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First published online July 25, 2008; 10.1104/pp.108.119107

Plant Physiology 148:328-336 (2008)
© 2008 American Society of Plant Biologists

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GENETICS, GENOMICS, AND MOLECULAR EVOLUTION

Transfer of Plastid DNA to the Nucleus Is Elevated during Male Gametogenesis in Tobacco1,[OA]

Anna E. Sheppard, Michael A. Ayliffe, Laura Blatch, Anil Day, Sven K. Delaney, Norfarhana Khairul-Fahmy, Yuan Li, Panagiotis Madesis, Anthony J. Pryor and Jeremy N. Timmis*

School of Molecular and Biomedical Science, University of Adelaide, South Australia 5005, Australia (A.E.S., S.K.D., Y.L., J.N.T.); CSIRO Plant Industry, Australian Capital Territory 2601, Australia (M.A.A., A.J.P.); and Faculty of Life Sciences, University of Manchester, Manchester M13 9PT, United Kingdom (L.B., A.D., N.K.-F., P.M.)

In eukaryotes, many genes were transferred to the nucleus from prokaryotic ancestors of the cytoplasmic organelles during endosymbiotic evolution. In plants, the transfer of genetic material from the plastid (chloroplast) and mitochondrion to the nucleus is a continuing process. The cellular location of a kanamycin resistance gene tailored for nuclear expression (35SneoSTLS2) was monitored in the progeny of reciprocal crosses of tobacco (Nicotiana tabacum) in which, at the start of the experiments, the reporter gene was confined either to the male or the female parental plastid genome. Among 146,000 progeny from crosses where the transplastomic parent was male, 13 transposition events were identified, whereas only one atypical transposition was identified in a screen of 273,000 transplastomic ovules. In a second experiment, a transplastomic β-glucuronidase reporter gene, tailored to be expressed only in the nucleus, showed frequent stochastic expression that was confined to the cytoplasm in the somatic cells of several plant tissues. This gene was stably transferred in two out of 98,000 seedlings derived from a male transplastomic line crossed with a female wild type. These data demonstrate relocation of plastid DNA to the nucleus in both somatic and gametophytic tissue and reveal a large elevation of the frequency of transposition in the male germline. The results suggest a new explanation for the occurrence of uniparental inheritance in eukaryotes.


1 This work was supported by the Australian Research Council (grant no. DP0557496).

The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Jeremy N. Timmis (jeremy.timmis{at}adelaide.edu.au).

[OA] Open Access articles can be viewed online without a subscription.

www.plantphysiol.org/cgi/doi/10.1104/pp.108.119107

* Corresponding author; e-mail jeremy.timmis{at}adelaide.edu.au.

Received March 13, 2008; accepted July 20, 2008; published July 25, 2008.


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