Evidence for Paternal Leakage in Hybrid Periodical Cicadas (Hemiptera: Magicicada spp.)

Fontaine, Kathryn; Cooley, John R.; Simon, Chris

doi:10.1371/journal.pone.0000892

Cited by 64 publications

(61 citation statements)

References 58 publications

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“…Both events have been documented to occur in mammals (Gyllensten et al, 1991;Schwartz and Vissing, 2002;Ladoukakis and Eyre-Walker, 2004;Zhao et al, 2004), birds (Kvist et al, 2003), fish (Magoulas and Zouros, 1993;Guo et al, 2006;Ciborowski et al, 2007), mollusks (Ladoukakis and Zouros, 2001), amphibians (Ujvari et al, 2007), arthropods (Meusel and Moritz, 1993;Gantenbein et al, 2005;Arunkumar et al, 2006;Sherengul et al, 2006;Fontaine et al, 2007) and nematodes (Lunt and Hyman, 1997;Armstrong et al, 2007). What is more, gender-associated and tissue-specific transmission of both paternal and maternal mtDNA ('doubly uniparental inheritance' (DUI)) appears to be the norm in some bivalves (Breton et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

Lost in the zygote: the dilution of paternal mtDNA upon fertilization

Wolff¹,

Gemmell²

2008

Heredity

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The mechanisms by which paternal inheritance of mitochondrial DNA (mtDNA) (paternal leakage) and, subsequently, recombination of mtDNA are prevented vary in a speciesspecific manner with one mechanism in common: paternally derived mtDNA is assumed to be vastly outnumbered by maternal mtDNA in the zygote. To date, this dilution effect has only been described for two mammalian species, human and mouse. Here, we estimate the mtDNA content of chinook salmon oocytes to evaluate the dilution effect operating in another vertebrate; the first such study outside a mammalian system. Employing real-time PCR, we determined the mtDNA content of chinook salmon oocytes to be 3.2 Â 10 9 ± 1.0 Â 10 9 , and recently, we determined the mtDNA content of chinook salmon sperm to be 5.73 ± 2.28 per gamete. Accordingly, the ratio of paternal-to-maternal mtDNA if paternal leakage occurs is estimated to be 1:5.5 Â 10 8 . This contribution of paternal mtDNA to the overall mtDNA pool in salmon zygotes is three to five orders of magnitude smaller than those revealed for the mammalian system, strongly suggesting that paternal inheritance of mtDNA per offspring will be much less likely in this system than in mammals.

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Section: Introductionmentioning

confidence: 99%

Lost in the zygote: the dilution of paternal mtDNA upon fertilization

Wolff¹,

Gemmell²

2008

Heredity

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“…Mitochondrial heteroplasmy is typically infrequent even within organisms in which it has been reported, and heteroplasmy is rarely documented in natural populations, with most examples coming from experimental hybrids and natural hybrid zones (Kvist et al 2003, Fontaine et al 2007; but see (Paduan andRibolla 2008, Fonseca et al 2009). Heteroplasmy often poses considerable problems to the health of the organism (Russell and Turnbull 2014) because the introgression of paternal haplotypes may disrupt nuclear-mitochondrial interactions and introduce male-specific deleterious mutations.…”

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confidence: 99%

Extensive Mitochondrial Heteroplasmy in Natural Populations of a Resurging Human Pest, the Bed Bug (Hemiptera: Cimicidae)

et al. 2015

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Homoplasmy, the occurrence of a single mitochondrial DNA haplotype within an individual, has been the accepted condition across most organisms in the animal kingdom. In recent years, a number of exceptions to this rule have been reported, largely due to the ease with which single nucleotide polymorphisms can be detected. Evidence of heteroplasmy-two or more mitochondrial variants within a single individual-has now been documented in a number of invertebrates; however, when present, heteroplasmy usually occurs at low frequencies both within individuals and within populations. The implications of heteroplasmy may be far reaching, both to the individual in relation to its health and fitness, and when considering the evolutionary dynamics of populations. We present novel evidence for frequent mtDNA heteroplasmy in the bed bug, Cimex lectularius L. (Hemiptera: Cimicidae). Our findings show that heteroplasmy is common, with 5 of 29 (17%) populations screened exhibiting two mitochondrial variants in a $1:2 ratio within each individual. We hypothesize that the mechanism underlying heteroplasmy in bed bugs is paternal leakage because some haplotypes were shared among unrelated populations and no evidence for nuclear mitochondrial DNA sequences was detected.

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“…Heteroplasmy has received considerable attention in recent years, partly because of reports showing the paternal leakage of organellar DNA inheritance in plants (Azhagiri and Maliga 2007;Svab and Maliga 2007), insects (Sherengul et al 2006;Fontaine et al 2007), and animals including humans (Schwartz and Vissing 2002); paternal leakage is thought to be the major source for heteroplasmy. While spa19 is an unusual heteroplasmic mutant given its stable heteroplasmy and inheritance pattern, it nonetheless offers insight into the possible impact in WT cells of switching on and off specific replication modes.…”

Section: Discussionmentioning

confidence: 99%

Differential Replication of Two Chloroplast Genome Forms in Heteroplasmic Chlamydomonas reinhardtii Gametes Contributes to Alternative Inheritance Patterns

Nishimura

Stern

2010

Genetics

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Two mechanisms for chloroplast DNA replication have been revealed through the study of an unusual heteroplasmic strain of the green alga Chlamydomonas reinhardtii. Heteroplasmy is a state in which more than one genome type occurs in a mitochondrion or chloroplast. The Chlamydomonas strain spa19 bears two distinct chloroplast genomes, termed PS1 and PSÀ. PS1 genomes predominate and are stably maintained in vegetative cells, despite their lack of known replication origins. In sexual crosses with spa19 as the mating type plus parent, however, PS1 genomes are transmitted in only $25% of tetrads, whereas the PSÀ genomes are faithfully inherited in all progeny. In this research, we have explored the mechanism underlying this biased uniparental inheritance. We show that the relative reduction and dilution of PS1 vs. PSÀ genomes takes place during gametogenesis. Bromodeoxyuridine labeling, followed by immunoprecipitation and PCR, was used to compare replication activities of PS1 and PSÀ genomes. We found that the replication of PS1 genomes is specifically suppressed during gametogenesis and germination of zygospores, a phenomenon that also was observed when spa19 cells were treated with rifampicin, an inhibitor of the chloroplast RNA polymerase. Furthermore, when bromodeoxyuridine incorporation was compared at 11 sites within the chloroplast genome between vegetative cells, gametes, and rifampicin-treated cells by quantitative PCR, we found that incorporation was often reduced at the same sites in gametes that were also sensitive to rifampicin treatment. We conclude that a transcription-mediated form of DNA replication priming, which may be downregulated during gametogenesis, is indispensable for robust maintenance of PS1 genomes. These results highlight the potential for chloroplast genome copy number regulation through alternative replication strategies.

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Evidence for Paternal Leakage in Hybrid Periodical Cicadas (Hemiptera: Magicicada spp.)

Cited by 64 publications

References 58 publications

Lost in the zygote: the dilution of paternal mtDNA upon fertilization

Lost in the zygote: the dilution of paternal mtDNA upon fertilization

Extensive Mitochondrial Heteroplasmy in Natural Populations of a Resurging Human Pest, the Bed Bug (Hemiptera: Cimicidae)

Differential Replication of Two Chloroplast Genome Forms in Heteroplasmic Chlamydomonas reinhardtii Gametes Contributes to Alternative Inheritance Patterns

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