker, Sebastian ; Bernat, Agata ; Skarzyńska, Agnieszka ; Pryszcz, Leszek ; Olberg, Madeline ; Havey, Michael J. ; Bartoszewski, Grzegorz. / Transcriptome Analyses of Mosaic (MSC) Mitochondrial Mutants of Cucumber in a Highly Inbred Nuclear Background. In: G3 : Genes, Genomes, Genetics. 2018 ; Vol. 8, No. 3. pp. 953-965.
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abstract = "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 up- and one down-regulated 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.",
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author = "Mr{\'o}z, {Tomasz L.} and {Eves-van den Akker}, Sebastian and Agata Bernat and Agnieszka Skarzyńska and Leszek Pryszcz and Madeline Olberg and Havey, {Michael J.} and Grzegorz Bartoszewski",
note = "This work was supported by the Polish National Science Center NCN project N N310 107740, the WULS-PLANT HEALTH project FP7-286093, and the USDA Agricultural Research Service. SE-vdA was supported by Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/M014207/1.",
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Mróz, TL, Eves-van den Akker, S, Bernat, A, Skarzyńska, A, Pryszcz, L, Olberg, M, Havey, MJ & Bartoszewski, G 2018, 'Transcriptome Analyses of Mosaic (MSC) Mitochondrial Mutants of Cucumber in a Highly Inbred Nuclear Background', G3 : Genes, Genomes, Genetics, vol. 8, no. 3, pp. 953-965. https://doi.org/10.1534/g3.117.300321

Transcriptome Analyses of Mosaic (MSC) Mitochondrial Mutants of Cucumber in a Highly Inbred Nuclear Background. / Mróz, Tomasz L.; Eves-van den Akker, Sebastian; Bernat, Agata; Skarzyńska, Agnieszka; Pryszcz, Leszek; Olberg, Madeline; Havey, Michael J.; Bartoszewski, Grzegorz (Lead / Corresponding author).

In: G3 : Genes, Genomes, Genetics, Vol. 8, No. 3, 29.01.2018, p. 953-965.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Transcriptome Analyses of Mosaic (MSC) Mitochondrial Mutants of Cucumber in a Highly Inbred Nuclear Background

AU - Mróz, Tomasz L.

AU - Eves-van den Akker, Sebastian

AU - Bernat, Agata

AU - Skarzyńska, Agnieszka

AU - Pryszcz, Leszek

AU - Olberg, Madeline

AU - Havey, Michael J.

AU - Bartoszewski, Grzegorz

N1 - This work was supported by the Polish National Science Center NCN project N N310 107740, the WULS-PLANT HEALTH project FP7-286093, and the USDA Agricultural Research Service. SE-vdA was supported by Biotechnology and Biological Sciences Research Council (BBSRC) grant BB/M014207/1.

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Y1 - 2018/1/29

N2 - 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 up- and one down-regulated 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.

AB - 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 up- and one down-regulated 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.

KW - Journal article

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KW - RNA-seq

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KW - Gene Expression Regulation, Plant

KW - Inbreeding

KW - Gene Library

KW - Signal Transduction

KW - Molecular Sequence Annotation

KW - Phenotype

KW - Mitochondria/genetics

KW - Mosaicism

KW - High-Throughput Nucleotide Sequencing

KW - Genome, Mitochondrial

KW - Mutation

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