Evidence for paternal transmission and heteroplasmy in the mitochondrial genome of Silene vulgaris, a gynodioecious plant

Abstract Background Gynodioecious species exist in two sexes – male-sterile females and hermaphrodites. Male sterility in higher plants often results from mitonuclear interaction between the CMS (cytoplasmic male sterility) gene(s) encoded by mitochondrial genome and by nuclear-encoded restorer genes. Mitochondrial and nuclear-encoded transcriptomes in females and hermaphrodites are intensively studied, but little is known about sex-specific gene expression in plastids. We have compared plastid transcriptomes between females and hermaphrodites in two haplotypes of a gynodioecious species Silene vulgaris with known CMS candidate genes. Results We generated complete plastid genome sequences from five haplotypes S. vulgaris including the haplotypes KRA and KOV, for which complete mitochondrial genome sequences were already published. We constructed a phylogenetic tree based on plastid sequences of S. vulgaris. Whereas lowland S. vulgaris haplotypes including KRA and KOV clustered together, the accessions from high European mountains diverged early in the phylogram. S. vulgaris belongs among Silene species with slowly evolving plastid genomes, but we still detected 212 substitutions and 112 indels between two accessions of this species. We estimated elevated Ka/Ks in the ndhF gene, which may reflect the adaptation of S. vulgaris to high altitudes, or relaxed selection. We compared depth of coverage and editing rates between female and hermaphrodite plastid transcriptomes and found no significant differences between the two sexes. We identified 51 unique C to U editing sites in the plastid genomes of S. vulgaris, 38 of them in protein coding regions, 2 in introns, and 11 in intergenic regions. The editing site in the psbZ gene was edited only in one of two plastid genomes under study. Conclusions We revealed no significant differences between the sexes in plastid transcriptomes of two haplotypes of S. vulgaris. It suggests that gene expression of plastid genes is not affected by CMS in flower buds of S. vulgaris, although both sexes may still differ in plastid gene expression in specific tissues. We revealed the difference between the plastid transcriptomes of two S. vulgaris haplotypes in editing rate and in the coverage of several antisense transcripts. Our results document the variation in plastid genomes and transcriptomes in S. vulgaris.

Download Full-text

Variation in plastid genomes and transcriptomes in the gynodioecious species Silene vulgaris

10.21203/rs.2.11276/v1 ◽

2019 ◽

Author(s):

Manuela Krüger ◽

Oushadee A.J. Abeyawardana ◽

Miloslav Juricek ◽

Claudia Krüger ◽

Helena Storchova

Keyword(s):

Gene Expression ◽

Mitochondrial Genome ◽

Male Sterility ◽

Higher Plants ◽

Complete Mitochondrial Genome ◽

Specific Gene ◽

Silene Vulgaris ◽

Male Sterile ◽

Genome Sequences ◽

Plastid Genomes

Abstract Background Gynodioecious species exist in two genders – male-sterile females and hermaphrodites. Male sterility in higher plants often results from mitonuclear interaction between the CMS (cytoplasmic male sterility) gene(s) encoded by mitochondrial genome and by nuclear-encoded restorer genes. Mitochondrial and nuclear-encoded transcriptomes in females and hermaphrodites are intensively studied, but little is known about gender-specific gene expression in plastids. We have compared plastid transcriptomes between females and hermaphrodites in two haplotypes of a gynodioecious species Silene vulgaris with known CMS candidate genes. Results We generated complete plastid genome sequences from five haplotypes S. vulgaris including the haplotypes KRA and KOV, for which complete mitochondrial genome sequences were already published. We constructed a phylogenetic tree based on plastid sequences of S. vulgaris. Whereas lowland S. vulgaris haplotypes including KRA and KOV clustered together, the accessions from high European mountains diverged early in the phylogram. S. vulgaris belongs among Silene species with slowly evolving plastid genomes, but we still detected 212 substitutions and 112 indels between two accessions of this species. We estimated elevated Ka/Ks in the ndhF gene, which may reflect the adaptation of S. vulgaris to high altitudes, or relaxed selection. We compared depth of coverage and editing rates between female and hermaphrodite plastid transcriptomes and found no significant differences between the two genders. We identified 51 unique C to U editing sites in the plastid genomes of S. vulgaris, 38 of them in protein coding regions, 2 in introns, and 11 in intergenic regions. The editing site in the psbZ gene was edited only in one of two plastid genomes under study. Conclusions We revealed no significant differences between the genders in plastid transcriptomes of two haplotypes of S. vulgaris. It suggests that gene expression of plastid genes is not affected by CMS in flower buds of S. vulgaris, although both genders may still differ in plastid gene expression in specific tissues. We revealed the difference between the plastid transcriptomes of two S. vulgaris haplotypes in editing rate and in the coverage of several antisense transcripts. Our results document the variation in plastid genomes and transcriptomes in S. vulgaris.

