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Plant and Cell Physiology Advance Access originally published online on April 29, 2008
Plant and Cell Physiology 2008 49(6):958-968; doi:10.1093/pcp/pcn069
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© The Author 2008. Published by Oxford University Press on behalf of Japanese Society of Plant Physiologists. All rights reserved. For permissions, please email: journals.permissions@oxfordjournals.org

Occurrence of Plastids in the Sperm Cells of Caprifoliaceae: Biparental Plastid Inheritance in Angiosperms is Unilaterally Derived from Maternal Inheritance

Yingchun Hu, Quan Zhang, Guangyuan Rao and Sodmergen*

Key Laboratory of Cell Proliferation and Differentiation (Ministry of Education), College of Life Sciences, Peking University, Beijing 100871, PR China

*Corresponding author: E-mail, sodmergn{at}pku.edu.cn; Fax, +86-10-62751526.


  Abstract

It is widely held that organelles inherit from the maternal lineage. However, the plastid genome in quite a few angiosperms appears to be biparentally transmitted. It is unclear how and why biparental inheritance of the genome became activated. Here, we detected widespread occurrence of plastids in the sperm cells (a cellular prerequisite for biparental inheritance) of traditional Caprifoliaceae. Of the 12 genera sampled, the sperm cells of Abelia, Dipelta, Heptacodium, Kolkwitzia, Leycesteria, Linnaea, Lonicera, Symphoricarpos, Triosteum and Weigela possessed inheritable plastids. The other genera, Sambucus and Viburnum, lacked plastids in sperm cells. Interestingly, such exclusion of plastids in the sperm cells of some Caprifoliaceae appeared to be associated with the divergence of Dipsacales phylogeny. Closer examination of Weigela florida revealed that both plastids and plastid DNA were highly duplicated in the generative cells. This implies that the appearance of plastids in sperm cells involved cellular mechanisms. Because such mechanisms must enhance the strength of plastid transmission through the paternal lineage and appear ubiquitous in species exhibiting biparental or potential biparental plastid inheritance, we presume that biparental plastid genetics may be a derived trait in angiosperms. This is consistent with our extended phylogenetic analysis using species with recently discovered modes of potential plastid inheritance. The results show that basal and early angiosperms have maternal plastid transmission, whereas all potential biparental transmission occurs at terminal branches of the tree. Thus, unlike previous studies, we suggest that biparental plastid inheritance in angiosperms was unilaterally converted from the maternal transmission mode during late angiosperm evolution.

Keywords: Angiosperm - Caprifoliaceae - Non-Mendelian genetics - Plastid inheritance

Abbreviations: DAPI, 4',6-diamidino-2-phenylindole; DiOC6, 3,3'-dihexyloxacarbocyanine iodide.

(Received January 30, 2008; Accepted April 25, 2008)
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