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

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...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 104; no. 17; pp. 7003 - 7008
Main Authors Svab, Zora, Maliga, Pal
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 24.04.2007
National Acad Sciences
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Summary: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.
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Author contributions: Z.S. and P.M. designed research; Z.S. and P.M. performed research; Z.S. and P.M. analyzed data; and P.M. wrote the paper.
Edited by Maarten Koornneef, Wageningen University and Research Centre, Wageningen, The Netherlands, and approved February 28, 2007
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.0700063104