Download Full-text

Predominant Paternal Transmission of the Mitochondrial Genome in Cucumber

Journal of Heredity ◽

10.1093/oxfordjournals.jhered.a023094 ◽

1997 ◽

Vol 88 (3) ◽

pp. 232-235 ◽

Cited By ~ 49

Author(s):

M. J. Havey

Keyword(s):

Mitochondrial Genome ◽

Paternal Transmission

Download Full-text

A protein binding site in the M mitochondrial genome of Mytilus galloprovincialis may be responsible for its paternal transmission

Gene ◽

10.1016/j.gene.2015.02.047 ◽

2015 ◽

Vol 562 (1) ◽

pp. 83-94 ◽

Cited By ~ 15

Author(s):

Eleni Kyriakou ◽

Lara Kravariti ◽

Themistoklis Vasilopoulos ◽

Eleftherios Zouros ◽

George C. Rodakis

Keyword(s):

Mitochondrial Genome ◽

Protein Binding ◽

Binding Site ◽

Mytilus Galloprovincialis ◽

Protein Binding Site ◽

Paternal Transmission

Download Full-text

Homologous recombination changes the context of Cytochrome b transcription in the mitochondrial genome of Silene vulgaris KRA

10.1101/422808 ◽

2018 ◽

Author(s):

Helena Štorchová ◽

James D. Stone ◽

Daniel B. Sloan ◽

Oushadee Abeyawardana ◽

Karel Müller ◽

...

Keyword(s):

Homologous Recombination ◽

Mitochondrial Genome ◽

Rna Editing ◽

Cytochrome B ◽

Mitochondrial Genes ◽

Mitochondrial Genomes ◽

Silene Vulgaris ◽

Fertility Restorer ◽

Restorer Genes ◽

Fertility Restorer Genes

AbstractBackgroundSilene vulgaris (bladder campion) is a gynodioecious species existing as two genders – male-sterile females and hermaphrodites. Cytoplasmic male sterility (CMS) is generally encoded by mitochondrial genes, which interact with nuclear fertility restorer genes. Mitochondrial genomes of this species vary in DNA sequence, gene order and gene content. Multiple CMS genes are expected to exist in S. vulgaris, but little is known about their molecular identity.ResultsWe assembled the complete mitochondrial genome from the haplotype KRA of S. vulgaris. It consists of five chromosomes, two of which recombine with each other. Two small non-recombining chromosomes exist in linear, supercoiled and relaxed circle forms. We compared the mitochondrial transcriptomes from females and hermaphrodites and confirmed the differentially expressed chimeric gene bobt as the strongest CMS candidate gene in S. vulgaris KRA. The chimeric gene bobt is co-transcribed with the Cytochrome b (cob) gene in some genomic configurations. The co-transcription of a CMS factor with an essential gene may constrain transcription inhibition as a mechanism for fertility restoration because of the need to maintain appropriate production of the necessary protein. Homologous recombination places the gene cob outside the control of bobt, which allows for the suppression the CMS gene by the fertility restorer genes. In addition, by analyzing RNA editing, we found the loss of three editing sites in the KRA mitochondrial genome and identified four sites with highly distinct editing rates between KRA and another S. vulgaris haplotypes (KOV). Three of these highly differentially edited sites were located in the transport membrane protein B (mttB) gene. They resulted in differences in MttB protein sequences between haplotypes despite completely identical gene sequences.ConclusionsFrequent homologous recombination events that are widespread in plant mitochondrial genomes may change chromosomal configurations and also the control of gene transcription including CMS gene expression. Posttranscriptional processes, e.g RNA editing shall be evaluated in evolutionary and co-evolutionary studies of mitochondrial genes, because they may change protein composition despite the sequence identity of the respective genes. The investigation of natural populations of wild species such as S. vulgaris are necessary to reveal important aspects of CMS missed in domesticated crops, the traditional focus of the CMS studies.

