Why Are Most Organelle Genomes Transmitted Maternally?

Overview

Journal Bioessays

Publisher Wiley

Specialties Biology
Cell Biology
Molecular Biology

Date 2014 Oct 11

PMID 25302405

Citations 124

Authors

Stephan Greiner

Johanna Sobanski

Ralph Bock

Affiliations

Soon will be listed here.

Abstract

Why the DNA-containing organelles, chloroplasts, and mitochondria, are inherited maternally is a long standing and unsolved question. However, recent years have seen a paradigm shift, in that the absoluteness of uniparental inheritance is increasingly questioned. Here, we review the field and propose a unifying model for organelle inheritance. We argue that the predominance of the maternal mode is a result of higher mutational load in the paternal gamete. Uniparental inheritance evolved from relaxed organelle inheritance patterns because it avoids the spread of selfish cytoplasmic elements. However, on evolutionary timescales, uniparentally inherited organelles are susceptible to mutational meltdown (Muller's ratchet). To prevent this, fall-back to relaxed inheritance patterns occurs, allowing low levels of sexual organelle recombination. Since sexual organelle recombination is insufficient to mitigate the effects of selfish cytoplasmic elements, various mechanisms for uniparental inheritance then evolve again independently. Organelle inheritance must therefore be seen as an evolutionary unstable trait, with a strong general bias to the uniparental, maternal, mode.

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References

Golczyk H, Greiner S, Wanner G, Weihe A, Bock R, Borner T . Chloroplast DNA in mature and senescing leaves: a reappraisal. Plant Cell. 2014; 26(3):847-54. PMC: 4001396. DOI: 10.1105/tpc.113.117465. View

Motomura T, Nagasato C, Kimura K . Cytoplasmic inheritance of organelles in brown algae. J Plant Res. 2010; 123(2):185-92. DOI: 10.1007/s10265-010-0313-x. View

Birky Jr C . The non-reciprocality of organelle gene recombination in Chlamydomonas reinhardtii and Saccharomyces cerevisiae: some new observations and a restatement of some old problems. Mol Gen Genet. 1978; 166(2):193-209. DOI: 10.1007/BF00285922. View

Medgyesy P, Fejes E, Maliga P . Interspecific chloroplast recombination in a Nicotiana somatic hybrid. Proc Natl Acad Sci U S A. 1985; 82(20):6960-4. PMC: 391289. DOI: 10.1073/pnas.82.20.6960. View

Hansen A, Escobar L, Gilbert L, Jansen R . Paternal, maternal, and biparental inheritance of the chloroplast genome in Passiflora (Passifloraceae): implications for phylogenetic studies. Am J Bot. 2011; 94(1):42-6. DOI: 10.3732/ajb.94.1.42. View

Hu Y, Zhang Q, Rao G, Sodmergen . Occurrence of plastids in the sperm cells of Caprifoliaceae: biparental plastid inheritance in angiosperms is unilaterally derived from maternal inheritance. Plant Cell Physiol. 2008; 49(6):958-68. DOI: 10.1093/pcp/pcn069. View

Birky Jr C . Relaxed cellular controls and organelle heredity. Science. 1983; 222(4623):468-75. DOI: 10.1126/science.6353578. View

Sager R, Ramanis Z . Chloroplast Genetics of Chlamydomonas. II. Mapping by Cosegregation Frequency Analysis. Genetics. 1976; 83(2):323-40. PMC: 1213516. DOI: 10.1093/genetics/83.2.323. View

Williamson D . The curious history of yeast mitochondrial DNA. Nat Rev Genet. 2002; 3(6):475-81. DOI: 10.1038/nrg814. View

10.

Zhang Q, Liu Y, Sodmergen . Examination of the cytoplasmic DNA in male reproductive cells to determine the potential for cytoplasmic inheritance in 295 angiosperm species. Plant Cell Physiol. 2003; 44(9):941-51. DOI: 10.1093/pcp/pcg121. View

11.

Vautrin E, Vavre F . Interactions between vertically transmitted symbionts: cooperation or conflict?. Trends Microbiol. 2009; 17(3):95-9. DOI: 10.1016/j.tim.2008.12.002. View

12.

Whittle C, Johnston M . Male-driven evolution of mitochondrial and chloroplastidial DNA sequences in plants. Mol Biol Evol. 2002; 19(6):938-49. DOI: 10.1093/oxfordjournals.molbev.a004151. View

13.

Harris E, Burkhart B, Gillham N, Boynton J . Antibiotic resistance mutations in the chloroplast 16S and 23S rRNA genes of Chlamydomonas reinhardtii: correlation of genetic and physical maps of the chloroplast genome. Genetics. 1989; 123(2):281-92. PMC: 1203800. DOI: 10.1093/genetics/123.2.281. View

14.

Kmiec B, Woloszynska M, Janska H . Heteroplasmy as a common state of mitochondrial genetic information in plants and animals. Curr Genet. 2006; 50(3):149-59. DOI: 10.1007/s00294-006-0082-1. View

15.

White D, Wolff J, Pierson M, Gemmell N . Revealing the hidden complexities of mtDNA inheritance. Mol Ecol. 2009; 17(23):4925-42. DOI: 10.1111/j.1365-294X.2008.03982.x. View

16.

Thanh N, Medgyesy P . Limited chloroplast gene transfer via recombination overcomes plastomegenome incompatibility between Nicotiana tabacum and Solanum tuberosum. Plant Mol Biol. 2013; 12(1):87-93. DOI: 10.1007/BF00017450. View

17.

Cosmides L, Tooby J . Cytoplasmic inheritance and intragenomic conflict. J Theor Biol. 1981; 89(1):83-129. DOI: 10.1016/0022-5193(81)90181-8. View

18.

Sato M, Sato K . Maternal inheritance of mitochondrial DNA by diverse mechanisms to eliminate paternal mitochondrial DNA. Biochim Biophys Acta. 2013; 1833(8):1979-84. DOI: 10.1016/j.bbamcr.2013.03.010. View

19.

Hadjivasiliou Z, Pomiankowski A, Seymour R, Lane N . Selection for mitonuclear co-adaptation could favour the evolution of two sexes. Proc Biol Sci. 2011; 279(1734):1865-72. PMC: 3297446. DOI: 10.1098/rspb.2011.1871. View

20.

Khakhlova O, Bock R . Elimination of deleterious mutations in plastid genomes by gene conversion. Plant J. 2006; 46(1):85-94. DOI: 10.1111/j.1365-313X.2006.02673.x. View