Exceptional paternal inheritance of plastids in Arabidopsis suggests that low‐frequency leakage of plastids via pollen may be universal in plants

Azhagiri, Arun K.; Maliga, Pál

doi:10.1111/j.1365-313x.2007.03278.x

Cited by 85 publications

(59 citation statements)

References 31 publications

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“…In Arabidopsis, no plastids are found in sperm cells (Tang et al, 2009;Wang et al, 2010), and DPD1 is unlikely to affect maternal ptDNA inheritance. Therefore, plastid maternal inheritance is determined primarily by the exclusion of plastids in germ cells rather than ptDNA amounts in Arabidopsis (Martínez et al, 1997;Azhagiri and Maliga, 2007). In fact, our F1 analysis between Cvi and dpd1 showed that DPD1 did not affect plastid inheritance (see Supplemental Figure 6 online).…”

Section: Maternal Inheritance and Possible Role Of Organelle Dna Degrmentioning

confidence: 76%

A Conserved, Mg2+-Dependent Exonuclease Degrades Organelle DNA duringArabidopsisPollen Development

et al. 2011

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In plant cells, mitochondria and plastids contain their own genomes derived from the ancestral bacteria endosymbiont. Despite their limited genetic capacity, these multicopy organelle genomes account for a substantial fraction of total cellular DNA, raising the question of whether organelle DNA quantity is controlled spatially or temporally. In this study, we genetically dissected the organelle DNA decrease in pollen, a phenomenon that appears to be common in most angiosperm species. By staining mature pollen grains with fluorescent DNA dye, we screened Arabidopsis thaliana for mutants in which extrachromosomal DNAs had accumulated. Such a recessive mutant, termed defective in pollen organelle DNA degradation1 (dpd1), showing elevated levels of DNAs in both plastids and mitochondria, was isolated and characterized. DPD1 encodes a protein belonging to the exonuclease family, whose homologs appear to be found in angiosperms. Indeed, DPD1 has Mg 2+ -dependent exonuclease activity when expressed as a fusion protein and when assayed in vitro and is highly active in developing pollen. Consistent with the dpd phenotype, DPD1 is dual-targeted to plastids and mitochondria. Therefore, we provide evidence of active organelle DNA degradation in the angiosperm male gametophyte, primarily independent of maternal inheritance; the biological function of organellar DNA degradation in pollen is currently unclear.

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Section: Maternal Inheritance and Possible Role Of Organelle Dna Degrmentioning

confidence: 76%

A Conserved, Mg2+-Dependent Exonuclease Degrades Organelle DNA duringArabidopsisPollen Development

et al. 2011

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“…Examples include the monocot species Setaria italica and the dicots tobacco (Avni and Edelman, 1991;Ruf et al, 2007;Svab and Maliga, 2007), petunia (Petunia hybrida;Derepas and Dulieu, 1992), and Arabidopsis (Arabidopsis thaliana; Azhagiri and Maliga, 2007). Another mechanism that could yield new combinations of plastids and CMS mitochondria is the horizontal gene transfer of mitochondrial DNA, an evolutionary mechanism described in multiple species (Richardson and Palmer, 2007;Bock, 2010).…”

