Inheritance of the Capacity to Transfer Plastids by the Pollen Parent in Petunia hybrida Hort

Derepas, A.; Dulieu, H.

doi:10.1093/oxfordjournals.jhered.a111158

Cited by 41 publications

(31 citation statements)

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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: 77%

“…Petit Havana. Indeed, line-specific differences within a species are important; in Petunia, lowfrequency paternal ptDNA transmission was detectable in only 5 of the 22 inbreds tested (25).…”

Section: Discussionmentioning

confidence: 99%

“…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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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.

150

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: 77%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

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.

150

108

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“…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). Moreover, testing chimeral individuals as male parents suggested that genes favouring paternal transfer acted at the male gametophytic level (Derepas, 1991;Derepas & Dulieu, 1992). Within Medicago sativa three genotypes have been recognized, one that is a strong transmitter of male plastids (301), one a weaker transmitter (7W) and *Correspondence complementary genes, Mendelian inheritance, 69 one even weaker (MS-5) (Zhu et al, 1990).…”

Section: Introductionmentioning

confidence: 85%

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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Biological Containment Strategies for Transgenic Crops

Maagd

Boutilier

2012

Genetically Modified and Non‐Genetically Modified Food Supply Chains: Co‐Existence and Traceability

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Inheritance of the Capacity to Transfer Plastids by the Pollen Parent in Petunia hybrida Hort

Cited by 41 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

Biological Containment Strategies for Transgenic Crops

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