Download Full-text

Variation in plastid genomes in the gynodioecious species Silene vulgaris

10.21203/rs.2.11276/v2 ◽

2019 ◽

Author(s):

Manuela Krüger ◽

Oushadee A.J. Abeyawardana ◽

Miloslav Juricek ◽

Claudia Krüger ◽

Helena Storchova

Keyword(s):

Gene Expression ◽

Mitochondrial Genome ◽

Male Sterility ◽

Higher Plants ◽

Complete Mitochondrial Genome ◽

Specific Gene ◽

Silene Vulgaris ◽

Male Sterile ◽

Genome Sequences ◽

Plastid Genomes

Abstract Background Gynodioecious species exist in two genders – male-sterile females and hermaphrodites. Male sterility in higher plants often results from mitonuclear interaction between the CMS (cytoplasmic male sterility) gene(s) encoded by mitochondrial genome and by nuclear-encoded restorer genes. Mitochondrial and nuclear-encoded transcriptomes in females and hermaphrodites are intensively studied, but little is known about gender-specific gene expression in plastids. We have compared plastid transcriptomes between females and hermaphrodites in two haplotypes of a gynodioecious species Silene vulgaris with known CMS candidate genes. Results We generated complete plastid genome sequences from five haplotypes S. vulgaris including the haplotypes KRA and KOV, for which complete mitochondrial genome sequences were already published. We constructed a phylogenetic tree based on plastid sequences of S. vulgaris. Whereas lowland S. vulgaris haplotypes including KRA and KOV clustered together, the accessions from high European mountains diverged early in the phylogram. S. vulgaris belongs among Silene species with slowly evolving plastid genomes, but we still detected 212 substitutions and 112 indels between two accessions of this species. We estimated elevated Ka/Ks in the ndhF gene, which may reflect the adaptation of S. vulgaris to high altitudes, or relaxed selection. We compared depth of coverage and editing rates between female and hermaphrodite plastid transcriptomes and found no significant differences between the two genders. We identified 51 unique C to U editing sites in the plastid genomes of S. vulgaris, 38 of them in protein coding regions, 2 in introns, and 11 in intergenic regions. The editing site in the psbZ gene was edited only in one of two plastid genomes under study. Conclusions We revealed no significant differences between the genders in plastid transcriptomes of two haplotypes of S. vulgaris. It suggests that gene expression of plastid genes is not affected by CMS in flower buds of S. vulgaris, although both genders may still differ in plastid gene expression in specific tissues. We revealed the difference between the plastid transcriptomes of two S. vulgaris haplotypes in editing rate and in the coverage of several antisense transcripts. Our results document the variation in plastid genomes and transcriptomes in S. vulgaris.

Download Full-text

Variation in plastid genomes in the gynodioecious species Silene vulgaris

10.21203/rs.2.11276/v3 ◽

2019 ◽

Author(s):

Manuela Krüger ◽

Oushadee A.J. Abeyawardana ◽

Miloslav Juricek ◽

Claudia Krüger ◽

Helena Storchova

Keyword(s):

Gene Expression ◽

Mitochondrial Genome ◽

Male Sterility ◽

Higher Plants ◽

Complete Mitochondrial Genome ◽

Specific Gene ◽

Silene Vulgaris ◽

Male Sterile ◽

Genome Sequences ◽

Plastid Genomes

Abstract Background Gynodioecious species exist in two sexes – male-sterile females and hermaphrodites. Male sterility in higher plants often results from mitonuclear interaction between the CMS (cytoplasmic male sterility) gene(s) encoded by mitochondrial genome and by nuclear-encoded restorer genes. Mitochondrial and nuclear-encoded transcriptomes in females and hermaphrodites are intensively studied, but little is known about sex-specific gene expression in plastids. We have compared plastid transcriptomes between females and hermaphrodites in two haplotypes of a gynodioecious species Silene vulgaris with known CMS candidate genes. Results We generated complete plastid genome sequences from five haplotypes S. vulgaris including the haplotypes KRA and KOV, for which complete mitochondrial genome sequences were already published. We constructed a phylogenetic tree based on plastid sequences of S. vulgaris. Whereas lowland S. vulgaris haplotypes including KRA and KOV clustered together, the accessions from high European mountains diverged early in the phylogram. S. vulgaris belongs among Silene species with slowly evolving plastid genomes, but we still detected 212 substitutions and 112 indels between two accessions of this species. We estimated elevated Ka/Ks in the ndhF gene, which may reflect the adaptation of S. vulgaris to high altitudes, or relaxed selection. We compared depth of coverage and editing rates between female and hermaphrodite plastid transcriptomes and found no significant differences between the two sexes. We identified 51 unique C to U editing sites in the plastid genomes of S. vulgaris, 38 of them in protein coding regions, 2 in introns, and 11 in intergenic regions. The editing site in the psbZ gene was edited only in one of two plastid genomes under study. Conclusions We revealed no significant differences between the sexes in plastid transcriptomes of two haplotypes of S. vulgaris. It suggests that gene expression of plastid genes is not affected by CMS in flower buds of S. vulgaris, although both sexes may still differ in plastid gene expression in specific tissues. We revealed the difference between the plastid transcriptomes of two S. vulgaris haplotypes in editing rate and in the coverage of several antisense transcripts. Our results document the variation in plastid genomes and transcriptomes in S. vulgaris.

Download Full-text