Evolution and consequences of paternal inheritance of plastid DNA in conifers

Tom J de Jong; Birgit Kersten; Avi Shmida

doi:10.1093/jeb/voag021

Evolution and consequences of paternal inheritance of plastid DNA in conifers

Tom J de Jong^*
, Birgit Kersten
, Avi Shmida

^*Corresponding author for this work

Alexander Silberman Institute of Life Sciences

Research output: Contribution to journal › Review article › peer-review

Abstract

In most seed plants, plastid DNA is inherited maternally. In conifers, however, plastid DNA is transferred paternally with pollen. The evolution of this strategy is unknown. With maternal transfer, plastid DNA is selected based on its effect in the sporophyte (plant) only, irrespective of its effect on the male gametophyte (pollen). This becomes problematic with antagonistic selection and when the pollen phase is long and stressful. With paternal transfer, only successful fathers pass on their plastid DNA to their offspring, which selects for sequences supporting pollen viability. If siring success is heritable, paternal inheritance of plastid DNA can evolve. We refer to this idea as the Male Gametophyte Selection Hypothesis. With paternal inheritance, plastid DNA alternates between sporophyte and male gametophyte, allowing selection in both phases. We review the consequences of mode of transfer for evolution of plastid DNA. The non-photosynthesis gene ycf1 is longer and under positive selection in conifers, making it an interesting candidate gene for further analysis.

Original language	English
Pages (from-to)	574-586
Number of pages	13
Journal	Journal of Evolutionary Biology
Volume	39
Issue number	5
DOIs	https://doi.org/10.1093/jeb/voag021
State	Published - May 2026

Bibliographical note

Publisher Copyright:
© The Author(s) 2026. Published by Oxford University Press on behalf of the European Society of Evolutionary Biology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

Keywords

antagonistic selection
chloroplast
genetic conflict
synergistic selection
uniparental inheritance
ycf1

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title = "Evolution and consequences of paternal inheritance of plastid DNA in conifers",

abstract = "In most seed plants, plastid DNA is inherited maternally. In conifers, however, plastid DNA is transferred paternally with pollen. The evolution of this strategy is unknown. With maternal transfer, plastid DNA is selected based on its effect in the sporophyte (plant) only, irrespective of its effect on the male gametophyte (pollen). This becomes problematic with antagonistic selection and when the pollen phase is long and stressful. With paternal transfer, only successful fathers pass on their plastid DNA to their offspring, which selects for sequences supporting pollen viability. If siring success is heritable, paternal inheritance of plastid DNA can evolve. We refer to this idea as the Male Gametophyte Selection Hypothesis. With paternal inheritance, plastid DNA alternates between sporophyte and male gametophyte, allowing selection in both phases. We review the consequences of mode of transfer for evolution of plastid DNA. The non-photosynthesis gene ycf1 is longer and under positive selection in conifers, making it an interesting candidate gene for further analysis.",

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author = "Tom J de Jong and Birgit Kersten and Avi Shmida",

note = "Publisher Copyright: {\textcopyright} The Author(s) 2026. Published by Oxford University Press on behalf of the European Society of Evolutionary Biology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.",

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N2 - In most seed plants, plastid DNA is inherited maternally. In conifers, however, plastid DNA is transferred paternally with pollen. The evolution of this strategy is unknown. With maternal transfer, plastid DNA is selected based on its effect in the sporophyte (plant) only, irrespective of its effect on the male gametophyte (pollen). This becomes problematic with antagonistic selection and when the pollen phase is long and stressful. With paternal transfer, only successful fathers pass on their plastid DNA to their offspring, which selects for sequences supporting pollen viability. If siring success is heritable, paternal inheritance of plastid DNA can evolve. We refer to this idea as the Male Gametophyte Selection Hypothesis. With paternal inheritance, plastid DNA alternates between sporophyte and male gametophyte, allowing selection in both phases. We review the consequences of mode of transfer for evolution of plastid DNA. The non-photosynthesis gene ycf1 is longer and under positive selection in conifers, making it an interesting candidate gene for further analysis.

AB - In most seed plants, plastid DNA is inherited maternally. In conifers, however, plastid DNA is transferred paternally with pollen. The evolution of this strategy is unknown. With maternal transfer, plastid DNA is selected based on its effect in the sporophyte (plant) only, irrespective of its effect on the male gametophyte (pollen). This becomes problematic with antagonistic selection and when the pollen phase is long and stressful. With paternal transfer, only successful fathers pass on their plastid DNA to their offspring, which selects for sequences supporting pollen viability. If siring success is heritable, paternal inheritance of plastid DNA can evolve. We refer to this idea as the Male Gametophyte Selection Hypothesis. With paternal inheritance, plastid DNA alternates between sporophyte and male gametophyte, allowing selection in both phases. We review the consequences of mode of transfer for evolution of plastid DNA. The non-photosynthesis gene ycf1 is longer and under positive selection in conifers, making it an interesting candidate gene for further analysis.

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Evolution and consequences of paternal inheritance of plastid DNA in conifers

Abstract

Bibliographical note

Keywords

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