Section: Single Origin Of Cms-t Cytoplasm In Maizementioning

confidence: 99%

Plastid Genotyping Reveals Uniformity of cms-T Maize Cytoplasms

2015

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ORCID IDs: 0000-0003-4454-9882 (M.B.); 0000-0002-8063-653X (C.G.); 0000-0002-6202-0029 (P.M.).Cytoplasmic male-sterile (CMS) lines in maize (Zea mays) have been classified by their response to specific restorer genes into three categories: cms-C, cms-S, and cms-T. A mitochondrial genome representing each of the CMS cytotypes has been sequenced, and male sterility in the cms-S and cms-T cytotypes is linked to chimeric mitochondrial genes. To identify markers for plastid genotyping, we sequenced the plastid genomes of three fertile maize lines (B37, B73, and A188) and the B37 cms-C, cms-S, and cms-T cytoplasmic substitution lines. We found that the plastid genomes of B37 and B73 lines are identical. Furthermore, the fertile and CMS plastid genomes are conserved, differing only by zero to three single-nucleotide polymorphisms (SNPs) in coding regions and by eight to 22 SNPs and 10 to 21 short insertions/deletions in noncoding regions. To gain insight into the origin and transmission of the cms-T trait, we identified three SNPs unique to the cms-T plastids and tested the three diagnostic SNPs in 27 cms-T lines, representing the HA, I, Q, RS, and T male-sterile cytoplasms. We report that each of the tested 27 cms-T group accessions have the same three diagnostic plastid SNPs, indicating a single origin and maternal cotransmission of the cms-T mitochondria and plastids to the seed progeny. Our data exclude exceptional pollen transmission of organelles or multiple horizontal gene transfer events as the source of the mitochondrial urf13-T (unidentified reading frame encoding 13-kD cms-T protein) gene in the cms-T cytoplasms. Plastid genotyping enables a reassessment of the evolutionary relationships of cytoplasms in cultivated maize.

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“…For example, the use of plastome mutants by Correns and Baur formed the foundation of cytoplasmic genetics (Baur, 1909;Correns, 1909;Baur, 1910;Hagemann, 2010). Plastome mutants continue to play an important role in elucidating the rules of nonMendelian inheritance (Chiu and Sears, 1985;Azhagiri and Maliga, 2007;Ruf et al, 2007) and in studying chloroplast gene expression and photosynthesis (Schaffner et al, 1995;Landau et al, 2009). Moreover, plastid mutants provide selectable markers for antibiotic or herbicide resistance that are widely used in molecular biology, biotechnology, and agriculture (Schmitz-Linneweber et al, 2005;Powles and Yu, 2010).…”

Section: Introductionmentioning

confidence: 99%

Spontaneous Chloroplast Mutants Mostly Occur by Replication Slippage and Show a Biased Pattern in the Plastome of Oenothera

et al. 2016

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Spontaneous plastome mutants have been used as a research tool since the beginning of genetics. However, technical restrictions have severely limited their contributions to research in physiology and molecular biology. Here, we used full plastome sequencing to systematically characterize a collection of 51 spontaneous chloroplast mutants in Oenothera (evening primrose). Most mutants carry only a single mutation. Unexpectedly, the vast majority of mutations do not represent single nucleotide polymorphisms but are insertions/deletions originating from DNA replication slippage events. Only very few mutations appear to be caused by imprecise double-strand break repair, nucleotide misincorporation during replication, or incorrect nucleotide excision repair following oxidative damage. U-turn inversions were not detected. Replication slippage is induced at repetitive sequences that can be very small and tend to have high A/T content. Interestingly, the mutations are not distributed randomly in the genome. The underrepresentation of mutations caused by faulty double-strand break repair might explain the high structural conservation of seed plant plastomes throughout evolution. In addition to providing a fully characterized mutant collection for future research on plastid genetics, gene expression, and photosynthesis, our work identified the spectrum of spontaneous mutations in plastids and reveals that this spectrum is very different from that in the nucleus.

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Exceptional paternal inheritance of plastids in Arabidopsis suggests that low‐frequency leakage of plastids via pollen may be universal in plants

Cited by 85 publications

References 31 publications

A Conserved, Mg2+-Dependent Exonuclease Degrades Organelle DNA duringArabidopsisPollen Development

A Conserved, Mg2+-Dependent Exonuclease Degrades Organelle DNA duringArabidopsisPollen Development

Plastid Genotyping Reveals Uniformity of cms-T Maize Cytoplasms

Spontaneous Chloroplast Mutants Mostly Occur by Replication Slippage and Show a Biased Pattern in the Plastome of Oenothera

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