Pollen Transmission of Plastid–DNA Under Genotypic Control in Petunia hybrida Hort

Cornu, A.; Dulieu, H.

doi:10.1093/oxfordjournals.jhered.a110443

Cited by 45 publications

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“…Because of the lack of suitable genetic markers, transmission of paternal ptDNA by pollen thus far had been shown only in alloplasmic crosses, leaving open the possibility that paternal ptDNA transmission is due to the breakdown of normal control processes in the alloplasmic cross. Indeed, the frequency of paternal pollen transmission reported in alloplasmic crosses, in general, was significantly higher, 0.5-2.5% of seed progeny (10)(11)(12)(13)(14) than the value we found, 9 ϫ 10 Ϫ5 , in the cross with the normal cytoplasm. However, the frequency of paternal pollen transmission in our alloplasmic cross was also relatively low, 2 ϫ 10 Ϫ4 , and only Ϸ2-fold higher than the frequency in the cross between the normal parental lines.…”

Section: Discussioncontrasting

confidence: 78%

“…The reason for skepticism was the reported relatively high-frequency paternal ptDNA transmission in species in which plastids were assumed to be inherited strictly by the maternal parent. Paternal ptDNA transmission was detected in crosses by using streptomycin resistance (in 0.07-2.5%) (10, 11) and tentoxin resistance (0.5-2.5%) (12) in tobacco, pigment deficiency in petunia (2%) (13,14), and atrazine resistance in foxtail or birdseed millet (0.03%) (15).Common in these studies was utilization of alloplasmic substitution lines, in which plastids and mitochondria of one species were combined with the nuclear genome of another species. We therefore decided to test whether rare paternal plastid transmission occurs in Nicotiana tabacum if no alloplasmic substitution line is involved in the cross.…”

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Exceptional transmission of plastids and mitochondria from the transplastomic pollen parent and its impact on transgene containment

Sváb

Maliga

2007

Proc. Natl. Acad. Sci. U.S.A.

154

108

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Plastids in Nicotiana tabacum are normally transmitted to the progeny by the maternal parent only. However, low-frequency paternal plastid transmission has been reported in crosses involving parents with an alien cytoplasm. Our objective was to determine whether paternal plastids are transmitted in crosses between parents with the normal cytoplasm. The transplastomic father lines carried a spectinomycin resistance (aadA) transgene incorporated in the plastid genome. The mother lines in the crosses were either (i) alloplasmic, with the Nicotiana undulata cytoplasm that confers cytoplasmic male sterility (CMS92) or (ii) normal, with the fertile N. tabacum cytoplasm. Here we report that plastids from the transplastomic father were transmitted in both cases at low (10 ؊4 -10 ؊5 ) frequencies; therefore, rare paternal pollen transmission is not simply due to breakdown of normal controls caused by the alien cytoplasm. Furthermore, we have found that the entire plastid genome was transmitted by pollen rather than small plastid genome (ptDNA) fragments. Interestingly, the plants, which inherited paternal plastids, also carried paternal mitochondrial DNA, indicating cotransmission of plastids and mitochondria in the same pollen. The detection of rare paternal plastid transmission described here was facilitated by direct selection for the transplastomic spectinomycin resistance marker in tissue culture; therefore, recovery of rare paternal plastids in the germline is less likely to occur under field conditions. Nicotiana tabacum ͉ organelle inheritance ͉ plastid transformation ͉ pollen transmission D NA in a plant cell is found in three cellular compartments: the nucleus, plastids, and mitochondria. Genes encoded in the nucleus are inherited biparentally, according to Mendel's rules. In contrast, plastids and mitochondria may be inherited maternally, paternally, or from both parents. In most crops, the maternal parent transmits plastids, because plastids are excluded from the sperm cell or, even if not excluded, are left behind in synergid cells during fertilization (1-3). In Chlamydomonas reinhardtii, a unicellular alga, in which maternal (mating-type ϩ ) and paternal (mating-type Ϫ ) chloroplasts fuse, only the maternal plastid genome (ptDNA) is inherited, because the maternal ptDNA is protected by methylation, whereas the nonmethylated paternal ptDNA is degraded (4). Once protocols for plastid transformation were developed (5, 6), localization of transgenes in the plastid genome was advocated as a means of transgene containment (7). Utility of plastid localization for containment became a hotly debated issue when the first herbicide-resistant transplastomic plants were obtained (8, 9). The reason for skepticism was the reported relatively high-frequency paternal ptDNA transmission in species in which plastids were assumed to be inherited strictly by the maternal parent. Paternal ptDNA transmission was detected in crosses by using streptomycin resistance (in 0.07-2.5%) (10, 11) and tentoxin resistance (0.5-2.5%) (12) in...

