Differential transmission of the Cucumis organellar genomes

Havey, Michael J.; McCreight, James D.; Rhodes, B. B.; Taurick, G.

doi:10.1007/s001220050875

Cited by 79 publications

(49 citation statements)

References 37 publications

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“…More examinations of such species will be required to determine this possibility. For Cucumis melo, the only angiosperm species known to employ paternal mitochondrial inheritance (Havey et al, 1998), insurmountable technical difficulties unfortunately prevented us from isolating intact egg cells.…”

Section: Mtdna Levels In Egg Cellsmentioning

confidence: 99%

The Levels of Male Gametic Mitochondrial DNA Are Highly Regulated in Angiosperms with Regard to Mitochondrial Inheritance

et al. 2010

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The mechanisms that regulate mitochondrial inheritance are not yet clear, even though it is 100 years since the first description of non-Mendelian genetics. Here, we quantified the copy numbers of mitochondrial DNA (mtDNA) in the gametic cells of angiosperm species. We demonstrate that each egg cell from Arabidopsis thaliana, Antirrhinum majus, and Nicotiana tabacum possesses 59.0, 42.7, and 73.0 copies of mtDNA on average, respectively. These values are equivalent to those in Arabidopsis mesophyll cells, at 61.7 copies per cell. On the other hand, sperm or generative cells from Arabidopsis, A. majus, and N. tabacum possess minor amounts of mtDNA, at 0.083, 0.47, and 1 copy on average, respectively. We further reveal a 50-fold degradation of mtDNA during pollen development in A. majus. In contrast, markedly high levels of mtDNA are found in the male gametic cells of Cucumis melo and Pelargonium zonale (1296.3 and 256.7 copies, respectively). Our results provide direct evidence for mitochondrial genomic insufficiency in the eggs and somatic cells and indicate that a male gamete of an angiosperm may possess mtDNA at concentrations as high as 21-fold (C. melo) or as low as 0.1% (Arabidopsis) of the levels in somatic cells. These observations reveal the existence of a strong regulatory system for the male gametic mtDNA levels in angiosperms with regard to mitochondrial inheritance.

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Section: Mtdna Levels In Egg Cellsmentioning

confidence: 99%

The Levels of Male Gametic Mitochondrial DNA Are Highly Regulated in Angiosperms with Regard to Mitochondrial Inheritance

et al. 2010

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“…The mitochondrial genomes of two of these species, watermelon (Citrullus lanatus) and zucchini (Cucurbita pepo), have been sequenced, and their 2.6-fold size difference (379 kb in watermelon and 983 kb in zucchini) reflects in large part vast differences in the amounts of repetitive DNA and integrated chloroplast sequences . Limited data on the largest two genomes, from cucumber (Cucumis sativus; ;1.8 Mb) and muskmelon (;2.9 Mb), suggest that they do not contain disproportionately more genes (Stern and Newton, 1985) or chloroplast-derived DNA (Stern et al, 1983;Havey et al, 1998). Although neither genome is thought to contain large-scale segmental duplications (Havey et al, 1998), limited sequencing suggests that short dispersed repeats might account for as much as 13% of the cucumber mitochondrial genome (Lilly and Havey, 2001).…”

Section: Introductionmentioning

confidence: 99%

“…Limited data on the largest two genomes, from cucumber (Cucumis sativus; ;1.8 Mb) and muskmelon (;2.9 Mb), suggest that they do not contain disproportionately more genes (Stern and Newton, 1985) or chloroplast-derived DNA (Stern et al, 1983;Havey et al, 1998). Although neither genome is thought to contain large-scale segmental duplications (Havey et al, 1998), limited sequencing suggests that short dispersed repeats might account for as much as 13% of the cucumber mitochondrial genome (Lilly and Havey, 2001). In short, the factors underlying the growth of these extraordinarily large mitochondrial genomes remain unclear.…”

Section: Introductionmentioning

confidence: 99%

Origins and Recombination of the Bacterial-Sized Multichromosomal Mitochondrial Genome of Cucumber

et al. 2011

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Members of the flowering plant family Cucurbitaceae harbor the largest known mitochondrial genomes. Here, we report the 1685-kb mitochondrial genome of cucumber (Cucumis sativus). We help solve a 30-year mystery about the origins of its large size by showing that it mainly reflects the proliferation of dispersed repeats, expansions of existing introns, and the acquisition of sequences from diverse sources, including the cucumber nuclear and chloroplast genomes, viruses, and bacteria. The cucumber genome has a novel structure for plant mitochondria, mapping as three entirely or largely autonomous circular chromosomes (lengths 1556, 84, and 45 kb) that vary in relative abundance over a twofold range. These properties suggest that the three chromosomes replicate independently of one another. The two smaller chromosomes are devoid of known functional genes but nonetheless contain diagnostic mitochondrial features. Paired-end sequencing conflicts reveal differences in recombination dynamics among chromosomes, for which an explanatory model is developed, as well as a large pool of low-frequency genome conformations, many of which may result from asymmetric recombination across intermediate-sized and sometimes highly divergent repeats. These findings highlight the promise of genome sequencing for elucidating the recombinational dynamics of plant mitochondrial genomes.

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“…The mitochondrial genome of cucumber is unique for its large size (Ward et al 1981), paternal transmission (Havey 1997;Havey et al 1998), and the production of mosaic phenotypes after in vitro culture (Malepszy et al 1996) associated with mitochondrial DNA rearrangements Bartoszewski et al 2004b). The paternal transmission of cucumber mtDNA makes it easy to distinguish phenotypes conditioned by the chloroplast or mitochondrial DNAs.…”

Section: Discussionmentioning

confidence: 99%

“…Species in genus Cucumis show a differential transmission of the three plant genomes, maternal for the chloroplast, paternal for the mitochondrial, and biparental for the nuclear DNA (Havey 1997;Havey et al 1998). The MSC phenotype shows paternal inheritance (Malepszy et al 1996), indicating that MSC is conditioned by the mitochondrial DNA.…”

Section: Introductionmentioning

confidence: 99%

The selection of mosaic (MSC) phenotype after passage of cucumber (Cucumis sativus L.) through cell culture — a method to obtain plant mitochondrial mutants

Bartoszewski¹,

Havey

Ziółkowska³

et al. 2007

J Appl Genet

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Mosaic (MSC) mutants of cucumber (Cucumis sativus L.) appear after passage through cell cultures. The MSC phenotype shows paternal transmission and is associated with mitochondrial DNA rearrangements. This review describes the origins and phenotypes of independently produced MSC mutants of cucumber, including current knowledge on their mitochondrial DNA rearrangements, and similarities of MSC with other plant mitochondrial mutants. Finally we propose that passage of cucumber through cell culture can be used as a unique and efficient method to generate mitochondrial mutants of a higher plant in a highly homozygous nuclear background.

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Differential transmission of the Cucumis organellar genomes

Cited by 79 publications

References 37 publications

The Levels of Male Gametic Mitochondrial DNA Are Highly Regulated in Angiosperms with Regard to Mitochondrial Inheritance

The Levels of Male Gametic Mitochondrial DNA Are Highly Regulated in Angiosperms with Regard to Mitochondrial Inheritance

Origins and Recombination of the Bacterial-Sized Multichromosomal Mitochondrial Genome of Cucumber

The selection of mosaic (MSC) phenotype after passage of cucumber (Cucumis sativus L.) through cell culture — a method to obtain plant mitochondrial mutants

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