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Section: Discussioncontrasting

confidence: 78%

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confidence: 99%

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confidence: 99%

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Exceptional transmission of plastids and mitochondria from the transplastomic pollen parent and its impact on transgene containment

Sváb

Maliga

2007

Proc. Natl. Acad. Sci. U.S.A.

154

108

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“…A regular transmission of about 2 per cent of plastids from the male parent occurs in the inbred line Tbl-3 of Petunia hybrida (Cornu & Dulieu, 1988). Analysis of one backcross generation supported the hypothesis that two major loci Tpl and Tp2 determined the difference between Tbl-3 and a non-transmitter line Skr4 (Dulieu et al, 1990).…”

Section: Introductionmentioning

confidence: 70%

A test of the complementary gene model for the control of biparental plastid inheritance in zonal pelargoniums

Amoatey

Tilney-Bassett

1994

Heredity

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Zonal pelargoniums have a mixed plastid inheritance. After G XW plastid crosses, the progeny are a mixture of green, variegated and white embryos corresponding to a maternal, biparental or paternal plastid inheritance. There are two patterns of segregation: type I females produce families with a majority of green embryos, variegated intermediate and white least frequent. Type II females give rise to families in which green and white embryos are of about the same frequency and variegated the least common. The complementary gene model proposes that the alternative patterns are determined by two genes called Pr] /pri and Pr2/pr2. Plants giving rise to the type II pattern contain one or two copies of the dominant alleles of both genes whereas in the absence of either one or both dominant alleles the plants are type I. The model was tested and confirmed in the classical Mendelian manner in which a single cross between two different true-breeding type I plants was followed by scoring the parents, the F1 hybrid progeny and the F2 and backcross generations. The results supported the interpretation that one type I parent had the genotype PriPri, pr2pr2 and the other type I parent had the genotype pripri, Pr2pr2. The range, variance and confidence limits are given for the estimates of percentage maternal plastid transmission within groups of type I and type II plants in 18 segregating families.

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“…Nonsexual vertical transmission would occur by parent to offspring contact, for example, during lactation. In plants, such vertically transmitted pathogens include many viruses (Pathipanawat et al ., 1995), plasmids (Cornu & Dulieu, 1988), dsRNA molecules (Osaki et al ., 1998), and transposons (Wright & Schoen, 1999). This perspective of self-replicating genetic elements as vertically transmitted STDs (Hickey, 1982) has led to important insights into the evolution of uniparental inheritance ( Hurst & Hamilton 1992;Law & Hutson 1992) and into the relationships between breeding systems, transposable elements, and genomic evolution (Wright & Schoen, 1999).…”

Section: The Definitional Approachmentioning

confidence: 99%

Plant venereal diseases: insights from a messy metaphor

Antonovics

2004

New Phytologist

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SummaryThe concept of plant venereal disease is examined from definitional, operational and axiomatic viewpoints. The transmission of many plant pathogens occurs during the flowering phase and is effected either by pollinators or by wind dispersal of spores from inflorescences. Attraction of insects by pseudo-flowers or sugary secretions also serves to spread many diseases. Given the diversity of processes involved, a simple all-encompassing parallel with animal venereal diseases is not possible. Operationally establishing the routes of disease transmission, as well as quantifying the relative magnitudes of these different routes, remains critical for understanding disease dynamics and controlling spread in agricultural contexts. From an axiomatic viewpoint, sexually transmitted diseases are characterized by frequency-dependent transmission, transmission in the adult stage, and by virulence effects involving sterility rather than mortality. These characteristics serve to differentiate the dynamics and evolution of sexually transmitted diseases from that of other diseases and are features that are also shared by many pollinator-transmitted diseases. However, the majority of plant diseases that involve the reproductive structures show a rich biology that defies easy categorization. The experimental convenience of plants and their pathogens is likely to play an important role in understanding the evolution of disease traits, irrespective of what descriptive terms are applied to the natural history of the transmission process.

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Pollen Transmission of Plastid–DNA Under Genotypic Control in Petunia hybrida Hort

Cited by 45 publications

References 0 publications

Exceptional transmission of plastids and mitochondria from the transplastomic pollen parent and its impact on transgene containment

Exceptional transmission of plastids and mitochondria from the transplastomic pollen parent and its impact on transgene containment

A test of the complementary gene model for the control of biparental plastid inheritance in zonal pelargoniums

Plant venereal diseases: insights from a messy metaphor

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